Ecological character displacement and the study of adaptation.

T study of adaptation—a central issue in biology since before the time of Darwin—is currently enjoying a renaissance. Ridiculed two decades ago as following a panglossian paradigm (1) that promulgated ‘‘just so stories’’ rather than testing hypotheses, evolutionary biology has become a vibrant field in which a wide variety of methods—ranging from molecular developmental biology to manipulative field experiments—are used to rigorously test adaptive hypotheses (2). Nowhere is this more evident than in the study of ecological character displacement; a paper by Adams and Rohlf (3) in a recent issue of PNAS is one of a growing number of studies that have used integrative, multidisciplinary approaches and have demonstrated that ecological character displacement appears to be an important ecological and evolutionary phenomenon. The theory of ecological character displacement was first explicitly developed by W. L. Brown and E. O. Wilson in 1956 (4). The idea underlying this theory is quite simple: Suppose that two very similar species come into contact. If resources are limiting, the species are likely to compete strongly. One possible outcome is competitive exclusion: the superior competitor will triumph and the inferior one will become extinct. But an alternative possibility is that natural selection will favor, in each population, those individuals whose phenotype allows them to use resources not used by members of the other species (Fig. 1). The result may be that the populations diverge in phenotype and resource use (hence the term displacement), thus reducing resource competition and permitting coexistence (Fig. 1). Soon after the theory was promulgated, ecologists and evolutionary biologists were seeing evidence for character displacement everywhere. Because the theory of limiting similarity indicated that species that were too morphologically similar could not coexist (5), seemingly any difference between two sympatric species was interpreted as the evolutionary outcome of selection favoring divergence between sympatric species—character displacement was seen as a powerful and pervasive force structuring ecological communities. These interpretations corresponded nicely with the prevailing adaptationist thinking of the time that viewed almost all interspecific differences as the result of adaptation to different regimes of natural selection. The decade from the mid-1970s to the mid-1980s were tumultuous times in both evolutionary biology and ecology. Even as the primacy of natural selection as the engine of evolutionary change was under attack (1, 6), parallel arguments were being leveled against character displacement. Statistical analyses showed that, in many cases, differences between sympatric species were no greater than would be expected by chance (7, 8). Moreover, even when sympatric species were significantly different in morphology, ecological character displacement was but one of many possible explanations. Some of these alternatives still relied on interspecific competition as the underlying cause (e.g., ref. 9), but others did not. Further, theoretical treatments suggested that the conditions under which ecological character displacement might occur were much more restrictive than previously appreciated (10–13). The net result was that character displacement’s importance as a force structuring communities was severely downgraded; many considered it to be a rare phenomenon for which few convincing examples could be found (e.g., refs. 14–16). These debates—unpleasant as they sometimes were—served a good purpose: the study of evolutionary phenomena was recognized as an historical science— investigating what happened in the past thus requires an historical context (17– 20). Moreover, investigating whether a trait arose as an adaptation requires examination of the hypothesis that natural selection led to the evolution of a trait in response to a particular selective situation. A wide variety of approaches—combining functional, experimental, and genetic methods—have been proposed as means to test this hypothesis (21, 22). One conclusion stands out from these methods: we cannot go back in time and expressly determine why a trait evolved. The best we can do is enumerate tests suggested by a particular adaptive hypothesis: the more such tests a hypothesis survives, the stronger may be our confidence in it. Recent approaches to the study of character displacement exemplify this approach. Schluter and McPhail (23) outlined six tests of a hypothesis of ecological character displacement, which were further elaborated by Taper and Case (24): (i) Differences between sympatric taxa are greater than expected by chance—i.e.,