1-s2.0-S0031018201003467-main

Palaeotrends

The structure of species, outcomes of speciation and the`species problem': ideas for paleobiology

William Miller IIIGeology Department, Humboldt State University, Arcata, CA 95521, USA

Received 25 July 2001; received in revised form 23 August 2001; accepted 23 August 2001

Abstract

Paleobiologists reviewing the recent literature on species concepts are likely to come away with the impression thatthe fundamental unit of biodiversity is impossible to define in terms of a universal concept that applies to all forms ofcellular life and the varied outcomes of species-level evolution. Operational concepts are likely to differ from specialty tospecialty in biology, but a general theory of species has been available for nearly 50 yr in the form of G.G. Simpson'sevolutionary species concept. In addition to this, a general picture of species structure has been accepted for at least aslong, consisting of demes or habitat clusters that bud off other demes/clusters, split, fuse and often go extinct. Morerecently, it has become obvious that the outcomes or products of species-level evolution may include any of thefollowing: speciation with morphologic differentiation (producing the so-called `good species' of applied biology andprobably the stable entities resolved in patterns of stasis in the fossil record); speciation without pronounced phenotypicdifferentiation (cryptic species) ; or acquisition of diagnosable characters without either complete reproductive isolationor pronounced morphologic change. The view that species are lineages containing networks of demes (or habitatclusters of uniparental organisms), each with its own biologic tendencies and role ^ with a unique place within a cladecomposed of similar historical entities, each having a certain kind of internal structure and resulting from a differentevolutionary outcome ^ is the ultimate concept many of the operational approaches seem to be aiming to uncover.Considering species structure, speciation outcomes and the evolutionary species concept together brings the nature ofspecies into a much sharper focus. ß 2001 Elsevier Science B.V. All rights reserved.

Keywords: species-level evolution; species concepts; internal structure; evolutionary outcomes; historical entities; ontology

`Ìf we accept the assumption of most systemat-ists and evolutionists that species are real things innature, and if the sets of species speci¢ed by di¡er-ent concepts do not overlap, then it is reasonable toconclude that real entities of the world are beingconfused.''

Cracraft, 2000

``The problem is that no single de¢nition of thespecies category has proved optimal for all of itsdi¡erent uses. Consequently, although one de¢ni-tion or class of de¢nitions has often come to befavored for a certain period of time or by a certaingroup of biologists, none of them has enjoyed uni-versal endorsement within biology as a whole. Thissituation has come to be known as `the speciesproblem'.''

de Queiroz, 1998

0031-0182 / 01 / $ ^ see front matter ß 2001 Elsevier Science B.V. All rights reserved.PII: S 0 0 3 1 - 0 1 8 2 ( 0 1 ) 0 0 3 4 6 - 7

E-mail address: [email protected] (W. Miller III).

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Palaeogeography, Palaeoclimatology, Palaeoecology 176 (2001) 1^10

www.elsevier.com/locate/palaeo

``Theory neutral concepts are impossible, buteven if they were possible, they would be undesir-able.''

Hull, 1997

1. Introduction

Sampling the vast literature on species conceptsprobably leaves most readers with the unsettlingfeeling that one of the central issues or core con-cepts of biology ^ the nature of species as thefundamental units of biodiversity and evolution-ary patterns ^ is becoming hopelessly confused bya seemingly endless proliferation of ideas. Themore pragmatic readers have always investigatedthe various proposals and, like discriminatingshoppers, selected the versions that best suitedtheir favorite group of organisms or research pro-grams. My reaction to the so-called `species prob-lem' is entirely di¡erent: I think the problem hasbeen solved, or nearly so, and that the ongoingdebate is really about ironing out details.

There are three reasons for my reaction. First,we have had a realistic picture of the internalorganization of species for at least 50 yr (reallysince Wright's (e.g., 1932) early contributions inpopulation genetics) : we know that species usu-ally consist of multiple populations geographicallyand temporally separated from one another; thatthese subdivisions bud o¡ from other populations,divide, fuse or go extinct; and therefore the struc-ture of species is like the bundle of ¢bers makingup a hemp rope (G.G. Simpson's (1953, ¢gure 48)classic line-drawing is the basic model). Second,the `conceptual space' of possible species conceptsalready has been rather thoroughly explored. Themajor categories of concept include those thatstress reproductive isolation, recognition or cohe-sion (integration of the genotype) ; those that viewspecies as historical entities or lineages that can beobjectively identi¢ed as being more or less relatedto other such entities (phylogenetic units) ; andthose that stress some form of compositional(phenotypic, genetic) similarity or separationwithout paying too much attention to evolutiontheory (Hull, 1997). Any future proposal of a newconcept is likely to be a variation or expansion of

one of these three major themes. And third, theoutcomes or products of species-level evolutionare fairly well known, and include speciationwith or without pronounced morphologic di¡er-entiation (Vrba, 1980).

In this essay I will argue that a universal con-cept of species, one that could potentially includeall kinds of cellular life and evolutionary prod-ucts, is within view and depends on the three de-velopments mentioned above. This is not to saythat all the problems associated with the speciescategory have been settled. It is still unclear, insome important practical cases, how to accommo-date uniparental or asexual organisms, the out-comes of hybridization (two problems that havealways dogged the neobiology community), andthe results of apparently transspeci¢c anageneticevolution (a problem close to home for paleobiol-ogists). I will begin with a brief review of the largeamount of recent work on species concepts, thenillustrate what I call the structure of species, relatethis to outcomes or products of species-level evo-lution, and end by claiming that the most realisticspecies theory ^ not the most e¡ectual or univer-sal operational concept (see the recent discussionsby de Queiroz (1999) and Hey (2001)) ^ has beenavailable for 50 yr.

2. Progress in the conceptualization of species

To begin to understand what the phylogeneticsystematists and evolution theorists are discussingthese days, paleobiologists will need to do somehomework. In order to come up to full speedwithout getting lost in the scattered literature, Irecommend the comprehensive (and surprisinglyreadable) summary of species concepts by May-den (1997) as the starting place. Mayden reviewed25 more or less di¡erent concepts, attempted tosynonymize some of the concepts, and used directquotes of the de¢nitions proposed by various au-thors, producing a handy identi¢cation manual ofspecies concepts. The briefer reviews by Harrison(1998) and de Queiroz (1998) also are useful.After a sti¡ dose of de¢nitions (Table 1 lists thepractical concepts most often mentioned in sum-maries), I recommend some critical re£ection in

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W. Miller III / Palaeogeography, Palaeoclimatology, Palaeoecology 176 (2001) 1^102

the form of two recent essays by Hull (1997;1999). Stocked with possible concepts and know-ing something about what the philosophers of bi-ology are saying to the apparent inability of biol-ogists to settle on a single concept for the basicunit of biodiversity, it would be time to plungeinto the freshest controversies surrounding theseissues by reading the extended debate by some ofthe most visible participants, edited by Wheelerand Meier (2000).

Going that far, readers are likely to make some

of the same generalizations that I have made inthe following list :

b Concepts stressing reproductive isolation, co-hesion or recognition are now seen by an increas-ing number of workers as secondary attributes ofpotentially more robust concepts, or simply to belimited to certain kinds of (bisexual, biparental)organisms.

b Most recent concepts view species as realthings in nature, not subjectively delineated clus-ters of specimens, with beginnings (speciation),

Table 1De¢nitions or characterizations of the most prominent operational species concepts related mostly to sexually reproducing organ-isms (based on Mayden, 1997; Harrison, 1998; de Queiroz, 1998; Wheeler and Meier, 2000)

Concepts related to reproductive isolation, internal cohesion or species recognition (e.g., isolation and maintance of reproductivenetworks)Reproductive isolationÌ de¢ne biological species as groups of interbreeding natural populations that are reproductively isolated from other such groups.Alternatively, one can say that a biological species is a reproductively cohesive assemblage of populations.'(Mayr, 2000, p.17)Cohesion`The cohesion concept species is the most inclusive population of individuals having the potential for phenotypic cohesionthrough intristic mechanismsT'(Templeton, 1989, p.12)RecognitionÀ species is that most inclusive population of inidvidual, biparental organisms which share a common fertilization system.'(Paterson, 1993, p.105)

Concepts depending on the properties of identi¢ed lineages (e.g., the various concepts within phylogenetic systematics)Hennigian`Species are reproductively isolated natural populations or groups of natural populations. They originate via the dissolution ofthe stem species in a speciation event and cease to exist either through extinction or speciation.'(Meier and Willmann, 2000, p.31)Diagnosable`We de¢ne species as the smallest aggregation of (sexual) populations or (asexual) lineages diagnosable by a unique combinationof character states.'(Wheeler and Platnick, 2000, p.58)MonophyleticÀ species is the least inclusive taxon recognized in a formal phylogenetic classi¢cation. As with all hierarchical levels of taxa insuch a classi¢cation, organisms are grouped into species because of evidence of monophyly.'(Mishler and Theriot, 2000, p.46-47)

Concepts based largely on compositional properties of specimensMorphologicA group of organisms delineated from other such groups based on possession of èssential morphologic attributes'.(Mayden, 1997, p.403)PheneticÒperationally, where variation in a set of characters is less within a group than between groups the entitiy is recognized as adistinct taxon.'(Mayden, 1997, p.404)Genetic`This concept is similar to the morphological species concept except that the method used to delineate species is a measure of ge-netic di¡erencesT independence is assessed using methods varying from chromatography, to protein electrophoresis, to sequencing.'(Mayden, 1997, p.399)

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W. Miller III / Palaeogeography, Palaeoclimatology, Palaeoecology 176 (2001) 1^10 3

individual histories and ends of some kind (extinc-tion).

b Many workers, but not all, can visualize spe-cies as the level of biologic organization at thetransition from dominance of tokogenesis to thedominance of phylogenesis (i.e., species undergomostly cladogenesis, but their component popula-tions have reticulated patterns of relationshipthrough time).

b Patterns of descent are paramount; pheneticpatterns are not always the most reliable sourcesof information in phylogenetic reconstructions.

b Most of the noise in the debate about whatspecies are comes from inside the phylogeneticsystematists' camp and involves operational issuessuch as whether or not ancestral species survivespeciation events, the signi¢cance and interpreta-tion of apomorphy and monophyly, and whether

or not theory should color the application of an-alytic methods.

b There appears to be no consensus aboutwhether a universal (or monistic) species conceptis available, or if pluralism is the best bet(although most participants in the debate prob-ably hold out hope for a universal theory of spe-cies).

Having said all of this, most applied biologists(neoecologists and paleoecologists, biogeogra-phers, biostratigraphers, conservation biologists)would still say that a `good species' ought to bereproductively isolated from other species andthat morphologic (really compositional) di¡eren-ces can be used to diagnose or recognize di¡erentspecies. And most theorists would agree that asex-ual or agamospecies, hybrid-forming species com-plexes or syngameons, and `chronospecies' (mor-

Fig. 1. The possible internal structures of species-lineages. In general, species consist of demes or habitat clusters, and compriseclades. A) A lineage consisting of a bundle of demes that oscillate through the phenotypic/habitat space of an established speciesbut does not ¢ll up the space, as in the other models. A variation of this structure involving the splitting and fusion of the bun-dles of lineages could be used to represent geographic races or population groups. B, D: Reminiscent of Simpson's (1953, ¢gure48) line-drawing of species structure, in which demes explore most of the phenotypic/habitat possibilities of a species or de¢nethose possibilities through time. The component demes bud o¡ from other demes, fuse or go extinct. B) consists of many demespacked into the space of the species, so that phenotypic distance between neighboring demes is not pronounced; D) featuresdemes having greater phenotypic separation (di¡erent traits associated with di¡erent habitats). C) represents a single, well-mixedpopulation ¢lling essentially the entire phenotypic/habitat space of an established species. Lineages that èscape' from the bounda-ries of adjacent cylinders and fuse could be used to represent hybrids. The phylogenetic tree to the right gives a sense of theupper level of organization (species-lineages 1^3 within a clade). Each of the cylinders represents an idealized internal structure.Small crosses are demic or habitat cluster extinctions. Speciation associated with pronounced phenotypic di¡erentiation (suggest-ing adaptive species-level evolution) is indicated with sm; speciation without this kind of di¡erentiation is indicated with s. Spe-cies-lineage boundaries are idealized as circular cylinders to emphasize prevalence of stasis; boundaries could be the result of ex-ternal controls or internal constraints.

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phologically di¡erentiated anagenetic species) stillare the sources of unresolved problems.

At this point I can o¡er two pieces of advice.Paleobiologists obviously need to test the watersand determine if their notion of species needs ad-justment to accommodate the recent thinking out-lined above. More importantly, generalizationsabout causation will always contain inherentweaknesses if the issue of ontology is never ad-equately addressed. What follows is an attempt toclarify the ontology^causation linkage.

3. The structure of species and species-levelevolution

Simpson ^ a paleontologist with the time di-mension clearly in mind ^ portrayed the internalstructure of a species-lineage (Simpson, 1953, ¢g-ure 48) as a bundle of anastomosing ¢bers orstrands (representing demes drawn throughtime), which in turn consist of trellis-like networksof sexually reproducing individual organisms. Thepurpose was to illustrate species as historical en-tities, as opposed to non-dimensional clusters ofsimilar specimens or isolated groups of organisms,

and to emphasize ``Tthat joining and anastomosisin phylogeny concern (major features of evolu-tion) only to the extent that they are part of theintimate mechanism of evolution which does riseto levels where joining no longer occurs'' (p. 378).I have used the same approach in Fig. 1 to at-tempt to illustrate the possible range of internalstructures of species-lineages, which is based onthe same kind of hierarchical thinking. By com-parison, the lineage structure diagrams used inrecent papers by phylogenetic systematists resem-ble more closely the structural model illustratedby Hennig (1966, ¢gures 4 and 6) in leaving outthe strands of demic systems and only showingnetworks of individuals within the lineages.Nevertheless, the general purpose is the same: tobegin to understand speciation one must under-stand what species are, and to do that one mustbe able to visualize their internal structure.

Each of the lineage segments in Fig. 1 repre-sents possible demic or population system struc-ture within an established biparental species overperhaps 103 to 104 generations (or if the species isuniparental, possibly 10 to 102 iterations of hab-itat separation). The individual strands are demesseparated in terms of phenotypic variation that

Fig. 2. Possible outcomes of species-level evolution. The matrix shown in (A) is based on Vrba's diagram (Vrba, 1980, ¢gure 5),and scores morphologic di¡erentiation against speciation. Most paleobiologists would agree that a `good' species ought to be dif-ferentiated and isolated (black square), and presume that cryptic species (gray square) are insigni¢cant. A more comprehensivepicture is shown in (B) in which the additional complication of diagnosable characters has been added. In this view of outcomes,the black cube is equivalent to isolated, di¡erentiated species-lineages produced when speciation and adaptive phenotypic trans-formation are associated (sm in Fig. 1). Many other possibilities are possible, including isolation without di¡erentiation or acqui-sition of new character states without complete isolation (gray cubes; represented by s in Fig. 1).

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corresponds to habitat separation. Boundaries ofthe species-lineages are idealized; they could havebeen depicted as meandering instead of straight-sided cylinders to emphasize the moving averageof phenotypic properties of the species, or theycould have been drawn having alternating wideand narrow sections indicating changes in themaximum variation in phenotypic properties orhabitat variation through time. I have used thevertical boundaries to emphasize overall species-lineage stability, which is realistic considering theprevalence of stasis in the fossil record (Jacksonand Cheetham, 1999; Jablonski, 2000; Bentonand Pearson, 2001). Demic systems bud o¡ fromestablished systems; drift or undergo directional,stabilizing or disruptive selection; fuse with otherdemes; or experience local extinction. Demes con-sisting of biparental organisms are in potentialreproductive connection within the cylinders, buthave potentially severed the connection or at leasthave acquired a unique diagnosable characterwhen they cross the boundary (begin toèscape'from the cylinder or domain of the establishedspecies). For uniparental organisms, the represen-tation of `demes' as separate strands also repre-sents spatial or habitat separation. Fusion wouldoccur when these separate clusters are reunited ina mixed habitat cluster or possibly owing to `lat-eral' genetic exchanges (Templeton, 1989 Margu-lis, 1993; Sapp, 1994); extinction would occurwhen a local cluster or variant is eliminated.Crossing the boundary would again represent in-cipient speciation by acquisition of new charactersand potentially permanent habitat separation.

Several species structures are possible. In Fig. 1,structures B and D, consisting of reticulateddemes and many instances of local extinction ofpopulations/variants, are probably typical for an-imal and plant species deployed in multiple pop-ulations. The internal structure shown in A, in-volving a sinuous, vine-like pattern of demes,might result from environmental pacing or devel-opmental changes in regional ecosystems, with thedomain of the species-lineage remaining essen-tially ¢xed (de¢ned by the potential range of phe-notypes of population systems). Structure C issupposed to represent one large `deme' ¢llingthe potential phenotypic/habitat space of an es-

tablished species without signi¢cant internal dis-continuity. This might occur in some pelagic spe-cies (but see the recent review by Norris (2000)suggesting previously undetected populationstructure and di¡erentiation in pelagic systems)or in well-mixed cultures of micro-organisms.

Demes of biparental organisms or habitat clus-ters of phenotypically identical uniparental clonesare mainly con¢ned to cylinders because the crosssections represent the range of (externally or in-ternally controlled) conditions in which survivaland ¢tness are supported (see the discussion of`cohesion mechanisms' in Templeton, 1989);crossing the boundary amounts to relinquishinga stable association with environmental and eco-logic factors or exceeding some form of cohesion(small arrows marked with s). A thorough discus-sion of processes occurring at the boundary ^where speciation begins ^ can be found in Futuy-ma's (1986) excellent book. Rarely, and perhapsonly when new adaptive opportunities occur, willthese excursions result in a speciation event thatcoincides with morphologic (adaptive) di¡erentia-tion (marked with sm in the phylogenetic tree). Inother words, the escape of population systemsfrom established species, or the àttempt' to es-cape, could be a fairly common phenomenon(Williams, 1992), but the successful establishmentof isolated, di¡erentiated new species-lineageswould have to coincide with the provision of en-vironmental or ecologic opportunity (Eldredge,1995; Miller, in press). The resulting entities areexpected to become the essentially static species-lineages emphasized in the theory of punctuatedequilibria (Eldredge and Gould, 1972; Gould andEldredge, 1993).

The possible outcomes of species-level evolu-tion were depicted by Vrba (1980, ¢gure 5), interms of speciation with or without morphologicdi¡erentiation (Fig. 2A). These model outcomeshave been discussed recently by Eldredge (1989,1995). I have expanded this generalization to in-clude acquisition of a diagnosable character,which may or may not coincide with completereproductive isolation and pronounced morpho-logic di¡erentiation (Fig. 2B). Is there any speciesconcept that could accommodate all of these po-tential structures, outcomes and complications?

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4. The `species problem' has been solved! (around50 yr ago)

We know that the internal structure of species-lineages must look something like one of the mod-els in Fig. 1, perhaps typically like versions B andD that recall the diagram used by Simpson (1953)to help visualize the same pattern. Species usuallyconsist of multiple demes or habitat clusters ofsome sort, which change through time, and inturn comprise clades of genealogically related lin-eages (Eldredge, 1985; 1989). Species-level evolu-tion could involve any of the outcomes depictedin Fig. 2B. At the same time, there is an increas-ing realization that species concepts based on op-erational criteria (gene £ow, tests of lineage re-latedness, purely compositional attributes) aresecondary, empirical approaches ^ they do nottake us all the way to the desired goal of a uni-versal concept, one that encompasses all evolu-tionary outcomes in all kinds of cellular life.

Many systematists and evolution theorists pic-ture the work on the `species problem' as a long,hard march that will take us to the ultimate van-tagepoint, and there we will see what speciesreally are like. In fact, the ultimate picture waspainted decades ago in the form of the theoreticalevolutionary species concept (Simpson, 1951;1961). The expanding work on operational con-cepts is extremely signi¢cant, but from a theoret-ical point of view it all amounts to clearing multi-ple paths toward the same goal (compare thiswith the similar assessment o¡ered by de Queiroz(1999)). Recent advocates (e.g., Wiley and May-den, 2000) of the evolutionary concept describe itas if it were a new solution to a old problem whenit has been with us since Simpson was attemptingto draw the broadest outlines of species and spe-ciation. The most widely quoted version is fromhis Principles of Animal Taxonomy (Simpson,1961, p. 153): `Àn evolutionary species is a line-age (an ancestral-descendant sequence of popula-tions) evolving separately from others and with itsown unitary evolutionary role and tendencies.''Critics of the concept point to vagueness of theterms `role' and `tendency', and declare it uselessas an operational approach. Proponents empha-size that the concept accommodates all kinds of

organisms and provides an ùltimate picture' (notan operational concept) ^ a conceptual goal ornecessary adjustment in the core concept ^ of spe-cies as historical entities (Mayden, 1997; Wileyand Mayden, 2000).

The possible structure of species, as depicted inFig. 1, is clearly compatible with this well-knownde¢nition of species. How could all the possibleoutcomes of species-level transformation (Fig. 2B)be accommodated within the concept? The estab-lishment of a new species probably involves some-thing like the following chain of events: (1) ap-pearance of an innovation (new character state,either as minor as a new protein structure or asmajor as a new anatomic feature, developmentalvariant, behavioral pattern or physiologic process)at the demic level ; (2) isolation or separation toconserve or protect the innovation (incipient spe-ciation) or simply geographic separation to keepthe new character from disappearing owing tointerbreeding; and in some cases (3) signi¢cantmorphologic di¡erentiation (adaptive transforma-tion) matching a resource opportunity or newecologic position. When the sequence includesthese steps, most paleobiologists would agreethat a new species-lineage has been established.The new species really emerges at the interfaceof tokogenetic processes and phylogenesis ^when the cylinder boundary has been crossed. Ap-pearance of a new character state without protec-tive reproductive isolation (for biparental organ-isms)/habitat separation (for asexuals) wouldleave the new lineage vulnerable when contact ismade with the ancestral lineage (by interbreeding(biparentals) if isolation has not been achieved;by competitive exclusion at the initiation of repro-ductive isolation/habitat separation) (Futuyma,1986; 1987). After establishment, intraspeci¢c an-agenetic evolution might result in the honing ofphenotypic properties to environmental or eco-logic windfall, or the new species-lineage mightemerge fully out¢tted for the opportunity orrole. In any case, if the steps produce a new, in-dependent lineage, Simpson's concept would ap-ply.

The ¢rst two steps described above could occuressentially simultaneously, or in reversed order. Itis also possible that reproductive isolation could

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occur without transformation of any other char-acter states except those producing or enforcingisolation. The result could be cryptic species thatresemble very closely ancestral or sister species interms of phenotypic properties. Traditional mor-phologic approaches to species delineation andidenti¢cation, in both neo- and paleobiology, arelikely to overlook these products of species-levelevolution (see discussion in Knowlton and Weigt,1997).

A di¡erent set of circumstances might producea spatially separated lineage having a single diag-nosable character, which could be maintained forlong intervals of time without complete reproduc-tive isolation (see Cracraft, 1989). Because thislineage would have èscaped' the domain of theancestral species-lineage (a cylinder boundary inFig. 1), it too could be accommodated in the evo-lutionary species concept. Prolonged separationwould result inevitably in reproductive isolationin biparentals (Turelli et al., 2001).

Strongly di¡erentiated new lineages are specialcases of outcome in which a non-trivial economicopportunity or role has been `discovered' or `cap-tured' by the new species. These are probably thestable lineages preserved in the fossil record aspatterns of species-lineage stasis. Species neverconquering a resource or capturing a signi¢canteconomic position may remain rare or vanishsoon after they emerge (see Stanley, 1979; El-dredge, 1995; McKinney et al., 1996), but theywould still qualify as evolutionary species. Thus,cellular life is composed of economically promi-nent `haves' and the less conspicuous `have-nots',both qualifying as good evolutionary species. Anynumber of operational approaches could be usedto discover them.

5. Conclusions

Debates about what makes a species a species,both from an operational and a theoretical pointof view, have always been at the heart of under-standing the processes and products of speciation:the issues of ontology and causation ^ as in manyother biologic problems ^ are inseparable. Paleobi-ologists need to pay close attention to recent de-

velopments surrounding the species problem, andto re-examine their own ideas about species con-cepts to incorporate the recent thinking outlinedabove. This is especially true in light of the wide-spread adoption of cladistic methods and the vis-ualization of species as historical entities (lineages).

There are interesting theoretical issues brewingthat relate directly to the problem of ontology.Not all species are born equal: some speciationevents produce new lineages that become thedominant players (the source of many local pop-ulations) in regional economies, while others pro-duce new species that never conquer a resource oracquire a prominent ecologic position. The formerare expected to be fully di¡erentiated in pheno-typic characters compared to ancestral species(i.e., to feature new adaptations) ; the latter maynever achieve such di¡erentiation. Both, however,are kinds of species-lineages and are accommo-dated in the evolutionary species concept. Line-ages of organisms that feature a few diagnosablecharacters, e¡ectively separated from the ancestrallineage preventing interbreeding but not achievingreproductive isolation, also are accommodated inthe concept. The relative frequency of these out-comes in various groups of organisms is not welldocumented, although typical occurrence ofstrong morphologic di¡erentiation during specia-tion as opposed to frequent formation of crypticspecies seems to be a more common event in somegroups than in others (compare the assessments oflate Cenozoic bryozoans in which speciation andmorphologic di¡erentiation apparently go hand inhand (Jackson and Cheetham, 1990) and modernbirds with possibly many cryptic species (Graham,1996)). Uniparental organisms are likewise ac-commodated if descendent lineages are at leastminimally di¡erentiated from ancestors andachieve habitat separation, so that their speciesstructure resembles that of biparental species.The signi¢cance of chronospecies (anagenetic lin-eage segments interpreted as separate species bysome taxonomists) may have been exaggerated inpaleontology; higher resolution records of speci-ation would probably reveal some form of clado-genesis as the dominant pattern in groups sup-posed to contain chronospecies (e.g., Norris,2000).

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Based upon what we now know about the in-ternal structure of species, the hierarchical rela-tionships of genealogic entities, and the possibleoutcomes of species-level evolution, a broadly ac-ceptable picture of species is within view, and has,in fact, been available as a formal de¢nition sinceSimpson (1951; 1953; 1961) grappled with thesesame issues nearly a half century ago. Viewing the`species problem' in terms of possible structureand speciation outcomes brings the picture of spe-cies as real things in nature into a much sharperfocus.

Acknowledgements

This essay resulted from involvement in theEcological Processes and Evolutionary RatesWorking Group supported by the National Centerfor Ecological Analysis and Synthesis (SantaBarbara, California), a center funded by theNational Science Foundation (Grant #DEB-94-21535), the University of California at SantaBarbara and the State of California. I am gratefulto Mike Benton and Niles Eldredge for theirreviews.

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