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What Darwins Finches Can Teach Us about the Evolutionary Origin andRegulation of BiodiversityAuthor(s) B ROSEMARY GRANT and PETER R GRANTSource BioScience 53(10)965-975 2003Published By American Institute of Biological SciencesDOI httpdxdoiorg1016410006-3568(2003)053[0965WDFCTU]20CO2URL httpwwwbiooneorgdoifull1016410006-3568282003290535B09653AWDFCTU5D20CO3B2

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October 2003 Vol 53 No 10 bull BioScience 965

Plenary

Biologists are increasingly interested in diversityOne major source of interest is the conservation of bio-

diversity in a world threatened with anthropogenic habitat de-struction and environmental pollution A second majorsource of interest is the regulation and maintenance of existingbiodiversity by natural processes and the functioning of thisbiodiversity in units that vary from small communities to largeecosystems Finally the biodiversity puzzle has a third piecewithout which our understanding is bound to be incom-plete the evolutionary origins of diversity Reduced to itssimplest form this is the Darwinian question of how newspecies arise and multiply This question is the main focus ofthis article and we illustrate our points with Darwinrsquos finchesof the Galaacutepagos Islands

Some organisms are unusually suitable for answering par-ticular questions The squid for example has served neuro-biology well because it has a giant axon Drosophila specieshave contributed much to cytogenetics because of the giantchromosomes in their salivary glands and ArabidopsisCaenorhabdites and a few other small organisms have beenwell chosen to investigate the construction of entire genomesDarwinrsquos finches are particularly suitable for asking evolu-tionary questions about adaptation and the multiplication ofspecies how these processes happen and how to interpretthem

All species of Darwinrsquos finches are closely related havingderived recently (in geological terms) from a common

ancestor They live in the largely undisturbed environment inwhich they evolved and none has become extinct as a resultof human activity Consequently whatever we can learnabout their ecology and evolution gives us insights into theprocess of speciation under entirely natural conditions Pop-ulations of the same species occur on different islands andin some cases they have different ecologies This allows us toinvestigate the reasons for their divergence Closely relatedspecies occur together on the same island and differ This allows us to investigate the nature of the reproductive barrierbetween them and the question of how and why species stayapart Thus considering populations across the entire archi-pelago we can see all stages of the speciation process fromstart to finish at the same time

In this article we survey the evidence from field studies ofthe ecological causes of diversification The explanation for

B Rosemary Grant (e-mail rgrantprincetonedu) is a senior research scholar

and professor in the Department of Ecology and Evolutionary Biology and

Peter R Grant is the Class of 1877 Professor of Zoology at Princeton University

Princeton NJ 085440 They have studied the ecology behavior biogeography

and genetics of Darwinrsquos finches for the last 30 years This article is an expanded

version of a plenary address delivered at the 53rd annual meeting of the

American Institute of Biological Sciences held in Arlington Virginia 22ndash24

March 2002 The title of the symposium was ldquoEvolution Understanding Life

on Earthrdquo copy 2003 American Institute of Biological Sciences

What Darwinrsquos Finches Can Teach Us about theEvolutionary Origin andRegulation of Biodiversity

B ROSEMARY GRANT AND PETER R GRANT

Darwinrsquos finches on the Galaacutepagos Islands are particularly suitable for asking evolutionary questions about adaptation and the multiplication ofspecies how these processes happen and how to interpret them All 14 species of Darwinrsquos finches are closely related having been derived from acommon ancestor 2 million to 3 million years ago They live in the environment in which they evolved and none has become extinct as a result ofhuman activity Key factors in their evolutionary diversification are environmental change natural selection and cultural evolution A long-termstudy of finch populations on the island of Daphne Major has revealed that evolution occurs by natural selection when the finchesrsquo food supplychanges during droughts Extending this finding to the past we discuss how environmental change has influenced the opportunities for speciationand diversification of finches throughout their history The number of islands has increased the climate has cooled and the vegetation and foodsupply have changed

Keywords adaptation natural selection speciation song learning Galaacutepagos history

diversification involves natural selection genetic drift intro-gressive hybridization and genetic as well as cultural evolu-tion Linking all these factors are the frequent and strongfluctuations in climatic conditions between droughts on theone hand and extremely wet (El Nintildeo) conditions on theother An important conclusion of this study is that environmental change is an observable driving force in the origin of new species Using information from the study ofcontemporary finches we then turn to questions of how andwhy their adaptive radiation unfolded in the way that it didWe focus on how environmental change in the past hasguided the multiplication of finch species Whereas the microevolutionary principles were probably the same through-out the finchesrsquo radiation the circumstances differed in important ways at different times General principles coupledwith specific circumstances explain the particular features ofthe radiation

The pattern of adaptationAt least 14 species of Darwinrsquos finches were formed in the last2 million to 3 million years in the Galaacutepagos archipelagoand on Cocos Island They stand as a model of adaptive radiation that is the production in a short period of time ofmany species from one occupying different ecological niches(Schluter 2000) Figure 1 shows the four points of the Darwinrsquos finch compass to illustrate the finchesrsquo diversityand figure 2 shows three closely related species to illustrate howsimilar the intervening species are That similarity makes itrelatively easy to reconstruct the evolutionary transition fromone species to another Darwin (1842) wrote about this phe-nomenon 7 years after he FitzRoy and their assistants collectedthe first specimensldquoThe most curious fact is the perfect gra-dation in the size of the beaks of the different species ofGeospiza Seeing this gradation and diversity of structurein one small intimately related group of birds one might fancythat from an original paucity of birds in this archipelago onespecies has been taken and modified for different endsrdquo(p 458)

Translated into the modern language of evolutionary bio-logy ldquomodified for different endsrdquo means adaptated by nat-ural selection (figure 3) The modern evidence for this beginswith an association between beak size and diet (Lack 1947Bowman 1961) There is a strong relationship between thebeak size of ground finch species and the maximum size andhardness of the seeds that the birds can crack (figure 4) Theassociation between beak size and diet is most obvious whencomparing the species that have contrasting morphologysuch as the insectivorous small warbler finches (about 8grams [g]) and the granivorous large ground finch (about 30g) It is less obvious when comparing populations of thesame species on different islands Nevertheless different pop-ulations of the sharp-beaked ground finch Geospiza difficilisfeed in different ways on different foods with beaks of differentsize and shape On the high islands of Santiago Fernandinaand Pinta they have relatively blunt beaks and feed on arthro-pods and mollusks as well as fruits and seeds in the dry

season On the low island of Genovesa where their beaks aremuch smaller they are more dependent on small seeds as wellas on nectar and pollen from plants including the Opuntiacactus Apparently uniquely on the low island of Wolf they exploit seabirds (boobies Sula spp) in two dramatic waysFirst they kick the booby eggs until the eggs fall or hit a rockand crack enabling the finches to open them and consumethe contents They also inflict wounds at the base of the sitting boobiesrsquo wing feathers and consume the blood On thisisland the finchesrsquo beaks are long

In contrast to the sharp-beaked ground finches birds withlarge robust beaks such as the large tree finch Camarhynchuspsittacula do not probe Opuntia flowers or poke at eggsInstead the beak of this finch is a tool for tearing bark andcrushing twigs and small branchesmdasha beak modified for a different end These examples illustrate some of the waysthat Darwinrsquos finches vary in beak morphology and are versatile in their feeding habits This versatility is fostered by ecological opportunity and impelled by food scarcity in thedry season and in dry years

As evidence of adaptive diversification associations like thisdo not satisfy everyone because causality can be argued frombeaks to diets as well as from diets to beaks For example itcan be said that finches feed in different ways because they havedifferent beak sizes and shapes (eg Newton 1967) Theysurely do but this begs the question of why the speciesrsquo beaksdiffer in the first place Another objection has been raised onthe grounds of insufficiency of evidence When David Lack(1947) argued that evolution had caused the fit betweenbirdsrsquo beaks and their food an ecologist commented ldquoTheproblem for instance of whether certain specific characters(eg beaks of Geospizinae) are or are not adaptive (vagueterm) is one involving studies of field populations geneticsand variation It is a problem which might be largely solvedby teams of workers dealing for a number of years with a par-ticularly favourable example It is not one I think whichcan be settled in a four months stay even if supplemented bythe examination of skins in museumsrdquo(Richards 1948 p 84)

Without knowing about this critique at the time we pickedup the challenge 30 years ago Over the years the team consisted of Ian Abbott Peter Boag Trevor Price Lisle Gibbsseveral assistants and ourselves Our study took place on theisland of Daphne Majormdasha particularly favorable locationalthough one would not think so judging from its steeptopography (see the photograph on p 970)

Adaptation as a processBy virtue of its small size (034 square kilometers [km])moderate degree of isolation (8 km from the nearest island)undisturbed habitat and resident populations of finchesDaphne Major is a particularly favorable location for study-ing Darwinrsquos three essential ingredients of adaptive evolutionvariation inheritance and selection We accomplished this bycapturing and measuring many finches to determine pheno-typic variation comparing offspring with their parents to determine inheritance and following their fates across years

966 BioScience bull October 2003 Vol 53 No 10

Plenary

to detect selection We found pronounced heritable variationin beak size and body size within populations of the mediumground finch (Geospiza fortis) and the cactus finch (Geospizascandens) We also found that when the environment changessome of the variants in each population survive while othersdie This amounts to a vindication of David Lackrsquos views onadaptation

Birds with small beaks and small body size suffered selec-tive mortality in 1977 during a severe drought (figure 5) Thelarger members of the medium ground finch populationsurvived on a diet of large hard seeds which increasingly dominated the food supply as a result of an initial preferen-tial consumption of small seeds Smaller birds lacking the mechanical power to crack the large seeds of Tribulus cistoidesand Opuntia echios died at a higher rate than large birdsAn evolutionary response to directional natural selectionfollowed in the next generation (figure 5) because beak sizevariation is highly heritable (Keller et al 2001)

Natural selection in the opposite direction with smallbirds surviving disproportionately occurred 8 years laterThe island experienced a major prolonged El Nintildeo eventfrom November 1982 to August 1983 The abundant rain andhigh temperatures transformed the vegetation and food sup-ply of the finches and they bred for 8 months as opposed tothe usual 1 or 2 monthsVines and other plants multiplied and

spread smothering the low-growing Tribulus plants and Opuntia cactus bushes The seed supply became dominatedby small seeds and seeds of Tribulus and Opuntia becamescarce When the island entered the next drying-out episodeduring the drought of 1985 the supply of seeds fell and sodid the numbers of finches from high points in the produc-tive years of 1983 and 1984 Large birds died at the highest ratehence the medium ground finches that were small with rel-atively pointed beaks were selectively favored

Thus selection oscillates in directionWe have observed thisrepeatedly over the full 30-year period (Grant and Grant2002a) As a consequence neither the medium ground finchnor the cactus finch has remained morphologically constantor static In fact the mean body size and beak shape of the twospecies are not the same now as they were at the beginningof the study (figure 6) In an environment subject to climaticand floristic change the finches have changed (evolved) Wehave directly observed the sort of adaptive change that isnormally only inferred from a comparison of related popu-lations differing in mean morphology

Summarizing this study has taught us four things aboutnatural selection

bull It is an observable interpretable and repeatable processin a natural environment

October 2003 Vol 53 No 10 bull BioScience 967

Plenary

Figure 1 Four points of the Darwinrsquos finch compass Species with contrastingmorphology (Certhidea olivacea Geospiza difficilis Geospiza magnirostris andPlatyspiza crassirostris) show the range of sizes and shapes in beaks from smallto large and from blunt to pointed Photographs B Rosemary Grant and PeterR Grant

Figure 2 Three recently evolvedspecies of Darwinrsquos finches (Geospizafuliginosa Geospiza fortis andGeospiza magnirostris) differ principally in size but also in beakshape Photographs B Rosemary Grant and Peter R Grant

bull It oscillates in direction

bull It happens when the environment changes

bull It has evolutionary consequences (adaptive change)

Almost 100 years after Darwinrsquos visit to the Galaacutepagos asystematist Harry Swarth came close to suggesting that evo-lution was not over and done with but could actually be witnessed when he wrote that ldquothe extraordinary variantsthat crop up in a series [of museum specimens] give an im-pression of change and experiment going onrdquo(Swarth 1934)Based on the evidence of Darwinrsquos finches evolutionarychanges are indeed going on

Speciation The beginningSpeciation begins with the divergence of apopulation and is completed when two pop-ulations that have diverged on different islandsestablish coexistence with little or no inter-breeding (Mayr 1942 Grant 2001) We obtained insight into the initial process ofdivergence on Daphne Major thanks to ahighly fortuitous circumstance the foundingof a new population

The large ground finch (Geospiza magni-rostris) became a breeding member of thecommunity in late 1982 when two femalesand three males began to breed In precedingyears we had observed immigrant membersof this species on the island in the dry seasonbut when the rains began they disappearedpresumably returning to their island oforigin to breed Not so in El Nintildeo The breed-ing birds produced 17 fledglings in 1982ndash1983 but only one of the breeding pairs produced the next generation A daughterbred at different times with two brothersone of which can be ignored because the offspring did not survive to breed Thus thepopulation was effectively founded by a single pair and the next generation com-prised a sisterndashbrother pairWe have followedthe fate of this population ever since (Grantet al 2001) There are now 30 to 40 breedingpairs on the island

Observations of a newly founded popu-lation go to the heart of the question of howbiodiversity generation begins Environ-mental change appears to have been a keyfactor in facilitating population establish-ment and subsequent exponential growthThe G magnirostris population experienceda genetic bottleneck (microsatellite allelicdiversity fell) and inbreeding depressionoccurred as shown by the relatively poorsurvival of the 1991 cohort Small additionalchanges were caused by natural selection onbeak morphology and probably by genetic

drift All of this is to be expected but some other featureswere surprising Immigration did not occur just once but repeatedly especially in the 1990s With one exception im-migrants that stayed to breed came not from the obvious andclosest potential source (Santa Cruz Island) but mainlyfrom one farther away (Santiago) as revealed by their micro-satellite DNA A major change took place in the frequency of song types in the population This change wasinitiated by a single male that bred for the first time in1991 In addition to this nongenetic culturally transmittedcontribution he introduced a total of 11 new alleles at the16 microsatellite loci surveyed

968 BioScience bull October 2003 Vol 53 No 10

Plenary

Figure 3 The intergradation of beak sizes and shapes illustrated with outlinesof the six species in the genus Geospiza 1ndash3 Geospiza magnirostris 4ndash7Geospiza conirostris 8ndash13 Geospiza fortis 14ndash15 Geospiza fuliginosa16ndash21 Geospiza difficilis 22ndash24 Geospiza scandens Illustration by Swarth(1931) from Abbott and colleagues (1977)

Thus while environmental change was the key factor thattriggered the founding of a new population some idiosyn-cratic genetic and nongenetic factors determined the fate de-velopment and composition of the population Even thoughone individual made a large contribution to the populationoverall changes were relatively small in magnitude for threereasons Selection pressures were weak the population did notremain small enough for random genetic drift to be effectiveand continuing immigration would have retarded diver-gence If the case of G magnirostris can be considered repre-sentative of how speciation begins we would have to concludethat it starts slowly with small steps

Speciation The endSpeciation is completed when two populations that have diverged in allopatry can coexist with little or no inter-breeding Medium ground finches and cactus finches occupy different ecological niches although their diets over-lap The ecological differences presumably permit coexistencein sympatry in an environment (eg Daphne Major) whosefood supply fluctuates in abundance and composition Toparaphrase David Lack (1947) the species are ecologically isolated through niche differences that evolved by natural selection in allopatry The differences may have been enhanced by selection in sympatry thereby reducing inter-specific competition for food But how do the species maintain coexistence without interbreeding What are the dif-ferences that keep them reproductively isolated and howdid the differences evolve

Members of the group of closely related ground finchspecies do not differ in plumage or courtship behavior butthey do differ in beak morphology and they differ conspic-uously in song (Grant 1999) These two sets of cues visual andvocal have been shown in separate field experiments to beused by finches in discriminating between their own and

other species (Ratcliffe and Grant 1983a 1983b 1985) Thuspart of the answer to the question of reproductive isolationis that it evolves as a consequence of adaptive evolution of beaksizes and shapes in allopatry The other part centered onsong is more complex

Song differences play a major role in keeping species apartLike beak differences song differences presumably arisethrough divergence in allopatry for reasons that are not en-tirely clear Song is an interesting trait because it is culturallyand not genetically inherited We know this from a few

October 2003 Vol 53 No 10 bull BioScience 969

Plenary

Figure 4 As the average beak depth of a population ofgranivorous Geospiza species increases so does the maxi-mum size and hardness of the seeds they can crack Basedon Schluter and Grant (1984)

Figure 5 Evolutionary change in beak depth in the popu-lation of Geospiza fortis on the island of Daphne MajorThe upper panel shows the distribution of beak depths inthe breeding population in 1976 with the survivors of the1977 drought that bred in 1978 indicated in black Thedifference between the means indicated by a caret is ameasure of the strength of natural selection The middleand lower panels show the distributions of beak depths offully grown offspring hatched in 1976 and 1978 respec-tively Evolutionary change between generations is mea-sured by the difference in mean between the 1976 popula-tion before selection and the birds hatched in 1978

Beak depth

Num

bersLog seed hardness

Log

beak

dep

th

experiments with captive birds (Bowman 1983) supple-mented by field observations of songs of offspring parentsand even grandparents (Grant and Grant 1989 1996) Onlymales sing an advertising song it is simple and is sung un-altered throughout life which may be as long as 16 years Mostsons sing the same song subtype as their fathers while a minority sing a different song subtype that is sung by othermale members of the same population Thus song is acquired through learning early in life in a process that resembles imprinting it is generally acquired from fathers during the period of parental dependence in associationwith parental morphology By their pairing patterns femalesgive evidence of learning song at the same time and from thesame sources

Rare exceptions to these rules provide additional valuableinformation on the role of learning and its bearing on thequestion of what keeps species apart Once again environ-mental change associated with an El Nintildeo event has pro-vided crucial information Medium ground finches and cactus finches hybridize rarely Before 1983 the hybrids diedwithout breeding at a time when most of the ldquopurerdquo speciesproduced in the same years also died without breeding TheEl Nintildeo event of 1983 resulting in an abundance of smallseeds altered the environment in a way that was favorable tothe survival of the hybrids The hybrids that were producedin 1983 backcrossed to medium ground finches in 1987 andothers that were produced in 1987 backcrossed to cactusfinches in 1991 The direction of backcrossing differed becausein 1983 the hybridizing male was a cactus finch that sang amedium ground finch song whereas in 1987 the hybridizingmales were cactus finches that sang cactus finch songsSons of all families sang the same song as their fathers anddaughters in each case mated with males that sang the samesong type as their fathers

Hybridization is sometimes the re-sult of heterospecific singing throughapparent misimprinting The causesof misimprinting and hybridizationare idiosyncratic and difficult to determine They include extra-pairmating interspecific takeover of nestswith eggs and dominant singing of aclose neighbor Ecologically the sig-nificant feature is a change in the environment that has facilitated theintrogression of genes F1 hybrid andbackcross survival is not intrinsicallylower than the survival of the parentalspecies and there is no sign of dimin-ished fitness when hybrids breed Infact in the 1990s and up to the presentthe flow of genes from the mediumground finch to the cactus finch population has contributed to a decrease in mean body size and ablunter beak morphology of cactus

finches (Grant and Grant 2002a) The barrier to gene exchangeerected by song differences has been breached and environ-mental change appears to have been the most important factor

To summarize the coexistence of finch species is facilitatedby divergence in beak morphology and song Beaks divergeunder natural selection but why songs diverge is less clear Cul-tural drift a process of random change in culturally trans-mitted (learned) traits is probably involved and sexual se-lection may be involved as well The end point of speciationis the complete absence of gene exchange Many if not all co-existing populations of Darwinrsquos finches have not quitereached that point although they function as species by re-maining distinct even in the face of occasional gene exchangeThis offers two important lessons First species diverge in matepreferences before genetic incompatibilities evolve Seconddifferent populations can function as biological species beforethey would be recognized as species solely on the basis of ge-netic distinctness

History The initial colonizationThe present is known the past is inferred To understand thepast of Darwinrsquos finches the first question that needs to be ad-dressed is when the radiation began because the answer setsthe boundary on relevant Galaacutepagos history In the absenceof fossils genes are our best source of information aboutthis history (Price et al 2000) The closest genetic relatives ofDarwinrsquos finches on the South American continent in Central America and in the Caribbean are a group of seed-eaters (Tiaris and relatives) allied to tanagers (Sato et al 1999Burns et al 2002) Darwinrsquos finches diverged from them in thelast 2 million or possibly 3 million years according to calcu-lations based on an assumed molecular clock applied to mitochondrial DNA and allozyme data (Grant 1999) The

970 BioScience bull October 2003 Vol 53 No 10

Plenary

Daphne Major a volcanic remnant in the Galaacutepagos archipelago is the site of theauthorsrsquo long-term study of evolution in Darwinrsquos finches Photograph David Parer

recent origin of Darwinrsquos finches helps to explain why theyare still capable of exchanging genes

Divergence from their mainland relatives began when thefinches colonized the Galaacutepagos islands Situated 900 kmfrom continental Ecuador on the Nazca plate and moving imperceptibly toward the mainland the archipelago is a re-mote place for birds to visit Colonization is an improbableevent Nevertheless according to one calculation ancestralDarwinrsquos finches arrived in a moderately large flock (or several small ones) Modern finches are genetically diverse atthe major histocompatibility complex locus and Vincek andcolleagues (1996) used the allelic diversity of class II genes to calculate that the original colonists numbered at least 30individuals

Improbable events may arise in improbable and hencerare circumstances What might those circumstances havebeen Any answer must be speculative even if rooted in current phenomena The circumstances that promote dispersalof contemporary finches within the Galaacutepagos archipelago are(a) high finch density following prolific breeding in El Nintildeoyears and (b) forest fires caused by volcanic eruptions If the

unusual dispersal activity from the mainland followed sim-ilar patterns it may have been induced by unusual volcanicactivity in the Andes Burning of the forests in one suchepisode would be followed by the establishment of large areas of shrub and secondary growth With the buildup offinch populations in secondary forest and another round offires and burning large numbers of finches and other birdsin coastal regions would fly out to sea to escape the flames andsmoke The colonists would be helped if mats of vegetationwere rafted out to sea by strong El Nintildeondashassociated floodingfrom the Guayas River Global temperatures were warmer 2million to 3 million years ago and permanent El Nintildeo con-ditions are thought to have occurred until about that time(Cane and Molnar 2001) The most marked shift in climateseems to have occurred at 24 million to 25 million years agoThis may be when the ancestral Darwinrsquos finches arrived

Relevant history of the GalaacutepagosTo understand the past the second question that needs to beaddressed is how the islands have changed if at all since thefirst finches arrived The simplest possible answer would be

October 2003 Vol 53 No 10 bull BioScience 971

Plenary

Figure 6 Changes in the beak size and shape of Geospiza fortis and Geospiza scandens on the islandof Daphne Major Mean trait values for each year are indicated by solid circles and 95 confidenceintervals are shown by vertical bars above and below the mean In the absence of change the meansshould remain within the 95 confidence intervals (horizontal broken lines) of the mean estimatesfrom the 1973 samples PC refers to principal component obtained from a principal componentsanalysis of size and shape variables From Grant and Grant (2002a)

PC2 b

eak

shap

ePC

1 b

eak

shap

e

that the islands have always been much as they are today interms of geography climate and vegetation If this is correctthe finchesrsquo adaptive radiation can be viewed as a process ofdifferentiation that results in the occupancy of all ecologicalniches present at the outsetmdashrather like filling empty boxesone species per box Indeed this is how early writers on thesubject viewed the radiation of the finches stressing the absence or scarcity of competitors in the boxes as a facilitat-ing factor (Huxley 1942 Simpson 1944 Lack 1947 Grant1999) In the modern version the boxes are replaced by adap-tive peaks in a more or less fixed landscape This view impliesthat diversification is rapid early in the radiation and thenslows down as ecological opportunities diminish Some radiations of other organisms elsewhere conform to this pattern (Schluter 2000) However taken at face value thephylogeny of Darwinrsquos finches shows exactly the oppositepattern a slow start followed by recent rapid diversification(figure 7) The species occupy adaptive peaks but the fixityof the ecological landscape that allowed them to do so isquestionable

In fact the islands and their inhabitants have changedradically Three million years ago there were far fewer islands than today perhaps only five (Grant and Grant 1998)The number of islands increased as a result of volcanic activitycentered on and near a hotspot beneath the western island of Fernandina Climate changed as well The average air

temperature declined but more important thanthis the worldrsquos climate underwent a sharp transi-tion 275 million years ago with the abrupt onset of glaciation (Cane and Molnar 2001) In the lastmillion years the climate has oscillated betweenglacial and interglacial conditions at about 100000-year intervals Global fluctuations in climate wereexperienced locally in the Galaacutepagos and elsewherein tropical America This has been revealed by theisotopic oxygen signatures of temperature in Andean ice cores (Seltzer et al 2002) by coral coresin Galaacutepagos (Dunbar et al 1994) and by pollencores in Galaacutepagos (Colinvaux 1972 1984) and incontinental South and Central American lakes(Bush et al 1992)

Most of the contemporary finches evolved inthe last million years so it is important to knowwhat happened during these cycles The two majoreffects of glacialndashinterglacial cycles were the de-pression of temperatures and of sea level relative to contemporary levels The last Ice Agecooling resulted in a drop of 3degC to 4degC in theequatorial Pacific reaching a minimum about21000 years ago (Kerr 2001) The previous deglacia-tion about 130000 years ago was associated witha drop of 2degC to 6degC (Tudhope et al 2001) Sea levelfell with the temperature The decline was gradualfrom the current level (about 120000 years ago) toabout 60 meters (m) lower (about 30000 yearsago) then an abrupt further decrease occurred to

about 125 m below the current level (Lambeck and Chappell2001) As a consequence islands were larger and distances between them were shorter Thus both temperature and sealevel were usually lower and never much higher than they aretoday

The food of finchesmdashplants and arthropods the latterfeeding on the plants and on each othermdashmust have beenaffected by these geophysical and climatic changes Firstnew species of plants and arthropods would have arrivedby immigration We do not know when this happened or which species were involved For Galaacutepagos unlikeHawaii (eg Givnish 1998 Wright et al 2000) there are nomolecular phylogenies of plants to help in reconstructingpaleofloras and the phylogenies of insects are too scarceto be useful (Finston and Peck 1997 Sequeira et al 2000)That situation needs to be rectified Second other speciesperhaps influenced by the immigrants would have become extinct Severe and extensive droughts would have been particularly crucial and cruel times for many organisms including finches Third the temperature- andmoisture-dependent altitudinal zonation of plants wouldhave shifted upward and downward at different timeshence the highest and lowest habitats would have beenmost vulnerable to elimination as noted elsewhere (Prodonet al 2002) Plant distributions would have changed acrossthe archipelago

972 BioScience bull October 2003 Vol 53 No 10

Plenary

Figure 7 The accumulation of species of Darwinrsquos finches with timeback-calculated from the estimated ages (in millions of years or MY) ofcontemporary species in the absence of known extinctions The accumu-lation of species parallels the accumulation of islands with time as de-termined from estimations of island age and elevation in relation to sealevel More islands provide more conditions for speciation to occur andspecies to persist From Grant (2001)

The evidence of a change in the upland forests is the rel-ative scarcity of endemic plants (Johnson and Raven 1973)The evidence of a change in the lowest zone is the anomalousoccurrence of plants on some islands with apparently un-suitable climates and soil For example the tree Erythrina velu-tina occurs at mid elevations on the high islands of Santa CruzSantiago and Isabela A single tree of this species occurs onthe low arid island of Genovesa and fewer than a dozen oc-cur on the low arid and even more remote island of WolfSimilarly a few Zanthoxylum fagara trees on Santa Cruz andSan Cristoacutebal occur close to the coast These may be theremnants of much larger populations on these islands undercooler wetter or less seasonally arid conditions than those thatprevail today Temperatures and precipitation changedmarkedly from one state to another long enough (gt 1000years Colinvaux 1972 Riedinger et al 2002) for vegetationzones to shift (Woodward 1987) On some occasions how-ever significant changes in temperature occurred in as shorta time as a hundred years perhaps less (Bush et al 1992)Large abrupt and widespread climate changes with majorconsequences for the biota have occurred repeatedly in thepast when the Earth system was forced across thresholds(Alley et al 2003)

The macroevolutionary pattern and the buildup ofcomplex communities from simple ones In view of the strong environmental changes in the archi-pelago it is scarcely likely that all current ecological niches wereavailable when the finchesrsquo ancestors arrived Rather thenumbers and types of opportunities for finch evolution increased as the number of islands increased and the climate and vegetation changed According to this view theadaptive radiation and the buildup of species-rich commu-nities were largely molded by environmental change theparticular species originated when they did and no earlierin response to particular environments prevailing then

When the first finches arrived on Galaacutepagos they mayhave encountered a climate and vegetation more like those ofmodern-day Cocos Island warmer wetter and more humidconditions fostering rain forest from the coast to the islandpeaks (Grant 1999 Grant and Grant 2002b) Cocos Island hastemperatures similar to those of the coastal habitats in theGalaacutepagos and rainfall equivalent to what the Galaacutepagosnow receives in an El Nintildeo year at high elevations Reason-ing from the evidence of modern finches we suggest the ini-tial evolutionary pathway taken by the finches was toward theexploitation of small arthropods and of nectar and pollenfrom small flowers in a rain forestndashlike environment

The radiation began when the initial species split into twolineages of Certhidea warbler finches (figure 8) after the ini-tial pathway had been taken One group of populations(Certhidea olivacea) inhabits moist upland forest and theother group (Certhidea fusca) occupies lower habitats onother mainly low islands Remarkably despite their longseparation the two groups have retained similar mate recog-nition systems and for that reason we refer to them as lineages

October 2003 Vol 53 No 10 bull BioScience 973

Plenary

Figure 8 Reconstruction of finch phylogeny based on microsatellite DNA Horizontal branch lengths are pro-portional to units of genetic distance (GST) as indicated bythe scale Numbers refer to percentage bootstrap supportfor the nodes by two methods Mean weights are given onthe right together with symbols of male plumage fullyblack partially black or brown or green Alternative reconstructions that use morphology allozymes or mito-chondrial DNA are similar differing in relatively smalldetails Species from top to bottom Geospiza fuliginosaGeospiza fortis Geospiza magnirostris Geospiza scandensGeospiza conirostris Geospiza difficilis Camarhynchusparvulus Camarhynchus psittacula Camarhynchus pauperCamarhynchus pallida Platyspiza crassirostris Certhideafusca Pinaroloxias inornata and Certhidea olivacea FromPetren and colleagues (1999)

and not species (Grant and Grant 2002b) Another remark-able feature is that they have remained relatively undifferen-tiated in morphology ecology and behavior This is not expected on the basis of the view that niches were varied plen-tiful and evolutionarily within reach at that time Howeverwe must acknowledge the possibility perhaps even the prob-ability that extinction has robbed us of other species that wereformed then The morphological similarity of these finchescontrasting with their distinctness from continental rela-tives argues for an early adaptation to an unusual niche

One of the warbler finch lineages gave rise to all otherfinch species Early products of the diversification were the veg-etarian finch (Platyspiza crassirostris) the Cocos finch(Pinaroloxias inornata) on either Galaacutepagos or Cocos Island(Grant and Grant 2002b) and the sharp-beaked groundfinch (G difficilis) The most recent products were a group ofground finch species (Geospiza) and a group of tree finchspecies (Camarhynchus and Cactospiza) (figure 8)

Effects of environmental change have left a different his-torical imprint on the older species Populations of G diffi-cilis differ strongly in morphology and ecology to a degree un-matched by all other and younger species in the genusGeospiza and by the warbler finches that preceded themSome G difficilis have persisted in Zanthoxylum forest at midand upper elevations which we believe to be old and others have entered arid lowland habitat perhaps when theZanthoxylum forest gradually disappeared from low islandsas the climate changed This may have been the first step ofthe radiation of ground finches In contrast to the G difficilispopulations populations of the vegetarian finch are mor-phologically and ecologically very similar Limited genetic data(Petren et al 1999) suggest that they separated from each otherrecently This is surprising as it is not expected from the ageof the species or from the presumed stability of its mid-elevation transition zone habitat The vegetarian finch mayhave become restricted to one or two islands and other pop-ulations or even related species may have become extinctin response to one of the recent extreme fluctuations in climate Its vegetarian diet may have made it vulnerable intimes of drought and competition with other species may havebeen an additional factor

The importance of environmental change in speciation isfurther suggested by the fact that in the last million years newspecies evolved in the habitats most vulnerable to changeGeospiza were added to lowland habitats and Camarhynchuswere added to the upland humid forest The change in climatetoward seasonal aridity and the development of arid lowlandhabitat provided the opportunity for a new granivorous wayof finch life now adopted by Geospiza species Some of thesemodern species may have contributed to the extinction ofolder ones through competitive superiority in a changingenvironment This is one possible interpretation of the contrast between the morphological distinctness of the threeolder groups Certhidea Platyspiza and G difficilis and themorphological similarity of species in the younger generaCamarhynchus Cactospiza and Geospiza

These ideas on speciation and extinction together with ob-servations of the colonization of Daphne Major by G magni-rostris (Grant et al 2001) suggest that periods of expansionsuch as the one in progress are preceded and followed by periods of range contraction and extinction caused by envi-ronmental change Distributions of habitats sea level islandand population sizes and degrees of isolation provide favorable conditions for divergence of small populations inisolation at some times and for dispersal mixing establish-ment of sympatry and hybridization at others The buildupof complex communities from simple ones is not smooth con-tinuous and regular but a process of gains and losses with anet accumulation of species over the long term

ConclusionsAccording to the standard allopatric model speciation beginswith the establishment of a new population continues withthe divergence of that population from its parent populationand is completed when members of two diverged populationscan coexist in sympatry without interbreeding We stand a virtually negligible chance of observing the whole process under natural circumstances Nevertheless it is possible tomake relevant observations in nature of all steps in theprocess We have described the strong role played by envi-ronmental change at each of the three steps in the speciationof Darwinrsquos finches The full adaptive radiation was pro-duced by a repetition of these steps each with a different product under somewhat different circumstances The challenge now is to account for the differences in terms of pastenvironments without the help of fossils of finches or ofother members of the biota We have sketched a frameworkfor doing this by using molecular genetic information to estimate the finch phylogeny and using geological and climaticinformation to reconstruct Galaacutepagos environments in thepast 2 million to 3 million years A better understanding ofenvironmental change on this time scale will help to explainwhy 14 species were formed what their sequence of origin wasand why they evolved their particular unique features Theremay be more history to uncover in finch DNA if only we canwork out how to read it

Acknowledgments We thank Ken Petren for figure 8 and Phil Hedrick FritzTrillmich and an anonymous reviewer for comments on themanuscript We are grateful to the Galaacutepagos National Parkand the Charles Darwin Research Station for permission andlogistical support for the fieldwork and to the National Sciences and Engineering Research Council of Canada and theNational Science Foundation for funding support

References citedAbbott I Abbott LK Grant PR 1977 Comparative ecology of Galaacutepagos

ground finches (Geospiza Gould) Evaluation of the importance of floris-tic diversity and interspecific competition Ecological Monographs 47151ndash184

Alley RB et al 2003 Abrupt climate change Science 299 2005ndash2010

974 BioScience bull October 2003 Vol 53 No 10

Plenary

Bowman RI 1961 Morphological Differentiation and Adaptation in theGalaacutepagos Finches University of California Publications in ZoologyVol 58 Berkeley University of California Press

mdashmdashmdash 1983 The songs of Darwinrsquos finches Pages 237ndash537 in Bowman RILeviton AE Berson M eds Galaacutepagos Organisms San Francisco Amer-ican Association for the Advancement of Science Pacific Division

Burns KJ Hackett SJ Klein NK 2002 Phylogenetic relationships andmorphological diversity in Darwinrsquos finches and their relatives Evo-lution 56 1240ndash1252

Bush MB Piperno DR Colinvaux PA DeOleveira PE Krissek LA Miller MCRowe WE 1992 A 14300-yr paleoecological profile of a lowland tropi-cal lake in Panama Ecological Monographs 62 251ndash275

Cane MA Molnar P 2001 Closing of the Indonesian seaway as a precursorto east African aridification around 3ndash4 million years ago Nature 411157ndash162

Colinvaux PA 1972 Climate and the Galaacutepagos Islands Nature 240 17ndash20mdashmdashmdash 1984 The Galaacutepagos climate Present and past Pages 55ndash69 in

Perry R ed Galaacutepagos Oxford (United Kingdom) Pergamon PressDarwin CR 1842 Journal of Researches into the Geology and Natural

History of the Various Countries Visited during the Voyage of H M SBeagle under the Command of Captain FitzRoy RN from 1832 to 1836London Henry Colburn

Dunbar RB Wellington GM Colgan MW Glynn PW 1994 Eastern Pacificsea surface temperature since 1600 AD The O18 record of climate vari-ability in Galaacutepagos corals Paleoceanography 9 291ndash315

Finston TL Peck SB 1997 Genetic differentiation and speciation in Stomion(Coleoptera Tenebrionidae) Flightless beetles of the Galaacutepagos IslandsEcuador Biological Journal of the Linnean Society 61 243ndash266

Givnish TJ 1998Adaptive plant evolution on islands Classical patterns mole-cular data new insights Pages 281ndash304 in Grant PR ed Evolution on Islands Oxford (United Kingdom) Oxford University Press

Grant BR Grant PR 1989 Evolutionary Dynamics of a Natural PopulationThe Large Cactus Finch of the Galaacutepagos Chicago University of ChicagoPress

mdashmdashmdash 1996 Cultural inheritance of song and its role in the evolution ofDarwinrsquos finches Evolution 50 2471ndash2487

Grant PR 1999 Ecology and Evolution of Darwinrsquos Finches Princeton (NJ)Princeton University Press

mdashmdashmdash 2001 Reconstructing the evolution of birds on islands 100 years ofresearch Oikos 92 385ndash403

Grant PR Grant BR 1998 Speciation and hybridization in island birds Pages142ndash162 in Grant PR ed Evolution on Islands Oxford (United Kingdom)Oxford University Press

mdashmdashmdash 2002a Unpredictable evolution in a 30-year study of Darwinrsquosfinches Science 296 707ndash711

mdashmdashmdash 2002b Adaptive radiation of Darwinrsquos finches American Scientist90 131ndash139

Grant PR Grant BR Petren K 2001 The founding of a new population by a single pair of individuals Establishment selection and populationexpansion Genetica 112113 359ndash382

Huxley JS 1942 Evolution The Modern Synthesis London Allen and Unwin

Johnson MP Raven PH 1973 Species number and endemism The Galaacutepagosarchipelago revisited Science 179 893ndash895

Keller LF Grant PR Grant BR Petren K 2001 Heritability of morphologi-cal traits in Darwinrsquos finches Misidentified paternity and maternal effects Heredity 87 325ndash336

Kerr RA 2001 The tropics return to the climate system Science 292 660ndash661Lack D 1947 Darwinrsquos finches Cambridge (United Kingdom) Cambridge

University PressLambeck K Chappell J 2001 Sea level change through the last glacial cycle

Science 292 679ndash686Mayr E 1942 Systematics and the Origin of Species New York Columbia

University Press

Newton I 1967 The adaptive variation and feeding ecology of some British

finches Ibis 109 33ndash98

Petren K Grant BR Grant PR 1999 A phylogeny of Darwinrsquos finches based

on microsatellite DNA length variation Proceedings of the Royal Soci-

ety of London B 266 321ndash329

Price T Lovette IJ Bermingham E Gibbs HL Richman AD 2000 The

imprint of history on communities of North American and Asian

warblers American Naturalist 156 354ndash367

Prodon R Thibault J-C Dejaifve P-A 2002 Expansion vs compression of

bird altitudinal ranges on a Mediterranean island Ecology 83 1294ndash1306

Ratcliffe LM Grant PR 1983a Species recognition in Darwinrsquos finches

(Geospiza Gould) I Discrimination by morphological cues Animal

Behaviour 31 1139ndash1153

mdashmdashmdash 1983b Species recognition in Darwinrsquos finches (Geospiza Gould)

II Geographic variation in mate preference Animal Behaviour 31

1154ndash1165

mdashmdashmdash 1985 Species recognition in Darwinrsquos finches (Geospiza Gould) III

Male responses to playback of different song types dialects and hetero-

specific songs Animal Behaviour 33 290ndash307

Richards OW 1948 Species formation in islands (review of Darwinrsquos Finches

by Lack D) Journal of Animal Ecology 17 83ndash84

Riedinger MA Steinitz-Kannan M Last WM Brenner M 2002 A ~6100 14C

yr record of El Nintildeo activity from the Galaacutepagos Islands Journal of

Paleontology 27 1ndash7

Sato A OrsquoHuigin C Figueroa F Grant PR Grant BR Tichy H Klein J 1999

Phylogeny of Darwinrsquos finches as revealed by mtDNA sequences

Proceedings of the National Academy of Sciences 96 5101ndash5106

Schluter D 2000 The Ecology of Adaptive Radiations Oxford (United King-

dom) Oxford University Press

Schluter D Grant PR 1984 Determinants of morphological patterns in

communities of Darwinrsquos finches American Naturalist 123 175ndash196

Seltzer GO Rodbell DT Baker PA Fritz SC Tapia PM Rowe HD Dunbar

RB 2002 Early warming of tropical South America at the last glacialndash

interglacial transition Science 296 1685ndash1686

Sequeira AS Lanteri AA Scataglini MA Confalonieri VA Farrell BD 2000

Are flightless Galapaganus weevils older than the Galaacutepagos Islands they

inhabit Heredity 85 20ndash29

Simpson GG 1944 Tempo and Mode in Evolution New York Columbia

University Press

Swarth HS 1931 The avifauna of the Galaacutepagos islands Occasional Papers

of the California Academy of Sciences 18 1ndash299

mdashmdashmdash 1934 The bird fauna of the Galaacutepagos islands in relation to species

formation Biological Reviews 9 213ndash234

Tudhope AW Chilcott CP McCulloch MT Cook ER Chappell J Ellam RM

Lea DW Lough JM Shimmield GB 2001 Variability in the El

NintildeondashSouthern Oscillation through a glacialndashinterglacial cycle Science

291 1511ndash1517

Vincek V OrsquoHuigin C Satta Y Takahata N Boag PT Grant PR Grant BR

Klein J 1996 How large was the founding population of Darwinrsquos

finches Proceedings of the Royal Society of London B 264 111ndash118

Woodward FI 1987 Climate and Plant Distribution London Cambridge Uni-

versity Press

Wright SD Young CG Dawson JW Whittaker DJ Gardner RC 2000

Riding the ice age El Nintildeo Pacific biogeography and evolution of

Metrosideros subg Metrosideros (Myrtaceae) inferred from nuclear

ribosomal DNA Proceedings of the National Academy of Sciences 97

4110ndash4123

October 2003 Vol 53 No 10 bull BioScience 975

Plenary

to detect selection We found pronounced heritable variationin beak size and body size within populations of the mediumground finch (Geospiza fortis) and the cactus finch (Geospizascandens) We also found that when the environment changessome of the variants in each population survive while othersdie This amounts to a vindication of David Lackrsquos views onadaptation

Birds with small beaks and small body size suffered selec-tive mortality in 1977 during a severe drought (figure 5) Thelarger members of the medium ground finch populationsurvived on a diet of large hard seeds which increasingly dominated the food supply as a result of an initial preferen-tial consumption of small seeds Smaller birds lacking the mechanical power to crack the large seeds of Tribulus cistoidesand Opuntia echios died at a higher rate than large birdsAn evolutionary response to directional natural selectionfollowed in the next generation (figure 5) because beak sizevariation is highly heritable (Keller et al 2001)

Natural selection in the opposite direction with smallbirds surviving disproportionately occurred 8 years laterThe island experienced a major prolonged El Nintildeo eventfrom November 1982 to August 1983 The abundant rain andhigh temperatures transformed the vegetation and food sup-ply of the finches and they bred for 8 months as opposed tothe usual 1 or 2 monthsVines and other plants multiplied and

spread smothering the low-growing Tribulus plants and Opuntia cactus bushes The seed supply became dominatedby small seeds and seeds of Tribulus and Opuntia becamescarce When the island entered the next drying-out episodeduring the drought of 1985 the supply of seeds fell and sodid the numbers of finches from high points in the produc-tive years of 1983 and 1984 Large birds died at the highest ratehence the medium ground finches that were small with rel-atively pointed beaks were selectively favored

Thus selection oscillates in directionWe have observed thisrepeatedly over the full 30-year period (Grant and Grant2002a) As a consequence neither the medium ground finchnor the cactus finch has remained morphologically constantor static In fact the mean body size and beak shape of the twospecies are not the same now as they were at the beginningof the study (figure 6) In an environment subject to climaticand floristic change the finches have changed (evolved) Wehave directly observed the sort of adaptive change that isnormally only inferred from a comparison of related popu-lations differing in mean morphology

Summarizing this study has taught us four things aboutnatural selection

bull It is an observable interpretable and repeatable processin a natural environment

October 2003 Vol 53 No 10 bull BioScience 967

Plenary

Figure 1 Four points of the Darwinrsquos finch compass Species with contrastingmorphology (Certhidea olivacea Geospiza difficilis Geospiza magnirostris andPlatyspiza crassirostris) show the range of sizes and shapes in beaks from smallto large and from blunt to pointed Photographs B Rosemary Grant and PeterR Grant

Figure 2 Three recently evolvedspecies of Darwinrsquos finches (Geospizafuliginosa Geospiza fortis andGeospiza magnirostris) differ principally in size but also in beakshape Photographs B Rosemary Grant and Peter R Grant

bull It oscillates in direction

bull It happens when the environment changes

bull It has evolutionary consequences (adaptive change)

Almost 100 years after Darwinrsquos visit to the Galaacutepagos asystematist Harry Swarth came close to suggesting that evo-lution was not over and done with but could actually be witnessed when he wrote that ldquothe extraordinary variantsthat crop up in a series [of museum specimens] give an im-pression of change and experiment going onrdquo(Swarth 1934)Based on the evidence of Darwinrsquos finches evolutionarychanges are indeed going on

Speciation The beginningSpeciation begins with the divergence of apopulation and is completed when two pop-ulations that have diverged on different islandsestablish coexistence with little or no inter-breeding (Mayr 1942 Grant 2001) We obtained insight into the initial process ofdivergence on Daphne Major thanks to ahighly fortuitous circumstance the foundingof a new population

The large ground finch (Geospiza magni-rostris) became a breeding member of thecommunity in late 1982 when two femalesand three males began to breed In precedingyears we had observed immigrant membersof this species on the island in the dry seasonbut when the rains began they disappearedpresumably returning to their island oforigin to breed Not so in El Nintildeo The breed-ing birds produced 17 fledglings in 1982ndash1983 but only one of the breeding pairs produced the next generation A daughterbred at different times with two brothersone of which can be ignored because the offspring did not survive to breed Thus thepopulation was effectively founded by a single pair and the next generation com-prised a sisterndashbrother pairWe have followedthe fate of this population ever since (Grantet al 2001) There are now 30 to 40 breedingpairs on the island

Observations of a newly founded popu-lation go to the heart of the question of howbiodiversity generation begins Environ-mental change appears to have been a keyfactor in facilitating population establish-ment and subsequent exponential growthThe G magnirostris population experienceda genetic bottleneck (microsatellite allelicdiversity fell) and inbreeding depressionoccurred as shown by the relatively poorsurvival of the 1991 cohort Small additionalchanges were caused by natural selection onbeak morphology and probably by genetic

drift All of this is to be expected but some other featureswere surprising Immigration did not occur just once but repeatedly especially in the 1990s With one exception im-migrants that stayed to breed came not from the obvious andclosest potential source (Santa Cruz Island) but mainlyfrom one farther away (Santiago) as revealed by their micro-satellite DNA A major change took place in the frequency of song types in the population This change wasinitiated by a single male that bred for the first time in1991 In addition to this nongenetic culturally transmittedcontribution he introduced a total of 11 new alleles at the16 microsatellite loci surveyed

968 BioScience bull October 2003 Vol 53 No 10

Plenary

Figure 3 The intergradation of beak sizes and shapes illustrated with outlinesof the six species in the genus Geospiza 1ndash3 Geospiza magnirostris 4ndash7Geospiza conirostris 8ndash13 Geospiza fortis 14ndash15 Geospiza fuliginosa16ndash21 Geospiza difficilis 22ndash24 Geospiza scandens Illustration by Swarth(1931) from Abbott and colleagues (1977)

Thus while environmental change was the key factor thattriggered the founding of a new population some idiosyn-cratic genetic and nongenetic factors determined the fate de-velopment and composition of the population Even thoughone individual made a large contribution to the populationoverall changes were relatively small in magnitude for threereasons Selection pressures were weak the population did notremain small enough for random genetic drift to be effectiveand continuing immigration would have retarded diver-gence If the case of G magnirostris can be considered repre-sentative of how speciation begins we would have to concludethat it starts slowly with small steps

Speciation The endSpeciation is completed when two populations that have diverged in allopatry can coexist with little or no inter-breeding Medium ground finches and cactus finches occupy different ecological niches although their diets over-lap The ecological differences presumably permit coexistencein sympatry in an environment (eg Daphne Major) whosefood supply fluctuates in abundance and composition Toparaphrase David Lack (1947) the species are ecologically isolated through niche differences that evolved by natural selection in allopatry The differences may have been enhanced by selection in sympatry thereby reducing inter-specific competition for food But how do the species maintain coexistence without interbreeding What are the dif-ferences that keep them reproductively isolated and howdid the differences evolve

Members of the group of closely related ground finchspecies do not differ in plumage or courtship behavior butthey do differ in beak morphology and they differ conspic-uously in song (Grant 1999) These two sets of cues visual andvocal have been shown in separate field experiments to beused by finches in discriminating between their own and

other species (Ratcliffe and Grant 1983a 1983b 1985) Thuspart of the answer to the question of reproductive isolationis that it evolves as a consequence of adaptive evolution of beaksizes and shapes in allopatry The other part centered onsong is more complex

Song differences play a major role in keeping species apartLike beak differences song differences presumably arisethrough divergence in allopatry for reasons that are not en-tirely clear Song is an interesting trait because it is culturallyand not genetically inherited We know this from a few

October 2003 Vol 53 No 10 bull BioScience 969

Plenary

Figure 4 As the average beak depth of a population ofgranivorous Geospiza species increases so does the maxi-mum size and hardness of the seeds they can crack Basedon Schluter and Grant (1984)

Figure 5 Evolutionary change in beak depth in the popu-lation of Geospiza fortis on the island of Daphne MajorThe upper panel shows the distribution of beak depths inthe breeding population in 1976 with the survivors of the1977 drought that bred in 1978 indicated in black Thedifference between the means indicated by a caret is ameasure of the strength of natural selection The middleand lower panels show the distributions of beak depths offully grown offspring hatched in 1976 and 1978 respec-tively Evolutionary change between generations is mea-sured by the difference in mean between the 1976 popula-tion before selection and the birds hatched in 1978

Beak depth

Num

bersLog seed hardness

Log

beak

dep

th

experiments with captive birds (Bowman 1983) supple-mented by field observations of songs of offspring parentsand even grandparents (Grant and Grant 1989 1996) Onlymales sing an advertising song it is simple and is sung un-altered throughout life which may be as long as 16 years Mostsons sing the same song subtype as their fathers while a minority sing a different song subtype that is sung by othermale members of the same population Thus song is acquired through learning early in life in a process that resembles imprinting it is generally acquired from fathers during the period of parental dependence in associationwith parental morphology By their pairing patterns femalesgive evidence of learning song at the same time and from thesame sources

Rare exceptions to these rules provide additional valuableinformation on the role of learning and its bearing on thequestion of what keeps species apart Once again environ-mental change associated with an El Nintildeo event has pro-vided crucial information Medium ground finches and cactus finches hybridize rarely Before 1983 the hybrids diedwithout breeding at a time when most of the ldquopurerdquo speciesproduced in the same years also died without breeding TheEl Nintildeo event of 1983 resulting in an abundance of smallseeds altered the environment in a way that was favorable tothe survival of the hybrids The hybrids that were producedin 1983 backcrossed to medium ground finches in 1987 andothers that were produced in 1987 backcrossed to cactusfinches in 1991 The direction of backcrossing differed becausein 1983 the hybridizing male was a cactus finch that sang amedium ground finch song whereas in 1987 the hybridizingmales were cactus finches that sang cactus finch songsSons of all families sang the same song as their fathers anddaughters in each case mated with males that sang the samesong type as their fathers

Hybridization is sometimes the re-sult of heterospecific singing throughapparent misimprinting The causesof misimprinting and hybridizationare idiosyncratic and difficult to determine They include extra-pairmating interspecific takeover of nestswith eggs and dominant singing of aclose neighbor Ecologically the sig-nificant feature is a change in the environment that has facilitated theintrogression of genes F1 hybrid andbackcross survival is not intrinsicallylower than the survival of the parentalspecies and there is no sign of dimin-ished fitness when hybrids breed Infact in the 1990s and up to the presentthe flow of genes from the mediumground finch to the cactus finch population has contributed to a decrease in mean body size and ablunter beak morphology of cactus

finches (Grant and Grant 2002a) The barrier to gene exchangeerected by song differences has been breached and environ-mental change appears to have been the most important factor

To summarize the coexistence of finch species is facilitatedby divergence in beak morphology and song Beaks divergeunder natural selection but why songs diverge is less clear Cul-tural drift a process of random change in culturally trans-mitted (learned) traits is probably involved and sexual se-lection may be involved as well The end point of speciationis the complete absence of gene exchange Many if not all co-existing populations of Darwinrsquos finches have not quitereached that point although they function as species by re-maining distinct even in the face of occasional gene exchangeThis offers two important lessons First species diverge in matepreferences before genetic incompatibilities evolve Seconddifferent populations can function as biological species beforethey would be recognized as species solely on the basis of ge-netic distinctness

History The initial colonizationThe present is known the past is inferred To understand thepast of Darwinrsquos finches the first question that needs to be ad-dressed is when the radiation began because the answer setsthe boundary on relevant Galaacutepagos history In the absenceof fossils genes are our best source of information aboutthis history (Price et al 2000) The closest genetic relatives ofDarwinrsquos finches on the South American continent in Central America and in the Caribbean are a group of seed-eaters (Tiaris and relatives) allied to tanagers (Sato et al 1999Burns et al 2002) Darwinrsquos finches diverged from them in thelast 2 million or possibly 3 million years according to calcu-lations based on an assumed molecular clock applied to mitochondrial DNA and allozyme data (Grant 1999) The

970 BioScience bull October 2003 Vol 53 No 10

Plenary

Daphne Major a volcanic remnant in the Galaacutepagos archipelago is the site of theauthorsrsquo long-term study of evolution in Darwinrsquos finches Photograph David Parer

recent origin of Darwinrsquos finches helps to explain why theyare still capable of exchanging genes

Divergence from their mainland relatives began when thefinches colonized the Galaacutepagos islands Situated 900 kmfrom continental Ecuador on the Nazca plate and moving imperceptibly toward the mainland the archipelago is a re-mote place for birds to visit Colonization is an improbableevent Nevertheless according to one calculation ancestralDarwinrsquos finches arrived in a moderately large flock (or several small ones) Modern finches are genetically diverse atthe major histocompatibility complex locus and Vincek andcolleagues (1996) used the allelic diversity of class II genes to calculate that the original colonists numbered at least 30individuals

Improbable events may arise in improbable and hencerare circumstances What might those circumstances havebeen Any answer must be speculative even if rooted in current phenomena The circumstances that promote dispersalof contemporary finches within the Galaacutepagos archipelago are(a) high finch density following prolific breeding in El Nintildeoyears and (b) forest fires caused by volcanic eruptions If the

unusual dispersal activity from the mainland followed sim-ilar patterns it may have been induced by unusual volcanicactivity in the Andes Burning of the forests in one suchepisode would be followed by the establishment of large areas of shrub and secondary growth With the buildup offinch populations in secondary forest and another round offires and burning large numbers of finches and other birdsin coastal regions would fly out to sea to escape the flames andsmoke The colonists would be helped if mats of vegetationwere rafted out to sea by strong El Nintildeondashassociated floodingfrom the Guayas River Global temperatures were warmer 2million to 3 million years ago and permanent El Nintildeo con-ditions are thought to have occurred until about that time(Cane and Molnar 2001) The most marked shift in climateseems to have occurred at 24 million to 25 million years agoThis may be when the ancestral Darwinrsquos finches arrived

Relevant history of the GalaacutepagosTo understand the past the second question that needs to beaddressed is how the islands have changed if at all since thefirst finches arrived The simplest possible answer would be

October 2003 Vol 53 No 10 bull BioScience 971

Plenary

Figure 6 Changes in the beak size and shape of Geospiza fortis and Geospiza scandens on the islandof Daphne Major Mean trait values for each year are indicated by solid circles and 95 confidenceintervals are shown by vertical bars above and below the mean In the absence of change the meansshould remain within the 95 confidence intervals (horizontal broken lines) of the mean estimatesfrom the 1973 samples PC refers to principal component obtained from a principal componentsanalysis of size and shape variables From Grant and Grant (2002a)

PC2 b

eak

shap

ePC

1 b

eak

shap

e

that the islands have always been much as they are today interms of geography climate and vegetation If this is correctthe finchesrsquo adaptive radiation can be viewed as a process ofdifferentiation that results in the occupancy of all ecologicalniches present at the outsetmdashrather like filling empty boxesone species per box Indeed this is how early writers on thesubject viewed the radiation of the finches stressing the absence or scarcity of competitors in the boxes as a facilitat-ing factor (Huxley 1942 Simpson 1944 Lack 1947 Grant1999) In the modern version the boxes are replaced by adap-tive peaks in a more or less fixed landscape This view impliesthat diversification is rapid early in the radiation and thenslows down as ecological opportunities diminish Some radiations of other organisms elsewhere conform to this pattern (Schluter 2000) However taken at face value thephylogeny of Darwinrsquos finches shows exactly the oppositepattern a slow start followed by recent rapid diversification(figure 7) The species occupy adaptive peaks but the fixityof the ecological landscape that allowed them to do so isquestionable

In fact the islands and their inhabitants have changedradically Three million years ago there were far fewer islands than today perhaps only five (Grant and Grant 1998)The number of islands increased as a result of volcanic activitycentered on and near a hotspot beneath the western island of Fernandina Climate changed as well The average air

temperature declined but more important thanthis the worldrsquos climate underwent a sharp transi-tion 275 million years ago with the abrupt onset of glaciation (Cane and Molnar 2001) In the lastmillion years the climate has oscillated betweenglacial and interglacial conditions at about 100000-year intervals Global fluctuations in climate wereexperienced locally in the Galaacutepagos and elsewherein tropical America This has been revealed by theisotopic oxygen signatures of temperature in Andean ice cores (Seltzer et al 2002) by coral coresin Galaacutepagos (Dunbar et al 1994) and by pollencores in Galaacutepagos (Colinvaux 1972 1984) and incontinental South and Central American lakes(Bush et al 1992)

Most of the contemporary finches evolved inthe last million years so it is important to knowwhat happened during these cycles The two majoreffects of glacialndashinterglacial cycles were the de-pression of temperatures and of sea level relative to contemporary levels The last Ice Agecooling resulted in a drop of 3degC to 4degC in theequatorial Pacific reaching a minimum about21000 years ago (Kerr 2001) The previous deglacia-tion about 130000 years ago was associated witha drop of 2degC to 6degC (Tudhope et al 2001) Sea levelfell with the temperature The decline was gradualfrom the current level (about 120000 years ago) toabout 60 meters (m) lower (about 30000 yearsago) then an abrupt further decrease occurred to

about 125 m below the current level (Lambeck and Chappell2001) As a consequence islands were larger and distances between them were shorter Thus both temperature and sealevel were usually lower and never much higher than they aretoday

The food of finchesmdashplants and arthropods the latterfeeding on the plants and on each othermdashmust have beenaffected by these geophysical and climatic changes Firstnew species of plants and arthropods would have arrivedby immigration We do not know when this happened or which species were involved For Galaacutepagos unlikeHawaii (eg Givnish 1998 Wright et al 2000) there are nomolecular phylogenies of plants to help in reconstructingpaleofloras and the phylogenies of insects are too scarceto be useful (Finston and Peck 1997 Sequeira et al 2000)That situation needs to be rectified Second other speciesperhaps influenced by the immigrants would have become extinct Severe and extensive droughts would have been particularly crucial and cruel times for many organisms including finches Third the temperature- andmoisture-dependent altitudinal zonation of plants wouldhave shifted upward and downward at different timeshence the highest and lowest habitats would have beenmost vulnerable to elimination as noted elsewhere (Prodonet al 2002) Plant distributions would have changed acrossthe archipelago

972 BioScience bull October 2003 Vol 53 No 10

Plenary

Figure 7 The accumulation of species of Darwinrsquos finches with timeback-calculated from the estimated ages (in millions of years or MY) ofcontemporary species in the absence of known extinctions The accumu-lation of species parallels the accumulation of islands with time as de-termined from estimations of island age and elevation in relation to sealevel More islands provide more conditions for speciation to occur andspecies to persist From Grant (2001)

The evidence of a change in the upland forests is the rel-ative scarcity of endemic plants (Johnson and Raven 1973)The evidence of a change in the lowest zone is the anomalousoccurrence of plants on some islands with apparently un-suitable climates and soil For example the tree Erythrina velu-tina occurs at mid elevations on the high islands of Santa CruzSantiago and Isabela A single tree of this species occurs onthe low arid island of Genovesa and fewer than a dozen oc-cur on the low arid and even more remote island of WolfSimilarly a few Zanthoxylum fagara trees on Santa Cruz andSan Cristoacutebal occur close to the coast These may be theremnants of much larger populations on these islands undercooler wetter or less seasonally arid conditions than those thatprevail today Temperatures and precipitation changedmarkedly from one state to another long enough (gt 1000years Colinvaux 1972 Riedinger et al 2002) for vegetationzones to shift (Woodward 1987) On some occasions how-ever significant changes in temperature occurred in as shorta time as a hundred years perhaps less (Bush et al 1992)Large abrupt and widespread climate changes with majorconsequences for the biota have occurred repeatedly in thepast when the Earth system was forced across thresholds(Alley et al 2003)

The macroevolutionary pattern and the buildup ofcomplex communities from simple ones In view of the strong environmental changes in the archi-pelago it is scarcely likely that all current ecological niches wereavailable when the finchesrsquo ancestors arrived Rather thenumbers and types of opportunities for finch evolution increased as the number of islands increased and the climate and vegetation changed According to this view theadaptive radiation and the buildup of species-rich commu-nities were largely molded by environmental change theparticular species originated when they did and no earlierin response to particular environments prevailing then

When the first finches arrived on Galaacutepagos they mayhave encountered a climate and vegetation more like those ofmodern-day Cocos Island warmer wetter and more humidconditions fostering rain forest from the coast to the islandpeaks (Grant 1999 Grant and Grant 2002b) Cocos Island hastemperatures similar to those of the coastal habitats in theGalaacutepagos and rainfall equivalent to what the Galaacutepagosnow receives in an El Nintildeo year at high elevations Reason-ing from the evidence of modern finches we suggest the ini-tial evolutionary pathway taken by the finches was toward theexploitation of small arthropods and of nectar and pollenfrom small flowers in a rain forestndashlike environment

The radiation began when the initial species split into twolineages of Certhidea warbler finches (figure 8) after the ini-tial pathway had been taken One group of populations(Certhidea olivacea) inhabits moist upland forest and theother group (Certhidea fusca) occupies lower habitats onother mainly low islands Remarkably despite their longseparation the two groups have retained similar mate recog-nition systems and for that reason we refer to them as lineages

October 2003 Vol 53 No 10 bull BioScience 973

Plenary

Figure 8 Reconstruction of finch phylogeny based on microsatellite DNA Horizontal branch lengths are pro-portional to units of genetic distance (GST) as indicated bythe scale Numbers refer to percentage bootstrap supportfor the nodes by two methods Mean weights are given onthe right together with symbols of male plumage fullyblack partially black or brown or green Alternative reconstructions that use morphology allozymes or mito-chondrial DNA are similar differing in relatively smalldetails Species from top to bottom Geospiza fuliginosaGeospiza fortis Geospiza magnirostris Geospiza scandensGeospiza conirostris Geospiza difficilis Camarhynchusparvulus Camarhynchus psittacula Camarhynchus pauperCamarhynchus pallida Platyspiza crassirostris Certhideafusca Pinaroloxias inornata and Certhidea olivacea FromPetren and colleagues (1999)

and not species (Grant and Grant 2002b) Another remark-able feature is that they have remained relatively undifferen-tiated in morphology ecology and behavior This is not expected on the basis of the view that niches were varied plen-tiful and evolutionarily within reach at that time Howeverwe must acknowledge the possibility perhaps even the prob-ability that extinction has robbed us of other species that wereformed then The morphological similarity of these finchescontrasting with their distinctness from continental rela-tives argues for an early adaptation to an unusual niche

One of the warbler finch lineages gave rise to all otherfinch species Early products of the diversification were the veg-etarian finch (Platyspiza crassirostris) the Cocos finch(Pinaroloxias inornata) on either Galaacutepagos or Cocos Island(Grant and Grant 2002b) and the sharp-beaked groundfinch (G difficilis) The most recent products were a group ofground finch species (Geospiza) and a group of tree finchspecies (Camarhynchus and Cactospiza) (figure 8)

Effects of environmental change have left a different his-torical imprint on the older species Populations of G diffi-cilis differ strongly in morphology and ecology to a degree un-matched by all other and younger species in the genusGeospiza and by the warbler finches that preceded themSome G difficilis have persisted in Zanthoxylum forest at midand upper elevations which we believe to be old and others have entered arid lowland habitat perhaps when theZanthoxylum forest gradually disappeared from low islandsas the climate changed This may have been the first step ofthe radiation of ground finches In contrast to the G difficilispopulations populations of the vegetarian finch are mor-phologically and ecologically very similar Limited genetic data(Petren et al 1999) suggest that they separated from each otherrecently This is surprising as it is not expected from the ageof the species or from the presumed stability of its mid-elevation transition zone habitat The vegetarian finch mayhave become restricted to one or two islands and other pop-ulations or even related species may have become extinctin response to one of the recent extreme fluctuations in climate Its vegetarian diet may have made it vulnerable intimes of drought and competition with other species may havebeen an additional factor

The importance of environmental change in speciation isfurther suggested by the fact that in the last million years newspecies evolved in the habitats most vulnerable to changeGeospiza were added to lowland habitats and Camarhynchuswere added to the upland humid forest The change in climatetoward seasonal aridity and the development of arid lowlandhabitat provided the opportunity for a new granivorous wayof finch life now adopted by Geospiza species Some of thesemodern species may have contributed to the extinction ofolder ones through competitive superiority in a changingenvironment This is one possible interpretation of the contrast between the morphological distinctness of the threeolder groups Certhidea Platyspiza and G difficilis and themorphological similarity of species in the younger generaCamarhynchus Cactospiza and Geospiza

These ideas on speciation and extinction together with ob-servations of the colonization of Daphne Major by G magni-rostris (Grant et al 2001) suggest that periods of expansionsuch as the one in progress are preceded and followed by periods of range contraction and extinction caused by envi-ronmental change Distributions of habitats sea level islandand population sizes and degrees of isolation provide favorable conditions for divergence of small populations inisolation at some times and for dispersal mixing establish-ment of sympatry and hybridization at others The buildupof complex communities from simple ones is not smooth con-tinuous and regular but a process of gains and losses with anet accumulation of species over the long term

ConclusionsAccording to the standard allopatric model speciation beginswith the establishment of a new population continues withthe divergence of that population from its parent populationand is completed when members of two diverged populationscan coexist in sympatry without interbreeding We stand a virtually negligible chance of observing the whole process under natural circumstances Nevertheless it is possible tomake relevant observations in nature of all steps in theprocess We have described the strong role played by envi-ronmental change at each of the three steps in the speciationof Darwinrsquos finches The full adaptive radiation was pro-duced by a repetition of these steps each with a different product under somewhat different circumstances The challenge now is to account for the differences in terms of pastenvironments without the help of fossils of finches or ofother members of the biota We have sketched a frameworkfor doing this by using molecular genetic information to estimate the finch phylogeny and using geological and climaticinformation to reconstruct Galaacutepagos environments in thepast 2 million to 3 million years A better understanding ofenvironmental change on this time scale will help to explainwhy 14 species were formed what their sequence of origin wasand why they evolved their particular unique features Theremay be more history to uncover in finch DNA if only we canwork out how to read it

Acknowledgments We thank Ken Petren for figure 8 and Phil Hedrick FritzTrillmich and an anonymous reviewer for comments on themanuscript We are grateful to the Galaacutepagos National Parkand the Charles Darwin Research Station for permission andlogistical support for the fieldwork and to the National Sciences and Engineering Research Council of Canada and theNational Science Foundation for funding support

References citedAbbott I Abbott LK Grant PR 1977 Comparative ecology of Galaacutepagos

ground finches (Geospiza Gould) Evaluation of the importance of floris-tic diversity and interspecific competition Ecological Monographs 47151ndash184

Alley RB et al 2003 Abrupt climate change Science 299 2005ndash2010

974 BioScience bull October 2003 Vol 53 No 10

Plenary

Bowman RI 1961 Morphological Differentiation and Adaptation in theGalaacutepagos Finches University of California Publications in ZoologyVol 58 Berkeley University of California Press

mdashmdashmdash 1983 The songs of Darwinrsquos finches Pages 237ndash537 in Bowman RILeviton AE Berson M eds Galaacutepagos Organisms San Francisco Amer-ican Association for the Advancement of Science Pacific Division

Burns KJ Hackett SJ Klein NK 2002 Phylogenetic relationships andmorphological diversity in Darwinrsquos finches and their relatives Evo-lution 56 1240ndash1252

Bush MB Piperno DR Colinvaux PA DeOleveira PE Krissek LA Miller MCRowe WE 1992 A 14300-yr paleoecological profile of a lowland tropi-cal lake in Panama Ecological Monographs 62 251ndash275

Cane MA Molnar P 2001 Closing of the Indonesian seaway as a precursorto east African aridification around 3ndash4 million years ago Nature 411157ndash162

Colinvaux PA 1972 Climate and the Galaacutepagos Islands Nature 240 17ndash20mdashmdashmdash 1984 The Galaacutepagos climate Present and past Pages 55ndash69 in

Perry R ed Galaacutepagos Oxford (United Kingdom) Pergamon PressDarwin CR 1842 Journal of Researches into the Geology and Natural

History of the Various Countries Visited during the Voyage of H M SBeagle under the Command of Captain FitzRoy RN from 1832 to 1836London Henry Colburn

Dunbar RB Wellington GM Colgan MW Glynn PW 1994 Eastern Pacificsea surface temperature since 1600 AD The O18 record of climate vari-ability in Galaacutepagos corals Paleoceanography 9 291ndash315

Finston TL Peck SB 1997 Genetic differentiation and speciation in Stomion(Coleoptera Tenebrionidae) Flightless beetles of the Galaacutepagos IslandsEcuador Biological Journal of the Linnean Society 61 243ndash266

Givnish TJ 1998Adaptive plant evolution on islands Classical patterns mole-cular data new insights Pages 281ndash304 in Grant PR ed Evolution on Islands Oxford (United Kingdom) Oxford University Press

Grant BR Grant PR 1989 Evolutionary Dynamics of a Natural PopulationThe Large Cactus Finch of the Galaacutepagos Chicago University of ChicagoPress

mdashmdashmdash 1996 Cultural inheritance of song and its role in the evolution ofDarwinrsquos finches Evolution 50 2471ndash2487

Grant PR 1999 Ecology and Evolution of Darwinrsquos Finches Princeton (NJ)Princeton University Press

mdashmdashmdash 2001 Reconstructing the evolution of birds on islands 100 years ofresearch Oikos 92 385ndash403

Grant PR Grant BR 1998 Speciation and hybridization in island birds Pages142ndash162 in Grant PR ed Evolution on Islands Oxford (United Kingdom)Oxford University Press

mdashmdashmdash 2002a Unpredictable evolution in a 30-year study of Darwinrsquosfinches Science 296 707ndash711

mdashmdashmdash 2002b Adaptive radiation of Darwinrsquos finches American Scientist90 131ndash139

Grant PR Grant BR Petren K 2001 The founding of a new population by a single pair of individuals Establishment selection and populationexpansion Genetica 112113 359ndash382

Huxley JS 1942 Evolution The Modern Synthesis London Allen and Unwin

Johnson MP Raven PH 1973 Species number and endemism The Galaacutepagosarchipelago revisited Science 179 893ndash895

Keller LF Grant PR Grant BR Petren K 2001 Heritability of morphologi-cal traits in Darwinrsquos finches Misidentified paternity and maternal effects Heredity 87 325ndash336

Kerr RA 2001 The tropics return to the climate system Science 292 660ndash661Lack D 1947 Darwinrsquos finches Cambridge (United Kingdom) Cambridge

University PressLambeck K Chappell J 2001 Sea level change through the last glacial cycle

Science 292 679ndash686Mayr E 1942 Systematics and the Origin of Species New York Columbia

University Press

Newton I 1967 The adaptive variation and feeding ecology of some British

finches Ibis 109 33ndash98

Petren K Grant BR Grant PR 1999 A phylogeny of Darwinrsquos finches based

on microsatellite DNA length variation Proceedings of the Royal Soci-

ety of London B 266 321ndash329

Price T Lovette IJ Bermingham E Gibbs HL Richman AD 2000 The

imprint of history on communities of North American and Asian

warblers American Naturalist 156 354ndash367

Prodon R Thibault J-C Dejaifve P-A 2002 Expansion vs compression of

bird altitudinal ranges on a Mediterranean island Ecology 83 1294ndash1306

Ratcliffe LM Grant PR 1983a Species recognition in Darwinrsquos finches

(Geospiza Gould) I Discrimination by morphological cues Animal

Behaviour 31 1139ndash1153

mdashmdashmdash 1983b Species recognition in Darwinrsquos finches (Geospiza Gould)

II Geographic variation in mate preference Animal Behaviour 31

1154ndash1165

mdashmdashmdash 1985 Species recognition in Darwinrsquos finches (Geospiza Gould) III

Male responses to playback of different song types dialects and hetero-

specific songs Animal Behaviour 33 290ndash307

Richards OW 1948 Species formation in islands (review of Darwinrsquos Finches

by Lack D) Journal of Animal Ecology 17 83ndash84

Riedinger MA Steinitz-Kannan M Last WM Brenner M 2002 A ~6100 14C

yr record of El Nintildeo activity from the Galaacutepagos Islands Journal of

Paleontology 27 1ndash7

Sato A OrsquoHuigin C Figueroa F Grant PR Grant BR Tichy H Klein J 1999

Phylogeny of Darwinrsquos finches as revealed by mtDNA sequences

Proceedings of the National Academy of Sciences 96 5101ndash5106

Schluter D 2000 The Ecology of Adaptive Radiations Oxford (United King-

dom) Oxford University Press

Schluter D Grant PR 1984 Determinants of morphological patterns in

communities of Darwinrsquos finches American Naturalist 123 175ndash196

Seltzer GO Rodbell DT Baker PA Fritz SC Tapia PM Rowe HD Dunbar

RB 2002 Early warming of tropical South America at the last glacialndash

interglacial transition Science 296 1685ndash1686

Sequeira AS Lanteri AA Scataglini MA Confalonieri VA Farrell BD 2000

Are flightless Galapaganus weevils older than the Galaacutepagos Islands they

inhabit Heredity 85 20ndash29

Simpson GG 1944 Tempo and Mode in Evolution New York Columbia

University Press

Swarth HS 1931 The avifauna of the Galaacutepagos islands Occasional Papers

of the California Academy of Sciences 18 1ndash299

mdashmdashmdash 1934 The bird fauna of the Galaacutepagos islands in relation to species

formation Biological Reviews 9 213ndash234

Tudhope AW Chilcott CP McCulloch MT Cook ER Chappell J Ellam RM

Lea DW Lough JM Shimmield GB 2001 Variability in the El

NintildeondashSouthern Oscillation through a glacialndashinterglacial cycle Science

291 1511ndash1517

Vincek V OrsquoHuigin C Satta Y Takahata N Boag PT Grant PR Grant BR

Klein J 1996 How large was the founding population of Darwinrsquos

finches Proceedings of the Royal Society of London B 264 111ndash118

Woodward FI 1987 Climate and Plant Distribution London Cambridge Uni-

versity Press

Wright SD Young CG Dawson JW Whittaker DJ Gardner RC 2000

Riding the ice age El Nintildeo Pacific biogeography and evolution of

Metrosideros subg Metrosideros (Myrtaceae) inferred from nuclear

ribosomal DNA Proceedings of the National Academy of Sciences 97

4110ndash4123

October 2003 Vol 53 No 10 bull BioScience 975

Plenary

bull It oscillates in direction

bull It happens when the environment changes

bull It has evolutionary consequences (adaptive change)

Almost 100 years after Darwinrsquos visit to the Galaacutepagos asystematist Harry Swarth came close to suggesting that evo-lution was not over and done with but could actually be witnessed when he wrote that ldquothe extraordinary variantsthat crop up in a series [of museum specimens] give an im-pression of change and experiment going onrdquo(Swarth 1934)Based on the evidence of Darwinrsquos finches evolutionarychanges are indeed going on

Speciation The beginningSpeciation begins with the divergence of apopulation and is completed when two pop-ulations that have diverged on different islandsestablish coexistence with little or no inter-breeding (Mayr 1942 Grant 2001) We obtained insight into the initial process ofdivergence on Daphne Major thanks to ahighly fortuitous circumstance the foundingof a new population

The large ground finch (Geospiza magni-rostris) became a breeding member of thecommunity in late 1982 when two femalesand three males began to breed In precedingyears we had observed immigrant membersof this species on the island in the dry seasonbut when the rains began they disappearedpresumably returning to their island oforigin to breed Not so in El Nintildeo The breed-ing birds produced 17 fledglings in 1982ndash1983 but only one of the breeding pairs produced the next generation A daughterbred at different times with two brothersone of which can be ignored because the offspring did not survive to breed Thus thepopulation was effectively founded by a single pair and the next generation com-prised a sisterndashbrother pairWe have followedthe fate of this population ever since (Grantet al 2001) There are now 30 to 40 breedingpairs on the island

Observations of a newly founded popu-lation go to the heart of the question of howbiodiversity generation begins Environ-mental change appears to have been a keyfactor in facilitating population establish-ment and subsequent exponential growthThe G magnirostris population experienceda genetic bottleneck (microsatellite allelicdiversity fell) and inbreeding depressionoccurred as shown by the relatively poorsurvival of the 1991 cohort Small additionalchanges were caused by natural selection onbeak morphology and probably by genetic

drift All of this is to be expected but some other featureswere surprising Immigration did not occur just once but repeatedly especially in the 1990s With one exception im-migrants that stayed to breed came not from the obvious andclosest potential source (Santa Cruz Island) but mainlyfrom one farther away (Santiago) as revealed by their micro-satellite DNA A major change took place in the frequency of song types in the population This change wasinitiated by a single male that bred for the first time in1991 In addition to this nongenetic culturally transmittedcontribution he introduced a total of 11 new alleles at the16 microsatellite loci surveyed

968 BioScience bull October 2003 Vol 53 No 10

Plenary

Figure 3 The intergradation of beak sizes and shapes illustrated with outlinesof the six species in the genus Geospiza 1ndash3 Geospiza magnirostris 4ndash7Geospiza conirostris 8ndash13 Geospiza fortis 14ndash15 Geospiza fuliginosa16ndash21 Geospiza difficilis 22ndash24 Geospiza scandens Illustration by Swarth(1931) from Abbott and colleagues (1977)

Thus while environmental change was the key factor thattriggered the founding of a new population some idiosyn-cratic genetic and nongenetic factors determined the fate de-velopment and composition of the population Even thoughone individual made a large contribution to the populationoverall changes were relatively small in magnitude for threereasons Selection pressures were weak the population did notremain small enough for random genetic drift to be effectiveand continuing immigration would have retarded diver-gence If the case of G magnirostris can be considered repre-sentative of how speciation begins we would have to concludethat it starts slowly with small steps

Speciation The endSpeciation is completed when two populations that have diverged in allopatry can coexist with little or no inter-breeding Medium ground finches and cactus finches occupy different ecological niches although their diets over-lap The ecological differences presumably permit coexistencein sympatry in an environment (eg Daphne Major) whosefood supply fluctuates in abundance and composition Toparaphrase David Lack (1947) the species are ecologically isolated through niche differences that evolved by natural selection in allopatry The differences may have been enhanced by selection in sympatry thereby reducing inter-specific competition for food But how do the species maintain coexistence without interbreeding What are the dif-ferences that keep them reproductively isolated and howdid the differences evolve

Members of the group of closely related ground finchspecies do not differ in plumage or courtship behavior butthey do differ in beak morphology and they differ conspic-uously in song (Grant 1999) These two sets of cues visual andvocal have been shown in separate field experiments to beused by finches in discriminating between their own and

other species (Ratcliffe and Grant 1983a 1983b 1985) Thuspart of the answer to the question of reproductive isolationis that it evolves as a consequence of adaptive evolution of beaksizes and shapes in allopatry The other part centered onsong is more complex

Song differences play a major role in keeping species apartLike beak differences song differences presumably arisethrough divergence in allopatry for reasons that are not en-tirely clear Song is an interesting trait because it is culturallyand not genetically inherited We know this from a few

October 2003 Vol 53 No 10 bull BioScience 969

Plenary

Figure 4 As the average beak depth of a population ofgranivorous Geospiza species increases so does the maxi-mum size and hardness of the seeds they can crack Basedon Schluter and Grant (1984)

Figure 5 Evolutionary change in beak depth in the popu-lation of Geospiza fortis on the island of Daphne MajorThe upper panel shows the distribution of beak depths inthe breeding population in 1976 with the survivors of the1977 drought that bred in 1978 indicated in black Thedifference between the means indicated by a caret is ameasure of the strength of natural selection The middleand lower panels show the distributions of beak depths offully grown offspring hatched in 1976 and 1978 respec-tively Evolutionary change between generations is mea-sured by the difference in mean between the 1976 popula-tion before selection and the birds hatched in 1978

Beak depth

Num

bersLog seed hardness

Log

beak

dep

th

experiments with captive birds (Bowman 1983) supple-mented by field observations of songs of offspring parentsand even grandparents (Grant and Grant 1989 1996) Onlymales sing an advertising song it is simple and is sung un-altered throughout life which may be as long as 16 years Mostsons sing the same song subtype as their fathers while a minority sing a different song subtype that is sung by othermale members of the same population Thus song is acquired through learning early in life in a process that resembles imprinting it is generally acquired from fathers during the period of parental dependence in associationwith parental morphology By their pairing patterns femalesgive evidence of learning song at the same time and from thesame sources

Rare exceptions to these rules provide additional valuableinformation on the role of learning and its bearing on thequestion of what keeps species apart Once again environ-mental change associated with an El Nintildeo event has pro-vided crucial information Medium ground finches and cactus finches hybridize rarely Before 1983 the hybrids diedwithout breeding at a time when most of the ldquopurerdquo speciesproduced in the same years also died without breeding TheEl Nintildeo event of 1983 resulting in an abundance of smallseeds altered the environment in a way that was favorable tothe survival of the hybrids The hybrids that were producedin 1983 backcrossed to medium ground finches in 1987 andothers that were produced in 1987 backcrossed to cactusfinches in 1991 The direction of backcrossing differed becausein 1983 the hybridizing male was a cactus finch that sang amedium ground finch song whereas in 1987 the hybridizingmales were cactus finches that sang cactus finch songsSons of all families sang the same song as their fathers anddaughters in each case mated with males that sang the samesong type as their fathers

Hybridization is sometimes the re-sult of heterospecific singing throughapparent misimprinting The causesof misimprinting and hybridizationare idiosyncratic and difficult to determine They include extra-pairmating interspecific takeover of nestswith eggs and dominant singing of aclose neighbor Ecologically the sig-nificant feature is a change in the environment that has facilitated theintrogression of genes F1 hybrid andbackcross survival is not intrinsicallylower than the survival of the parentalspecies and there is no sign of dimin-ished fitness when hybrids breed Infact in the 1990s and up to the presentthe flow of genes from the mediumground finch to the cactus finch population has contributed to a decrease in mean body size and ablunter beak morphology of cactus

finches (Grant and Grant 2002a) The barrier to gene exchangeerected by song differences has been breached and environ-mental change appears to have been the most important factor

To summarize the coexistence of finch species is facilitatedby divergence in beak morphology and song Beaks divergeunder natural selection but why songs diverge is less clear Cul-tural drift a process of random change in culturally trans-mitted (learned) traits is probably involved and sexual se-lection may be involved as well The end point of speciationis the complete absence of gene exchange Many if not all co-existing populations of Darwinrsquos finches have not quitereached that point although they function as species by re-maining distinct even in the face of occasional gene exchangeThis offers two important lessons First species diverge in matepreferences before genetic incompatibilities evolve Seconddifferent populations can function as biological species beforethey would be recognized as species solely on the basis of ge-netic distinctness

History The initial colonizationThe present is known the past is inferred To understand thepast of Darwinrsquos finches the first question that needs to be ad-dressed is when the radiation began because the answer setsthe boundary on relevant Galaacutepagos history In the absenceof fossils genes are our best source of information aboutthis history (Price et al 2000) The closest genetic relatives ofDarwinrsquos finches on the South American continent in Central America and in the Caribbean are a group of seed-eaters (Tiaris and relatives) allied to tanagers (Sato et al 1999Burns et al 2002) Darwinrsquos finches diverged from them in thelast 2 million or possibly 3 million years according to calcu-lations based on an assumed molecular clock applied to mitochondrial DNA and allozyme data (Grant 1999) The

970 BioScience bull October 2003 Vol 53 No 10

Plenary

Daphne Major a volcanic remnant in the Galaacutepagos archipelago is the site of theauthorsrsquo long-term study of evolution in Darwinrsquos finches Photograph David Parer

recent origin of Darwinrsquos finches helps to explain why theyare still capable of exchanging genes

Divergence from their mainland relatives began when thefinches colonized the Galaacutepagos islands Situated 900 kmfrom continental Ecuador on the Nazca plate and moving imperceptibly toward the mainland the archipelago is a re-mote place for birds to visit Colonization is an improbableevent Nevertheless according to one calculation ancestralDarwinrsquos finches arrived in a moderately large flock (or several small ones) Modern finches are genetically diverse atthe major histocompatibility complex locus and Vincek andcolleagues (1996) used the allelic diversity of class II genes to calculate that the original colonists numbered at least 30individuals

Improbable events may arise in improbable and hencerare circumstances What might those circumstances havebeen Any answer must be speculative even if rooted in current phenomena The circumstances that promote dispersalof contemporary finches within the Galaacutepagos archipelago are(a) high finch density following prolific breeding in El Nintildeoyears and (b) forest fires caused by volcanic eruptions If the

unusual dispersal activity from the mainland followed sim-ilar patterns it may have been induced by unusual volcanicactivity in the Andes Burning of the forests in one suchepisode would be followed by the establishment of large areas of shrub and secondary growth With the buildup offinch populations in secondary forest and another round offires and burning large numbers of finches and other birdsin coastal regions would fly out to sea to escape the flames andsmoke The colonists would be helped if mats of vegetationwere rafted out to sea by strong El Nintildeondashassociated floodingfrom the Guayas River Global temperatures were warmer 2million to 3 million years ago and permanent El Nintildeo con-ditions are thought to have occurred until about that time(Cane and Molnar 2001) The most marked shift in climateseems to have occurred at 24 million to 25 million years agoThis may be when the ancestral Darwinrsquos finches arrived

Relevant history of the GalaacutepagosTo understand the past the second question that needs to beaddressed is how the islands have changed if at all since thefirst finches arrived The simplest possible answer would be

October 2003 Vol 53 No 10 bull BioScience 971

Plenary

Figure 6 Changes in the beak size and shape of Geospiza fortis and Geospiza scandens on the islandof Daphne Major Mean trait values for each year are indicated by solid circles and 95 confidenceintervals are shown by vertical bars above and below the mean In the absence of change the meansshould remain within the 95 confidence intervals (horizontal broken lines) of the mean estimatesfrom the 1973 samples PC refers to principal component obtained from a principal componentsanalysis of size and shape variables From Grant and Grant (2002a)

PC2 b

eak

shap

ePC

1 b

eak

shap

e

that the islands have always been much as they are today interms of geography climate and vegetation If this is correctthe finchesrsquo adaptive radiation can be viewed as a process ofdifferentiation that results in the occupancy of all ecologicalniches present at the outsetmdashrather like filling empty boxesone species per box Indeed this is how early writers on thesubject viewed the radiation of the finches stressing the absence or scarcity of competitors in the boxes as a facilitat-ing factor (Huxley 1942 Simpson 1944 Lack 1947 Grant1999) In the modern version the boxes are replaced by adap-tive peaks in a more or less fixed landscape This view impliesthat diversification is rapid early in the radiation and thenslows down as ecological opportunities diminish Some radiations of other organisms elsewhere conform to this pattern (Schluter 2000) However taken at face value thephylogeny of Darwinrsquos finches shows exactly the oppositepattern a slow start followed by recent rapid diversification(figure 7) The species occupy adaptive peaks but the fixityof the ecological landscape that allowed them to do so isquestionable

In fact the islands and their inhabitants have changedradically Three million years ago there were far fewer islands than today perhaps only five (Grant and Grant 1998)The number of islands increased as a result of volcanic activitycentered on and near a hotspot beneath the western island of Fernandina Climate changed as well The average air

temperature declined but more important thanthis the worldrsquos climate underwent a sharp transi-tion 275 million years ago with the abrupt onset of glaciation (Cane and Molnar 2001) In the lastmillion years the climate has oscillated betweenglacial and interglacial conditions at about 100000-year intervals Global fluctuations in climate wereexperienced locally in the Galaacutepagos and elsewherein tropical America This has been revealed by theisotopic oxygen signatures of temperature in Andean ice cores (Seltzer et al 2002) by coral coresin Galaacutepagos (Dunbar et al 1994) and by pollencores in Galaacutepagos (Colinvaux 1972 1984) and incontinental South and Central American lakes(Bush et al 1992)

Most of the contemporary finches evolved inthe last million years so it is important to knowwhat happened during these cycles The two majoreffects of glacialndashinterglacial cycles were the de-pression of temperatures and of sea level relative to contemporary levels The last Ice Agecooling resulted in a drop of 3degC to 4degC in theequatorial Pacific reaching a minimum about21000 years ago (Kerr 2001) The previous deglacia-tion about 130000 years ago was associated witha drop of 2degC to 6degC (Tudhope et al 2001) Sea levelfell with the temperature The decline was gradualfrom the current level (about 120000 years ago) toabout 60 meters (m) lower (about 30000 yearsago) then an abrupt further decrease occurred to

about 125 m below the current level (Lambeck and Chappell2001) As a consequence islands were larger and distances between them were shorter Thus both temperature and sealevel were usually lower and never much higher than they aretoday

The food of finchesmdashplants and arthropods the latterfeeding on the plants and on each othermdashmust have beenaffected by these geophysical and climatic changes Firstnew species of plants and arthropods would have arrivedby immigration We do not know when this happened or which species were involved For Galaacutepagos unlikeHawaii (eg Givnish 1998 Wright et al 2000) there are nomolecular phylogenies of plants to help in reconstructingpaleofloras and the phylogenies of insects are too scarceto be useful (Finston and Peck 1997 Sequeira et al 2000)That situation needs to be rectified Second other speciesperhaps influenced by the immigrants would have become extinct Severe and extensive droughts would have been particularly crucial and cruel times for many organisms including finches Third the temperature- andmoisture-dependent altitudinal zonation of plants wouldhave shifted upward and downward at different timeshence the highest and lowest habitats would have beenmost vulnerable to elimination as noted elsewhere (Prodonet al 2002) Plant distributions would have changed acrossthe archipelago

972 BioScience bull October 2003 Vol 53 No 10

Plenary

Figure 7 The accumulation of species of Darwinrsquos finches with timeback-calculated from the estimated ages (in millions of years or MY) ofcontemporary species in the absence of known extinctions The accumu-lation of species parallels the accumulation of islands with time as de-termined from estimations of island age and elevation in relation to sealevel More islands provide more conditions for speciation to occur andspecies to persist From Grant (2001)

The evidence of a change in the upland forests is the rel-ative scarcity of endemic plants (Johnson and Raven 1973)The evidence of a change in the lowest zone is the anomalousoccurrence of plants on some islands with apparently un-suitable climates and soil For example the tree Erythrina velu-tina occurs at mid elevations on the high islands of Santa CruzSantiago and Isabela A single tree of this species occurs onthe low arid island of Genovesa and fewer than a dozen oc-cur on the low arid and even more remote island of WolfSimilarly a few Zanthoxylum fagara trees on Santa Cruz andSan Cristoacutebal occur close to the coast These may be theremnants of much larger populations on these islands undercooler wetter or less seasonally arid conditions than those thatprevail today Temperatures and precipitation changedmarkedly from one state to another long enough (gt 1000years Colinvaux 1972 Riedinger et al 2002) for vegetationzones to shift (Woodward 1987) On some occasions how-ever significant changes in temperature occurred in as shorta time as a hundred years perhaps less (Bush et al 1992)Large abrupt and widespread climate changes with majorconsequences for the biota have occurred repeatedly in thepast when the Earth system was forced across thresholds(Alley et al 2003)

The macroevolutionary pattern and the buildup ofcomplex communities from simple ones In view of the strong environmental changes in the archi-pelago it is scarcely likely that all current ecological niches wereavailable when the finchesrsquo ancestors arrived Rather thenumbers and types of opportunities for finch evolution increased as the number of islands increased and the climate and vegetation changed According to this view theadaptive radiation and the buildup of species-rich commu-nities were largely molded by environmental change theparticular species originated when they did and no earlierin response to particular environments prevailing then

When the first finches arrived on Galaacutepagos they mayhave encountered a climate and vegetation more like those ofmodern-day Cocos Island warmer wetter and more humidconditions fostering rain forest from the coast to the islandpeaks (Grant 1999 Grant and Grant 2002b) Cocos Island hastemperatures similar to those of the coastal habitats in theGalaacutepagos and rainfall equivalent to what the Galaacutepagosnow receives in an El Nintildeo year at high elevations Reason-ing from the evidence of modern finches we suggest the ini-tial evolutionary pathway taken by the finches was toward theexploitation of small arthropods and of nectar and pollenfrom small flowers in a rain forestndashlike environment

The radiation began when the initial species split into twolineages of Certhidea warbler finches (figure 8) after the ini-tial pathway had been taken One group of populations(Certhidea olivacea) inhabits moist upland forest and theother group (Certhidea fusca) occupies lower habitats onother mainly low islands Remarkably despite their longseparation the two groups have retained similar mate recog-nition systems and for that reason we refer to them as lineages

October 2003 Vol 53 No 10 bull BioScience 973

Plenary

Figure 8 Reconstruction of finch phylogeny based on microsatellite DNA Horizontal branch lengths are pro-portional to units of genetic distance (GST) as indicated bythe scale Numbers refer to percentage bootstrap supportfor the nodes by two methods Mean weights are given onthe right together with symbols of male plumage fullyblack partially black or brown or green Alternative reconstructions that use morphology allozymes or mito-chondrial DNA are similar differing in relatively smalldetails Species from top to bottom Geospiza fuliginosaGeospiza fortis Geospiza magnirostris Geospiza scandensGeospiza conirostris Geospiza difficilis Camarhynchusparvulus Camarhynchus psittacula Camarhynchus pauperCamarhynchus pallida Platyspiza crassirostris Certhideafusca Pinaroloxias inornata and Certhidea olivacea FromPetren and colleagues (1999)

and not species (Grant and Grant 2002b) Another remark-able feature is that they have remained relatively undifferen-tiated in morphology ecology and behavior This is not expected on the basis of the view that niches were varied plen-tiful and evolutionarily within reach at that time Howeverwe must acknowledge the possibility perhaps even the prob-ability that extinction has robbed us of other species that wereformed then The morphological similarity of these finchescontrasting with their distinctness from continental rela-tives argues for an early adaptation to an unusual niche

One of the warbler finch lineages gave rise to all otherfinch species Early products of the diversification were the veg-etarian finch (Platyspiza crassirostris) the Cocos finch(Pinaroloxias inornata) on either Galaacutepagos or Cocos Island(Grant and Grant 2002b) and the sharp-beaked groundfinch (G difficilis) The most recent products were a group ofground finch species (Geospiza) and a group of tree finchspecies (Camarhynchus and Cactospiza) (figure 8)

Effects of environmental change have left a different his-torical imprint on the older species Populations of G diffi-cilis differ strongly in morphology and ecology to a degree un-matched by all other and younger species in the genusGeospiza and by the warbler finches that preceded themSome G difficilis have persisted in Zanthoxylum forest at midand upper elevations which we believe to be old and others have entered arid lowland habitat perhaps when theZanthoxylum forest gradually disappeared from low islandsas the climate changed This may have been the first step ofthe radiation of ground finches In contrast to the G difficilispopulations populations of the vegetarian finch are mor-phologically and ecologically very similar Limited genetic data(Petren et al 1999) suggest that they separated from each otherrecently This is surprising as it is not expected from the ageof the species or from the presumed stability of its mid-elevation transition zone habitat The vegetarian finch mayhave become restricted to one or two islands and other pop-ulations or even related species may have become extinctin response to one of the recent extreme fluctuations in climate Its vegetarian diet may have made it vulnerable intimes of drought and competition with other species may havebeen an additional factor

The importance of environmental change in speciation isfurther suggested by the fact that in the last million years newspecies evolved in the habitats most vulnerable to changeGeospiza were added to lowland habitats and Camarhynchuswere added to the upland humid forest The change in climatetoward seasonal aridity and the development of arid lowlandhabitat provided the opportunity for a new granivorous wayof finch life now adopted by Geospiza species Some of thesemodern species may have contributed to the extinction ofolder ones through competitive superiority in a changingenvironment This is one possible interpretation of the contrast between the morphological distinctness of the threeolder groups Certhidea Platyspiza and G difficilis and themorphological similarity of species in the younger generaCamarhynchus Cactospiza and Geospiza

These ideas on speciation and extinction together with ob-servations of the colonization of Daphne Major by G magni-rostris (Grant et al 2001) suggest that periods of expansionsuch as the one in progress are preceded and followed by periods of range contraction and extinction caused by envi-ronmental change Distributions of habitats sea level islandand population sizes and degrees of isolation provide favorable conditions for divergence of small populations inisolation at some times and for dispersal mixing establish-ment of sympatry and hybridization at others The buildupof complex communities from simple ones is not smooth con-tinuous and regular but a process of gains and losses with anet accumulation of species over the long term

ConclusionsAccording to the standard allopatric model speciation beginswith the establishment of a new population continues withthe divergence of that population from its parent populationand is completed when members of two diverged populationscan coexist in sympatry without interbreeding We stand a virtually negligible chance of observing the whole process under natural circumstances Nevertheless it is possible tomake relevant observations in nature of all steps in theprocess We have described the strong role played by envi-ronmental change at each of the three steps in the speciationof Darwinrsquos finches The full adaptive radiation was pro-duced by a repetition of these steps each with a different product under somewhat different circumstances The challenge now is to account for the differences in terms of pastenvironments without the help of fossils of finches or ofother members of the biota We have sketched a frameworkfor doing this by using molecular genetic information to estimate the finch phylogeny and using geological and climaticinformation to reconstruct Galaacutepagos environments in thepast 2 million to 3 million years A better understanding ofenvironmental change on this time scale will help to explainwhy 14 species were formed what their sequence of origin wasand why they evolved their particular unique features Theremay be more history to uncover in finch DNA if only we canwork out how to read it

Acknowledgments We thank Ken Petren for figure 8 and Phil Hedrick FritzTrillmich and an anonymous reviewer for comments on themanuscript We are grateful to the Galaacutepagos National Parkand the Charles Darwin Research Station for permission andlogistical support for the fieldwork and to the National Sciences and Engineering Research Council of Canada and theNational Science Foundation for funding support

References citedAbbott I Abbott LK Grant PR 1977 Comparative ecology of Galaacutepagos

ground finches (Geospiza Gould) Evaluation of the importance of floris-tic diversity and interspecific competition Ecological Monographs 47151ndash184

Alley RB et al 2003 Abrupt climate change Science 299 2005ndash2010

974 BioScience bull October 2003 Vol 53 No 10

Plenary

Bowman RI 1961 Morphological Differentiation and Adaptation in theGalaacutepagos Finches University of California Publications in ZoologyVol 58 Berkeley University of California Press

mdashmdashmdash 1983 The songs of Darwinrsquos finches Pages 237ndash537 in Bowman RILeviton AE Berson M eds Galaacutepagos Organisms San Francisco Amer-ican Association for the Advancement of Science Pacific Division

Burns KJ Hackett SJ Klein NK 2002 Phylogenetic relationships andmorphological diversity in Darwinrsquos finches and their relatives Evo-lution 56 1240ndash1252

Bush MB Piperno DR Colinvaux PA DeOleveira PE Krissek LA Miller MCRowe WE 1992 A 14300-yr paleoecological profile of a lowland tropi-cal lake in Panama Ecological Monographs 62 251ndash275

Cane MA Molnar P 2001 Closing of the Indonesian seaway as a precursorto east African aridification around 3ndash4 million years ago Nature 411157ndash162

Colinvaux PA 1972 Climate and the Galaacutepagos Islands Nature 240 17ndash20mdashmdashmdash 1984 The Galaacutepagos climate Present and past Pages 55ndash69 in

Perry R ed Galaacutepagos Oxford (United Kingdom) Pergamon PressDarwin CR 1842 Journal of Researches into the Geology and Natural

History of the Various Countries Visited during the Voyage of H M SBeagle under the Command of Captain FitzRoy RN from 1832 to 1836London Henry Colburn

Dunbar RB Wellington GM Colgan MW Glynn PW 1994 Eastern Pacificsea surface temperature since 1600 AD The O18 record of climate vari-ability in Galaacutepagos corals Paleoceanography 9 291ndash315

Finston TL Peck SB 1997 Genetic differentiation and speciation in Stomion(Coleoptera Tenebrionidae) Flightless beetles of the Galaacutepagos IslandsEcuador Biological Journal of the Linnean Society 61 243ndash266

Givnish TJ 1998Adaptive plant evolution on islands Classical patterns mole-cular data new insights Pages 281ndash304 in Grant PR ed Evolution on Islands Oxford (United Kingdom) Oxford University Press

Grant BR Grant PR 1989 Evolutionary Dynamics of a Natural PopulationThe Large Cactus Finch of the Galaacutepagos Chicago University of ChicagoPress

mdashmdashmdash 1996 Cultural inheritance of song and its role in the evolution ofDarwinrsquos finches Evolution 50 2471ndash2487

Grant PR 1999 Ecology and Evolution of Darwinrsquos Finches Princeton (NJ)Princeton University Press

mdashmdashmdash 2001 Reconstructing the evolution of birds on islands 100 years ofresearch Oikos 92 385ndash403

Grant PR Grant BR 1998 Speciation and hybridization in island birds Pages142ndash162 in Grant PR ed Evolution on Islands Oxford (United Kingdom)Oxford University Press

mdashmdashmdash 2002a Unpredictable evolution in a 30-year study of Darwinrsquosfinches Science 296 707ndash711

mdashmdashmdash 2002b Adaptive radiation of Darwinrsquos finches American Scientist90 131ndash139

Grant PR Grant BR Petren K 2001 The founding of a new population by a single pair of individuals Establishment selection and populationexpansion Genetica 112113 359ndash382

Huxley JS 1942 Evolution The Modern Synthesis London Allen and Unwin

Johnson MP Raven PH 1973 Species number and endemism The Galaacutepagosarchipelago revisited Science 179 893ndash895

Keller LF Grant PR Grant BR Petren K 2001 Heritability of morphologi-cal traits in Darwinrsquos finches Misidentified paternity and maternal effects Heredity 87 325ndash336

Kerr RA 2001 The tropics return to the climate system Science 292 660ndash661Lack D 1947 Darwinrsquos finches Cambridge (United Kingdom) Cambridge

University PressLambeck K Chappell J 2001 Sea level change through the last glacial cycle

Science 292 679ndash686Mayr E 1942 Systematics and the Origin of Species New York Columbia

University Press

Newton I 1967 The adaptive variation and feeding ecology of some British

finches Ibis 109 33ndash98

Petren K Grant BR Grant PR 1999 A phylogeny of Darwinrsquos finches based

on microsatellite DNA length variation Proceedings of the Royal Soci-

ety of London B 266 321ndash329

Price T Lovette IJ Bermingham E Gibbs HL Richman AD 2000 The

imprint of history on communities of North American and Asian

warblers American Naturalist 156 354ndash367

Prodon R Thibault J-C Dejaifve P-A 2002 Expansion vs compression of

bird altitudinal ranges on a Mediterranean island Ecology 83 1294ndash1306

Ratcliffe LM Grant PR 1983a Species recognition in Darwinrsquos finches

(Geospiza Gould) I Discrimination by morphological cues Animal

Behaviour 31 1139ndash1153

mdashmdashmdash 1983b Species recognition in Darwinrsquos finches (Geospiza Gould)

II Geographic variation in mate preference Animal Behaviour 31

1154ndash1165

mdashmdashmdash 1985 Species recognition in Darwinrsquos finches (Geospiza Gould) III

Male responses to playback of different song types dialects and hetero-

specific songs Animal Behaviour 33 290ndash307

Richards OW 1948 Species formation in islands (review of Darwinrsquos Finches

by Lack D) Journal of Animal Ecology 17 83ndash84

Riedinger MA Steinitz-Kannan M Last WM Brenner M 2002 A ~6100 14C

yr record of El Nintildeo activity from the Galaacutepagos Islands Journal of

Paleontology 27 1ndash7

Sato A OrsquoHuigin C Figueroa F Grant PR Grant BR Tichy H Klein J 1999

Phylogeny of Darwinrsquos finches as revealed by mtDNA sequences

Proceedings of the National Academy of Sciences 96 5101ndash5106

Schluter D 2000 The Ecology of Adaptive Radiations Oxford (United King-

dom) Oxford University Press

Schluter D Grant PR 1984 Determinants of morphological patterns in

communities of Darwinrsquos finches American Naturalist 123 175ndash196

Seltzer GO Rodbell DT Baker PA Fritz SC Tapia PM Rowe HD Dunbar

RB 2002 Early warming of tropical South America at the last glacialndash

interglacial transition Science 296 1685ndash1686

Sequeira AS Lanteri AA Scataglini MA Confalonieri VA Farrell BD 2000

Are flightless Galapaganus weevils older than the Galaacutepagos Islands they

inhabit Heredity 85 20ndash29

Simpson GG 1944 Tempo and Mode in Evolution New York Columbia

University Press

Swarth HS 1931 The avifauna of the Galaacutepagos islands Occasional Papers

of the California Academy of Sciences 18 1ndash299

mdashmdashmdash 1934 The bird fauna of the Galaacutepagos islands in relation to species

formation Biological Reviews 9 213ndash234

Tudhope AW Chilcott CP McCulloch MT Cook ER Chappell J Ellam RM

Lea DW Lough JM Shimmield GB 2001 Variability in the El

NintildeondashSouthern Oscillation through a glacialndashinterglacial cycle Science

291 1511ndash1517

Vincek V OrsquoHuigin C Satta Y Takahata N Boag PT Grant PR Grant BR

Klein J 1996 How large was the founding population of Darwinrsquos

finches Proceedings of the Royal Society of London B 264 111ndash118

Woodward FI 1987 Climate and Plant Distribution London Cambridge Uni-

versity Press

Wright SD Young CG Dawson JW Whittaker DJ Gardner RC 2000

Riding the ice age El Nintildeo Pacific biogeography and evolution of

Metrosideros subg Metrosideros (Myrtaceae) inferred from nuclear

ribosomal DNA Proceedings of the National Academy of Sciences 97

4110ndash4123

October 2003 Vol 53 No 10 bull BioScience 975

Plenary

Thus while environmental change was the key factor thattriggered the founding of a new population some idiosyn-cratic genetic and nongenetic factors determined the fate de-velopment and composition of the population Even thoughone individual made a large contribution to the populationoverall changes were relatively small in magnitude for threereasons Selection pressures were weak the population did notremain small enough for random genetic drift to be effectiveand continuing immigration would have retarded diver-gence If the case of G magnirostris can be considered repre-sentative of how speciation begins we would have to concludethat it starts slowly with small steps

Speciation The endSpeciation is completed when two populations that have diverged in allopatry can coexist with little or no inter-breeding Medium ground finches and cactus finches occupy different ecological niches although their diets over-lap The ecological differences presumably permit coexistencein sympatry in an environment (eg Daphne Major) whosefood supply fluctuates in abundance and composition Toparaphrase David Lack (1947) the species are ecologically isolated through niche differences that evolved by natural selection in allopatry The differences may have been enhanced by selection in sympatry thereby reducing inter-specific competition for food But how do the species maintain coexistence without interbreeding What are the dif-ferences that keep them reproductively isolated and howdid the differences evolve

Members of the group of closely related ground finchspecies do not differ in plumage or courtship behavior butthey do differ in beak morphology and they differ conspic-uously in song (Grant 1999) These two sets of cues visual andvocal have been shown in separate field experiments to beused by finches in discriminating between their own and

other species (Ratcliffe and Grant 1983a 1983b 1985) Thuspart of the answer to the question of reproductive isolationis that it evolves as a consequence of adaptive evolution of beaksizes and shapes in allopatry The other part centered onsong is more complex

Song differences play a major role in keeping species apartLike beak differences song differences presumably arisethrough divergence in allopatry for reasons that are not en-tirely clear Song is an interesting trait because it is culturallyand not genetically inherited We know this from a few

October 2003 Vol 53 No 10 bull BioScience 969

Plenary

Figure 4 As the average beak depth of a population ofgranivorous Geospiza species increases so does the maxi-mum size and hardness of the seeds they can crack Basedon Schluter and Grant (1984)

Figure 5 Evolutionary change in beak depth in the popu-lation of Geospiza fortis on the island of Daphne MajorThe upper panel shows the distribution of beak depths inthe breeding population in 1976 with the survivors of the1977 drought that bred in 1978 indicated in black Thedifference between the means indicated by a caret is ameasure of the strength of natural selection The middleand lower panels show the distributions of beak depths offully grown offspring hatched in 1976 and 1978 respec-tively Evolutionary change between generations is mea-sured by the difference in mean between the 1976 popula-tion before selection and the birds hatched in 1978

Beak depth

Num

bersLog seed hardness

Log

beak

dep

th

experiments with captive birds (Bowman 1983) supple-mented by field observations of songs of offspring parentsand even grandparents (Grant and Grant 1989 1996) Onlymales sing an advertising song it is simple and is sung un-altered throughout life which may be as long as 16 years Mostsons sing the same song subtype as their fathers while a minority sing a different song subtype that is sung by othermale members of the same population Thus song is acquired through learning early in life in a process that resembles imprinting it is generally acquired from fathers during the period of parental dependence in associationwith parental morphology By their pairing patterns femalesgive evidence of learning song at the same time and from thesame sources

Rare exceptions to these rules provide additional valuableinformation on the role of learning and its bearing on thequestion of what keeps species apart Once again environ-mental change associated with an El Nintildeo event has pro-vided crucial information Medium ground finches and cactus finches hybridize rarely Before 1983 the hybrids diedwithout breeding at a time when most of the ldquopurerdquo speciesproduced in the same years also died without breeding TheEl Nintildeo event of 1983 resulting in an abundance of smallseeds altered the environment in a way that was favorable tothe survival of the hybrids The hybrids that were producedin 1983 backcrossed to medium ground finches in 1987 andothers that were produced in 1987 backcrossed to cactusfinches in 1991 The direction of backcrossing differed becausein 1983 the hybridizing male was a cactus finch that sang amedium ground finch song whereas in 1987 the hybridizingmales were cactus finches that sang cactus finch songsSons of all families sang the same song as their fathers anddaughters in each case mated with males that sang the samesong type as their fathers

Hybridization is sometimes the re-sult of heterospecific singing throughapparent misimprinting The causesof misimprinting and hybridizationare idiosyncratic and difficult to determine They include extra-pairmating interspecific takeover of nestswith eggs and dominant singing of aclose neighbor Ecologically the sig-nificant feature is a change in the environment that has facilitated theintrogression of genes F1 hybrid andbackcross survival is not intrinsicallylower than the survival of the parentalspecies and there is no sign of dimin-ished fitness when hybrids breed Infact in the 1990s and up to the presentthe flow of genes from the mediumground finch to the cactus finch population has contributed to a decrease in mean body size and ablunter beak morphology of cactus

finches (Grant and Grant 2002a) The barrier to gene exchangeerected by song differences has been breached and environ-mental change appears to have been the most important factor

To summarize the coexistence of finch species is facilitatedby divergence in beak morphology and song Beaks divergeunder natural selection but why songs diverge is less clear Cul-tural drift a process of random change in culturally trans-mitted (learned) traits is probably involved and sexual se-lection may be involved as well The end point of speciationis the complete absence of gene exchange Many if not all co-existing populations of Darwinrsquos finches have not quitereached that point although they function as species by re-maining distinct even in the face of occasional gene exchangeThis offers two important lessons First species diverge in matepreferences before genetic incompatibilities evolve Seconddifferent populations can function as biological species beforethey would be recognized as species solely on the basis of ge-netic distinctness

History The initial colonizationThe present is known the past is inferred To understand thepast of Darwinrsquos finches the first question that needs to be ad-dressed is when the radiation began because the answer setsthe boundary on relevant Galaacutepagos history In the absenceof fossils genes are our best source of information aboutthis history (Price et al 2000) The closest genetic relatives ofDarwinrsquos finches on the South American continent in Central America and in the Caribbean are a group of seed-eaters (Tiaris and relatives) allied to tanagers (Sato et al 1999Burns et al 2002) Darwinrsquos finches diverged from them in thelast 2 million or possibly 3 million years according to calcu-lations based on an assumed molecular clock applied to mitochondrial DNA and allozyme data (Grant 1999) The

970 BioScience bull October 2003 Vol 53 No 10

Plenary

Daphne Major a volcanic remnant in the Galaacutepagos archipelago is the site of theauthorsrsquo long-term study of evolution in Darwinrsquos finches Photograph David Parer

recent origin of Darwinrsquos finches helps to explain why theyare still capable of exchanging genes

Divergence from their mainland relatives began when thefinches colonized the Galaacutepagos islands Situated 900 kmfrom continental Ecuador on the Nazca plate and moving imperceptibly toward the mainland the archipelago is a re-mote place for birds to visit Colonization is an improbableevent Nevertheless according to one calculation ancestralDarwinrsquos finches arrived in a moderately large flock (or several small ones) Modern finches are genetically diverse atthe major histocompatibility complex locus and Vincek andcolleagues (1996) used the allelic diversity of class II genes to calculate that the original colonists numbered at least 30individuals

Improbable events may arise in improbable and hencerare circumstances What might those circumstances havebeen Any answer must be speculative even if rooted in current phenomena The circumstances that promote dispersalof contemporary finches within the Galaacutepagos archipelago are(a) high finch density following prolific breeding in El Nintildeoyears and (b) forest fires caused by volcanic eruptions If the

unusual dispersal activity from the mainland followed sim-ilar patterns it may have been induced by unusual volcanicactivity in the Andes Burning of the forests in one suchepisode would be followed by the establishment of large areas of shrub and secondary growth With the buildup offinch populations in secondary forest and another round offires and burning large numbers of finches and other birdsin coastal regions would fly out to sea to escape the flames andsmoke The colonists would be helped if mats of vegetationwere rafted out to sea by strong El Nintildeondashassociated floodingfrom the Guayas River Global temperatures were warmer 2million to 3 million years ago and permanent El Nintildeo con-ditions are thought to have occurred until about that time(Cane and Molnar 2001) The most marked shift in climateseems to have occurred at 24 million to 25 million years agoThis may be when the ancestral Darwinrsquos finches arrived

Relevant history of the GalaacutepagosTo understand the past the second question that needs to beaddressed is how the islands have changed if at all since thefirst finches arrived The simplest possible answer would be

October 2003 Vol 53 No 10 bull BioScience 971

Plenary

Figure 6 Changes in the beak size and shape of Geospiza fortis and Geospiza scandens on the islandof Daphne Major Mean trait values for each year are indicated by solid circles and 95 confidenceintervals are shown by vertical bars above and below the mean In the absence of change the meansshould remain within the 95 confidence intervals (horizontal broken lines) of the mean estimatesfrom the 1973 samples PC refers to principal component obtained from a principal componentsanalysis of size and shape variables From Grant and Grant (2002a)

PC2 b

eak

shap

ePC

1 b

eak

shap

e

that the islands have always been much as they are today interms of geography climate and vegetation If this is correctthe finchesrsquo adaptive radiation can be viewed as a process ofdifferentiation that results in the occupancy of all ecologicalniches present at the outsetmdashrather like filling empty boxesone species per box Indeed this is how early writers on thesubject viewed the radiation of the finches stressing the absence or scarcity of competitors in the boxes as a facilitat-ing factor (Huxley 1942 Simpson 1944 Lack 1947 Grant1999) In the modern version the boxes are replaced by adap-tive peaks in a more or less fixed landscape This view impliesthat diversification is rapid early in the radiation and thenslows down as ecological opportunities diminish Some radiations of other organisms elsewhere conform to this pattern (Schluter 2000) However taken at face value thephylogeny of Darwinrsquos finches shows exactly the oppositepattern a slow start followed by recent rapid diversification(figure 7) The species occupy adaptive peaks but the fixityof the ecological landscape that allowed them to do so isquestionable

In fact the islands and their inhabitants have changedradically Three million years ago there were far fewer islands than today perhaps only five (Grant and Grant 1998)The number of islands increased as a result of volcanic activitycentered on and near a hotspot beneath the western island of Fernandina Climate changed as well The average air

temperature declined but more important thanthis the worldrsquos climate underwent a sharp transi-tion 275 million years ago with the abrupt onset of glaciation (Cane and Molnar 2001) In the lastmillion years the climate has oscillated betweenglacial and interglacial conditions at about 100000-year intervals Global fluctuations in climate wereexperienced locally in the Galaacutepagos and elsewherein tropical America This has been revealed by theisotopic oxygen signatures of temperature in Andean ice cores (Seltzer et al 2002) by coral coresin Galaacutepagos (Dunbar et al 1994) and by pollencores in Galaacutepagos (Colinvaux 1972 1984) and incontinental South and Central American lakes(Bush et al 1992)

Most of the contemporary finches evolved inthe last million years so it is important to knowwhat happened during these cycles The two majoreffects of glacialndashinterglacial cycles were the de-pression of temperatures and of sea level relative to contemporary levels The last Ice Agecooling resulted in a drop of 3degC to 4degC in theequatorial Pacific reaching a minimum about21000 years ago (Kerr 2001) The previous deglacia-tion about 130000 years ago was associated witha drop of 2degC to 6degC (Tudhope et al 2001) Sea levelfell with the temperature The decline was gradualfrom the current level (about 120000 years ago) toabout 60 meters (m) lower (about 30000 yearsago) then an abrupt further decrease occurred to

about 125 m below the current level (Lambeck and Chappell2001) As a consequence islands were larger and distances between them were shorter Thus both temperature and sealevel were usually lower and never much higher than they aretoday

The food of finchesmdashplants and arthropods the latterfeeding on the plants and on each othermdashmust have beenaffected by these geophysical and climatic changes Firstnew species of plants and arthropods would have arrivedby immigration We do not know when this happened or which species were involved For Galaacutepagos unlikeHawaii (eg Givnish 1998 Wright et al 2000) there are nomolecular phylogenies of plants to help in reconstructingpaleofloras and the phylogenies of insects are too scarceto be useful (Finston and Peck 1997 Sequeira et al 2000)That situation needs to be rectified Second other speciesperhaps influenced by the immigrants would have become extinct Severe and extensive droughts would have been particularly crucial and cruel times for many organisms including finches Third the temperature- andmoisture-dependent altitudinal zonation of plants wouldhave shifted upward and downward at different timeshence the highest and lowest habitats would have beenmost vulnerable to elimination as noted elsewhere (Prodonet al 2002) Plant distributions would have changed acrossthe archipelago

972 BioScience bull October 2003 Vol 53 No 10

Plenary

Figure 7 The accumulation of species of Darwinrsquos finches with timeback-calculated from the estimated ages (in millions of years or MY) ofcontemporary species in the absence of known extinctions The accumu-lation of species parallels the accumulation of islands with time as de-termined from estimations of island age and elevation in relation to sealevel More islands provide more conditions for speciation to occur andspecies to persist From Grant (2001)

The evidence of a change in the upland forests is the rel-ative scarcity of endemic plants (Johnson and Raven 1973)The evidence of a change in the lowest zone is the anomalousoccurrence of plants on some islands with apparently un-suitable climates and soil For example the tree Erythrina velu-tina occurs at mid elevations on the high islands of Santa CruzSantiago and Isabela A single tree of this species occurs onthe low arid island of Genovesa and fewer than a dozen oc-cur on the low arid and even more remote island of WolfSimilarly a few Zanthoxylum fagara trees on Santa Cruz andSan Cristoacutebal occur close to the coast These may be theremnants of much larger populations on these islands undercooler wetter or less seasonally arid conditions than those thatprevail today Temperatures and precipitation changedmarkedly from one state to another long enough (gt 1000years Colinvaux 1972 Riedinger et al 2002) for vegetationzones to shift (Woodward 1987) On some occasions how-ever significant changes in temperature occurred in as shorta time as a hundred years perhaps less (Bush et al 1992)Large abrupt and widespread climate changes with majorconsequences for the biota have occurred repeatedly in thepast when the Earth system was forced across thresholds(Alley et al 2003)

The macroevolutionary pattern and the buildup ofcomplex communities from simple ones In view of the strong environmental changes in the archi-pelago it is scarcely likely that all current ecological niches wereavailable when the finchesrsquo ancestors arrived Rather thenumbers and types of opportunities for finch evolution increased as the number of islands increased and the climate and vegetation changed According to this view theadaptive radiation and the buildup of species-rich commu-nities were largely molded by environmental change theparticular species originated when they did and no earlierin response to particular environments prevailing then

When the first finches arrived on Galaacutepagos they mayhave encountered a climate and vegetation more like those ofmodern-day Cocos Island warmer wetter and more humidconditions fostering rain forest from the coast to the islandpeaks (Grant 1999 Grant and Grant 2002b) Cocos Island hastemperatures similar to those of the coastal habitats in theGalaacutepagos and rainfall equivalent to what the Galaacutepagosnow receives in an El Nintildeo year at high elevations Reason-ing from the evidence of modern finches we suggest the ini-tial evolutionary pathway taken by the finches was toward theexploitation of small arthropods and of nectar and pollenfrom small flowers in a rain forestndashlike environment

The radiation began when the initial species split into twolineages of Certhidea warbler finches (figure 8) after the ini-tial pathway had been taken One group of populations(Certhidea olivacea) inhabits moist upland forest and theother group (Certhidea fusca) occupies lower habitats onother mainly low islands Remarkably despite their longseparation the two groups have retained similar mate recog-nition systems and for that reason we refer to them as lineages

October 2003 Vol 53 No 10 bull BioScience 973

Plenary

Figure 8 Reconstruction of finch phylogeny based on microsatellite DNA Horizontal branch lengths are pro-portional to units of genetic distance (GST) as indicated bythe scale Numbers refer to percentage bootstrap supportfor the nodes by two methods Mean weights are given onthe right together with symbols of male plumage fullyblack partially black or brown or green Alternative reconstructions that use morphology allozymes or mito-chondrial DNA are similar differing in relatively smalldetails Species from top to bottom Geospiza fuliginosaGeospiza fortis Geospiza magnirostris Geospiza scandensGeospiza conirostris Geospiza difficilis Camarhynchusparvulus Camarhynchus psittacula Camarhynchus pauperCamarhynchus pallida Platyspiza crassirostris Certhideafusca Pinaroloxias inornata and Certhidea olivacea FromPetren and colleagues (1999)

and not species (Grant and Grant 2002b) Another remark-able feature is that they have remained relatively undifferen-tiated in morphology ecology and behavior This is not expected on the basis of the view that niches were varied plen-tiful and evolutionarily within reach at that time Howeverwe must acknowledge the possibility perhaps even the prob-ability that extinction has robbed us of other species that wereformed then The morphological similarity of these finchescontrasting with their distinctness from continental rela-tives argues for an early adaptation to an unusual niche

One of the warbler finch lineages gave rise to all otherfinch species Early products of the diversification were the veg-etarian finch (Platyspiza crassirostris) the Cocos finch(Pinaroloxias inornata) on either Galaacutepagos or Cocos Island(Grant and Grant 2002b) and the sharp-beaked groundfinch (G difficilis) The most recent products were a group ofground finch species (Geospiza) and a group of tree finchspecies (Camarhynchus and Cactospiza) (figure 8)

Effects of environmental change have left a different his-torical imprint on the older species Populations of G diffi-cilis differ strongly in morphology and ecology to a degree un-matched by all other and younger species in the genusGeospiza and by the warbler finches that preceded themSome G difficilis have persisted in Zanthoxylum forest at midand upper elevations which we believe to be old and others have entered arid lowland habitat perhaps when theZanthoxylum forest gradually disappeared from low islandsas the climate changed This may have been the first step ofthe radiation of ground finches In contrast to the G difficilispopulations populations of the vegetarian finch are mor-phologically and ecologically very similar Limited genetic data(Petren et al 1999) suggest that they separated from each otherrecently This is surprising as it is not expected from the ageof the species or from the presumed stability of its mid-elevation transition zone habitat The vegetarian finch mayhave become restricted to one or two islands and other pop-ulations or even related species may have become extinctin response to one of the recent extreme fluctuations in climate Its vegetarian diet may have made it vulnerable intimes of drought and competition with other species may havebeen an additional factor

The importance of environmental change in speciation isfurther suggested by the fact that in the last million years newspecies evolved in the habitats most vulnerable to changeGeospiza were added to lowland habitats and Camarhynchuswere added to the upland humid forest The change in climatetoward seasonal aridity and the development of arid lowlandhabitat provided the opportunity for a new granivorous wayof finch life now adopted by Geospiza species Some of thesemodern species may have contributed to the extinction ofolder ones through competitive superiority in a changingenvironment This is one possible interpretation of the contrast between the morphological distinctness of the threeolder groups Certhidea Platyspiza and G difficilis and themorphological similarity of species in the younger generaCamarhynchus Cactospiza and Geospiza

These ideas on speciation and extinction together with ob-servations of the colonization of Daphne Major by G magni-rostris (Grant et al 2001) suggest that periods of expansionsuch as the one in progress are preceded and followed by periods of range contraction and extinction caused by envi-ronmental change Distributions of habitats sea level islandand population sizes and degrees of isolation provide favorable conditions for divergence of small populations inisolation at some times and for dispersal mixing establish-ment of sympatry and hybridization at others The buildupof complex communities from simple ones is not smooth con-tinuous and regular but a process of gains and losses with anet accumulation of species over the long term

ConclusionsAccording to the standard allopatric model speciation beginswith the establishment of a new population continues withthe divergence of that population from its parent populationand is completed when members of two diverged populationscan coexist in sympatry without interbreeding We stand a virtually negligible chance of observing the whole process under natural circumstances Nevertheless it is possible tomake relevant observations in nature of all steps in theprocess We have described the strong role played by envi-ronmental change at each of the three steps in the speciationof Darwinrsquos finches The full adaptive radiation was pro-duced by a repetition of these steps each with a different product under somewhat different circumstances The challenge now is to account for the differences in terms of pastenvironments without the help of fossils of finches or ofother members of the biota We have sketched a frameworkfor doing this by using molecular genetic information to estimate the finch phylogeny and using geological and climaticinformation to reconstruct Galaacutepagos environments in thepast 2 million to 3 million years A better understanding ofenvironmental change on this time scale will help to explainwhy 14 species were formed what their sequence of origin wasand why they evolved their particular unique features Theremay be more history to uncover in finch DNA if only we canwork out how to read it

Acknowledgments We thank Ken Petren for figure 8 and Phil Hedrick FritzTrillmich and an anonymous reviewer for comments on themanuscript We are grateful to the Galaacutepagos National Parkand the Charles Darwin Research Station for permission andlogistical support for the fieldwork and to the National Sciences and Engineering Research Council of Canada and theNational Science Foundation for funding support

References citedAbbott I Abbott LK Grant PR 1977 Comparative ecology of Galaacutepagos

ground finches (Geospiza Gould) Evaluation of the importance of floris-tic diversity and interspecific competition Ecological Monographs 47151ndash184

Alley RB et al 2003 Abrupt climate change Science 299 2005ndash2010

974 BioScience bull October 2003 Vol 53 No 10

Plenary

Bowman RI 1961 Morphological Differentiation and Adaptation in theGalaacutepagos Finches University of California Publications in ZoologyVol 58 Berkeley University of California Press

mdashmdashmdash 1983 The songs of Darwinrsquos finches Pages 237ndash537 in Bowman RILeviton AE Berson M eds Galaacutepagos Organisms San Francisco Amer-ican Association for the Advancement of Science Pacific Division

Burns KJ Hackett SJ Klein NK 2002 Phylogenetic relationships andmorphological diversity in Darwinrsquos finches and their relatives Evo-lution 56 1240ndash1252

Bush MB Piperno DR Colinvaux PA DeOleveira PE Krissek LA Miller MCRowe WE 1992 A 14300-yr paleoecological profile of a lowland tropi-cal lake in Panama Ecological Monographs 62 251ndash275

Cane MA Molnar P 2001 Closing of the Indonesian seaway as a precursorto east African aridification around 3ndash4 million years ago Nature 411157ndash162

Colinvaux PA 1972 Climate and the Galaacutepagos Islands Nature 240 17ndash20mdashmdashmdash 1984 The Galaacutepagos climate Present and past Pages 55ndash69 in

Perry R ed Galaacutepagos Oxford (United Kingdom) Pergamon PressDarwin CR 1842 Journal of Researches into the Geology and Natural

History of the Various Countries Visited during the Voyage of H M SBeagle under the Command of Captain FitzRoy RN from 1832 to 1836London Henry Colburn

Dunbar RB Wellington GM Colgan MW Glynn PW 1994 Eastern Pacificsea surface temperature since 1600 AD The O18 record of climate vari-ability in Galaacutepagos corals Paleoceanography 9 291ndash315

Finston TL Peck SB 1997 Genetic differentiation and speciation in Stomion(Coleoptera Tenebrionidae) Flightless beetles of the Galaacutepagos IslandsEcuador Biological Journal of the Linnean Society 61 243ndash266

Givnish TJ 1998Adaptive plant evolution on islands Classical patterns mole-cular data new insights Pages 281ndash304 in Grant PR ed Evolution on Islands Oxford (United Kingdom) Oxford University Press

Grant BR Grant PR 1989 Evolutionary Dynamics of a Natural PopulationThe Large Cactus Finch of the Galaacutepagos Chicago University of ChicagoPress

mdashmdashmdash 1996 Cultural inheritance of song and its role in the evolution ofDarwinrsquos finches Evolution 50 2471ndash2487

Grant PR 1999 Ecology and Evolution of Darwinrsquos Finches Princeton (NJ)Princeton University Press

mdashmdashmdash 2001 Reconstructing the evolution of birds on islands 100 years ofresearch Oikos 92 385ndash403

Grant PR Grant BR 1998 Speciation and hybridization in island birds Pages142ndash162 in Grant PR ed Evolution on Islands Oxford (United Kingdom)Oxford University Press

mdashmdashmdash 2002a Unpredictable evolution in a 30-year study of Darwinrsquosfinches Science 296 707ndash711

mdashmdashmdash 2002b Adaptive radiation of Darwinrsquos finches American Scientist90 131ndash139

Grant PR Grant BR Petren K 2001 The founding of a new population by a single pair of individuals Establishment selection and populationexpansion Genetica 112113 359ndash382

Huxley JS 1942 Evolution The Modern Synthesis London Allen and Unwin

Johnson MP Raven PH 1973 Species number and endemism The Galaacutepagosarchipelago revisited Science 179 893ndash895

Keller LF Grant PR Grant BR Petren K 2001 Heritability of morphologi-cal traits in Darwinrsquos finches Misidentified paternity and maternal effects Heredity 87 325ndash336

Kerr RA 2001 The tropics return to the climate system Science 292 660ndash661Lack D 1947 Darwinrsquos finches Cambridge (United Kingdom) Cambridge

University PressLambeck K Chappell J 2001 Sea level change through the last glacial cycle

Science 292 679ndash686Mayr E 1942 Systematics and the Origin of Species New York Columbia

University Press

Newton I 1967 The adaptive variation and feeding ecology of some British

finches Ibis 109 33ndash98

Petren K Grant BR Grant PR 1999 A phylogeny of Darwinrsquos finches based

on microsatellite DNA length variation Proceedings of the Royal Soci-

ety of London B 266 321ndash329

Price T Lovette IJ Bermingham E Gibbs HL Richman AD 2000 The

imprint of history on communities of North American and Asian

warblers American Naturalist 156 354ndash367

Prodon R Thibault J-C Dejaifve P-A 2002 Expansion vs compression of

bird altitudinal ranges on a Mediterranean island Ecology 83 1294ndash1306

Ratcliffe LM Grant PR 1983a Species recognition in Darwinrsquos finches

(Geospiza Gould) I Discrimination by morphological cues Animal

Behaviour 31 1139ndash1153

mdashmdashmdash 1983b Species recognition in Darwinrsquos finches (Geospiza Gould)

II Geographic variation in mate preference Animal Behaviour 31

1154ndash1165

mdashmdashmdash 1985 Species recognition in Darwinrsquos finches (Geospiza Gould) III

Male responses to playback of different song types dialects and hetero-

specific songs Animal Behaviour 33 290ndash307

Richards OW 1948 Species formation in islands (review of Darwinrsquos Finches

by Lack D) Journal of Animal Ecology 17 83ndash84

Riedinger MA Steinitz-Kannan M Last WM Brenner M 2002 A ~6100 14C

yr record of El Nintildeo activity from the Galaacutepagos Islands Journal of

Paleontology 27 1ndash7

Sato A OrsquoHuigin C Figueroa F Grant PR Grant BR Tichy H Klein J 1999

Phylogeny of Darwinrsquos finches as revealed by mtDNA sequences

Proceedings of the National Academy of Sciences 96 5101ndash5106

Schluter D 2000 The Ecology of Adaptive Radiations Oxford (United King-

dom) Oxford University Press

Schluter D Grant PR 1984 Determinants of morphological patterns in

communities of Darwinrsquos finches American Naturalist 123 175ndash196

Seltzer GO Rodbell DT Baker PA Fritz SC Tapia PM Rowe HD Dunbar

RB 2002 Early warming of tropical South America at the last glacialndash

interglacial transition Science 296 1685ndash1686

Sequeira AS Lanteri AA Scataglini MA Confalonieri VA Farrell BD 2000

Are flightless Galapaganus weevils older than the Galaacutepagos Islands they

inhabit Heredity 85 20ndash29

Simpson GG 1944 Tempo and Mode in Evolution New York Columbia

University Press

Swarth HS 1931 The avifauna of the Galaacutepagos islands Occasional Papers

of the California Academy of Sciences 18 1ndash299

mdashmdashmdash 1934 The bird fauna of the Galaacutepagos islands in relation to species

formation Biological Reviews 9 213ndash234

Tudhope AW Chilcott CP McCulloch MT Cook ER Chappell J Ellam RM

Lea DW Lough JM Shimmield GB 2001 Variability in the El

NintildeondashSouthern Oscillation through a glacialndashinterglacial cycle Science

291 1511ndash1517

Vincek V OrsquoHuigin C Satta Y Takahata N Boag PT Grant PR Grant BR

Klein J 1996 How large was the founding population of Darwinrsquos

finches Proceedings of the Royal Society of London B 264 111ndash118

Woodward FI 1987 Climate and Plant Distribution London Cambridge Uni-

versity Press

Wright SD Young CG Dawson JW Whittaker DJ Gardner RC 2000

Riding the ice age El Nintildeo Pacific biogeography and evolution of

Metrosideros subg Metrosideros (Myrtaceae) inferred from nuclear

ribosomal DNA Proceedings of the National Academy of Sciences 97

4110ndash4123

October 2003 Vol 53 No 10 bull BioScience 975

Plenary

experiments with captive birds (Bowman 1983) supple-mented by field observations of songs of offspring parentsand even grandparents (Grant and Grant 1989 1996) Onlymales sing an advertising song it is simple and is sung un-altered throughout life which may be as long as 16 years Mostsons sing the same song subtype as their fathers while a minority sing a different song subtype that is sung by othermale members of the same population Thus song is acquired through learning early in life in a process that resembles imprinting it is generally acquired from fathers during the period of parental dependence in associationwith parental morphology By their pairing patterns femalesgive evidence of learning song at the same time and from thesame sources

Rare exceptions to these rules provide additional valuableinformation on the role of learning and its bearing on thequestion of what keeps species apart Once again environ-mental change associated with an El Nintildeo event has pro-vided crucial information Medium ground finches and cactus finches hybridize rarely Before 1983 the hybrids diedwithout breeding at a time when most of the ldquopurerdquo speciesproduced in the same years also died without breeding TheEl Nintildeo event of 1983 resulting in an abundance of smallseeds altered the environment in a way that was favorable tothe survival of the hybrids The hybrids that were producedin 1983 backcrossed to medium ground finches in 1987 andothers that were produced in 1987 backcrossed to cactusfinches in 1991 The direction of backcrossing differed becausein 1983 the hybridizing male was a cactus finch that sang amedium ground finch song whereas in 1987 the hybridizingmales were cactus finches that sang cactus finch songsSons of all families sang the same song as their fathers anddaughters in each case mated with males that sang the samesong type as their fathers

Hybridization is sometimes the re-sult of heterospecific singing throughapparent misimprinting The causesof misimprinting and hybridizationare idiosyncratic and difficult to determine They include extra-pairmating interspecific takeover of nestswith eggs and dominant singing of aclose neighbor Ecologically the sig-nificant feature is a change in the environment that has facilitated theintrogression of genes F1 hybrid andbackcross survival is not intrinsicallylower than the survival of the parentalspecies and there is no sign of dimin-ished fitness when hybrids breed Infact in the 1990s and up to the presentthe flow of genes from the mediumground finch to the cactus finch population has contributed to a decrease in mean body size and ablunter beak morphology of cactus

finches (Grant and Grant 2002a) The barrier to gene exchangeerected by song differences has been breached and environ-mental change appears to have been the most important factor

To summarize the coexistence of finch species is facilitatedby divergence in beak morphology and song Beaks divergeunder natural selection but why songs diverge is less clear Cul-tural drift a process of random change in culturally trans-mitted (learned) traits is probably involved and sexual se-lection may be involved as well The end point of speciationis the complete absence of gene exchange Many if not all co-existing populations of Darwinrsquos finches have not quitereached that point although they function as species by re-maining distinct even in the face of occasional gene exchangeThis offers two important lessons First species diverge in matepreferences before genetic incompatibilities evolve Seconddifferent populations can function as biological species beforethey would be recognized as species solely on the basis of ge-netic distinctness

History The initial colonizationThe present is known the past is inferred To understand thepast of Darwinrsquos finches the first question that needs to be ad-dressed is when the radiation began because the answer setsthe boundary on relevant Galaacutepagos history In the absenceof fossils genes are our best source of information aboutthis history (Price et al 2000) The closest genetic relatives ofDarwinrsquos finches on the South American continent in Central America and in the Caribbean are a group of seed-eaters (Tiaris and relatives) allied to tanagers (Sato et al 1999Burns et al 2002) Darwinrsquos finches diverged from them in thelast 2 million or possibly 3 million years according to calcu-lations based on an assumed molecular clock applied to mitochondrial DNA and allozyme data (Grant 1999) The

970 BioScience bull October 2003 Vol 53 No 10

Plenary

Daphne Major a volcanic remnant in the Galaacutepagos archipelago is the site of theauthorsrsquo long-term study of evolution in Darwinrsquos finches Photograph David Parer

recent origin of Darwinrsquos finches helps to explain why theyare still capable of exchanging genes

Divergence from their mainland relatives began when thefinches colonized the Galaacutepagos islands Situated 900 kmfrom continental Ecuador on the Nazca plate and moving imperceptibly toward the mainland the archipelago is a re-mote place for birds to visit Colonization is an improbableevent Nevertheless according to one calculation ancestralDarwinrsquos finches arrived in a moderately large flock (or several small ones) Modern finches are genetically diverse atthe major histocompatibility complex locus and Vincek andcolleagues (1996) used the allelic diversity of class II genes to calculate that the original colonists numbered at least 30individuals

Improbable events may arise in improbable and hencerare circumstances What might those circumstances havebeen Any answer must be speculative even if rooted in current phenomena The circumstances that promote dispersalof contemporary finches within the Galaacutepagos archipelago are(a) high finch density following prolific breeding in El Nintildeoyears and (b) forest fires caused by volcanic eruptions If the

unusual dispersal activity from the mainland followed sim-ilar patterns it may have been induced by unusual volcanicactivity in the Andes Burning of the forests in one suchepisode would be followed by the establishment of large areas of shrub and secondary growth With the buildup offinch populations in secondary forest and another round offires and burning large numbers of finches and other birdsin coastal regions would fly out to sea to escape the flames andsmoke The colonists would be helped if mats of vegetationwere rafted out to sea by strong El Nintildeondashassociated floodingfrom the Guayas River Global temperatures were warmer 2million to 3 million years ago and permanent El Nintildeo con-ditions are thought to have occurred until about that time(Cane and Molnar 2001) The most marked shift in climateseems to have occurred at 24 million to 25 million years agoThis may be when the ancestral Darwinrsquos finches arrived

Relevant history of the GalaacutepagosTo understand the past the second question that needs to beaddressed is how the islands have changed if at all since thefirst finches arrived The simplest possible answer would be

October 2003 Vol 53 No 10 bull BioScience 971

Plenary

Figure 6 Changes in the beak size and shape of Geospiza fortis and Geospiza scandens on the islandof Daphne Major Mean trait values for each year are indicated by solid circles and 95 confidenceintervals are shown by vertical bars above and below the mean In the absence of change the meansshould remain within the 95 confidence intervals (horizontal broken lines) of the mean estimatesfrom the 1973 samples PC refers to principal component obtained from a principal componentsanalysis of size and shape variables From Grant and Grant (2002a)

PC2 b

eak

shap

ePC

1 b

eak

shap

e

that the islands have always been much as they are today interms of geography climate and vegetation If this is correctthe finchesrsquo adaptive radiation can be viewed as a process ofdifferentiation that results in the occupancy of all ecologicalniches present at the outsetmdashrather like filling empty boxesone species per box Indeed this is how early writers on thesubject viewed the radiation of the finches stressing the absence or scarcity of competitors in the boxes as a facilitat-ing factor (Huxley 1942 Simpson 1944 Lack 1947 Grant1999) In the modern version the boxes are replaced by adap-tive peaks in a more or less fixed landscape This view impliesthat diversification is rapid early in the radiation and thenslows down as ecological opportunities diminish Some radiations of other organisms elsewhere conform to this pattern (Schluter 2000) However taken at face value thephylogeny of Darwinrsquos finches shows exactly the oppositepattern a slow start followed by recent rapid diversification(figure 7) The species occupy adaptive peaks but the fixityof the ecological landscape that allowed them to do so isquestionable

In fact the islands and their inhabitants have changedradically Three million years ago there were far fewer islands than today perhaps only five (Grant and Grant 1998)The number of islands increased as a result of volcanic activitycentered on and near a hotspot beneath the western island of Fernandina Climate changed as well The average air

temperature declined but more important thanthis the worldrsquos climate underwent a sharp transi-tion 275 million years ago with the abrupt onset of glaciation (Cane and Molnar 2001) In the lastmillion years the climate has oscillated betweenglacial and interglacial conditions at about 100000-year intervals Global fluctuations in climate wereexperienced locally in the Galaacutepagos and elsewherein tropical America This has been revealed by theisotopic oxygen signatures of temperature in Andean ice cores (Seltzer et al 2002) by coral coresin Galaacutepagos (Dunbar et al 1994) and by pollencores in Galaacutepagos (Colinvaux 1972 1984) and incontinental South and Central American lakes(Bush et al 1992)

Most of the contemporary finches evolved inthe last million years so it is important to knowwhat happened during these cycles The two majoreffects of glacialndashinterglacial cycles were the de-pression of temperatures and of sea level relative to contemporary levels The last Ice Agecooling resulted in a drop of 3degC to 4degC in theequatorial Pacific reaching a minimum about21000 years ago (Kerr 2001) The previous deglacia-tion about 130000 years ago was associated witha drop of 2degC to 6degC (Tudhope et al 2001) Sea levelfell with the temperature The decline was gradualfrom the current level (about 120000 years ago) toabout 60 meters (m) lower (about 30000 yearsago) then an abrupt further decrease occurred to

about 125 m below the current level (Lambeck and Chappell2001) As a consequence islands were larger and distances between them were shorter Thus both temperature and sealevel were usually lower and never much higher than they aretoday

The food of finchesmdashplants and arthropods the latterfeeding on the plants and on each othermdashmust have beenaffected by these geophysical and climatic changes Firstnew species of plants and arthropods would have arrivedby immigration We do not know when this happened or which species were involved For Galaacutepagos unlikeHawaii (eg Givnish 1998 Wright et al 2000) there are nomolecular phylogenies of plants to help in reconstructingpaleofloras and the phylogenies of insects are too scarceto be useful (Finston and Peck 1997 Sequeira et al 2000)That situation needs to be rectified Second other speciesperhaps influenced by the immigrants would have become extinct Severe and extensive droughts would have been particularly crucial and cruel times for many organisms including finches Third the temperature- andmoisture-dependent altitudinal zonation of plants wouldhave shifted upward and downward at different timeshence the highest and lowest habitats would have beenmost vulnerable to elimination as noted elsewhere (Prodonet al 2002) Plant distributions would have changed acrossthe archipelago

972 BioScience bull October 2003 Vol 53 No 10

Plenary

Figure 7 The accumulation of species of Darwinrsquos finches with timeback-calculated from the estimated ages (in millions of years or MY) ofcontemporary species in the absence of known extinctions The accumu-lation of species parallels the accumulation of islands with time as de-termined from estimations of island age and elevation in relation to sealevel More islands provide more conditions for speciation to occur andspecies to persist From Grant (2001)

The evidence of a change in the upland forests is the rel-ative scarcity of endemic plants (Johnson and Raven 1973)The evidence of a change in the lowest zone is the anomalousoccurrence of plants on some islands with apparently un-suitable climates and soil For example the tree Erythrina velu-tina occurs at mid elevations on the high islands of Santa CruzSantiago and Isabela A single tree of this species occurs onthe low arid island of Genovesa and fewer than a dozen oc-cur on the low arid and even more remote island of WolfSimilarly a few Zanthoxylum fagara trees on Santa Cruz andSan Cristoacutebal occur close to the coast These may be theremnants of much larger populations on these islands undercooler wetter or less seasonally arid conditions than those thatprevail today Temperatures and precipitation changedmarkedly from one state to another long enough (gt 1000years Colinvaux 1972 Riedinger et al 2002) for vegetationzones to shift (Woodward 1987) On some occasions how-ever significant changes in temperature occurred in as shorta time as a hundred years perhaps less (Bush et al 1992)Large abrupt and widespread climate changes with majorconsequences for the biota have occurred repeatedly in thepast when the Earth system was forced across thresholds(Alley et al 2003)

The macroevolutionary pattern and the buildup ofcomplex communities from simple ones In view of the strong environmental changes in the archi-pelago it is scarcely likely that all current ecological niches wereavailable when the finchesrsquo ancestors arrived Rather thenumbers and types of opportunities for finch evolution increased as the number of islands increased and the climate and vegetation changed According to this view theadaptive radiation and the buildup of species-rich commu-nities were largely molded by environmental change theparticular species originated when they did and no earlierin response to particular environments prevailing then

When the first finches arrived on Galaacutepagos they mayhave encountered a climate and vegetation more like those ofmodern-day Cocos Island warmer wetter and more humidconditions fostering rain forest from the coast to the islandpeaks (Grant 1999 Grant and Grant 2002b) Cocos Island hastemperatures similar to those of the coastal habitats in theGalaacutepagos and rainfall equivalent to what the Galaacutepagosnow receives in an El Nintildeo year at high elevations Reason-ing from the evidence of modern finches we suggest the ini-tial evolutionary pathway taken by the finches was toward theexploitation of small arthropods and of nectar and pollenfrom small flowers in a rain forestndashlike environment

The radiation began when the initial species split into twolineages of Certhidea warbler finches (figure 8) after the ini-tial pathway had been taken One group of populations(Certhidea olivacea) inhabits moist upland forest and theother group (Certhidea fusca) occupies lower habitats onother mainly low islands Remarkably despite their longseparation the two groups have retained similar mate recog-nition systems and for that reason we refer to them as lineages

October 2003 Vol 53 No 10 bull BioScience 973

Plenary

Figure 8 Reconstruction of finch phylogeny based on microsatellite DNA Horizontal branch lengths are pro-portional to units of genetic distance (GST) as indicated bythe scale Numbers refer to percentage bootstrap supportfor the nodes by two methods Mean weights are given onthe right together with symbols of male plumage fullyblack partially black or brown or green Alternative reconstructions that use morphology allozymes or mito-chondrial DNA are similar differing in relatively smalldetails Species from top to bottom Geospiza fuliginosaGeospiza fortis Geospiza magnirostris Geospiza scandensGeospiza conirostris Geospiza difficilis Camarhynchusparvulus Camarhynchus psittacula Camarhynchus pauperCamarhynchus pallida Platyspiza crassirostris Certhideafusca Pinaroloxias inornata and Certhidea olivacea FromPetren and colleagues (1999)

and not species (Grant and Grant 2002b) Another remark-able feature is that they have remained relatively undifferen-tiated in morphology ecology and behavior This is not expected on the basis of the view that niches were varied plen-tiful and evolutionarily within reach at that time Howeverwe must acknowledge the possibility perhaps even the prob-ability that extinction has robbed us of other species that wereformed then The morphological similarity of these finchescontrasting with their distinctness from continental rela-tives argues for an early adaptation to an unusual niche

One of the warbler finch lineages gave rise to all otherfinch species Early products of the diversification were the veg-etarian finch (Platyspiza crassirostris) the Cocos finch(Pinaroloxias inornata) on either Galaacutepagos or Cocos Island(Grant and Grant 2002b) and the sharp-beaked groundfinch (G difficilis) The most recent products were a group ofground finch species (Geospiza) and a group of tree finchspecies (Camarhynchus and Cactospiza) (figure 8)

Effects of environmental change have left a different his-torical imprint on the older species Populations of G diffi-cilis differ strongly in morphology and ecology to a degree un-matched by all other and younger species in the genusGeospiza and by the warbler finches that preceded themSome G difficilis have persisted in Zanthoxylum forest at midand upper elevations which we believe to be old and others have entered arid lowland habitat perhaps when theZanthoxylum forest gradually disappeared from low islandsas the climate changed This may have been the first step ofthe radiation of ground finches In contrast to the G difficilispopulations populations of the vegetarian finch are mor-phologically and ecologically very similar Limited genetic data(Petren et al 1999) suggest that they separated from each otherrecently This is surprising as it is not expected from the ageof the species or from the presumed stability of its mid-elevation transition zone habitat The vegetarian finch mayhave become restricted to one or two islands and other pop-ulations or even related species may have become extinctin response to one of the recent extreme fluctuations in climate Its vegetarian diet may have made it vulnerable intimes of drought and competition with other species may havebeen an additional factor

The importance of environmental change in speciation isfurther suggested by the fact that in the last million years newspecies evolved in the habitats most vulnerable to changeGeospiza were added to lowland habitats and Camarhynchuswere added to the upland humid forest The change in climatetoward seasonal aridity and the development of arid lowlandhabitat provided the opportunity for a new granivorous wayof finch life now adopted by Geospiza species Some of thesemodern species may have contributed to the extinction ofolder ones through competitive superiority in a changingenvironment This is one possible interpretation of the contrast between the morphological distinctness of the threeolder groups Certhidea Platyspiza and G difficilis and themorphological similarity of species in the younger generaCamarhynchus Cactospiza and Geospiza

These ideas on speciation and extinction together with ob-servations of the colonization of Daphne Major by G magni-rostris (Grant et al 2001) suggest that periods of expansionsuch as the one in progress are preceded and followed by periods of range contraction and extinction caused by envi-ronmental change Distributions of habitats sea level islandand population sizes and degrees of isolation provide favorable conditions for divergence of small populations inisolation at some times and for dispersal mixing establish-ment of sympatry and hybridization at others The buildupof complex communities from simple ones is not smooth con-tinuous and regular but a process of gains and losses with anet accumulation of species over the long term

ConclusionsAccording to the standard allopatric model speciation beginswith the establishment of a new population continues withthe divergence of that population from its parent populationand is completed when members of two diverged populationscan coexist in sympatry without interbreeding We stand a virtually negligible chance of observing the whole process under natural circumstances Nevertheless it is possible tomake relevant observations in nature of all steps in theprocess We have described the strong role played by envi-ronmental change at each of the three steps in the speciationof Darwinrsquos finches The full adaptive radiation was pro-duced by a repetition of these steps each with a different product under somewhat different circumstances The challenge now is to account for the differences in terms of pastenvironments without the help of fossils of finches or ofother members of the biota We have sketched a frameworkfor doing this by using molecular genetic information to estimate the finch phylogeny and using geological and climaticinformation to reconstruct Galaacutepagos environments in thepast 2 million to 3 million years A better understanding ofenvironmental change on this time scale will help to explainwhy 14 species were formed what their sequence of origin wasand why they evolved their particular unique features Theremay be more history to uncover in finch DNA if only we canwork out how to read it

Acknowledgments We thank Ken Petren for figure 8 and Phil Hedrick FritzTrillmich and an anonymous reviewer for comments on themanuscript We are grateful to the Galaacutepagos National Parkand the Charles Darwin Research Station for permission andlogistical support for the fieldwork and to the National Sciences and Engineering Research Council of Canada and theNational Science Foundation for funding support

References citedAbbott I Abbott LK Grant PR 1977 Comparative ecology of Galaacutepagos

ground finches (Geospiza Gould) Evaluation of the importance of floris-tic diversity and interspecific competition Ecological Monographs 47151ndash184

Alley RB et al 2003 Abrupt climate change Science 299 2005ndash2010

974 BioScience bull October 2003 Vol 53 No 10

Plenary

Bowman RI 1961 Morphological Differentiation and Adaptation in theGalaacutepagos Finches University of California Publications in ZoologyVol 58 Berkeley University of California Press

mdashmdashmdash 1983 The songs of Darwinrsquos finches Pages 237ndash537 in Bowman RILeviton AE Berson M eds Galaacutepagos Organisms San Francisco Amer-ican Association for the Advancement of Science Pacific Division

Burns KJ Hackett SJ Klein NK 2002 Phylogenetic relationships andmorphological diversity in Darwinrsquos finches and their relatives Evo-lution 56 1240ndash1252

Bush MB Piperno DR Colinvaux PA DeOleveira PE Krissek LA Miller MCRowe WE 1992 A 14300-yr paleoecological profile of a lowland tropi-cal lake in Panama Ecological Monographs 62 251ndash275

Cane MA Molnar P 2001 Closing of the Indonesian seaway as a precursorto east African aridification around 3ndash4 million years ago Nature 411157ndash162

Colinvaux PA 1972 Climate and the Galaacutepagos Islands Nature 240 17ndash20mdashmdashmdash 1984 The Galaacutepagos climate Present and past Pages 55ndash69 in

Perry R ed Galaacutepagos Oxford (United Kingdom) Pergamon PressDarwin CR 1842 Journal of Researches into the Geology and Natural

History of the Various Countries Visited during the Voyage of H M SBeagle under the Command of Captain FitzRoy RN from 1832 to 1836London Henry Colburn

Dunbar RB Wellington GM Colgan MW Glynn PW 1994 Eastern Pacificsea surface temperature since 1600 AD The O18 record of climate vari-ability in Galaacutepagos corals Paleoceanography 9 291ndash315

Finston TL Peck SB 1997 Genetic differentiation and speciation in Stomion(Coleoptera Tenebrionidae) Flightless beetles of the Galaacutepagos IslandsEcuador Biological Journal of the Linnean Society 61 243ndash266

Givnish TJ 1998Adaptive plant evolution on islands Classical patterns mole-cular data new insights Pages 281ndash304 in Grant PR ed Evolution on Islands Oxford (United Kingdom) Oxford University Press

Grant BR Grant PR 1989 Evolutionary Dynamics of a Natural PopulationThe Large Cactus Finch of the Galaacutepagos Chicago University of ChicagoPress

mdashmdashmdash 1996 Cultural inheritance of song and its role in the evolution ofDarwinrsquos finches Evolution 50 2471ndash2487

Grant PR 1999 Ecology and Evolution of Darwinrsquos Finches Princeton (NJ)Princeton University Press

mdashmdashmdash 2001 Reconstructing the evolution of birds on islands 100 years ofresearch Oikos 92 385ndash403

Grant PR Grant BR 1998 Speciation and hybridization in island birds Pages142ndash162 in Grant PR ed Evolution on Islands Oxford (United Kingdom)Oxford University Press

mdashmdashmdash 2002a Unpredictable evolution in a 30-year study of Darwinrsquosfinches Science 296 707ndash711

mdashmdashmdash 2002b Adaptive radiation of Darwinrsquos finches American Scientist90 131ndash139

Grant PR Grant BR Petren K 2001 The founding of a new population by a single pair of individuals Establishment selection and populationexpansion Genetica 112113 359ndash382

Huxley JS 1942 Evolution The Modern Synthesis London Allen and Unwin

Johnson MP Raven PH 1973 Species number and endemism The Galaacutepagosarchipelago revisited Science 179 893ndash895

Keller LF Grant PR Grant BR Petren K 2001 Heritability of morphologi-cal traits in Darwinrsquos finches Misidentified paternity and maternal effects Heredity 87 325ndash336

Kerr RA 2001 The tropics return to the climate system Science 292 660ndash661Lack D 1947 Darwinrsquos finches Cambridge (United Kingdom) Cambridge

University PressLambeck K Chappell J 2001 Sea level change through the last glacial cycle

Science 292 679ndash686Mayr E 1942 Systematics and the Origin of Species New York Columbia

University Press

Newton I 1967 The adaptive variation and feeding ecology of some British

finches Ibis 109 33ndash98

Petren K Grant BR Grant PR 1999 A phylogeny of Darwinrsquos finches based

on microsatellite DNA length variation Proceedings of the Royal Soci-

ety of London B 266 321ndash329

Price T Lovette IJ Bermingham E Gibbs HL Richman AD 2000 The

imprint of history on communities of North American and Asian

warblers American Naturalist 156 354ndash367

Prodon R Thibault J-C Dejaifve P-A 2002 Expansion vs compression of

bird altitudinal ranges on a Mediterranean island Ecology 83 1294ndash1306

Ratcliffe LM Grant PR 1983a Species recognition in Darwinrsquos finches

(Geospiza Gould) I Discrimination by morphological cues Animal

Behaviour 31 1139ndash1153

mdashmdashmdash 1983b Species recognition in Darwinrsquos finches (Geospiza Gould)

II Geographic variation in mate preference Animal Behaviour 31

1154ndash1165

mdashmdashmdash 1985 Species recognition in Darwinrsquos finches (Geospiza Gould) III

Male responses to playback of different song types dialects and hetero-

specific songs Animal Behaviour 33 290ndash307

Richards OW 1948 Species formation in islands (review of Darwinrsquos Finches

by Lack D) Journal of Animal Ecology 17 83ndash84

Riedinger MA Steinitz-Kannan M Last WM Brenner M 2002 A ~6100 14C

yr record of El Nintildeo activity from the Galaacutepagos Islands Journal of

Paleontology 27 1ndash7

Sato A OrsquoHuigin C Figueroa F Grant PR Grant BR Tichy H Klein J 1999

Phylogeny of Darwinrsquos finches as revealed by mtDNA sequences

Proceedings of the National Academy of Sciences 96 5101ndash5106

Schluter D 2000 The Ecology of Adaptive Radiations Oxford (United King-

dom) Oxford University Press

Schluter D Grant PR 1984 Determinants of morphological patterns in

communities of Darwinrsquos finches American Naturalist 123 175ndash196

Seltzer GO Rodbell DT Baker PA Fritz SC Tapia PM Rowe HD Dunbar

RB 2002 Early warming of tropical South America at the last glacialndash

interglacial transition Science 296 1685ndash1686

Sequeira AS Lanteri AA Scataglini MA Confalonieri VA Farrell BD 2000

Are flightless Galapaganus weevils older than the Galaacutepagos Islands they

inhabit Heredity 85 20ndash29

Simpson GG 1944 Tempo and Mode in Evolution New York Columbia

University Press

Swarth HS 1931 The avifauna of the Galaacutepagos islands Occasional Papers

of the California Academy of Sciences 18 1ndash299

mdashmdashmdash 1934 The bird fauna of the Galaacutepagos islands in relation to species

formation Biological Reviews 9 213ndash234

Tudhope AW Chilcott CP McCulloch MT Cook ER Chappell J Ellam RM

Lea DW Lough JM Shimmield GB 2001 Variability in the El

NintildeondashSouthern Oscillation through a glacialndashinterglacial cycle Science

291 1511ndash1517

Vincek V OrsquoHuigin C Satta Y Takahata N Boag PT Grant PR Grant BR

Klein J 1996 How large was the founding population of Darwinrsquos

finches Proceedings of the Royal Society of London B 264 111ndash118

Woodward FI 1987 Climate and Plant Distribution London Cambridge Uni-

versity Press

Wright SD Young CG Dawson JW Whittaker DJ Gardner RC 2000

Riding the ice age El Nintildeo Pacific biogeography and evolution of

Metrosideros subg Metrosideros (Myrtaceae) inferred from nuclear

ribosomal DNA Proceedings of the National Academy of Sciences 97

4110ndash4123

October 2003 Vol 53 No 10 bull BioScience 975

Plenary

recent origin of Darwinrsquos finches helps to explain why theyare still capable of exchanging genes

Divergence from their mainland relatives began when thefinches colonized the Galaacutepagos islands Situated 900 kmfrom continental Ecuador on the Nazca plate and moving imperceptibly toward the mainland the archipelago is a re-mote place for birds to visit Colonization is an improbableevent Nevertheless according to one calculation ancestralDarwinrsquos finches arrived in a moderately large flock (or several small ones) Modern finches are genetically diverse atthe major histocompatibility complex locus and Vincek andcolleagues (1996) used the allelic diversity of class II genes to calculate that the original colonists numbered at least 30individuals

Improbable events may arise in improbable and hencerare circumstances What might those circumstances havebeen Any answer must be speculative even if rooted in current phenomena The circumstances that promote dispersalof contemporary finches within the Galaacutepagos archipelago are(a) high finch density following prolific breeding in El Nintildeoyears and (b) forest fires caused by volcanic eruptions If the

unusual dispersal activity from the mainland followed sim-ilar patterns it may have been induced by unusual volcanicactivity in the Andes Burning of the forests in one suchepisode would be followed by the establishment of large areas of shrub and secondary growth With the buildup offinch populations in secondary forest and another round offires and burning large numbers of finches and other birdsin coastal regions would fly out to sea to escape the flames andsmoke The colonists would be helped if mats of vegetationwere rafted out to sea by strong El Nintildeondashassociated floodingfrom the Guayas River Global temperatures were warmer 2million to 3 million years ago and permanent El Nintildeo con-ditions are thought to have occurred until about that time(Cane and Molnar 2001) The most marked shift in climateseems to have occurred at 24 million to 25 million years agoThis may be when the ancestral Darwinrsquos finches arrived

Relevant history of the GalaacutepagosTo understand the past the second question that needs to beaddressed is how the islands have changed if at all since thefirst finches arrived The simplest possible answer would be

October 2003 Vol 53 No 10 bull BioScience 971

Plenary

Figure 6 Changes in the beak size and shape of Geospiza fortis and Geospiza scandens on the islandof Daphne Major Mean trait values for each year are indicated by solid circles and 95 confidenceintervals are shown by vertical bars above and below the mean In the absence of change the meansshould remain within the 95 confidence intervals (horizontal broken lines) of the mean estimatesfrom the 1973 samples PC refers to principal component obtained from a principal componentsanalysis of size and shape variables From Grant and Grant (2002a)

PC2 b

eak

shap

ePC

1 b

eak

shap

e

that the islands have always been much as they are today interms of geography climate and vegetation If this is correctthe finchesrsquo adaptive radiation can be viewed as a process ofdifferentiation that results in the occupancy of all ecologicalniches present at the outsetmdashrather like filling empty boxesone species per box Indeed this is how early writers on thesubject viewed the radiation of the finches stressing the absence or scarcity of competitors in the boxes as a facilitat-ing factor (Huxley 1942 Simpson 1944 Lack 1947 Grant1999) In the modern version the boxes are replaced by adap-tive peaks in a more or less fixed landscape This view impliesthat diversification is rapid early in the radiation and thenslows down as ecological opportunities diminish Some radiations of other organisms elsewhere conform to this pattern (Schluter 2000) However taken at face value thephylogeny of Darwinrsquos finches shows exactly the oppositepattern a slow start followed by recent rapid diversification(figure 7) The species occupy adaptive peaks but the fixityof the ecological landscape that allowed them to do so isquestionable

In fact the islands and their inhabitants have changedradically Three million years ago there were far fewer islands than today perhaps only five (Grant and Grant 1998)The number of islands increased as a result of volcanic activitycentered on and near a hotspot beneath the western island of Fernandina Climate changed as well The average air

temperature declined but more important thanthis the worldrsquos climate underwent a sharp transi-tion 275 million years ago with the abrupt onset of glaciation (Cane and Molnar 2001) In the lastmillion years the climate has oscillated betweenglacial and interglacial conditions at about 100000-year intervals Global fluctuations in climate wereexperienced locally in the Galaacutepagos and elsewherein tropical America This has been revealed by theisotopic oxygen signatures of temperature in Andean ice cores (Seltzer et al 2002) by coral coresin Galaacutepagos (Dunbar et al 1994) and by pollencores in Galaacutepagos (Colinvaux 1972 1984) and incontinental South and Central American lakes(Bush et al 1992)

Most of the contemporary finches evolved inthe last million years so it is important to knowwhat happened during these cycles The two majoreffects of glacialndashinterglacial cycles were the de-pression of temperatures and of sea level relative to contemporary levels The last Ice Agecooling resulted in a drop of 3degC to 4degC in theequatorial Pacific reaching a minimum about21000 years ago (Kerr 2001) The previous deglacia-tion about 130000 years ago was associated witha drop of 2degC to 6degC (Tudhope et al 2001) Sea levelfell with the temperature The decline was gradualfrom the current level (about 120000 years ago) toabout 60 meters (m) lower (about 30000 yearsago) then an abrupt further decrease occurred to

about 125 m below the current level (Lambeck and Chappell2001) As a consequence islands were larger and distances between them were shorter Thus both temperature and sealevel were usually lower and never much higher than they aretoday

The food of finchesmdashplants and arthropods the latterfeeding on the plants and on each othermdashmust have beenaffected by these geophysical and climatic changes Firstnew species of plants and arthropods would have arrivedby immigration We do not know when this happened or which species were involved For Galaacutepagos unlikeHawaii (eg Givnish 1998 Wright et al 2000) there are nomolecular phylogenies of plants to help in reconstructingpaleofloras and the phylogenies of insects are too scarceto be useful (Finston and Peck 1997 Sequeira et al 2000)That situation needs to be rectified Second other speciesperhaps influenced by the immigrants would have become extinct Severe and extensive droughts would have been particularly crucial and cruel times for many organisms including finches Third the temperature- andmoisture-dependent altitudinal zonation of plants wouldhave shifted upward and downward at different timeshence the highest and lowest habitats would have beenmost vulnerable to elimination as noted elsewhere (Prodonet al 2002) Plant distributions would have changed acrossthe archipelago

972 BioScience bull October 2003 Vol 53 No 10

Plenary

Figure 7 The accumulation of species of Darwinrsquos finches with timeback-calculated from the estimated ages (in millions of years or MY) ofcontemporary species in the absence of known extinctions The accumu-lation of species parallels the accumulation of islands with time as de-termined from estimations of island age and elevation in relation to sealevel More islands provide more conditions for speciation to occur andspecies to persist From Grant (2001)

The evidence of a change in the upland forests is the rel-ative scarcity of endemic plants (Johnson and Raven 1973)The evidence of a change in the lowest zone is the anomalousoccurrence of plants on some islands with apparently un-suitable climates and soil For example the tree Erythrina velu-tina occurs at mid elevations on the high islands of Santa CruzSantiago and Isabela A single tree of this species occurs onthe low arid island of Genovesa and fewer than a dozen oc-cur on the low arid and even more remote island of WolfSimilarly a few Zanthoxylum fagara trees on Santa Cruz andSan Cristoacutebal occur close to the coast These may be theremnants of much larger populations on these islands undercooler wetter or less seasonally arid conditions than those thatprevail today Temperatures and precipitation changedmarkedly from one state to another long enough (gt 1000years Colinvaux 1972 Riedinger et al 2002) for vegetationzones to shift (Woodward 1987) On some occasions how-ever significant changes in temperature occurred in as shorta time as a hundred years perhaps less (Bush et al 1992)Large abrupt and widespread climate changes with majorconsequences for the biota have occurred repeatedly in thepast when the Earth system was forced across thresholds(Alley et al 2003)

The macroevolutionary pattern and the buildup ofcomplex communities from simple ones In view of the strong environmental changes in the archi-pelago it is scarcely likely that all current ecological niches wereavailable when the finchesrsquo ancestors arrived Rather thenumbers and types of opportunities for finch evolution increased as the number of islands increased and the climate and vegetation changed According to this view theadaptive radiation and the buildup of species-rich commu-nities were largely molded by environmental change theparticular species originated when they did and no earlierin response to particular environments prevailing then

When the first finches arrived on Galaacutepagos they mayhave encountered a climate and vegetation more like those ofmodern-day Cocos Island warmer wetter and more humidconditions fostering rain forest from the coast to the islandpeaks (Grant 1999 Grant and Grant 2002b) Cocos Island hastemperatures similar to those of the coastal habitats in theGalaacutepagos and rainfall equivalent to what the Galaacutepagosnow receives in an El Nintildeo year at high elevations Reason-ing from the evidence of modern finches we suggest the ini-tial evolutionary pathway taken by the finches was toward theexploitation of small arthropods and of nectar and pollenfrom small flowers in a rain forestndashlike environment

The radiation began when the initial species split into twolineages of Certhidea warbler finches (figure 8) after the ini-tial pathway had been taken One group of populations(Certhidea olivacea) inhabits moist upland forest and theother group (Certhidea fusca) occupies lower habitats onother mainly low islands Remarkably despite their longseparation the two groups have retained similar mate recog-nition systems and for that reason we refer to them as lineages

October 2003 Vol 53 No 10 bull BioScience 973

Plenary

Figure 8 Reconstruction of finch phylogeny based on microsatellite DNA Horizontal branch lengths are pro-portional to units of genetic distance (GST) as indicated bythe scale Numbers refer to percentage bootstrap supportfor the nodes by two methods Mean weights are given onthe right together with symbols of male plumage fullyblack partially black or brown or green Alternative reconstructions that use morphology allozymes or mito-chondrial DNA are similar differing in relatively smalldetails Species from top to bottom Geospiza fuliginosaGeospiza fortis Geospiza magnirostris Geospiza scandensGeospiza conirostris Geospiza difficilis Camarhynchusparvulus Camarhynchus psittacula Camarhynchus pauperCamarhynchus pallida Platyspiza crassirostris Certhideafusca Pinaroloxias inornata and Certhidea olivacea FromPetren and colleagues (1999)

and not species (Grant and Grant 2002b) Another remark-able feature is that they have remained relatively undifferen-tiated in morphology ecology and behavior This is not expected on the basis of the view that niches were varied plen-tiful and evolutionarily within reach at that time Howeverwe must acknowledge the possibility perhaps even the prob-ability that extinction has robbed us of other species that wereformed then The morphological similarity of these finchescontrasting with their distinctness from continental rela-tives argues for an early adaptation to an unusual niche

One of the warbler finch lineages gave rise to all otherfinch species Early products of the diversification were the veg-etarian finch (Platyspiza crassirostris) the Cocos finch(Pinaroloxias inornata) on either Galaacutepagos or Cocos Island(Grant and Grant 2002b) and the sharp-beaked groundfinch (G difficilis) The most recent products were a group ofground finch species (Geospiza) and a group of tree finchspecies (Camarhynchus and Cactospiza) (figure 8)

Effects of environmental change have left a different his-torical imprint on the older species Populations of G diffi-cilis differ strongly in morphology and ecology to a degree un-matched by all other and younger species in the genusGeospiza and by the warbler finches that preceded themSome G difficilis have persisted in Zanthoxylum forest at midand upper elevations which we believe to be old and others have entered arid lowland habitat perhaps when theZanthoxylum forest gradually disappeared from low islandsas the climate changed This may have been the first step ofthe radiation of ground finches In contrast to the G difficilispopulations populations of the vegetarian finch are mor-phologically and ecologically very similar Limited genetic data(Petren et al 1999) suggest that they separated from each otherrecently This is surprising as it is not expected from the ageof the species or from the presumed stability of its mid-elevation transition zone habitat The vegetarian finch mayhave become restricted to one or two islands and other pop-ulations or even related species may have become extinctin response to one of the recent extreme fluctuations in climate Its vegetarian diet may have made it vulnerable intimes of drought and competition with other species may havebeen an additional factor

The importance of environmental change in speciation isfurther suggested by the fact that in the last million years newspecies evolved in the habitats most vulnerable to changeGeospiza were added to lowland habitats and Camarhynchuswere added to the upland humid forest The change in climatetoward seasonal aridity and the development of arid lowlandhabitat provided the opportunity for a new granivorous wayof finch life now adopted by Geospiza species Some of thesemodern species may have contributed to the extinction ofolder ones through competitive superiority in a changingenvironment This is one possible interpretation of the contrast between the morphological distinctness of the threeolder groups Certhidea Platyspiza and G difficilis and themorphological similarity of species in the younger generaCamarhynchus Cactospiza and Geospiza

These ideas on speciation and extinction together with ob-servations of the colonization of Daphne Major by G magni-rostris (Grant et al 2001) suggest that periods of expansionsuch as the one in progress are preceded and followed by periods of range contraction and extinction caused by envi-ronmental change Distributions of habitats sea level islandand population sizes and degrees of isolation provide favorable conditions for divergence of small populations inisolation at some times and for dispersal mixing establish-ment of sympatry and hybridization at others The buildupof complex communities from simple ones is not smooth con-tinuous and regular but a process of gains and losses with anet accumulation of species over the long term

ConclusionsAccording to the standard allopatric model speciation beginswith the establishment of a new population continues withthe divergence of that population from its parent populationand is completed when members of two diverged populationscan coexist in sympatry without interbreeding We stand a virtually negligible chance of observing the whole process under natural circumstances Nevertheless it is possible tomake relevant observations in nature of all steps in theprocess We have described the strong role played by envi-ronmental change at each of the three steps in the speciationof Darwinrsquos finches The full adaptive radiation was pro-duced by a repetition of these steps each with a different product under somewhat different circumstances The challenge now is to account for the differences in terms of pastenvironments without the help of fossils of finches or ofother members of the biota We have sketched a frameworkfor doing this by using molecular genetic information to estimate the finch phylogeny and using geological and climaticinformation to reconstruct Galaacutepagos environments in thepast 2 million to 3 million years A better understanding ofenvironmental change on this time scale will help to explainwhy 14 species were formed what their sequence of origin wasand why they evolved their particular unique features Theremay be more history to uncover in finch DNA if only we canwork out how to read it

Acknowledgments We thank Ken Petren for figure 8 and Phil Hedrick FritzTrillmich and an anonymous reviewer for comments on themanuscript We are grateful to the Galaacutepagos National Parkand the Charles Darwin Research Station for permission andlogistical support for the fieldwork and to the National Sciences and Engineering Research Council of Canada and theNational Science Foundation for funding support

References citedAbbott I Abbott LK Grant PR 1977 Comparative ecology of Galaacutepagos

ground finches (Geospiza Gould) Evaluation of the importance of floris-tic diversity and interspecific competition Ecological Monographs 47151ndash184

Alley RB et al 2003 Abrupt climate change Science 299 2005ndash2010

974 BioScience bull October 2003 Vol 53 No 10

Plenary

Bowman RI 1961 Morphological Differentiation and Adaptation in theGalaacutepagos Finches University of California Publications in ZoologyVol 58 Berkeley University of California Press

mdashmdashmdash 1983 The songs of Darwinrsquos finches Pages 237ndash537 in Bowman RILeviton AE Berson M eds Galaacutepagos Organisms San Francisco Amer-ican Association for the Advancement of Science Pacific Division

Burns KJ Hackett SJ Klein NK 2002 Phylogenetic relationships andmorphological diversity in Darwinrsquos finches and their relatives Evo-lution 56 1240ndash1252

Bush MB Piperno DR Colinvaux PA DeOleveira PE Krissek LA Miller MCRowe WE 1992 A 14300-yr paleoecological profile of a lowland tropi-cal lake in Panama Ecological Monographs 62 251ndash275

Cane MA Molnar P 2001 Closing of the Indonesian seaway as a precursorto east African aridification around 3ndash4 million years ago Nature 411157ndash162

Colinvaux PA 1972 Climate and the Galaacutepagos Islands Nature 240 17ndash20mdashmdashmdash 1984 The Galaacutepagos climate Present and past Pages 55ndash69 in

Perry R ed Galaacutepagos Oxford (United Kingdom) Pergamon PressDarwin CR 1842 Journal of Researches into the Geology and Natural

History of the Various Countries Visited during the Voyage of H M SBeagle under the Command of Captain FitzRoy RN from 1832 to 1836London Henry Colburn

Dunbar RB Wellington GM Colgan MW Glynn PW 1994 Eastern Pacificsea surface temperature since 1600 AD The O18 record of climate vari-ability in Galaacutepagos corals Paleoceanography 9 291ndash315

Finston TL Peck SB 1997 Genetic differentiation and speciation in Stomion(Coleoptera Tenebrionidae) Flightless beetles of the Galaacutepagos IslandsEcuador Biological Journal of the Linnean Society 61 243ndash266

Givnish TJ 1998Adaptive plant evolution on islands Classical patterns mole-cular data new insights Pages 281ndash304 in Grant PR ed Evolution on Islands Oxford (United Kingdom) Oxford University Press

Grant BR Grant PR 1989 Evolutionary Dynamics of a Natural PopulationThe Large Cactus Finch of the Galaacutepagos Chicago University of ChicagoPress

mdashmdashmdash 1996 Cultural inheritance of song and its role in the evolution ofDarwinrsquos finches Evolution 50 2471ndash2487

Grant PR 1999 Ecology and Evolution of Darwinrsquos Finches Princeton (NJ)Princeton University Press

mdashmdashmdash 2001 Reconstructing the evolution of birds on islands 100 years ofresearch Oikos 92 385ndash403

Grant PR Grant BR 1998 Speciation and hybridization in island birds Pages142ndash162 in Grant PR ed Evolution on Islands Oxford (United Kingdom)Oxford University Press

mdashmdashmdash 2002a Unpredictable evolution in a 30-year study of Darwinrsquosfinches Science 296 707ndash711

mdashmdashmdash 2002b Adaptive radiation of Darwinrsquos finches American Scientist90 131ndash139

Grant PR Grant BR Petren K 2001 The founding of a new population by a single pair of individuals Establishment selection and populationexpansion Genetica 112113 359ndash382

Huxley JS 1942 Evolution The Modern Synthesis London Allen and Unwin

Johnson MP Raven PH 1973 Species number and endemism The Galaacutepagosarchipelago revisited Science 179 893ndash895

Keller LF Grant PR Grant BR Petren K 2001 Heritability of morphologi-cal traits in Darwinrsquos finches Misidentified paternity and maternal effects Heredity 87 325ndash336

Kerr RA 2001 The tropics return to the climate system Science 292 660ndash661Lack D 1947 Darwinrsquos finches Cambridge (United Kingdom) Cambridge

University PressLambeck K Chappell J 2001 Sea level change through the last glacial cycle

Science 292 679ndash686Mayr E 1942 Systematics and the Origin of Species New York Columbia

University Press

Newton I 1967 The adaptive variation and feeding ecology of some British

finches Ibis 109 33ndash98

Petren K Grant BR Grant PR 1999 A phylogeny of Darwinrsquos finches based

on microsatellite DNA length variation Proceedings of the Royal Soci-

ety of London B 266 321ndash329

Price T Lovette IJ Bermingham E Gibbs HL Richman AD 2000 The

imprint of history on communities of North American and Asian

warblers American Naturalist 156 354ndash367

Prodon R Thibault J-C Dejaifve P-A 2002 Expansion vs compression of

bird altitudinal ranges on a Mediterranean island Ecology 83 1294ndash1306

Ratcliffe LM Grant PR 1983a Species recognition in Darwinrsquos finches

(Geospiza Gould) I Discrimination by morphological cues Animal

Behaviour 31 1139ndash1153

mdashmdashmdash 1983b Species recognition in Darwinrsquos finches (Geospiza Gould)

II Geographic variation in mate preference Animal Behaviour 31

1154ndash1165

mdashmdashmdash 1985 Species recognition in Darwinrsquos finches (Geospiza Gould) III

Male responses to playback of different song types dialects and hetero-

specific songs Animal Behaviour 33 290ndash307

Richards OW 1948 Species formation in islands (review of Darwinrsquos Finches

by Lack D) Journal of Animal Ecology 17 83ndash84

Riedinger MA Steinitz-Kannan M Last WM Brenner M 2002 A ~6100 14C

yr record of El Nintildeo activity from the Galaacutepagos Islands Journal of

Paleontology 27 1ndash7

Sato A OrsquoHuigin C Figueroa F Grant PR Grant BR Tichy H Klein J 1999

Phylogeny of Darwinrsquos finches as revealed by mtDNA sequences

Proceedings of the National Academy of Sciences 96 5101ndash5106

Schluter D 2000 The Ecology of Adaptive Radiations Oxford (United King-

dom) Oxford University Press

Schluter D Grant PR 1984 Determinants of morphological patterns in

communities of Darwinrsquos finches American Naturalist 123 175ndash196

Seltzer GO Rodbell DT Baker PA Fritz SC Tapia PM Rowe HD Dunbar

RB 2002 Early warming of tropical South America at the last glacialndash

interglacial transition Science 296 1685ndash1686

Sequeira AS Lanteri AA Scataglini MA Confalonieri VA Farrell BD 2000

Are flightless Galapaganus weevils older than the Galaacutepagos Islands they

inhabit Heredity 85 20ndash29

Simpson GG 1944 Tempo and Mode in Evolution New York Columbia

University Press

Swarth HS 1931 The avifauna of the Galaacutepagos islands Occasional Papers

of the California Academy of Sciences 18 1ndash299

mdashmdashmdash 1934 The bird fauna of the Galaacutepagos islands in relation to species

formation Biological Reviews 9 213ndash234

Tudhope AW Chilcott CP McCulloch MT Cook ER Chappell J Ellam RM

Lea DW Lough JM Shimmield GB 2001 Variability in the El

NintildeondashSouthern Oscillation through a glacialndashinterglacial cycle Science

291 1511ndash1517

Vincek V OrsquoHuigin C Satta Y Takahata N Boag PT Grant PR Grant BR

Klein J 1996 How large was the founding population of Darwinrsquos

finches Proceedings of the Royal Society of London B 264 111ndash118

Woodward FI 1987 Climate and Plant Distribution London Cambridge Uni-

versity Press

Wright SD Young CG Dawson JW Whittaker DJ Gardner RC 2000

Riding the ice age El Nintildeo Pacific biogeography and evolution of

Metrosideros subg Metrosideros (Myrtaceae) inferred from nuclear

ribosomal DNA Proceedings of the National Academy of Sciences 97

4110ndash4123

October 2003 Vol 53 No 10 bull BioScience 975

Plenary

that the islands have always been much as they are today interms of geography climate and vegetation If this is correctthe finchesrsquo adaptive radiation can be viewed as a process ofdifferentiation that results in the occupancy of all ecologicalniches present at the outsetmdashrather like filling empty boxesone species per box Indeed this is how early writers on thesubject viewed the radiation of the finches stressing the absence or scarcity of competitors in the boxes as a facilitat-ing factor (Huxley 1942 Simpson 1944 Lack 1947 Grant1999) In the modern version the boxes are replaced by adap-tive peaks in a more or less fixed landscape This view impliesthat diversification is rapid early in the radiation and thenslows down as ecological opportunities diminish Some radiations of other organisms elsewhere conform to this pattern (Schluter 2000) However taken at face value thephylogeny of Darwinrsquos finches shows exactly the oppositepattern a slow start followed by recent rapid diversification(figure 7) The species occupy adaptive peaks but the fixityof the ecological landscape that allowed them to do so isquestionable

In fact the islands and their inhabitants have changedradically Three million years ago there were far fewer islands than today perhaps only five (Grant and Grant 1998)The number of islands increased as a result of volcanic activitycentered on and near a hotspot beneath the western island of Fernandina Climate changed as well The average air

temperature declined but more important thanthis the worldrsquos climate underwent a sharp transi-tion 275 million years ago with the abrupt onset of glaciation (Cane and Molnar 2001) In the lastmillion years the climate has oscillated betweenglacial and interglacial conditions at about 100000-year intervals Global fluctuations in climate wereexperienced locally in the Galaacutepagos and elsewherein tropical America This has been revealed by theisotopic oxygen signatures of temperature in Andean ice cores (Seltzer et al 2002) by coral coresin Galaacutepagos (Dunbar et al 1994) and by pollencores in Galaacutepagos (Colinvaux 1972 1984) and incontinental South and Central American lakes(Bush et al 1992)

Most of the contemporary finches evolved inthe last million years so it is important to knowwhat happened during these cycles The two majoreffects of glacialndashinterglacial cycles were the de-pression of temperatures and of sea level relative to contemporary levels The last Ice Agecooling resulted in a drop of 3degC to 4degC in theequatorial Pacific reaching a minimum about21000 years ago (Kerr 2001) The previous deglacia-tion about 130000 years ago was associated witha drop of 2degC to 6degC (Tudhope et al 2001) Sea levelfell with the temperature The decline was gradualfrom the current level (about 120000 years ago) toabout 60 meters (m) lower (about 30000 yearsago) then an abrupt further decrease occurred to

about 125 m below the current level (Lambeck and Chappell2001) As a consequence islands were larger and distances between them were shorter Thus both temperature and sealevel were usually lower and never much higher than they aretoday

The food of finchesmdashplants and arthropods the latterfeeding on the plants and on each othermdashmust have beenaffected by these geophysical and climatic changes Firstnew species of plants and arthropods would have arrivedby immigration We do not know when this happened or which species were involved For Galaacutepagos unlikeHawaii (eg Givnish 1998 Wright et al 2000) there are nomolecular phylogenies of plants to help in reconstructingpaleofloras and the phylogenies of insects are too scarceto be useful (Finston and Peck 1997 Sequeira et al 2000)That situation needs to be rectified Second other speciesperhaps influenced by the immigrants would have become extinct Severe and extensive droughts would have been particularly crucial and cruel times for many organisms including finches Third the temperature- andmoisture-dependent altitudinal zonation of plants wouldhave shifted upward and downward at different timeshence the highest and lowest habitats would have beenmost vulnerable to elimination as noted elsewhere (Prodonet al 2002) Plant distributions would have changed acrossthe archipelago

972 BioScience bull October 2003 Vol 53 No 10

Plenary

Figure 7 The accumulation of species of Darwinrsquos finches with timeback-calculated from the estimated ages (in millions of years or MY) ofcontemporary species in the absence of known extinctions The accumu-lation of species parallels the accumulation of islands with time as de-termined from estimations of island age and elevation in relation to sealevel More islands provide more conditions for speciation to occur andspecies to persist From Grant (2001)

The evidence of a change in the upland forests is the rel-ative scarcity of endemic plants (Johnson and Raven 1973)The evidence of a change in the lowest zone is the anomalousoccurrence of plants on some islands with apparently un-suitable climates and soil For example the tree Erythrina velu-tina occurs at mid elevations on the high islands of Santa CruzSantiago and Isabela A single tree of this species occurs onthe low arid island of Genovesa and fewer than a dozen oc-cur on the low arid and even more remote island of WolfSimilarly a few Zanthoxylum fagara trees on Santa Cruz andSan Cristoacutebal occur close to the coast These may be theremnants of much larger populations on these islands undercooler wetter or less seasonally arid conditions than those thatprevail today Temperatures and precipitation changedmarkedly from one state to another long enough (gt 1000years Colinvaux 1972 Riedinger et al 2002) for vegetationzones to shift (Woodward 1987) On some occasions how-ever significant changes in temperature occurred in as shorta time as a hundred years perhaps less (Bush et al 1992)Large abrupt and widespread climate changes with majorconsequences for the biota have occurred repeatedly in thepast when the Earth system was forced across thresholds(Alley et al 2003)

The macroevolutionary pattern and the buildup ofcomplex communities from simple ones In view of the strong environmental changes in the archi-pelago it is scarcely likely that all current ecological niches wereavailable when the finchesrsquo ancestors arrived Rather thenumbers and types of opportunities for finch evolution increased as the number of islands increased and the climate and vegetation changed According to this view theadaptive radiation and the buildup of species-rich commu-nities were largely molded by environmental change theparticular species originated when they did and no earlierin response to particular environments prevailing then

When the first finches arrived on Galaacutepagos they mayhave encountered a climate and vegetation more like those ofmodern-day Cocos Island warmer wetter and more humidconditions fostering rain forest from the coast to the islandpeaks (Grant 1999 Grant and Grant 2002b) Cocos Island hastemperatures similar to those of the coastal habitats in theGalaacutepagos and rainfall equivalent to what the Galaacutepagosnow receives in an El Nintildeo year at high elevations Reason-ing from the evidence of modern finches we suggest the ini-tial evolutionary pathway taken by the finches was toward theexploitation of small arthropods and of nectar and pollenfrom small flowers in a rain forestndashlike environment

The radiation began when the initial species split into twolineages of Certhidea warbler finches (figure 8) after the ini-tial pathway had been taken One group of populations(Certhidea olivacea) inhabits moist upland forest and theother group (Certhidea fusca) occupies lower habitats onother mainly low islands Remarkably despite their longseparation the two groups have retained similar mate recog-nition systems and for that reason we refer to them as lineages

October 2003 Vol 53 No 10 bull BioScience 973

Plenary

Figure 8 Reconstruction of finch phylogeny based on microsatellite DNA Horizontal branch lengths are pro-portional to units of genetic distance (GST) as indicated bythe scale Numbers refer to percentage bootstrap supportfor the nodes by two methods Mean weights are given onthe right together with symbols of male plumage fullyblack partially black or brown or green Alternative reconstructions that use morphology allozymes or mito-chondrial DNA are similar differing in relatively smalldetails Species from top to bottom Geospiza fuliginosaGeospiza fortis Geospiza magnirostris Geospiza scandensGeospiza conirostris Geospiza difficilis Camarhynchusparvulus Camarhynchus psittacula Camarhynchus pauperCamarhynchus pallida Platyspiza crassirostris Certhideafusca Pinaroloxias inornata and Certhidea olivacea FromPetren and colleagues (1999)

and not species (Grant and Grant 2002b) Another remark-able feature is that they have remained relatively undifferen-tiated in morphology ecology and behavior This is not expected on the basis of the view that niches were varied plen-tiful and evolutionarily within reach at that time Howeverwe must acknowledge the possibility perhaps even the prob-ability that extinction has robbed us of other species that wereformed then The morphological similarity of these finchescontrasting with their distinctness from continental rela-tives argues for an early adaptation to an unusual niche

One of the warbler finch lineages gave rise to all otherfinch species Early products of the diversification were the veg-etarian finch (Platyspiza crassirostris) the Cocos finch(Pinaroloxias inornata) on either Galaacutepagos or Cocos Island(Grant and Grant 2002b) and the sharp-beaked groundfinch (G difficilis) The most recent products were a group ofground finch species (Geospiza) and a group of tree finchspecies (Camarhynchus and Cactospiza) (figure 8)

Effects of environmental change have left a different his-torical imprint on the older species Populations of G diffi-cilis differ strongly in morphology and ecology to a degree un-matched by all other and younger species in the genusGeospiza and by the warbler finches that preceded themSome G difficilis have persisted in Zanthoxylum forest at midand upper elevations which we believe to be old and others have entered arid lowland habitat perhaps when theZanthoxylum forest gradually disappeared from low islandsas the climate changed This may have been the first step ofthe radiation of ground finches In contrast to the G difficilispopulations populations of the vegetarian finch are mor-phologically and ecologically very similar Limited genetic data(Petren et al 1999) suggest that they separated from each otherrecently This is surprising as it is not expected from the ageof the species or from the presumed stability of its mid-elevation transition zone habitat The vegetarian finch mayhave become restricted to one or two islands and other pop-ulations or even related species may have become extinctin response to one of the recent extreme fluctuations in climate Its vegetarian diet may have made it vulnerable intimes of drought and competition with other species may havebeen an additional factor

The importance of environmental change in speciation isfurther suggested by the fact that in the last million years newspecies evolved in the habitats most vulnerable to changeGeospiza were added to lowland habitats and Camarhynchuswere added to the upland humid forest The change in climatetoward seasonal aridity and the development of arid lowlandhabitat provided the opportunity for a new granivorous wayof finch life now adopted by Geospiza species Some of thesemodern species may have contributed to the extinction ofolder ones through competitive superiority in a changingenvironment This is one possible interpretation of the contrast between the morphological distinctness of the threeolder groups Certhidea Platyspiza and G difficilis and themorphological similarity of species in the younger generaCamarhynchus Cactospiza and Geospiza

These ideas on speciation and extinction together with ob-servations of the colonization of Daphne Major by G magni-rostris (Grant et al 2001) suggest that periods of expansionsuch as the one in progress are preceded and followed by periods of range contraction and extinction caused by envi-ronmental change Distributions of habitats sea level islandand population sizes and degrees of isolation provide favorable conditions for divergence of small populations inisolation at some times and for dispersal mixing establish-ment of sympatry and hybridization at others The buildupof complex communities from simple ones is not smooth con-tinuous and regular but a process of gains and losses with anet accumulation of species over the long term

ConclusionsAccording to the standard allopatric model speciation beginswith the establishment of a new population continues withthe divergence of that population from its parent populationand is completed when members of two diverged populationscan coexist in sympatry without interbreeding We stand a virtually negligible chance of observing the whole process under natural circumstances Nevertheless it is possible tomake relevant observations in nature of all steps in theprocess We have described the strong role played by envi-ronmental change at each of the three steps in the speciationof Darwinrsquos finches The full adaptive radiation was pro-duced by a repetition of these steps each with a different product under somewhat different circumstances The challenge now is to account for the differences in terms of pastenvironments without the help of fossils of finches or ofother members of the biota We have sketched a frameworkfor doing this by using molecular genetic information to estimate the finch phylogeny and using geological and climaticinformation to reconstruct Galaacutepagos environments in thepast 2 million to 3 million years A better understanding ofenvironmental change on this time scale will help to explainwhy 14 species were formed what their sequence of origin wasand why they evolved their particular unique features Theremay be more history to uncover in finch DNA if only we canwork out how to read it

Acknowledgments We thank Ken Petren for figure 8 and Phil Hedrick FritzTrillmich and an anonymous reviewer for comments on themanuscript We are grateful to the Galaacutepagos National Parkand the Charles Darwin Research Station for permission andlogistical support for the fieldwork and to the National Sciences and Engineering Research Council of Canada and theNational Science Foundation for funding support

References citedAbbott I Abbott LK Grant PR 1977 Comparative ecology of Galaacutepagos

ground finches (Geospiza Gould) Evaluation of the importance of floris-tic diversity and interspecific competition Ecological Monographs 47151ndash184

Alley RB et al 2003 Abrupt climate change Science 299 2005ndash2010

974 BioScience bull October 2003 Vol 53 No 10

Plenary

Bowman RI 1961 Morphological Differentiation and Adaptation in theGalaacutepagos Finches University of California Publications in ZoologyVol 58 Berkeley University of California Press

mdashmdashmdash 1983 The songs of Darwinrsquos finches Pages 237ndash537 in Bowman RILeviton AE Berson M eds Galaacutepagos Organisms San Francisco Amer-ican Association for the Advancement of Science Pacific Division

Burns KJ Hackett SJ Klein NK 2002 Phylogenetic relationships andmorphological diversity in Darwinrsquos finches and their relatives Evo-lution 56 1240ndash1252

Bush MB Piperno DR Colinvaux PA DeOleveira PE Krissek LA Miller MCRowe WE 1992 A 14300-yr paleoecological profile of a lowland tropi-cal lake in Panama Ecological Monographs 62 251ndash275

Cane MA Molnar P 2001 Closing of the Indonesian seaway as a precursorto east African aridification around 3ndash4 million years ago Nature 411157ndash162

Colinvaux PA 1972 Climate and the Galaacutepagos Islands Nature 240 17ndash20mdashmdashmdash 1984 The Galaacutepagos climate Present and past Pages 55ndash69 in

Perry R ed Galaacutepagos Oxford (United Kingdom) Pergamon PressDarwin CR 1842 Journal of Researches into the Geology and Natural

History of the Various Countries Visited during the Voyage of H M SBeagle under the Command of Captain FitzRoy RN from 1832 to 1836London Henry Colburn

Dunbar RB Wellington GM Colgan MW Glynn PW 1994 Eastern Pacificsea surface temperature since 1600 AD The O18 record of climate vari-ability in Galaacutepagos corals Paleoceanography 9 291ndash315

Finston TL Peck SB 1997 Genetic differentiation and speciation in Stomion(Coleoptera Tenebrionidae) Flightless beetles of the Galaacutepagos IslandsEcuador Biological Journal of the Linnean Society 61 243ndash266

Givnish TJ 1998Adaptive plant evolution on islands Classical patterns mole-cular data new insights Pages 281ndash304 in Grant PR ed Evolution on Islands Oxford (United Kingdom) Oxford University Press

Grant BR Grant PR 1989 Evolutionary Dynamics of a Natural PopulationThe Large Cactus Finch of the Galaacutepagos Chicago University of ChicagoPress

mdashmdashmdash 1996 Cultural inheritance of song and its role in the evolution ofDarwinrsquos finches Evolution 50 2471ndash2487

Grant PR 1999 Ecology and Evolution of Darwinrsquos Finches Princeton (NJ)Princeton University Press

mdashmdashmdash 2001 Reconstructing the evolution of birds on islands 100 years ofresearch Oikos 92 385ndash403

Grant PR Grant BR 1998 Speciation and hybridization in island birds Pages142ndash162 in Grant PR ed Evolution on Islands Oxford (United Kingdom)Oxford University Press

mdashmdashmdash 2002a Unpredictable evolution in a 30-year study of Darwinrsquosfinches Science 296 707ndash711

mdashmdashmdash 2002b Adaptive radiation of Darwinrsquos finches American Scientist90 131ndash139

Grant PR Grant BR Petren K 2001 The founding of a new population by a single pair of individuals Establishment selection and populationexpansion Genetica 112113 359ndash382

Huxley JS 1942 Evolution The Modern Synthesis London Allen and Unwin

Johnson MP Raven PH 1973 Species number and endemism The Galaacutepagosarchipelago revisited Science 179 893ndash895

Keller LF Grant PR Grant BR Petren K 2001 Heritability of morphologi-cal traits in Darwinrsquos finches Misidentified paternity and maternal effects Heredity 87 325ndash336

Kerr RA 2001 The tropics return to the climate system Science 292 660ndash661Lack D 1947 Darwinrsquos finches Cambridge (United Kingdom) Cambridge

University PressLambeck K Chappell J 2001 Sea level change through the last glacial cycle

Science 292 679ndash686Mayr E 1942 Systematics and the Origin of Species New York Columbia

University Press

Newton I 1967 The adaptive variation and feeding ecology of some British

finches Ibis 109 33ndash98

Petren K Grant BR Grant PR 1999 A phylogeny of Darwinrsquos finches based

on microsatellite DNA length variation Proceedings of the Royal Soci-

ety of London B 266 321ndash329

Price T Lovette IJ Bermingham E Gibbs HL Richman AD 2000 The

imprint of history on communities of North American and Asian

warblers American Naturalist 156 354ndash367

Prodon R Thibault J-C Dejaifve P-A 2002 Expansion vs compression of

bird altitudinal ranges on a Mediterranean island Ecology 83 1294ndash1306

Ratcliffe LM Grant PR 1983a Species recognition in Darwinrsquos finches

(Geospiza Gould) I Discrimination by morphological cues Animal

Behaviour 31 1139ndash1153

mdashmdashmdash 1983b Species recognition in Darwinrsquos finches (Geospiza Gould)

II Geographic variation in mate preference Animal Behaviour 31

1154ndash1165

mdashmdashmdash 1985 Species recognition in Darwinrsquos finches (Geospiza Gould) III

Male responses to playback of different song types dialects and hetero-

specific songs Animal Behaviour 33 290ndash307

Richards OW 1948 Species formation in islands (review of Darwinrsquos Finches

by Lack D) Journal of Animal Ecology 17 83ndash84

Riedinger MA Steinitz-Kannan M Last WM Brenner M 2002 A ~6100 14C

yr record of El Nintildeo activity from the Galaacutepagos Islands Journal of

Paleontology 27 1ndash7

Sato A OrsquoHuigin C Figueroa F Grant PR Grant BR Tichy H Klein J 1999

Phylogeny of Darwinrsquos finches as revealed by mtDNA sequences

Proceedings of the National Academy of Sciences 96 5101ndash5106

Schluter D 2000 The Ecology of Adaptive Radiations Oxford (United King-

dom) Oxford University Press

Schluter D Grant PR 1984 Determinants of morphological patterns in

communities of Darwinrsquos finches American Naturalist 123 175ndash196

Seltzer GO Rodbell DT Baker PA Fritz SC Tapia PM Rowe HD Dunbar

RB 2002 Early warming of tropical South America at the last glacialndash

interglacial transition Science 296 1685ndash1686

Sequeira AS Lanteri AA Scataglini MA Confalonieri VA Farrell BD 2000

Are flightless Galapaganus weevils older than the Galaacutepagos Islands they

inhabit Heredity 85 20ndash29

Simpson GG 1944 Tempo and Mode in Evolution New York Columbia

University Press

Swarth HS 1931 The avifauna of the Galaacutepagos islands Occasional Papers

of the California Academy of Sciences 18 1ndash299

mdashmdashmdash 1934 The bird fauna of the Galaacutepagos islands in relation to species

formation Biological Reviews 9 213ndash234

Tudhope AW Chilcott CP McCulloch MT Cook ER Chappell J Ellam RM

Lea DW Lough JM Shimmield GB 2001 Variability in the El

NintildeondashSouthern Oscillation through a glacialndashinterglacial cycle Science

291 1511ndash1517

Vincek V OrsquoHuigin C Satta Y Takahata N Boag PT Grant PR Grant BR

Klein J 1996 How large was the founding population of Darwinrsquos

finches Proceedings of the Royal Society of London B 264 111ndash118

Woodward FI 1987 Climate and Plant Distribution London Cambridge Uni-

versity Press

Wright SD Young CG Dawson JW Whittaker DJ Gardner RC 2000

Riding the ice age El Nintildeo Pacific biogeography and evolution of

Metrosideros subg Metrosideros (Myrtaceae) inferred from nuclear

ribosomal DNA Proceedings of the National Academy of Sciences 97

4110ndash4123

October 2003 Vol 53 No 10 bull BioScience 975

Plenary

The evidence of a change in the upland forests is the rel-ative scarcity of endemic plants (Johnson and Raven 1973)The evidence of a change in the lowest zone is the anomalousoccurrence of plants on some islands with apparently un-suitable climates and soil For example the tree Erythrina velu-tina occurs at mid elevations on the high islands of Santa CruzSantiago and Isabela A single tree of this species occurs onthe low arid island of Genovesa and fewer than a dozen oc-cur on the low arid and even more remote island of WolfSimilarly a few Zanthoxylum fagara trees on Santa Cruz andSan Cristoacutebal occur close to the coast These may be theremnants of much larger populations on these islands undercooler wetter or less seasonally arid conditions than those thatprevail today Temperatures and precipitation changedmarkedly from one state to another long enough (gt 1000years Colinvaux 1972 Riedinger et al 2002) for vegetationzones to shift (Woodward 1987) On some occasions how-ever significant changes in temperature occurred in as shorta time as a hundred years perhaps less (Bush et al 1992)Large abrupt and widespread climate changes with majorconsequences for the biota have occurred repeatedly in thepast when the Earth system was forced across thresholds(Alley et al 2003)

The macroevolutionary pattern and the buildup ofcomplex communities from simple ones In view of the strong environmental changes in the archi-pelago it is scarcely likely that all current ecological niches wereavailable when the finchesrsquo ancestors arrived Rather thenumbers and types of opportunities for finch evolution increased as the number of islands increased and the climate and vegetation changed According to this view theadaptive radiation and the buildup of species-rich commu-nities were largely molded by environmental change theparticular species originated when they did and no earlierin response to particular environments prevailing then

When the first finches arrived on Galaacutepagos they mayhave encountered a climate and vegetation more like those ofmodern-day Cocos Island warmer wetter and more humidconditions fostering rain forest from the coast to the islandpeaks (Grant 1999 Grant and Grant 2002b) Cocos Island hastemperatures similar to those of the coastal habitats in theGalaacutepagos and rainfall equivalent to what the Galaacutepagosnow receives in an El Nintildeo year at high elevations Reason-ing from the evidence of modern finches we suggest the ini-tial evolutionary pathway taken by the finches was toward theexploitation of small arthropods and of nectar and pollenfrom small flowers in a rain forestndashlike environment

The radiation began when the initial species split into twolineages of Certhidea warbler finches (figure 8) after the ini-tial pathway had been taken One group of populations(Certhidea olivacea) inhabits moist upland forest and theother group (Certhidea fusca) occupies lower habitats onother mainly low islands Remarkably despite their longseparation the two groups have retained similar mate recog-nition systems and for that reason we refer to them as lineages

October 2003 Vol 53 No 10 bull BioScience 973

Plenary

Figure 8 Reconstruction of finch phylogeny based on microsatellite DNA Horizontal branch lengths are pro-portional to units of genetic distance (GST) as indicated bythe scale Numbers refer to percentage bootstrap supportfor the nodes by two methods Mean weights are given onthe right together with symbols of male plumage fullyblack partially black or brown or green Alternative reconstructions that use morphology allozymes or mito-chondrial DNA are similar differing in relatively smalldetails Species from top to bottom Geospiza fuliginosaGeospiza fortis Geospiza magnirostris Geospiza scandensGeospiza conirostris Geospiza difficilis Camarhynchusparvulus Camarhynchus psittacula Camarhynchus pauperCamarhynchus pallida Platyspiza crassirostris Certhideafusca Pinaroloxias inornata and Certhidea olivacea FromPetren and colleagues (1999)

and not species (Grant and Grant 2002b) Another remark-able feature is that they have remained relatively undifferen-tiated in morphology ecology and behavior This is not expected on the basis of the view that niches were varied plen-tiful and evolutionarily within reach at that time Howeverwe must acknowledge the possibility perhaps even the prob-ability that extinction has robbed us of other species that wereformed then The morphological similarity of these finchescontrasting with their distinctness from continental rela-tives argues for an early adaptation to an unusual niche

One of the warbler finch lineages gave rise to all otherfinch species Early products of the diversification were the veg-etarian finch (Platyspiza crassirostris) the Cocos finch(Pinaroloxias inornata) on either Galaacutepagos or Cocos Island(Grant and Grant 2002b) and the sharp-beaked groundfinch (G difficilis) The most recent products were a group ofground finch species (Geospiza) and a group of tree finchspecies (Camarhynchus and Cactospiza) (figure 8)

Effects of environmental change have left a different his-torical imprint on the older species Populations of G diffi-cilis differ strongly in morphology and ecology to a degree un-matched by all other and younger species in the genusGeospiza and by the warbler finches that preceded themSome G difficilis have persisted in Zanthoxylum forest at midand upper elevations which we believe to be old and others have entered arid lowland habitat perhaps when theZanthoxylum forest gradually disappeared from low islandsas the climate changed This may have been the first step ofthe radiation of ground finches In contrast to the G difficilispopulations populations of the vegetarian finch are mor-phologically and ecologically very similar Limited genetic data(Petren et al 1999) suggest that they separated from each otherrecently This is surprising as it is not expected from the ageof the species or from the presumed stability of its mid-elevation transition zone habitat The vegetarian finch mayhave become restricted to one or two islands and other pop-ulations or even related species may have become extinctin response to one of the recent extreme fluctuations in climate Its vegetarian diet may have made it vulnerable intimes of drought and competition with other species may havebeen an additional factor

The importance of environmental change in speciation isfurther suggested by the fact that in the last million years newspecies evolved in the habitats most vulnerable to changeGeospiza were added to lowland habitats and Camarhynchuswere added to the upland humid forest The change in climatetoward seasonal aridity and the development of arid lowlandhabitat provided the opportunity for a new granivorous wayof finch life now adopted by Geospiza species Some of thesemodern species may have contributed to the extinction ofolder ones through competitive superiority in a changingenvironment This is one possible interpretation of the contrast between the morphological distinctness of the threeolder groups Certhidea Platyspiza and G difficilis and themorphological similarity of species in the younger generaCamarhynchus Cactospiza and Geospiza

These ideas on speciation and extinction together with ob-servations of the colonization of Daphne Major by G magni-rostris (Grant et al 2001) suggest that periods of expansionsuch as the one in progress are preceded and followed by periods of range contraction and extinction caused by envi-ronmental change Distributions of habitats sea level islandand population sizes and degrees of isolation provide favorable conditions for divergence of small populations inisolation at some times and for dispersal mixing establish-ment of sympatry and hybridization at others The buildupof complex communities from simple ones is not smooth con-tinuous and regular but a process of gains and losses with anet accumulation of species over the long term

ConclusionsAccording to the standard allopatric model speciation beginswith the establishment of a new population continues withthe divergence of that population from its parent populationand is completed when members of two diverged populationscan coexist in sympatry without interbreeding We stand a virtually negligible chance of observing the whole process under natural circumstances Nevertheless it is possible tomake relevant observations in nature of all steps in theprocess We have described the strong role played by envi-ronmental change at each of the three steps in the speciationof Darwinrsquos finches The full adaptive radiation was pro-duced by a repetition of these steps each with a different product under somewhat different circumstances The challenge now is to account for the differences in terms of pastenvironments without the help of fossils of finches or ofother members of the biota We have sketched a frameworkfor doing this by using molecular genetic information to estimate the finch phylogeny and using geological and climaticinformation to reconstruct Galaacutepagos environments in thepast 2 million to 3 million years A better understanding ofenvironmental change on this time scale will help to explainwhy 14 species were formed what their sequence of origin wasand why they evolved their particular unique features Theremay be more history to uncover in finch DNA if only we canwork out how to read it

Acknowledgments We thank Ken Petren for figure 8 and Phil Hedrick FritzTrillmich and an anonymous reviewer for comments on themanuscript We are grateful to the Galaacutepagos National Parkand the Charles Darwin Research Station for permission andlogistical support for the fieldwork and to the National Sciences and Engineering Research Council of Canada and theNational Science Foundation for funding support

References citedAbbott I Abbott LK Grant PR 1977 Comparative ecology of Galaacutepagos

ground finches (Geospiza Gould) Evaluation of the importance of floris-tic diversity and interspecific competition Ecological Monographs 47151ndash184

Alley RB et al 2003 Abrupt climate change Science 299 2005ndash2010

974 BioScience bull October 2003 Vol 53 No 10

Plenary

Bowman RI 1961 Morphological Differentiation and Adaptation in theGalaacutepagos Finches University of California Publications in ZoologyVol 58 Berkeley University of California Press

mdashmdashmdash 1983 The songs of Darwinrsquos finches Pages 237ndash537 in Bowman RILeviton AE Berson M eds Galaacutepagos Organisms San Francisco Amer-ican Association for the Advancement of Science Pacific Division

Burns KJ Hackett SJ Klein NK 2002 Phylogenetic relationships andmorphological diversity in Darwinrsquos finches and their relatives Evo-lution 56 1240ndash1252

Bush MB Piperno DR Colinvaux PA DeOleveira PE Krissek LA Miller MCRowe WE 1992 A 14300-yr paleoecological profile of a lowland tropi-cal lake in Panama Ecological Monographs 62 251ndash275

Cane MA Molnar P 2001 Closing of the Indonesian seaway as a precursorto east African aridification around 3ndash4 million years ago Nature 411157ndash162

Colinvaux PA 1972 Climate and the Galaacutepagos Islands Nature 240 17ndash20mdashmdashmdash 1984 The Galaacutepagos climate Present and past Pages 55ndash69 in

Perry R ed Galaacutepagos Oxford (United Kingdom) Pergamon PressDarwin CR 1842 Journal of Researches into the Geology and Natural

History of the Various Countries Visited during the Voyage of H M SBeagle under the Command of Captain FitzRoy RN from 1832 to 1836London Henry Colburn

Dunbar RB Wellington GM Colgan MW Glynn PW 1994 Eastern Pacificsea surface temperature since 1600 AD The O18 record of climate vari-ability in Galaacutepagos corals Paleoceanography 9 291ndash315

Finston TL Peck SB 1997 Genetic differentiation and speciation in Stomion(Coleoptera Tenebrionidae) Flightless beetles of the Galaacutepagos IslandsEcuador Biological Journal of the Linnean Society 61 243ndash266

Givnish TJ 1998Adaptive plant evolution on islands Classical patterns mole-cular data new insights Pages 281ndash304 in Grant PR ed Evolution on Islands Oxford (United Kingdom) Oxford University Press

Grant BR Grant PR 1989 Evolutionary Dynamics of a Natural PopulationThe Large Cactus Finch of the Galaacutepagos Chicago University of ChicagoPress

mdashmdashmdash 1996 Cultural inheritance of song and its role in the evolution ofDarwinrsquos finches Evolution 50 2471ndash2487

Grant PR 1999 Ecology and Evolution of Darwinrsquos Finches Princeton (NJ)Princeton University Press

mdashmdashmdash 2001 Reconstructing the evolution of birds on islands 100 years ofresearch Oikos 92 385ndash403

Grant PR Grant BR 1998 Speciation and hybridization in island birds Pages142ndash162 in Grant PR ed Evolution on Islands Oxford (United Kingdom)Oxford University Press

mdashmdashmdash 2002a Unpredictable evolution in a 30-year study of Darwinrsquosfinches Science 296 707ndash711

mdashmdashmdash 2002b Adaptive radiation of Darwinrsquos finches American Scientist90 131ndash139

Grant PR Grant BR Petren K 2001 The founding of a new population by a single pair of individuals Establishment selection and populationexpansion Genetica 112113 359ndash382

Huxley JS 1942 Evolution The Modern Synthesis London Allen and Unwin

Johnson MP Raven PH 1973 Species number and endemism The Galaacutepagosarchipelago revisited Science 179 893ndash895

Keller LF Grant PR Grant BR Petren K 2001 Heritability of morphologi-cal traits in Darwinrsquos finches Misidentified paternity and maternal effects Heredity 87 325ndash336

Kerr RA 2001 The tropics return to the climate system Science 292 660ndash661Lack D 1947 Darwinrsquos finches Cambridge (United Kingdom) Cambridge

University PressLambeck K Chappell J 2001 Sea level change through the last glacial cycle

Science 292 679ndash686Mayr E 1942 Systematics and the Origin of Species New York Columbia

University Press

Newton I 1967 The adaptive variation and feeding ecology of some British

finches Ibis 109 33ndash98

Petren K Grant BR Grant PR 1999 A phylogeny of Darwinrsquos finches based

on microsatellite DNA length variation Proceedings of the Royal Soci-

ety of London B 266 321ndash329

Price T Lovette IJ Bermingham E Gibbs HL Richman AD 2000 The

imprint of history on communities of North American and Asian

warblers American Naturalist 156 354ndash367

Prodon R Thibault J-C Dejaifve P-A 2002 Expansion vs compression of

bird altitudinal ranges on a Mediterranean island Ecology 83 1294ndash1306

Ratcliffe LM Grant PR 1983a Species recognition in Darwinrsquos finches

(Geospiza Gould) I Discrimination by morphological cues Animal

Behaviour 31 1139ndash1153

mdashmdashmdash 1983b Species recognition in Darwinrsquos finches (Geospiza Gould)

II Geographic variation in mate preference Animal Behaviour 31

1154ndash1165

mdashmdashmdash 1985 Species recognition in Darwinrsquos finches (Geospiza Gould) III

Male responses to playback of different song types dialects and hetero-

specific songs Animal Behaviour 33 290ndash307

Richards OW 1948 Species formation in islands (review of Darwinrsquos Finches

by Lack D) Journal of Animal Ecology 17 83ndash84

Riedinger MA Steinitz-Kannan M Last WM Brenner M 2002 A ~6100 14C

yr record of El Nintildeo activity from the Galaacutepagos Islands Journal of

Paleontology 27 1ndash7

Sato A OrsquoHuigin C Figueroa F Grant PR Grant BR Tichy H Klein J 1999

Phylogeny of Darwinrsquos finches as revealed by mtDNA sequences

Proceedings of the National Academy of Sciences 96 5101ndash5106

Schluter D 2000 The Ecology of Adaptive Radiations Oxford (United King-

dom) Oxford University Press

Schluter D Grant PR 1984 Determinants of morphological patterns in

communities of Darwinrsquos finches American Naturalist 123 175ndash196

Seltzer GO Rodbell DT Baker PA Fritz SC Tapia PM Rowe HD Dunbar

RB 2002 Early warming of tropical South America at the last glacialndash

interglacial transition Science 296 1685ndash1686

Sequeira AS Lanteri AA Scataglini MA Confalonieri VA Farrell BD 2000

Are flightless Galapaganus weevils older than the Galaacutepagos Islands they

inhabit Heredity 85 20ndash29

Simpson GG 1944 Tempo and Mode in Evolution New York Columbia

University Press

Swarth HS 1931 The avifauna of the Galaacutepagos islands Occasional Papers

of the California Academy of Sciences 18 1ndash299

mdashmdashmdash 1934 The bird fauna of the Galaacutepagos islands in relation to species

formation Biological Reviews 9 213ndash234

Tudhope AW Chilcott CP McCulloch MT Cook ER Chappell J Ellam RM

Lea DW Lough JM Shimmield GB 2001 Variability in the El

NintildeondashSouthern Oscillation through a glacialndashinterglacial cycle Science

291 1511ndash1517

Vincek V OrsquoHuigin C Satta Y Takahata N Boag PT Grant PR Grant BR

Klein J 1996 How large was the founding population of Darwinrsquos

finches Proceedings of the Royal Society of London B 264 111ndash118

Woodward FI 1987 Climate and Plant Distribution London Cambridge Uni-

versity Press

Wright SD Young CG Dawson JW Whittaker DJ Gardner RC 2000

Riding the ice age El Nintildeo Pacific biogeography and evolution of

Metrosideros subg Metrosideros (Myrtaceae) inferred from nuclear

ribosomal DNA Proceedings of the National Academy of Sciences 97

4110ndash4123

October 2003 Vol 53 No 10 bull BioScience 975

Plenary

and not species (Grant and Grant 2002b) Another remark-able feature is that they have remained relatively undifferen-tiated in morphology ecology and behavior This is not expected on the basis of the view that niches were varied plen-tiful and evolutionarily within reach at that time Howeverwe must acknowledge the possibility perhaps even the prob-ability that extinction has robbed us of other species that wereformed then The morphological similarity of these finchescontrasting with their distinctness from continental rela-tives argues for an early adaptation to an unusual niche

One of the warbler finch lineages gave rise to all otherfinch species Early products of the diversification were the veg-etarian finch (Platyspiza crassirostris) the Cocos finch(Pinaroloxias inornata) on either Galaacutepagos or Cocos Island(Grant and Grant 2002b) and the sharp-beaked groundfinch (G difficilis) The most recent products were a group ofground finch species (Geospiza) and a group of tree finchspecies (Camarhynchus and Cactospiza) (figure 8)

Effects of environmental change have left a different his-torical imprint on the older species Populations of G diffi-cilis differ strongly in morphology and ecology to a degree un-matched by all other and younger species in the genusGeospiza and by the warbler finches that preceded themSome G difficilis have persisted in Zanthoxylum forest at midand upper elevations which we believe to be old and others have entered arid lowland habitat perhaps when theZanthoxylum forest gradually disappeared from low islandsas the climate changed This may have been the first step ofthe radiation of ground finches In contrast to the G difficilispopulations populations of the vegetarian finch are mor-phologically and ecologically very similar Limited genetic data(Petren et al 1999) suggest that they separated from each otherrecently This is surprising as it is not expected from the ageof the species or from the presumed stability of its mid-elevation transition zone habitat The vegetarian finch mayhave become restricted to one or two islands and other pop-ulations or even related species may have become extinctin response to one of the recent extreme fluctuations in climate Its vegetarian diet may have made it vulnerable intimes of drought and competition with other species may havebeen an additional factor

The importance of environmental change in speciation isfurther suggested by the fact that in the last million years newspecies evolved in the habitats most vulnerable to changeGeospiza were added to lowland habitats and Camarhynchuswere added to the upland humid forest The change in climatetoward seasonal aridity and the development of arid lowlandhabitat provided the opportunity for a new granivorous wayof finch life now adopted by Geospiza species Some of thesemodern species may have contributed to the extinction ofolder ones through competitive superiority in a changingenvironment This is one possible interpretation of the contrast between the morphological distinctness of the threeolder groups Certhidea Platyspiza and G difficilis and themorphological similarity of species in the younger generaCamarhynchus Cactospiza and Geospiza

These ideas on speciation and extinction together with ob-servations of the colonization of Daphne Major by G magni-rostris (Grant et al 2001) suggest that periods of expansionsuch as the one in progress are preceded and followed by periods of range contraction and extinction caused by envi-ronmental change Distributions of habitats sea level islandand population sizes and degrees of isolation provide favorable conditions for divergence of small populations inisolation at some times and for dispersal mixing establish-ment of sympatry and hybridization at others The buildupof complex communities from simple ones is not smooth con-tinuous and regular but a process of gains and losses with anet accumulation of species over the long term

ConclusionsAccording to the standard allopatric model speciation beginswith the establishment of a new population continues withthe divergence of that population from its parent populationand is completed when members of two diverged populationscan coexist in sympatry without interbreeding We stand a virtually negligible chance of observing the whole process under natural circumstances Nevertheless it is possible tomake relevant observations in nature of all steps in theprocess We have described the strong role played by envi-ronmental change at each of the three steps in the speciationof Darwinrsquos finches The full adaptive radiation was pro-duced by a repetition of these steps each with a different product under somewhat different circumstances The challenge now is to account for the differences in terms of pastenvironments without the help of fossils of finches or ofother members of the biota We have sketched a frameworkfor doing this by using molecular genetic information to estimate the finch phylogeny and using geological and climaticinformation to reconstruct Galaacutepagos environments in thepast 2 million to 3 million years A better understanding ofenvironmental change on this time scale will help to explainwhy 14 species were formed what their sequence of origin wasand why they evolved their particular unique features Theremay be more history to uncover in finch DNA if only we canwork out how to read it

Acknowledgments We thank Ken Petren for figure 8 and Phil Hedrick FritzTrillmich and an anonymous reviewer for comments on themanuscript We are grateful to the Galaacutepagos National Parkand the Charles Darwin Research Station for permission andlogistical support for the fieldwork and to the National Sciences and Engineering Research Council of Canada and theNational Science Foundation for funding support

References citedAbbott I Abbott LK Grant PR 1977 Comparative ecology of Galaacutepagos

ground finches (Geospiza Gould) Evaluation of the importance of floris-tic diversity and interspecific competition Ecological Monographs 47151ndash184

Alley RB et al 2003 Abrupt climate change Science 299 2005ndash2010

974 BioScience bull October 2003 Vol 53 No 10

Plenary

Bowman RI 1961 Morphological Differentiation and Adaptation in theGalaacutepagos Finches University of California Publications in ZoologyVol 58 Berkeley University of California Press

mdashmdashmdash 1983 The songs of Darwinrsquos finches Pages 237ndash537 in Bowman RILeviton AE Berson M eds Galaacutepagos Organisms San Francisco Amer-ican Association for the Advancement of Science Pacific Division

Burns KJ Hackett SJ Klein NK 2002 Phylogenetic relationships andmorphological diversity in Darwinrsquos finches and their relatives Evo-lution 56 1240ndash1252

Bush MB Piperno DR Colinvaux PA DeOleveira PE Krissek LA Miller MCRowe WE 1992 A 14300-yr paleoecological profile of a lowland tropi-cal lake in Panama Ecological Monographs 62 251ndash275

Cane MA Molnar P 2001 Closing of the Indonesian seaway as a precursorto east African aridification around 3ndash4 million years ago Nature 411157ndash162

Colinvaux PA 1972 Climate and the Galaacutepagos Islands Nature 240 17ndash20mdashmdashmdash 1984 The Galaacutepagos climate Present and past Pages 55ndash69 in

Perry R ed Galaacutepagos Oxford (United Kingdom) Pergamon PressDarwin CR 1842 Journal of Researches into the Geology and Natural

History of the Various Countries Visited during the Voyage of H M SBeagle under the Command of Captain FitzRoy RN from 1832 to 1836London Henry Colburn

Dunbar RB Wellington GM Colgan MW Glynn PW 1994 Eastern Pacificsea surface temperature since 1600 AD The O18 record of climate vari-ability in Galaacutepagos corals Paleoceanography 9 291ndash315

Finston TL Peck SB 1997 Genetic differentiation and speciation in Stomion(Coleoptera Tenebrionidae) Flightless beetles of the Galaacutepagos IslandsEcuador Biological Journal of the Linnean Society 61 243ndash266

Givnish TJ 1998Adaptive plant evolution on islands Classical patterns mole-cular data new insights Pages 281ndash304 in Grant PR ed Evolution on Islands Oxford (United Kingdom) Oxford University Press

Grant BR Grant PR 1989 Evolutionary Dynamics of a Natural PopulationThe Large Cactus Finch of the Galaacutepagos Chicago University of ChicagoPress

mdashmdashmdash 1996 Cultural inheritance of song and its role in the evolution ofDarwinrsquos finches Evolution 50 2471ndash2487

Grant PR 1999 Ecology and Evolution of Darwinrsquos Finches Princeton (NJ)Princeton University Press

mdashmdashmdash 2001 Reconstructing the evolution of birds on islands 100 years ofresearch Oikos 92 385ndash403

Grant PR Grant BR 1998 Speciation and hybridization in island birds Pages142ndash162 in Grant PR ed Evolution on Islands Oxford (United Kingdom)Oxford University Press

mdashmdashmdash 2002a Unpredictable evolution in a 30-year study of Darwinrsquosfinches Science 296 707ndash711

mdashmdashmdash 2002b Adaptive radiation of Darwinrsquos finches American Scientist90 131ndash139

Grant PR Grant BR Petren K 2001 The founding of a new population by a single pair of individuals Establishment selection and populationexpansion Genetica 112113 359ndash382

Huxley JS 1942 Evolution The Modern Synthesis London Allen and Unwin

Johnson MP Raven PH 1973 Species number and endemism The Galaacutepagosarchipelago revisited Science 179 893ndash895

Keller LF Grant PR Grant BR Petren K 2001 Heritability of morphologi-cal traits in Darwinrsquos finches Misidentified paternity and maternal effects Heredity 87 325ndash336

Kerr RA 2001 The tropics return to the climate system Science 292 660ndash661Lack D 1947 Darwinrsquos finches Cambridge (United Kingdom) Cambridge

University PressLambeck K Chappell J 2001 Sea level change through the last glacial cycle

Science 292 679ndash686Mayr E 1942 Systematics and the Origin of Species New York Columbia

University Press

Newton I 1967 The adaptive variation and feeding ecology of some British

finches Ibis 109 33ndash98

Petren K Grant BR Grant PR 1999 A phylogeny of Darwinrsquos finches based

on microsatellite DNA length variation Proceedings of the Royal Soci-

ety of London B 266 321ndash329

Price T Lovette IJ Bermingham E Gibbs HL Richman AD 2000 The

imprint of history on communities of North American and Asian

warblers American Naturalist 156 354ndash367

Prodon R Thibault J-C Dejaifve P-A 2002 Expansion vs compression of

bird altitudinal ranges on a Mediterranean island Ecology 83 1294ndash1306

Ratcliffe LM Grant PR 1983a Species recognition in Darwinrsquos finches

(Geospiza Gould) I Discrimination by morphological cues Animal

Behaviour 31 1139ndash1153

mdashmdashmdash 1983b Species recognition in Darwinrsquos finches (Geospiza Gould)

II Geographic variation in mate preference Animal Behaviour 31

1154ndash1165

mdashmdashmdash 1985 Species recognition in Darwinrsquos finches (Geospiza Gould) III

Male responses to playback of different song types dialects and hetero-

specific songs Animal Behaviour 33 290ndash307

Richards OW 1948 Species formation in islands (review of Darwinrsquos Finches

by Lack D) Journal of Animal Ecology 17 83ndash84

Riedinger MA Steinitz-Kannan M Last WM Brenner M 2002 A ~6100 14C

yr record of El Nintildeo activity from the Galaacutepagos Islands Journal of

Paleontology 27 1ndash7

Sato A OrsquoHuigin C Figueroa F Grant PR Grant BR Tichy H Klein J 1999

Phylogeny of Darwinrsquos finches as revealed by mtDNA sequences

Proceedings of the National Academy of Sciences 96 5101ndash5106

Schluter D 2000 The Ecology of Adaptive Radiations Oxford (United King-

dom) Oxford University Press

Schluter D Grant PR 1984 Determinants of morphological patterns in

communities of Darwinrsquos finches American Naturalist 123 175ndash196

Seltzer GO Rodbell DT Baker PA Fritz SC Tapia PM Rowe HD Dunbar

RB 2002 Early warming of tropical South America at the last glacialndash

interglacial transition Science 296 1685ndash1686

Sequeira AS Lanteri AA Scataglini MA Confalonieri VA Farrell BD 2000

Are flightless Galapaganus weevils older than the Galaacutepagos Islands they

inhabit Heredity 85 20ndash29

Simpson GG 1944 Tempo and Mode in Evolution New York Columbia

University Press

Swarth HS 1931 The avifauna of the Galaacutepagos islands Occasional Papers

of the California Academy of Sciences 18 1ndash299

mdashmdashmdash 1934 The bird fauna of the Galaacutepagos islands in relation to species

formation Biological Reviews 9 213ndash234

Tudhope AW Chilcott CP McCulloch MT Cook ER Chappell J Ellam RM

Lea DW Lough JM Shimmield GB 2001 Variability in the El

NintildeondashSouthern Oscillation through a glacialndashinterglacial cycle Science

291 1511ndash1517

Vincek V OrsquoHuigin C Satta Y Takahata N Boag PT Grant PR Grant BR

Klein J 1996 How large was the founding population of Darwinrsquos

finches Proceedings of the Royal Society of London B 264 111ndash118

Woodward FI 1987 Climate and Plant Distribution London Cambridge Uni-

versity Press

Wright SD Young CG Dawson JW Whittaker DJ Gardner RC 2000

Riding the ice age El Nintildeo Pacific biogeography and evolution of

Metrosideros subg Metrosideros (Myrtaceae) inferred from nuclear

ribosomal DNA Proceedings of the National Academy of Sciences 97

4110ndash4123

October 2003 Vol 53 No 10 bull BioScience 975

Plenary

Bowman RI 1961 Morphological Differentiation and Adaptation in theGalaacutepagos Finches University of California Publications in ZoologyVol 58 Berkeley University of California Press

mdashmdashmdash 1983 The songs of Darwinrsquos finches Pages 237ndash537 in Bowman RILeviton AE Berson M eds Galaacutepagos Organisms San Francisco Amer-ican Association for the Advancement of Science Pacific Division

Burns KJ Hackett SJ Klein NK 2002 Phylogenetic relationships andmorphological diversity in Darwinrsquos finches and their relatives Evo-lution 56 1240ndash1252

Bush MB Piperno DR Colinvaux PA DeOleveira PE Krissek LA Miller MCRowe WE 1992 A 14300-yr paleoecological profile of a lowland tropi-cal lake in Panama Ecological Monographs 62 251ndash275

Cane MA Molnar P 2001 Closing of the Indonesian seaway as a precursorto east African aridification around 3ndash4 million years ago Nature 411157ndash162

Colinvaux PA 1972 Climate and the Galaacutepagos Islands Nature 240 17ndash20mdashmdashmdash 1984 The Galaacutepagos climate Present and past Pages 55ndash69 in

Perry R ed Galaacutepagos Oxford (United Kingdom) Pergamon PressDarwin CR 1842 Journal of Researches into the Geology and Natural

History of the Various Countries Visited during the Voyage of H M SBeagle under the Command of Captain FitzRoy RN from 1832 to 1836London Henry Colburn

Dunbar RB Wellington GM Colgan MW Glynn PW 1994 Eastern Pacificsea surface temperature since 1600 AD The O18 record of climate vari-ability in Galaacutepagos corals Paleoceanography 9 291ndash315

Finston TL Peck SB 1997 Genetic differentiation and speciation in Stomion(Coleoptera Tenebrionidae) Flightless beetles of the Galaacutepagos IslandsEcuador Biological Journal of the Linnean Society 61 243ndash266

Givnish TJ 1998Adaptive plant evolution on islands Classical patterns mole-cular data new insights Pages 281ndash304 in Grant PR ed Evolution on Islands Oxford (United Kingdom) Oxford University Press

Grant BR Grant PR 1989 Evolutionary Dynamics of a Natural PopulationThe Large Cactus Finch of the Galaacutepagos Chicago University of ChicagoPress

mdashmdashmdash 1996 Cultural inheritance of song and its role in the evolution ofDarwinrsquos finches Evolution 50 2471ndash2487

Grant PR 1999 Ecology and Evolution of Darwinrsquos Finches Princeton (NJ)Princeton University Press

mdashmdashmdash 2001 Reconstructing the evolution of birds on islands 100 years ofresearch Oikos 92 385ndash403

Grant PR Grant BR 1998 Speciation and hybridization in island birds Pages142ndash162 in Grant PR ed Evolution on Islands Oxford (United Kingdom)Oxford University Press

mdashmdashmdash 2002a Unpredictable evolution in a 30-year study of Darwinrsquosfinches Science 296 707ndash711

mdashmdashmdash 2002b Adaptive radiation of Darwinrsquos finches American Scientist90 131ndash139

Grant PR Grant BR Petren K 2001 The founding of a new population by a single pair of individuals Establishment selection and populationexpansion Genetica 112113 359ndash382

Huxley JS 1942 Evolution The Modern Synthesis London Allen and Unwin

Johnson MP Raven PH 1973 Species number and endemism The Galaacutepagosarchipelago revisited Science 179 893ndash895

Keller LF Grant PR Grant BR Petren K 2001 Heritability of morphologi-cal traits in Darwinrsquos finches Misidentified paternity and maternal effects Heredity 87 325ndash336

Kerr RA 2001 The tropics return to the climate system Science 292 660ndash661Lack D 1947 Darwinrsquos finches Cambridge (United Kingdom) Cambridge

University PressLambeck K Chappell J 2001 Sea level change through the last glacial cycle

Science 292 679ndash686Mayr E 1942 Systematics and the Origin of Species New York Columbia

University Press

Newton I 1967 The adaptive variation and feeding ecology of some British

finches Ibis 109 33ndash98

Petren K Grant BR Grant PR 1999 A phylogeny of Darwinrsquos finches based

on microsatellite DNA length variation Proceedings of the Royal Soci-

ety of London B 266 321ndash329

Price T Lovette IJ Bermingham E Gibbs HL Richman AD 2000 The

imprint of history on communities of North American and Asian

warblers American Naturalist 156 354ndash367

Prodon R Thibault J-C Dejaifve P-A 2002 Expansion vs compression of

bird altitudinal ranges on a Mediterranean island Ecology 83 1294ndash1306

Ratcliffe LM Grant PR 1983a Species recognition in Darwinrsquos finches

(Geospiza Gould) I Discrimination by morphological cues Animal

Behaviour 31 1139ndash1153

mdashmdashmdash 1983b Species recognition in Darwinrsquos finches (Geospiza Gould)

II Geographic variation in mate preference Animal Behaviour 31

1154ndash1165

mdashmdashmdash 1985 Species recognition in Darwinrsquos finches (Geospiza Gould) III

Male responses to playback of different song types dialects and hetero-

specific songs Animal Behaviour 33 290ndash307

Richards OW 1948 Species formation in islands (review of Darwinrsquos Finches

by Lack D) Journal of Animal Ecology 17 83ndash84

Riedinger MA Steinitz-Kannan M Last WM Brenner M 2002 A ~6100 14C

yr record of El Nintildeo activity from the Galaacutepagos Islands Journal of

Paleontology 27 1ndash7

Sato A OrsquoHuigin C Figueroa F Grant PR Grant BR Tichy H Klein J 1999

Phylogeny of Darwinrsquos finches as revealed by mtDNA sequences

Proceedings of the National Academy of Sciences 96 5101ndash5106

Schluter D 2000 The Ecology of Adaptive Radiations Oxford (United King-

dom) Oxford University Press

Schluter D Grant PR 1984 Determinants of morphological patterns in

communities of Darwinrsquos finches American Naturalist 123 175ndash196

Seltzer GO Rodbell DT Baker PA Fritz SC Tapia PM Rowe HD Dunbar

RB 2002 Early warming of tropical South America at the last glacialndash

interglacial transition Science 296 1685ndash1686

Sequeira AS Lanteri AA Scataglini MA Confalonieri VA Farrell BD 2000

Are flightless Galapaganus weevils older than the Galaacutepagos Islands they

inhabit Heredity 85 20ndash29

Simpson GG 1944 Tempo and Mode in Evolution New York Columbia

University Press

Swarth HS 1931 The avifauna of the Galaacutepagos islands Occasional Papers

of the California Academy of Sciences 18 1ndash299

mdashmdashmdash 1934 The bird fauna of the Galaacutepagos islands in relation to species

formation Biological Reviews 9 213ndash234

Tudhope AW Chilcott CP McCulloch MT Cook ER Chappell J Ellam RM

Lea DW Lough JM Shimmield GB 2001 Variability in the El

NintildeondashSouthern Oscillation through a glacialndashinterglacial cycle Science

291 1511ndash1517

Vincek V OrsquoHuigin C Satta Y Takahata N Boag PT Grant PR Grant BR

Klein J 1996 How large was the founding population of Darwinrsquos

finches Proceedings of the Royal Society of London B 264 111ndash118

Woodward FI 1987 Climate and Plant Distribution London Cambridge Uni-

versity Press

Wright SD Young CG Dawson JW Whittaker DJ Gardner RC 2000

Riding the ice age El Nintildeo Pacific biogeography and evolution of

Metrosideros subg Metrosideros (Myrtaceae) inferred from nuclear

ribosomal DNA Proceedings of the National Academy of Sciences 97

4110ndash4123

October 2003 Vol 53 No 10 bull BioScience 975

Plenary