Evolution of adult male horn developmental phenotypes and character displacement in Xylotrupes beetles (Scarabaeidae).

Selection against hybridization can cause mating traits to diverge between species in sympatry via reproductive character displacement (RCD). Additionally, selection against interspecific fighting can cause aggressive traits to diverge between sympatric species via agonistic character displacement (ACD). By directly affecting conspecific recognition traits, RCD and ACD between species can also incidentally cause divergence in mating and fighting traits among populations within a species [termed cascade RCD (CRCD) and cascade ACD]. Here, we demonstrate patterns consistent with male-driven RCD and ACD in 2 groups of darters (orangethroat darter clade Ceasia and rainbow darter Etheostoma caeruleum). In both groups, males that occur in sympatry (between Ceasia and E. caeruleum) have higher levels of preference for mating and fighting with conspecifics over heterospecifics than do males from allopatry. This is consistent with RCD and ACD. We also found patterns consistent with CRCD and cascade ACD among species of Ceasia. Ceasia males that are sympatric to E. caeruleum (but allopatric to one another) also have heightened preferences for mating and fighting with conspecific versus heterospecific Ceasia. In contrast, Ceasia males that are allopatric to E. caeruleum readily mate and fight with heterospecific Ceasia. We suggest that RCD and ACD between Ceasia and E. caeruleum has incidentally led to divergence in mating and fighting traits among Ceasia species. This study is unique in that male preferences evolve via both RCD (male preference for conspecific females) and ACD (male preference to fight conspecific males) which leads to subsequent divergence among allopatric lineages.

Character displacement, frequency-dependent selection, and divergence of shell colour in land snailsMandarina(Pulmonata)

In land snails, a change in the direction of coiling, being associated with a shift in the position of the genital apparatus, may act as a barrier against hybridization between sympatric species. Putative reproductive character displacement by an inversion in chirality has been reported in only a few land snails, based on observations in the field and interbreeding experiments. In this study, we present a new case of possible reproductive character displacement in the direction of coiling, in the clausiliid snail Isabellaria dextrorsa. This species is dextral, in contrast with its nearest relatives, including I. torifera and I. lophauchena, which share plesiomorphic sinistral coiling. Whereas I. dextrorsa occurs in sympatry and even syntopically with I. lophauchena throughout most of its range, the sinistral species have a mosaic distribution. Phylogenetic analyses of mitochondrial cytochrome c oxidase subunit I (COI) sequences demonstrated that I. dextrorsa constitutes a clade with I. torifera. In this clade, a shift in coiling direction occurred at least twice, maybe triggered by the presence of a sympatric congeneric sinistral species. The analyses separated the sequences of all I. dextrorsa samples from those of sympatric and syntopic I. lophauchena samples. The failure to demonstrate gene flow between these species is consistent with the hypothesis of genetic isolation by reproductive character displacement.

Generally, stronger reproductive isolation is expected between sympatric than between allopatric sibling species. Such reproductive character displacement should predominantly affect premating reproductive isolation and can be due to several mechanisms, including population extinction, fusion of insufficiently isolated incipient species and reinforcement of reproductive isolation in response to low hybrid fitness. Experimental data on several taxa have confirmed these theoretical expectations on reproductive character displacement, but they are restricted to animals and a few plants. Using results reported in the literature on crossing experiments in fungi, we compared the degree and the nature of reproductive isolation between allopatric and sympatric species pairs. In accordance with theoretical expectations, we found a pattern of enhanced premating isolation among sympatric sibling species in Homobasidiomycota. By contrast, we did not find evidence for reproductive character displacement in Ascomycota at similar genetic distances. Both allopatric and sympatric species of Ascomycota had similarly low levels of reproductive isolation, being mostly post-zygotic. This suggests that some phylogeny-dependent life-history trait may strongly influence the evolution of reproductive isolation between closely related species. A significant correlation was found between degree of reproductive isolation and genetic divergence among allopatric species of Homobasidiomycota, but not among sympatric ones or among Ascomycota species.

Interspecific territoriality may be adaptive if territories contain depletable resources that are valuable to both species, but it can also arise as a maladaptive by-product of intraspecific territoriality. In the latter scenario, sympatric species ought to diverge in ways that reduce interspecific fighting. We studied 4 Hetaerina damselfly species that can be found in sympatry in North America. Prior work showed that sympatric populations have diverged from each other in wing coloration and competitor recognition in 2 of the 4 sympatric species pairs (H. titia/H. occisa, H. titia/H. americana). Here, we show that sympatric populations of these 2 species pairs overlap completely in habitat use, and yet, interspecific territorial fights occur much less frequently than intraspecific fights. Experimentally manipulating the wing coloration of male H. occisa and H. americana to more closely resemble H. titia increased the rate of interspecific fights, which provides direct evidence that divergence in wing coloration is partly responsible for the low rate of interspecific fights. We found that interspecific fighting is also reduced in the other 2 species pairs (H. occisa/H. cruentata, H. americana/H. cruentata), even though prior work showed that heterospecific territory intruders are attacked just as aggressively as conspecific territory intruders. In these cases, however, the sympatric species differ sufficiently in habitat use to reduce the interspecific encounter rate and thereby account for the reduced rate of interspecific fighting. Thus, interspecific fighting is reduced relative to intraspecific fighting in all 4 species pairs, albeit through different mechanisms. Copyright 2011, Oxford University Press.

Ecological character displacement is unusual dissimilarity among sympatric species in features such as body size or trophic morphology (Grant, 1972), which allows coexistence by causing species to use the environment in fashions so different that competitive exclusion is avoided (Brown and Wilson, 1956). Character displacement could arise either as a result of divergent natural selection of coexisting species, or by selective survival of immigrating species as a function of distinctness from species already present (Grant, 1969, 1970). But what dissimilarity among species is unusual? What sympatric differences are character displacement? Most evidence for the phenomenon has been taken from species pairs with morphological size ratios that are greater between sympatric than between allopatric populations. The classic example treated a pair of rock nuthatch species (Vaurie, 1951; Brown and Wilson, 1956), populations of which appeared more different in sympatry than in allopatry. However, Grant (1975) has pointed out that bill length varies over geographic clines in both species, and that the zone of sympatry has no discernible influence upon clinal variation of either. A literature review led Grant (1972) to conclude that most examples of ecological character displacement are equivocal. In only two instances do known morphological differences really conform to the pattern, one between two congeneric skinks (Huey and Pianka, 1974; Huey et al., 1974), and another between two species of snails (Fenchel, 1975). The role of competition in these differences is not well established. Community-wide morphological patterns among species have also been taken as evidence of character displacement. The reasoning is that the degree of size difference required to allow coexistence is the same among all contiguous pairs of species within communities. Among species ranked by size, constant ratios of 1.14, 1.2, 1.4, and 2 have been used in this vein (Hutchinson, 1959; Schoener, 1965; Emlen, 1966; Wilson, 1975; Terborgh et al., 1978). However, Hespenheide (1971, 1973) has shown that arbitrary ratios among sympatric species are not good evidence for character displacement, because relationships between the size of trophic structure (or body size) and food size vary substantially within and among taxa. A ratio that provides food separation for one set of species, for one circumstance, will not do so for another. Horn and May (1977) have also commented upon some of the pitfalls of deducing species interaction from constant ratios. Yet, the enthusiasm for character displacement, and for inferring avoidance of interspecific competition from interspecific size ratios, continues. The notion is described as a community principle in recent textbooks of ecology (Odum, 1971; Colinvaux, 1973; Collier et al., 1973; Ricklefs, 1973; Smith, 1974; Pianka, 1978), and is not infrequently given as research motivation or as a theorem in the current primary literature (although under various names [fide Hespenheide, 1973]). Our interest is with the logic of empirical studies of character displacement that involve large fractions of faunas (e.g., Lack, 1947; Hutchinson, 1959; Schoener, 1965; Grant, 1968; Abbott et al., 1977), rather than with studies of particular species pairs. These community-wide studies have uniformly concluded that there is a tendency for coexisting species to be unusually dis-

According to the naturalists of the first half of this century, adaptive radiation is the outcome of three ecological processes: phenotypic differentiation of populations by resource-based divergent natural selection, phenotypic differentiation through resource competition (ecological opportunity and divergent character displacement), and ecological speciation (speciation as a consequence of adaptation to different resource environments). Despite a recent surge of interest in the phenomenon, especially in phylogenetic histories of radiations, we know too little about the ecology of most radiations to assess the roles of the three processes. I summarize our own efforts to test the theory with a radiation of three-spined sticklebacks apparently still in its early stages. The role of divergent selection is supported by a strong relationship among populations and species in mean morphology, feeding performance, habitat use, and growth rate. Trade-offs in feeding performance and growth rate between habitats are steep. Ecological character displacement is indicated by the large differences between sympatric species and the intermediate features of solitary species inhabiting lakes of similar size. A pond experiment showed that natural selection on a solitary species is altered following introduction of a competitor and favors divergence. Evidence for ecological speciation in sticklebacks is weakest, but there are several hints of its importance: speciation was rapid and accompanied by divergence into different ecological niches; selection against hybrids is stronger in the wild than in the laboratory, which suggests that hybrid fitness depends on ecological context; premating isolation depends in part on traits that diverged in association with the exploitation of different resources; and reproductive isolation may have evolved in parallel in different populations experiencing similar environmental conditions. Comparison with other studies suggests that these findings apply broadly.

Endemic land snails of the genus Mandarina of the oceanic Bonin Islands offer an exceptional example of habitat and character divergence among closely related species. In this study, microhabitat differences between sympatric ground-dwelling species were studied by distinguishing habitats on the basis of vegetation and types of litter. In all sites where two ground species coexisted, segregation occurred with each species showing preference for the microhabitat in which they were found. When they were in sympatry, one species was predominant in relatively wet and sheltered sites and the other in relatively dry and exposed sites. Although most species can live in both types of habitat, occupation by one species is inhibited by occupation by another. This suggests that competitive interaction between sympatric species caused segregation. Except for populations that have undergone interspecific hybridization, no examples were found of sympatric populations of two ground species sharing a similar shell colour. Species that were predominant in relatively wet and sheltered sites possessed shells with dark coloration and their colour patterns were mostly of one type. Species that were predominant in relatively dry and exposed sites possessed shells with bright coloration and their color patterns were polymorphic. Most populations from areas in which single species were distributed had shells with medium coloration. Microhabitat differentiation between sympatric species possibly caused diversification of shell colour, because bright shells are advantageous in sites where snails are largely exposed, and dark shells are advantageous in sites in where they are mostly sheltered from sunlight. In addition, frequency-dependent selection by predators hunting by sight may have operated to maintain colour polymorphism in the populations which are restricted to exposed habitats by competition with other sympatric species. This reveals the importance of interaction among closely related species as a cause of diversification in ecological and morphological traits.

Sympatric sister species generally have a degree of phenotypic differentiation that allows them to coexist. It has been well documented that phenotypic similarity results, through resource competition, in one of two major outcomes: local extinction of either competitor or character displacement. Limiting similarity suggests that there is a maximum degree of phenotypic niche overlap with which similar species may coexist. Breaching that maximum would result in exclusion. Character displacement, on the other hand, implies that the species differentiate phenotypically so that resource competition is reduced to the point where coexistence is possible. While it has been suggested that these theories have the potential to accelerate (character displacement) or limit phenotypic evolution (competitive exclusion) on microevolutionary time scales, their effects on macroevolution remain under-studied. If competition accelerates evolution on a macroevolutionary scale, one would expect that phenotypic diversity increases as novel species 'push aside' existing species. On the other hand, one might also expect that phenotypic evolution comes to a halt as novel species are trapped in the (ever decreasing) phenotypic space not yet occupied by existing species, except at the extremes of the phenotypic spectrum. Studying the current geographical ranges of more than 3000 extant species representing 29 mammalian families and their respective body masses, I found little evidence of competition accelerating body size differentiation between species.

Character displacement - the divergence of traits between species in response to competition for resources or mates - has long been viewed as a major cause of adaptive diversification and species coexistence. Yet, we lack answers to basic questions concerning the causes and consequences of character displacement, not the least of which is why some species are more prone than others to undergo character displacement. Here, we address these questions by describing how character displacement can proceed through two nonexclusive routes that differ in the source of phenotypic variation, and, hence, in the ease with which character displacement may unfold. During in situ evolution of novel phenotypes, new traits that are divergent from a heterospecific competitor are generated and spread in sympatry. During sorting of pre-existing variation, such traits are initially favoured in allopatry before the two species encounter one another. Later, when they come into contact, character displacement transpires when these pre-existing divergent phenotypes increase in frequency in sympatry relative to allopatry. Because such sorting of pre-existing variation should unfold relatively rapidly, we suggest that species that express resource or mating polymorphism prior to interactions with heterospecifics may be more prone to undergo character displacement. We discuss the key differences between these two routes, review possible examples of each, and describe how the distinction between them provides unique insights into the evolutionary consequences of species interactions, the origins of diversity, and the factors that govern species coexistence.

Phenotypic evolution in sympatric species can be strongly impacted by species interactions, either mutualistic or antagonistic. Heterospecific reproductive behaviours between sympatric species have been shown to favour phenotypic divergence of traits used as sexual cues. Those traits may also be involved in local adaptation or in other types of species interactions and, as a result, undergo complex evolutions across sympatric species. Here we focus on mimicry and study how reproductive interference may impair phenotypic convergence between species with various levels of defence. We use a deterministic model assuming two sympatric species where individuals can display two different warning colour patterns. This eco‐evolutionary model explores how ecological interactions shape phenotypic evolution within sympatric species. We investigate the effect of 1) the opposing density‐dependent selections exerted on colour patterns by predation and reproductive behaviour and 2) the impact of relative species and phenotype abundances on the fitness costs faced by each individual depending on their species and phenotype. Our model shows that reproductive interference may limit the convergent effect of mimetic interactions and may promote phenotypic divergence between Müllerian mimics. The divergent and convergent evolution of traits also strongly depends on the relative species and phenotype abundances and levels of trophic competition, highlighting how the eco‐evolutionary feedbacks between phenotypic evolution and species abundances may result in strikingly different evolutionary routes.

Natural enemies may contribute to the morphological divergence of sympatric species, yet their role has received little attention to date. We tested for character shifts in defensive armor of sympatric threespine sticklebacks (Gasterosteus aculeatus complex) previously shown to exhibit ecological character displacement in traits related to resource use. We scored five defensive armor traits in sympatric benthic and limnetic stickleback species from southwestern British Columbia and compared them with the same traits in nearby allopatric populations in the presence of the same predatory fish (Oncorhynchus sp.). This approach is analogous to tests of ecological character displacement that compare trophic traits of sympatric and allopatric species in the presence of the same community of resource types. Three patterns consistent with character displacement in defensive armor were found. First, limnetics in different lakes had consistently more armor than sympatric benthics. Second, the average amount of armor, averaged over both species, was reduced in sympatry compared to allopatric populations. This reduction was almost entirely the result of shifts by benthic species, whereas armor in limnetics was more similar to that in allopatric populations. Third, differences between sympatric benthics and limnetics in total armor were greater than expected from comparisons with allopatric populations. We interpret these patterns as the result of differences in habitat-specific predation regimes accompanying ecological character displacement and indirect interactions between sympatric stickleback species mediated by their top predators. These results suggest that predation may facilitate, rather than hinder, the process of divergence in sympatry.

Natural enemies may contribute to the morphological divergence of sympatric species, yet their role has received little attention to date. We tested for character shifts in defensive armor of sympatric threespine sticklebacks (Gasterosteus aculeatus complex) previously shown to exhibit ecological character displacement in traits related to resource use. We scored five defensive armor traits in sympatric benthic and limnetic stickleback species from southwestern British Columbia and compared them with the same traits in nearby allopatric populations in the presence of the same predatory fish (Oncorhynchus sp.). This approach is analogous to tests of ecological character displacement that compare trophic traits of sympatric and allopatric species in the presence of the same community of resource types. Three patterns consistent with character displacement in defensive armor were found. First, limnetics in different lakes had consistently more armor than sympatric benthics. Second, the average amount of armor, averaged over both species, was reduced in sympatry compared to allopatric populations. This reduction was almost entirely the result of shifts by benthic species, whereas armor in limnetics was more similar to that in allopatric populations. Third, differences between sympatric benthics and limnetics in total armor were greater than expected from comparisons with allopatric populations. We interpret these patterns as the result of differences in habitat-specific predation regimes accompanying ecological character displacement and indirect interactions between sympatric stickleback species mediated by their top predators. These results suggest that predation may facilitate, rather than hinder, the process of divergence in sympatry.

Odontocetes produce a range of different echolocation clicks but four groups in different families have converged on producing the same stereotyped narrow band high frequency (NBHF) click. In microchiropteran bats, sympatric species have evolved the use of different acoustic niches and subtly different echolocation signals to avoid competition among species. In this study, we examined whether similar adaptations are at play among sympatric porpoise species that use NBHF echolocation clicks. We used a six-element hydrophone array to record harbour and Dall’s porpoises in British Columbia (BC), Canada, and harbour porpoises in Denmark. The click source properties of all porpoise groups were remarkably similar and had an average directivity index of 25 dB. Yet there was a small, but consistent and significant 4 kHz difference in centroid frequency between sympatric Dall’s (137±3 kHz) and Canadian harbour porpoises (141±2 kHz). Danish harbour porpoise clicks (136±3 kHz) were more similar to Dall’s porpoise than to their conspecifics in Canada. We suggest that the spectral differences in echolocation clicks between the sympatric porpoises are consistent with evolution of a prezygotic isolating barrier (i.e., character displacement) to avoid hybridization of sympatric species. In practical terms, these spectral differences have immediate application to passive acoustic monitoring.

The idea that ecology and evolution can influence each other simultaneously in a feedback loop has become the lynchpin of the new field of eco-evolutionary dynamics (Pelletier et al. 2009). However, under a different name, eco-evolutionary dynamics is actually a venerable idea. Biologists, starting with Darwin (1859) and later Brown and Wilson (1956), have long recognized that competitive interactions between species lead to evolutionary divergence that facilitates coexistence, an eco-evolutionary process known as character displacement. Despite all the attention lavished on eco-evolutionary feedbacks in recent years, character displacement is often neglected. This neglect likely reflects an uneasy combination of over-familiarity (hasn’t it all been done many times over?) and a lingering skepticism after rancorous debates over ecological character displacement and reinforcement. With renewed interest in eco-evolutionary feedbacks, it is time for a synthetic review to resuscitate the original eco-evolutionary process. Pfennig and Pfennig (2012), who have produced a series of elegant touchstone studies on both ecological and reproductive character displacement in spadefoot toads (Spea), are ideally qualified to write such a review. With Evolution’s Wedge: Competition and the Origins of Diversity (2012), they have succeeded. The book posits that competition is a ubiquitous ecological process and that competition’s consequence, character displacement, is an evolutionary wedge that generates biodiversity. Pfennig and Pfennig argue that this wedge provides a unifying theory for fundamental questions throughout evolutionary biology and ecology. In the first chapter, Pfennig and Pfennig cover the basics: definitions, alternative outcomes, and criteria for demonstrating character displacement. The subsequent three chapters provide thorough, and at times speculative, discussions of why, when, and how character displacement occurs. Although each section addresses reproductive and ecological character displacement separately, Pfennig and Pfennig also provide insightful discussions of how the two types of character displacement facilitate and impede evolution of the other. The second half of the book examines how character displacement influences other ecological and evolutionary patterns and processes, like the formation of intraspecies diversity, niche formation, community composition, sexual selection, speciation, and macroevolution. Pfennig and Pfennig bring valuable perspective to aspects of character displacement that are usually overlooked. For example, they argue that phenotypic plasticity is a key component of character displacement. Plasticity can reveal cryptic genetic variation and consequently may delay competitive exclusion long enough for genetically canalized differences to evolve. Moreover, variation in plasticity itself can be heritable, and thus the strength of plasticity can evolve during character displacement. In addition, the authors attempt to dissolve the dichotomy between reproductive character displacement and reinforcement. Finally, the book includes many examples from the plant literature, something rarely done in the discussion of character displacement. Evolution’s Wedge is not an exhaustive summary of all relevant examples of each phenomenon discussed. Instead, Pfennig and Pfennig focus on historically important and iconic empirical examples with helpful diagrams to cover the essential concepts. The authors seem to have made a conscious decision not to discuss the extensive theoretical research on character displacement in detail. They often refer to general conclusions derived from mathematical models, but never discuss the mathematical details. Some readers may find the lack of equations inviting in a book primarily concerned with general concepts, whereas others may see this as an unfortunate missed opportunity to define and discuss