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Ecological Character Displacement and the Study of Adaptation

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Ecological Character Displacement and the Study of Adaptation Commentary Ecological character displacement and the study of adaptation Jonathan B. Losos* Department of Biology, Campus Box 1137, Washington University, St. Louis, MO 63130 he study of adaptation—a central is- Tsue in biology since before the time of Darwin—is currently enjoying a renais- sance. Ridiculed two decades ago as fol- lowing a panglossian paradigm (1) that Fig. 1. (Upper) Two sympatric promulgated ‘‘just so stories’’ rather than species with broadly overlapping distributions of resource use. If re- testing hypotheses, evolutionary biology sources are limiting, then natural has become a vibrant field in which a selection may favor individuals in wide variety of methods—ranging from each species with traits that allow molecular developmental biology to each of them to use that portion of manipulative field experiments—are used the resource spectrum not used by to rigorously test adaptive hypotheses (2). the other species, as indicated by Nowhere is this more evident than in the the arrows. (Lower) The result may study of ecological character displace- be that the species diverge in trait value and resource use, thus mini- ment; a paper by Adams and Rohlf (3) in mizing competition for resources. a recent issue of PNAS is one of a growing number of studies that have used integra- tive, multidisciplinary approaches and have demonstrated that ecological char- placement was seen as a powerful and enon for which few convincing examples acter displacement appears to be an pervasive force structuring ecological could be found (e.g., refs. 14–16). important ecological and evolutionary communities. These interpretations cor- These debates—unpleasant as they COMMENTARY phenomenon. responded nicely with the prevailing ad- sometimes were—served a good purpose: The theory of ecological character dis- aptationist thinking of the time that the study of evolutionary phenomena was placement was first explicitly developed by viewed almost all interspecific differences recognized as an historical science— W. L. Brown and E. O. Wilson in 1956 (4). as the result of adaptation to different investigating what happened in the past The idea underlying this theory is quite regimes of natural selection. thus requires an historical context (17– 20). Moreover, investigating whether a simple: Suppose that two very similar spe- The decade from the mid-1970s to the trait arose as an adaptation requires ex- cies come into contact. If resources are mid-1980s were tumultuous times in both amination of the hypothesis that natural limiting, the species are likely to compete evolutionary biology and ecology. Even as strongly. One possible outcome is com- selection led to the evolution of a trait in the primacy of natural selection as the response to a particular selective situation. petitive exclusion: the superior competitor engine of evolutionary change was under A wide variety of approaches—combining will triumph and the inferior one will attack (1, 6), parallel arguments were be- functional, experimental, and genetic become extinct. But an alternative possi- ing leveled against character displace- methods—have been proposed as means bility is that natural selection will favor, in ment. Statistical analyses showed that, in to test this hypothesis (21, 22). One con- each population, those individuals whose many cases, differences between sympat- clusion stands out from these methods: we phenotype allows them to use resources ric species were no greater than would be cannot go back in time and expressly not used by members of the other species expected by chance (7, 8). Moreover, even determine why a trait evolved. The best we (Fig. 1). The result may be that the pop- when sympatric species were significantly can do is enumerate tests suggested by a ulations diverge in phenotype and re- different in morphology, ecological char- particular adaptive hypothesis: the more source use (hence the term displacement), such tests a hypothesis survives, the stron- thus reducing resource competition and acter displacement was but one of many possible explanations. Some of these al- ger may be our confidence in it. permitting coexistence (Fig. 1). Recent approaches to the study of char- Soon after the theory was promulgated, ternatives still relied on interspecific com- petition as the underlying cause (e.g., ref. acter displacement exemplify this ap- ecologists and evolutionary biologists proach. Schluter and McPhail (23) out- 9), but others did not. Further, theoretical were seeing evidence for character dis- lined six tests of a hypothesis of ecological treatments suggested that the conditions placement everywhere. Because the the- character displacement, which were fur- ory of limiting similarity indicated that under which ecological character displace- ther elaborated by Taper and Case (24): species that were too morphologically sim- ment might occur were much more restric- (i) Differences between sympatric taxa ilar could not coexist (5), seemingly any tive than previously appreciated (10–13). are greater than expected by chance—i.e., difference between two sympatric species The net result was that character displace- was interpreted as the evolutionary out- ment’s importance as a force structuring come of selection favoring divergence be- communities was severely downgraded; See companion article on page 4106 in issue 8 of volume 97. tween sympatric species—character dis- many considered it to be a rare phenom- *E-mail: [email protected]. PNAS ͉ May 23, 2000 ͉ vol. 97 ͉ no. 11 ͉ 5693–5695 Downloaded by guest on October 2, 2021 Fig. 2. P. cinereus and P. hoffmani. Photos are courtesy of R. W. Van Devender. there is a deterministic phenomenon to Addressing all six of these tests in a single To find out, Adams and Rohlf sampled explain. study is a challenging task, as it requires populations of both species in allopatry (ii) Differences in character states are integrating a variety of different methods and in sympatry. They discovered that, in related to differences in resource use—if spanning the fields of ecology, genetics, and allopatry, the size of the two species was not, then the character divergence must evolutionary biology. Nonetheless, an in- very similar. In sympatry, however, pop- have some other cause than the amelio- creasing number of studies are testing many ulations of P. cinereus were smaller, and ration of competition for resources. of these hypotheses, as the paper by Adams populations of P. hoffmani were larger (iii) Resources are limiting, and inter- and Rohlf illustrates (3). (Fig. 3). This is the hallmark of character specific competition for these resources is Adams and Rohlf studied variation in displacement, but how well does this ex- a function of character similarity. body size and skull shape among popula- ample hold up to the six tests outlined (iv) Resource distributions are the same tions of two small and closely related above? in sympatry and allopatry such that dif- salamanders. Plethodon cinereus is wide- (i) Is the pattern nonrandom? To test ferences in character states do not simply spread throughout the eastern United this hypothesis, Adams and Rohlf mea- sured specimens from many allopatric reflect differences in resource availabili- States whereas Plethodon hoffmani has a populations of both species. They then ty—e.g., if some localities had an abun- limited distribution “centered” in south- computed the probability of finding dif- dance of large and small insects, but few central Pennsylvania (Fig. 2). The species intermediate sized ones, one might expect ferences as great as those actually ob- are for the most part allopatric; the range served if one randomly sampled one allo- two species to be able to coexist, one of P. hoffmani is surrounded on all sides by adapted to catching each size class of patric population from each species. The that of P. cinereus. This distribution, and result: sympatric populations of the two insects, whereas another locality with only the great similarity between the two spe- intermediate sized insects might only be species are more divergent than any pos- cies, suggests the possibility that lack of sible pair of allopatric populations. The able to support one species. These differ- widespread sympatry is the result of com- ences might not be the result of character pattern is thus not a result of random petitive exclusion: the species are too sim- sampling of existing morphological varia- displacement, but of ecological tracking of ilar ecologically to coexist. If this is the resource availability. tion in the two species. case, one might wonder what happens (ii) Are morphological differences re- (v) Differences must have evolved in when populations of the two species come lated to differences in resource use? situ—i.e., coexistence did not result from together at their range boundaries. Adams and Rohlf found that, in sympatry, taxa evolving differences in allopatry that subsequently permitted range ex- pansion and sympatry. Moreover, differ- ences in sympatry must not result be- cause character variation in both species is clinal and the geographic ranges of the species happen to overlap at the point where their morphological differences are greatest (25). (vi) Differences must be genetically based—Phenotypic differences between sympatric and allopatric populations could result from a variety of nongenetic Fig. 3. Body size (as represented causes, including adaptive phenotypic by snout-vent length) in allopatric and sympatric populations of the plasticity and differences in survival and two species. In allopatry, popula- growth rates. Coexistence mediated by tions are similar in size, but in sym- any of these nongenetic causes would cer- patry, P. hoffmani is larger and P. tainly be interesting but would not qualify cinereus is smaller (data courtesy of as character displacement. D. C. Adams). 5694 ͉ www.pnas.org Losos Downloaded by guest on October 2, 2021 P. cinereus eats smaller prey and P. hoff- (v) Did the differences actually evolve differences among the species; even small- mani larger prey than each eats in allo- in sympatry, or did they evolve before the scale morphological responses might be patry.
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