Concepts of coevolution

TREE vol. 4, no. 6, June 7989

Concepts The word coevolution has become a Stan- dard part of the lexicon of evolutionary 6iologg. More than 1000 papers during the past decade have used coevofution in the title or abstract. Hundreds more have used the word in passing in the body of the paper. A half dozen books now include coevolution in the title. As usage of coevolution has increased, so have the views on the processes and mechanisms of coevolutionarg change. The pro6lem now is to understand the ecological and genetic conditions that favor different modes and outcomes of coevolution.

Darwin did not use the word coevolution in the Origin of Species, but he did use coadaptation several times. Although he occasionally used coadaptation for describing the adaptation of one part of an organism to another, as in ‘the structure of a beetle which dives through the water’ (p. 61, 1st edn), he used it primarily for describing the adaptations ‘of one distinct organic being to another being’ (p. 60) in interspecific interactions. He thought of coadaptation as reciprocal change. Hence, in discussing the evolution of interactions between flowers and pollinators he writes: ‘Thus I can understand how a flower and a bee might slowly become, either simul- taneously or one after the other, modified and adapted in the most perfect manner to each other, by continued preservation of individuals presenting mutual and slightly favourable deviations of structure’ (p. 95).

The idea of reciprocal change in interacting species is what we now call coevolution. Although the word coevolution is occasionally appro- priated by some biologists to describe genetic correlations among traits within individuals or interactions among individuals within species, these usages have fortu- nately been rare. The utility and power of the concept of coevolution is in the idea that interactions between species can result in the partial coordination of non-mixing gene pools over evolutionary time.

in the 1940s through the 1960s three independent approaches were developed for the study of

John Thompson is at the Depts of Botany and Zoology, Washington State University, Pullman, WA 99164, USA.

reciprocal evolutionary change. Flor’ developed the concept of gene-for-gene interactions to ex- plain patterns of resistance and virulence between plants and pathogens, and Mode’s I958 paper* on gene-for-gene interactions, entitled ‘A mathematical model for the co-evolution of obligate parasites and their hosts’, seems to have been the first explicit mathematical model of coevolution. Beginning in 1961, Pimente13 developed the hypothesis of genetic feedback by which reciprocal genetic changes could regulate populations of interacting species. Both Flor’s and Pimentel’s approaches to reciprocal evolution in interacting species focused on changes in the adaptation of populations. In 1964 Ehrlich and Raven4 used the concept of reciprocal change much more broadly to link adaptation and speciation in interacting species. Their paper on the evolution of diversity in butterflies and flowering plants inspired most of the subsequent work on coevolution and promoted the development of a coevolutionary perspec- tive in ecology.

As the word coevolution increased in usage, so did its mean- ings. By the late 1970s coevolution was in danger of becoming syn- onymous with any aspect of evolution in interspecific interactions. lanzen5, in frustration, urged that the word not lose its important and distinct evolutionary meaning in a paper entitled ‘When is it coevolution?’ Since then, the word has been used more consistently as reciprocal evolutionary change in interacting species-. The key word is reciprocal, because the

of Coevolution John N. Thompson

central problem in coevolutionary studies is to understand the ecological and genetic conditions that permit interacting species to undergo repeated bouts of reciprocal genetic change specifically because of the interaction.

Although the general meaning of coevolution hds come into more consistent usage, it is becoming clear that this word is an umbrella for a variety of mechanisms and outcomes of reciprocal evolutionary change. Separating and understanding these different modes of coevolution will be one of the major problems for coevolutionary studies over the next decade. Here, I consider the five different modes of coevolution that have been suggested so far, beginning first with three that do not involve speciation (Table I). As we continue to learn more about the genetic mechanisms and ecological conditions governing coevolution, better ways of organizing our thinking on reciprocal evolutionary change will undoubtedly arise. The five modes that I consider here are intended only as an initial attempt to organ- ize the diversity of processes and outcomes that we collectively call coevolution.

Gene-for-gene coevolutlon The concept of gene-for-gene

coevolution is based upon the premise that parasites and hosts have complementary loci for virulence and resistance: each gene affecting virulence in the parasite population is matched by a specific gene affecting resistance in the host population. It is the para- digm under which much work on phytopathology in crop plants is

Table I. Suggested modes of coevolution and the kinds of species interaction in which they may be most likely to occur

Modes of coevolution Kinds of interaction

Gene-for-gene coevolution Pathogens and plants; some other parasites and hosts

Specific coevolution All interactions with reciprocal selection pressures; probably uncommon in competition

Guild r-,evolution All interactions

Diversirying coevolution Maternally-inherited symbionts and hosts; hosts and symbionts that regulate movement of host gametes; seed-parasitic pollinators and plants

Escape-and-radiation Parasites and hosts coevolution

0 1989. Elsev~er Scence PubIshers Ltd. (UK) 016%5347/89/$02 00 179


conducted. The most convincing evidence for gene-for-gene relationships in natural populations comes from Burdon’s work on interactions between wild oats (Avena spp.) and Puccinia rusts9ei0, and between Glycine canescens - a relative of soybeans - and soybean rust ( Phakopsora pachyrhizi) I I.

It is unlikely that all patterns of resistance and virulence will prove to be as discrete as predicted by a purely gene-for-gene interpret- ation. Although gene-for-gene relationships have been reported for at least 28 interactions between crop plants and pathogens, BarrettI has argued that the appar- ent commonness of these relationships may result from two biases. First, few quantitative genetic analyses have been made on interactions between plants and pathogens. Secondly, the commonness of gene-for-gene relationships within crop plants may be partially an artifact of plant breeding tech- niques and the cultivation of resis- tant varieties, which magnify single- gene effects.

Most coevolution between species will probably not fit the gene-for-gene hypothesis. Some, if not most, of the behavioral, mor- phological, physiological and life history characters affecting species interactions are likely to be deter- mined polygenically. Even in interactions between insects and plants, which share some simi- larities with plant-pathogen interactions, gene-for-gene coevolution is probably uncommon. Unlike pathogens, which have little direct control over their movements between plants, insects can often actively choose precisely where to lay their eggs. The genes involved in host selection by adults may be different from the genes that affect the ability of larvae or nymphs to survive on a particular host plant. Consequently, the evolutionary genetics of interactions between insects and plants is likely to be more complicated than that predicted by the gene-for-gene hypothesis unless adult preference and larval performance genes are few in number and are in strong linkage disequilibrium, or adult preference and larval performance are pleiotropic effects of the same gene.

Specific caevolution Coadaptation of two species

without specifying a gene-for-gene relationship is often referred to as specific coevolution, to differen- tiate it from interactions in which many species are interacting and coevolution between any two of the species may not be strictly reciprocal5. Specific coadaptation would probably be the better term for this kind of interaction, to separate it from modes of coevolution in which one species causes reproductive isolation in another species, but specific coevolution has become the more commonly used term.

Specific coevolution includes a variety of possible outcomes, such as ‘evolutionary arms races’, divergence of traits in competing species, and convergence of traits in mutualisms. Hairston’sr3 long- term observations and experiments on Hethodon salamanders provide perhaps the most convincing evidence for specific coevolution in competing species. Plethodon glu- tinosus and P. jordani vary geo- graphically in North Carolina in the intensity of interspecific competition. Hairston’s experiments, although indicating asymmetric re- sponses by these species, suggest that both species may have evolved increased interspecific in- terference mechanisms in the Great Smoky Mountains, where interspecific competition is strong, in comparison with populations in the Balsam Mountains, where interspecific competition is much weaker.

The results indicate that the salamanders may be involved in an ‘arms race’, through increases in interspecific aggressiveness, in communities where competitive interactions are intense. The alterna- tive response in these populations could have been divergence or convergence for limiting resources, or local extinction of one of the species - the expected results in most competitive interactionsr6i6, especially because asymmetries in competitive ability are com- monr7.r8. Hairston’s work highlights one of the pressing problems in studies of specific coevolution for all forms of species interaction: the need to understand the ecological and genetic conditions that favor

sustained arms races rather than some other coevolutionary or evolutionary outcome such as extinction, the development of polymorphisms, or a change in outcome (e.g. antagonism to commensalism or mutuaiisml19.20.

From work over the past two decades, it has become evident that demonstrating specific coevolution between two species is not a simple task. The problem for any particular interaction is to demonstrate that both species have evolved in response to the interaction. Reaching conclusions on coevolution will demand increasing links between population biology and systematics to decipher the kinds of ecological condition that favor coevolution rather than an evolutionary response in only one of the interacting species. Gilbert21, for example, has argued that the evolution of Mullerian mimicry complexes often involves convergence of species onto one model rather than coevolution of two or more distasteful species, except where the two species are approxi- mately equal in abundance and distastefulness.

Guild coevolution Reciprocal evolutionary change

may occur among groups of species rather than pairs of species. Although particular pairs of species in the interaction may undergo rare bouts of specific coevolutionary change, most of the change may be diffused among several or many species. This kind of reciprocal change has been called diffuse coevolution5 or guild coevolution22. Potential examples include the evolution of some mimicry complexes, and the interactions between frugivorous birds and fleshy- fruited plants, pollinators and flowering plants, and grazing mam- mals and grasses.

The concept of guild coevolution is important because it emphasizes that the evolutionary unit of an interaction may be broader than a pair of species. It is a useful heuris- tic tool for thinking about how interactions change and link together groups of species within communities. Interactions that begin as a pair of species may eventually grow to encompass more species. The original pair may speciate, creating

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complexes of related species, or unrelated species may be collected into the interactior6. This growth of an interaction may happen most easily in mutualistic associations in which a new resource (e.g. nectar, fruit) is being offered to attract a mutualist that visits host+.

Such easily exploitable new resources will often collect new species into the interaction. But accumulation of species can probably happen in most kinds of interaction. The growth of interactions will also create new lifestyles within communities. For example, some lifestyles of species involved in mutualisms are only possible once guilds of species interacting in similar ways have accumulated within a community. Obligately frugivorous birds are possible as evolutionary products only when there is a variety of fleshy-fruited plant species in a community, thereby creating year-round availability of fruit. Social bees that rely upon a variety of plant species throughout a season for pollen and nectar are another example.

The problem with the use of guild coevolution or diffuse coevolution is that it has no ob- vious limits short of some Gaia-like extreme of diffuse coevolution between &-consuming animals and C02-consuming plants. The concept loses its utility when it is applied so broadly that all possibility of analysis of the mechanisms of reciprocal change is lost. To be useful in studies of evolving interactions, the general concept of coevolution and the specific version called guild coevolution should be restricted to interactions in which we can see how natural selection is shaping reciprocal change in pairs or groups of species.

Diversifying coevolution The outcome of coevolution may

be restricted to changes in adaptation within the interacting populations as in the modes of coevolution above, or it may involve speciation in one or both species. The conditions under which coevolution produces reproductive isolation among populations are the least understood aspects of reciprocal evolutionary change.

Diversifying coevolution can be defined as reciprocal evolution be-

tween species in which the interaction causes at least one of the species to become subdivided into two or more reproductively isolated populations. Diversifying coevolution in which only one of the species undergoes speciation was previously called mixed- process coevolution23~24.

Some of the best potential examples of diversifying coevolution may be symbiont-induced speciation in organisms with maternally-inherited intracellular symbionts24. The acquisition of microorganisms (e.g. spiroplasmas or rickettsias) by a population can serve initially as a reproductive iso- lating barrier between host populations that either lack these symbionts or have them but interact with them in different ways. For example, reproductive isolation or hybrid inferiority among populations has been attributed to maternally-inherited symbionts in a variety of insect taxa, including flies, beetles and moth+. Sterility or death of hybrid males is one of the observed results of hybrid- ization between such populations. In some cases, natural selection could favor the reduction of hy brid inferiority, thereby preventing speciation. But if the populations are in different environments, the interactions between symbionts and hosts may differ initially or eventually in outcome, ranging from antagonism in one environ- ment to commensalism or mutualism in another. With different outcomes from these interactions driving natural selection, the various populations of symbionts and hosts could coadapt in different ways. The result of this differen- tial coevolution among populations could be a decreased likelihood that the initial reproductive barriers between the host populations would be overcome.

This view of symbiont-induced speciation requires that the outcomes of an interaction differ between populations and evolve rapidly in different directions. Rapid evolution of mutualism from antagonism in interactions between intracellular symbionts and hosts has, in fact, been observed twice under laboratory conditions during the past 15 years25t26. For example, Bouma and Lenski cultured a col-

Fig. I. Longitudinal cut through a globeflower. Coevolution between globeflowers (7’roNus europaeus) and Chiastocheta spp. flies has many similar- ities to the better known interactions between figs and fig wasps, and between yuccas and yucca moths. Unlike related species of Trokus, the petaloid sepals of T. europaeus do not open to allow pollinators to enter. Instead, adults of the several species of Chiastocheta flies, which are the sole pollinators of this plant species in northern Finland, must squeeze between the closed sepals to reach the plant carpels on which the flies lay their eggs. In the process, the flies passively deposit pollen on the stigmas. See Ref. 30 for more details. Photo by 0. Pellmyr.

ony of E. co/i and an antagonistic plasmid pACYCl84 in the presence of antibiotic for 500 generations. They then compared the fitness of each combination of host and plasmid (with and without antibiotic history) in competition with the baseline strain. They found that the treatment had resulted in increased adaptation of the host to the plasmid, but no change in adaptation in the plasmid. They also competed the evolved host and the baseline plasmid against an isogenic plasmid-free counterpart and found that the plasmid now increased the fitness of the host.

In a different set of interactions, M. Ebbert (PhD thesis, Yale Univer- sity, 1988) found that the mean and variance in the outcomes of interactions differ among inbred lines of Drosophila willistoni and their spiroplasma symbionts. Her results indicate that there is genetic variation in both the hosts and symbionts for traits that affect the outcomes of these interactions, and that coevolution between symbionts and hosts may be occurring.

In some cases, diversifying coevolution may result in reciprocal speciation induced by the interaction. Cospeciation would be the best word for this particular outcome of diversifying coevolution, but cospeciation has become en- trenched in the systematics litera- ture as a synonym for all instances of parallel cladogenesis of species regardless of whether reciprocal

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Fig. 2. Coevolution between butterflies and plants, although antagonistic rather than potentially mutualistic as in picture (a), provided the initial impetus for Paul Ehrlich and Peter Raven’s ideas on the process of reciprocal evolution in interacting species. (a) The western anise swallowtail butterfly, Papilio zelicaon, taking nectar from a thistle flower. Larvae of this species feed on plants in the family Umbelliferae throughout western North America, although some populations have shifted onto Citrus (Rutaceae) in recent decades in California. Photo by author. fbl Several Papilio species from western North America. Some of the species pictured here belong to the P. machaon group, which has radiated onto the plant families Umbelliferae. Rutaceae and Compositae; others belong to the P. glaucus group, which has radiated onto the Lauraceae, Rosaceae, Betulaceae, Salicaceae. and other plant families. Photo by W. Wehling.

evolution is involved27. Diversifying coevolution that results in multiple events of reciprocal speciation may be one of the least common outcomes of coevolution. The conditions most likely to favor this outcome seem to be those in which one species lives as a symbiont with a host and controls movement of gametes between hosts. In these cases, differentiation in the host and symbiont populations is mediated specifically through the pattern of movement of the symbionts among hosts6*24.

The interactions that seem to fit best these criteria for reciprocal diversification are those between plants and pollinators whose larvae feed as host-specific seed parasites on the same plants that the adults pollinate. These are interactions in which mutualism seems to have arisen from seed parasitism. At least three major pairs of taxa now

appear to be involved in these uncommon forms of pollinator- plant interaction: figs and agaonid wasps, yuccas and yucca moths, and globeflowers (Tro/hus) and Chiastocheta flies2a30 (Fig. 1 I. Whether reciprocal diversification actually is occurring has not yet been analysed for any of these interactions.

Escape-and-radiation coevolution Escape-and-radiation coevol-

ution is a specific form of how guild coevolution may involve both adaptation and speciation. It differs from other concepts of coevolution in that it explicitly includes, as an important component of the process, periods during which the interaction between the taxa does not occur. It was initially formulated by Ehrlich and Raven4 as a hypothesis for how coevolution may affect diversification in families of flowering plants and butterflies (Fig. 21. The hypothesis, however, can apply to all interactions between parasites and hosts.

Escape-and-radiation coevolution has five steps. (1 I Plants produce novel secondary compounds through mutation and recombi- nation. (2) The novel chemical compounds reduce the palatability of these plants to insects, and are therefore favored by natural selection. (3) Plants with these new compounds undergo evolutionary radiation into a new adaptive zone in which they are free of their former herbivores. (4) A novel mutation or recombinant appears in an insect population that permits individuals to overcome the new plant secondary compounds. (5) These insects enter a new adaptive zone and radiate in numbers of species onto the plants containing the novel secondary compounds, thereby form- ing a new taxon of herbivores.

Escape-and-radiation coevolution differs from diversifying coevolution in the way in which the interaction is involved in speciation. In diversifying coevolution, speciation in the host is caused by the interaction. In the hypothesis of escape-and-radiation coevolution, however, radiation in plant species occurs while the plants are tempor- arily free of herbivores. That is, attack by insects initially favors the evolution of new defenses, but radiation in plant species occurs

mostly during evolutionary periods in which the interaction is absent.

The Ehrlich-Raven hypothesis is both an important hypothesis and a difficult one to test. It requires a detailed understanding of the systematics, chemical ecology, population biology and biogeography of the interacting taxa. Recently, a few attempts have been made to apply the hypothesis to particular interactions. A preliminary analysis of the interactions among Heliconius butterflies and their host plants failed to provide evidence for the hypothesis3’. In contrast, a study of the interactions between the Umbelliferae and phytophagous insects concluded that the pattern of species radiation fits the hypothesis32. Reanalysis of these data, however, has indicated that they do not presently provide convincing evidence of escape-and- radiation coevolution23. The differences in the conclusions reached in these papers on interactions between the Umbelliferae and insects result from differences in how the authors view lumping and splitting traditions in Europe as compared with North America in the systematics of these groups, and in how the data are analysed. Resolution of the differences will demand a more thorough understanding of the systematics of both the plants and the insects, patterns of geo- graphic variation in host use within these insect species, the evolutionary genetics of host selection and speciation in these insects, and the chemical ecology of these interactions.

The relationship of parallel cladogenesis to coevolutfon

A prediction of the Ehrlich- Raven hypothesis of escape-and- radiation coevolution is that we should see some parallel radiation of interacting taxa, although not necessarily a one-to-one radiation of host and parasite species. This prediction has sometimes been equated with the hypothesis itself. The prediction of some parallel cladogenesis follows from the five steps of the hypothesis, but these five steps are not the only ways in which parallel radiation of species can occur. Parallel cladogenesis can occur without any reciprocal evolution as, for example, in com- mensals speciating with their

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hosts. Furthermore, nothing in the Ehrlich-Raven hypothesis demands that each speciation event in a plant lineage will be matched by a speciation event in the mutant insect lineage that has managed to colonize those plants. Nonetheless, it is the equating of hypothesis and prediction that has caused the word coevolution to be applied by some systematists to any instance of parallel cladogenesis in interacting taxa. Hence, Miller33 writes: ‘Stepwise coevolution, as defined by Ehrlich and Raven (1964) and others, can be equated with parallel cladogenesis or association by descent’. And Brooks27 argues that ‘while coevolution is like a new toy to students of free-living organisms, it is an old friend to parasitologists’.

Brooks’ statement is true only if we equate coevolution with parallel cladogenesis. The detailed work in parasitology on congruence of phy- logenies has been directed mostly at evaluation of association by descent in parasites and hosts rather than at the analysis of reciprocal evolution34. These systematic analyses cannot alone demonstrate coevolution in the sense of reciprocal evolutionary change. If we were to equate parallel cladogenesis or phylogenetic tracking with coevolution, then we would have to coin yet another word to describe reciprocal evolutionary change and the variety of possible outcomes that now seem possible through reciprocal evolution. What makes the study of coevolution currently exciting is that reciprocal evolution can produce a variety of outcomes, only one of which is parallel cladogenesis.

Coevolutionary rewach Future studies are likely to

generate even more hypotheses on the various modes of coevolution. Distinguishing among these different forms of coevolution, and the ecological and genetic conditions that favor different outcomes, is crucial for the development of a more precise theory of the variety of routes for coevolutionary change. It is through the search for the mechanisms of coevolution that a robust theory of reciprocal evolutionary change will develop, fur- ther uniting the studies of ecology, genetics and evolution.

Acknowledgements I thank Peter Abrams, Mercedes Ebbert.

Olle Pellmyr, Robert Podolsky, Peter Price, Lisa Valburg and two anonymous reviewers for very helpful comments on the manuscript, and Andrew Sugden for encourage- ment to write the manuscript. This work was supported by NSF grants BSR 8705394 and BSR 88 17337.

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15 Taper, M.L. and Case, T.I. (1985) Ecology 66,355-371 16 Abrams, P.A. (1987) Am. Nat. I30,271-282 17 Lawton, j.H. and Hassefl, M.P. (1981 I Nature 289,793-795 I8 Roughgarden, 1. (19831 in Lizard Ecology; Studies ofa Model Organism (Huey, R. B., Pianka. E.R.and Schoener, T.W., edsl, pp 371-4 IO. Harvard University Press 19 Lenski, R.E. and Levin, B.R. (1985) Am. Nat. I25,585-602 20 Thompson, I.N. ( 1986) Trends Ecol. Evol. I. 105-107 21 Gilbert, L.E. (1983) in Coevolotion (Futuyma, D.J. and Slatkin, M., eds), pp. 263-28 I, Sinauer Associates 22 Howe, H.F. and Westley, L.C. ( 1988) Ecological Relationships of Plants and Animals, Oxford University Press 23 Thompson, I.N. ( 1986) in Coevolution and Systematics (Stone, A.R. and Hawksworth, D.L., eds), pp. 119-143, Clarendon Press 24 Thompson, 1.N. (1987) Biol. 1. Linn. Sot. 32, 385-393 25 feon, K.W. and leon, M.S. (1976) /. Cell Physiol. 89,337-344 26 Bouma, I.E. and Lenski, R.E. (1988) Nature 335,351-352 27 Brooks, D.R. I 19871 Int. 1. Parasitol. 17. 29 l-297 28 Addicott, I.F. ( 1986) Oecoiogia 70,486-494 29 Bronstein, I.L. (1987) Oikos 48,39-46 30 Pellmyr. 0. ( 1988) Oecologia 78,53-59 31 Smiley, LT. ( 1985) Oeco/ogia 65,580-583 32 Berenbaum, M. (1983) Evolution 37, 163-179 33 Miller, IS. (1987) Cladistics 3. 105-120 34 Stone, A.R. and Hawksworth, D.L., eds ( 1986) Coevolution and Systematics, Clarendon Press

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Concepts of coevolution