How fluctuating competition and phenotypic plasticity mediate species divergence

Causal evidence linking resource competition to species divergence is scarce. In this study, we coupled field observations with experiments to ask if the degree of character displacement reflects the intensity of competition between two closely related spadefoot toads (Spea bombifrons and S. multiplicata). Tadpoles of both species develop into either a small-headed omnivorous morph, which feeds mostly on detritus, or a large-headed carnivorous morph, which specializes on and whose phenotype is induced by fairy shrimp. Previously, we found that S. multiplicata are inferior competitors for fairy shrimp and are less likely to develop into carnivores in sympatry with S. bombifrons. We compared four key trophic characters in S. multiplicata across natural ponds where the frequency of S. bombifrons varied. We found that S. multiplicata became increasingly more omnivore-like as the relative abundance of S. bombifrons increased. Moreover, in controlled laboratory populations, S. multiplicata became increasingly more omnivore-like and S. bombifrons became increasingly more carnivore-like as we increased the relative abundance of the other species. Phenotypic plasticity helped mediate this divergence: S. multiplicata became increasingly less likely to eat shrimp and develop into carnivores in the presence of S. bombifrons, a superior predator on shrimp. However, divergence also reflected differences in canalized traits: When reared under common conditions, S. multiplicata tadpoles became increasingly less likely to produce carnivores as their natal pond decreased in elevation. Presumably, this pattern reflected selection against carnivores in lower-elevation ponds, because S. bombifrons became increasingly more common with decreasing elevation. Local genetic adaptation to the presence of S. bombifrons was remarkably fine grained, with differences in carnivore production detected between populations a few kilometers apart. Our results suggest that the degree of character displacement potentially reflects the intensity of competition between interacting species and that both phenotypic plasticity and fine-scale genetic differentiation can mediate this response. Moreover, these results provide causal evidence linking resource competition to species divergence.     

Field and experimental evidence for competition's role in phenotypic divergence

Resource competition has long been viewed as a major cause of phenotypic divergence within and between species. Theory predicts that divergence arises because natural selection favors individuals that are phenotypically dissimilar from their competitors. Yet, there are few conclusive tests of this key prediction. Drawing on data from both natural populations and a controlled experiment, this paper presents such a test in tadpoles of two species of spadefoot toads (Spea bombifrons and S. multiplicata). These two species show exaggerated divergence in trophic morphology where they are found together (mixed-species ponds) but not where each is found alone (pure-species ponds), suggesting that they have undergone ecological character displacement. Moreover, in pure-species ponds, both species exhibit resource polymorphism. Using body size as a proxy for fitness, we found that in pure-species ponds disruptive selection favors extreme trophic phenotypes in both species, suggesting that intraspecific competition for food promotes resource polymorphism. In mixed-species ponds, by contrast, we found that trophic morphology was subject to stabilizing selection in S. multiplicata and directional selection in S. bombifrons. A controlled experiment revealed that the more similar an S. multiplicata was to its S. bombifrons tankmate in resource use, the worse was its performance. These results indicate that S. multiplicata individuals that differ from S. bombifrons would be selectively favored in competition. Our data therefore demonstrate how resource competition between phenotypically similar individuals can drive divergence between them. Moreover, our results indicate that how competition contributes to such divergence may be influenced not only by the degree to which competitors overlap in resource use, but also by the abundance and quality of resources. Finally, our finding that competitively mediated disruptive selection may promote resource polymorphism has potentially important implications for understanding how populations evolve in response to heterospecific competitors. In particular, once a population evolves resource polymorphism, it may be more prone to undergo ecological character displacement.     

Character displacement in polyphenic tadpoles

Biologists have long known that closely related species are often phenotypically different where they occur together, but are indistinguishable where they occur alone. The causes of such character displacement are controversial, however. We used polyphenic spadefoot toad tadpoles (Spea bombifrons and S. multiplicata) to test the hypothesis that character displacement evolves to minimize competition for food. We also sought to evaluate the role of phenotypic plasticity in the mediation of competitive interactions between these species. Depending on their diet, individuals of both species develop into either a small-headed omnivore morph, which feeds mostly on detritus, or a large-headed carnivore morph, which specializes on shrimp. Laboratory experiments and surveys of natural ponds revealed that the two species were more dissimilar in their tendency to produce carnivores when they occurred together than when they occurred alone. This divergence in carnivore production was expressed as both character displacement (where S. multiplicata's propensity to produce carnivores was lower in sympatry than in allopatry) and as phenotypic plasticity (where S. multiplicata facultatively enhanced carnivore production in S. bombifrons, and S. bombifrons facultatively suppressed carnivore production in S. multiplicata). In separate experiments, we established that S. bombifrons (the species for which carnivore production was enhanced) was the superior competitor for shrimp. Conversely, S. multiplicata (the species for which carnivore production was suppressed and omnivore production enhanced) was the superior competitor for detritus. These results therefore demonstrate that selection to minimize competition for food can cause character displacement. They also suggest that both character displacement and phenotypic plasticity may mediate competitive interactions between species.     

Asymmetric reproductive character displacement in male aggregation behaviour

Reproductive character displacement--the evolution of traits that minimize reproductive interactions between species--can promote striking divergence in male signals or female mate preferences between populations that do and do not occur with heterospecifics. However, reproductive character displacement can affect other aspects of mating behaviour. Indeed, avoidance of heterospecific interactions might contribute to spatial (or temporal) aggregation of conspecifics. We examined this possibility in two species of hybridizing spadefoot toad (genus Spea). We found that in Spea bombifrons sympatric males were more likely than allopatric males to associate with calling males. Moreover, contrary to allopatric males, sympatric S. bombifrons males preferentially associated with conspecific male calls. By contrast, Spea multiplicata showed no differences between sympatry and allopatry in likelihood to associate with calling males. Further, sympatric and allopatric males did not differ in preference for conspecifics. However, allopatric S. multiplicata were more variable than sympatric males in their responses. Thus, in S. multiplicata, character displacement may have refined pre-existing aggregation behaviour. Our results suggest that heterospecific interactions can foster aggregative behaviour that might ultimately contribute to clustering of conspecifics. Such clustering can generate spatial or temporal segregation of reproductive activities among species and ultimately promote reproductive isolation.     

Parallel evolution and ecological selection: replicated character displacement in spadefoot toads

Ecological character displacement—trait evolution stemming from selection to lessen resource competition between species—is most often inferred from a pattern in which species differ in resource-use traits in sympatry but not in allopatry, and in which sympatric populations within each species differ from conspecific allopatric populations. Yet, without information on population history, the presence of a divergent phenotype in multiple sympatric populations does not necessarily imply that there has been repeated evolution of character displacement. Instead, such a pattern may arise if there has been character displacement in a single ancestral population, followed by gene flow carrying the divergent phenotype into multiple, derived, sympatric populations. Here, we evaluate the likelihood of such historical events versus ongoing ecological selection in generating divergence in trophic morphology between multiple populations of spadefoot toad (Spea multiplicata) tadpoles that are in sympatry with a heterospecific and those that are in allopatry. We present both phylogenetic and population genetic evidence indicating that the same divergent trait, which minimizes resource competition with the heterospecific, has arisen independently in multiple sympatric populations. These data, therefore, provide strong indirect support for competition''s role in divergent trait evolution.     

Selection for character displacement is constrained by the genetic architecture of floral traits in the ivyleaf morning glory

Evolutionary theory predicts that interactions between species such as resource competition or reproductive interference will generate selection for character displacement where similar species co-occur. However, the rate and direction of character displacement will depend not only on the strength of selection for trait divergence, but also on the amount of genetic variation for selected traits and the nature of genetic correlations between them. To assess the importance of genetic constraints for the evolution of character displacement, we examined the genetic architecture of a suite of floral traits previously shown to be under selection in the annual plant Ipomoea hederacea when this species co-occurs with Ipomoea purpurea. We found that the six floral traits we measured are all positively genetically correlated. We also demonstrate, using new statistical approaches, that the predicted response to selection for four of these six traits is substantially constrained by their genetic correlation structure. Most notably, the response to selection for reduced separation of the tallest and shortest anthers, which reduces the degree of detrimental heterospecific pollen flow, is substantially constrained. Our results suggest that the rate of evolution of reproductive character displacement in I. hederacea is limited by the genetic architecture of floral traits.     

Character displacement and the origins of diversity

In The Origin of Species, Darwin proposed his principle of divergence of character (a process now termed "character displacement") to explain how new species arise and why they differ from each other phenotypically. Darwin maintained that the origin of species and the evolution of differences between them is ultimately caused by divergent selection acting to minimize competitive interactions between initially similar individuals, populations, and species. Here, we examine the empirical support for the various claims that constitute Darwin's principle, specifically that (1) competition promotes divergent trait evolution, (2) the strength of competitively mediated divergent selection increases with increasing phenotypic similarity between competitors, (3) divergence can occur within species, and (4) competitively mediated divergence can trigger speciation. We also explore aspects that Darwin failed to consider. In particular, we describe how (1) divergence can arise from selection acting to lessen reproductive interactions, (2) divergence is fueled by the intersection of character displacement and sexual selection, and (3) phenotypic plasticity may play a key role in promoting character displacement. Generally, character displacement is well supported empirically, and it remains a vital explanation for how new species arise and diversify.     

How does the magnitude of genetic variation affect ecological and reproductive character displacement?

While previous studies on character displacement tended to focus on trait divergence and convergence as a result of long-term evolution, recent studies suggest that character displacement can be a special case of evolutionary rescue, where rapid evolution prevents species extinction by weakening interspecific competition. Here we analyzed a simple model to examine how the magnitude of genetic variation affects evolutionary rescue via ecological and reproductive character displacement that weakens interspecific competition in exploitation of shared resources (i.e., resource competition) and in the mating process caused by incomplete species recognition (i.e., reproductive interference), respectively. We found that slow trait divergence due to small genetic variance results in species extinction in reproductive character displacement but not in ecological character displacement. This is because one species becomes rare in slow character displacement, and this causes deterministic extinction due to minority disadvantage of reproductive interference. On the other hand, there is no deterministic extinction in the process of ecological character displacement. Furthermore, species extinction becomes less likely in the case of positive covariance between ecological and reproductive traits as divergence of the ecological trait (e.g., root depths) increases the divergence speed of the reproductive trait (e.g., flower colors) and vice versa. It will be interesting to compare intraspecific genetic (co)variance of ecological and reproductive traits in future studies for understanding how ecological and reproductive character displacement occur without extinction.     

Does character displacement initiate speciation? Evidence of reduced gene flow between populations experiencing divergent selection

Character displacement – trait evolution stemming from selection to lessen resource competition or reproductive interactions between species – has long been regarded as important in finalizing speciation. By contrast, its role in initiating speciation has received less attention. Yet because selection for character displacement should act only where species co‐occur, individuals in sympatry will experience a different pattern of selection than conspecifics in allopatry. Such divergent selection might favour reduced gene flow between conspecific populations that have undergone character displacement and those that have not, thereby potentially triggering speciation. Here, we explore these ideas empirically by focusing on spadefoot toads, Spea multiplicata, which have undergone character displacement, and for which character displacement appears to cause post‐mating isolation between populations that are in sympatry with a heterospecific and those that are in allopatry. Using mitochondrial sequence data and nuclear microsatellite genotypes, we specifically asked whether gene flow is reduced between populations in different selective environments relative to that between populations in the same selective environment. We found a slight, but statistically significant, reduction in gene flow between selective environments, suggesting that reproductive isolation, and potentially ecological speciation, might indeed evolve as an indirect consequence of character displacement. Generally, character displacement may play a largely underappreciated role in instigating speciation.     

Character convergence under competition for nutritionally essential resources

Resource competition is thought to drive divergence in resource use traits (character displacement) by generating selection favoring individuals able to use resources unavailable to others. However, this picture assumes nutritionally substitutable resources (e.g., different prey species). When species compete for nutritionally essential resources (e.g., different nutrients), theory predicts that selection drives character convergence. We used models of two species competing for two essential resources to address several issues not considered by existing theory. The models incorporated either slow evolutionary change in resource use traits or fast physiological or behavioral change. We report four major results. First, competition always generates character convergence, but differences in resource requirements prevent competitors from evolving identical resource use traits. Second, character convergence promotes coexistence. Competing species always attain resource use traits that allow coexistence, and adaptive trait change stabilizes the ecological equilibrium. In contrast, adaptation in allopatry never preadapts species to coexist in sympatry. Third, feedbacks between ecological dynamics and trait dynamics lead to surprising dynamical trajectories such as transient divergence in resource use traits followed by subsequent convergence. Fourth, under sufficiently slow trait change, ecological dynamics often drive one of the competitors to near extinction, which would prevent realization of long-term character convergence in practice.     

Evolution of the elaborate male intromittent organ of Xiphophorus fishes

Internally fertilizing animals show a remarkable diversity in male genital morphology that is associated with sexual selection, and these traits are thought to be evolving particularly rapidly. Male fish in some internally fertilizing species have “gonopodia,” highly modified anal fins that are putatively important for sexual selection. However, our understanding of the evolution of genital diversity remains incomplete. Contrary to the prediction that male genital traits evolve more rapidly than other traits, here we show that gonopodial traits and other nongonopodial traits exhibit similar evolutionary rates of trait change and also follow similar evolutionary models in an iconic genus of poeciliid fish (Xiphophorus spp.). Furthermore, we find that both mating and nonmating natural selection mechanisms are unlikely to be driving the diverse Xiphophorus gonopodial morphology. Putative holdfast features of the male genital organ do not appear to be influenced by water flow, a candidate selective force in aquatic habitats. Additionally, interspecific divergence in gonopodial morphology is not significantly higher between sympatric species, than between allopatric species, suggesting that male genitals have not undergone reproductive character displacement. Slower rates of evolution in gonopodial traits compared with a subset of putatively sexually selected nongenital traits suggest that different selection mechanisms may be acting on the different trait types. Further investigations of this elaborate trait are imperative to determine whether it is ultimately an important driver of speciation.     

The evolution of species recognition in competitive and mating contexts: the relative efficacy of alternative mechanisms of character displacement

Sympatric divergence in traits affecting species recognition can result from selection against cross‐species mating (reproductive character displacement, RCD) or interspecific aggression (agonistic character displacement, ACD). When the same traits are used for species recognition in both contexts, empirically disentangling the relative contributions of RCD and ACD to observed character shifts may be impossible. Here, we develop a theoretical framework for partitioning the effects of these processes. We show that when both mate and competitor recognition depend on the same trait, RCD sets the pace of character shifts. Moreover, RCD can cause divergence in competitor recognition, but ACD cannot cause divergence in mate recognition. This asymmetry arises because males with divergent recognition traits may avoid needless interspecific conflicts, but suffer reduced attractiveness to conspecific females. Therefore, the key empirical issue is whether the same or different traits are used for mate recognition and competitor recognition.     

Competition drives trait evolution and character displacement between Mimulus species along an environmental gradient

Closely related species may evolve to coexist stably in sympatry through niche differentiation driven by in situ competition, a process termed character displacement. Alternatively, past evolution in allopatry may have already sufficiently reduced niche overlap to permit establishment in sympatry, a process called ecological sorting. The relative importance of each process to niche differentiation is contentious even though they are not mutually exclusive and are both mediated via multivariate trait evolution. We explore how competition has impacted niche differentiation in two monkeyflowers, Mimulus alsinoides and M. guttatus, which often co‐occur. Through field observations, common gardens, and competition experiments, we demonstrate that M. alsinoides is restricted to marginal habitats in sympatry and that the impacts of character displacement on niche differentiation are complex. Competition with M. guttatus alters selection gradients and has favored taller M. alsinoides with earlier seasonal flowering at low elevation and floral shape divergence at high elevation. However, no trait exhibits the pattern typically associated with character displacement, higher divergence between species in sympatry than allopatry. Thus, although character displacement was unlikely the process driving initial divergence along niche axes necessary for coexistence, we conclude that competition in sympatry has likely driven trait evolution along additional niche axes.     

Divergent sexual selection via male competition: ecology is key

Sexual selection and ecological differences are important drivers of speciation. Much research has focused on female choice, yet the role of male competition in ecological speciation has been understudied. Here, we test how mating habitats impact sexual selection and speciation through male competition. Using limnetic and benthic species of threespine stickleback fish, we find that different mating habitats select differently on male traits through male competition. In mixed habitat with both vegetated and open areas, selection favours two trait combinations of male body size and nuptial colour: large with little colour and small with lots of colour. This matches what we see in reproductively isolated stickleback species, suggesting male competition could promote trait divergence and reproductive isolation. In contrast, when only open habitat exists, selection favours one trait combination, large with lots of colour, which would hinder trait divergence and reproductive isolation. Other behavioural mechanisms in male competition that might promote divergence, such as avoiding aggression with heterospecifics, are insufficient to maintain separate species. This work highlights the importance of mating habitats in male competition for both sexual selection and speciation.     

Causes of male sexual trait divergence in introduced populations of guppies

Males from different populations of the same species often differ in their sexually selected traits. Variation in sexually selected traits can be attributed to sexual selection if phenotypic divergence matches the direction of sexual selection gradients among populations. However, phenotypic divergence of sexually selected traits may also be influenced by other factors, such as natural selection and genetic constraints. Here, we document differences in male sexual traits among six introduced Australian populations of guppies and untangle the forces driving divergence in these sexually selected traits. Using an experimental approach, we found that male size, area of orange coloration, number of sperm per ejaculate and linear sexual selection gradients for male traits differed among populations. Within populations, a large mismatch between the direction of selection and male traits suggests that constraints may be important in preventing male traits from evolving in the direction of selection. Among populations, however, variation in sexual selection explained more than half of the differences in trait variation, suggesting that, despite within‐population constraints, sexual selection has contributed to population divergence of male traits. Differences in sexual traits were also associated with predation risk and neutral genetic distance. Our study highlights the importance of sexual selection in trait divergence in introduced populations, despite the presence of constraining factors such as predation risk and evolutionary history.     

Differential selection to avoid hybridization in two toad species

Abstract.— The fitness consequences of hybridization critically affect the speciation process. When hybridization is costly, selection favors the evolution of prezygotic isolating mechanisms (e.g., mating behaviors) that reduce heter-ospecific matings and, consequently, enhance reproductive isolation between species (a process termed reinforcement). If, however, selection to avoid hybridization differs between species, reinforcement may be impeded. Here, we examined both the frequency and fitness effects of hybridization between plains spadefoot toads ( Spea bombifrons ) and New Mexico spadefoot toads ( S. multiplicata ). Hybridization was most frequent in smaller breeding ponds that tend to be ephemeral, and heterospecific pairs consisted almost entirely of S. bombifrons females and S. multiplicata males. Moreover, in controlled experimental crosses, hybrid offspring from crosses in which S. multiplicata was maternal had significantly lower survival and longer development time than pure S. multiplicata offspring. By contrast, hybrid offspring from crosses in which S. bombifrons was maternal outperformed pure S. bombifrons offspring by reaching metamorphosis faster. These data suggest that, although S. multiplicata females are under selection to avoid hybridization, selection might favor those S. bombifrons females that hybridize with S. multiplicata if their breeding pond is highly ephemeral. Generally, the strength of selection to avoid hybridization may differ for hybridizing species, possibly impeding reinforcement.     

Reproductive character displacement and the genetics of gamete recognition in tropical sea urchins

Reproductive character displacement occurs when sympatric and allopatric populations of a species differ in traits crucial to reproduction, and it is commonly thought of as a signal of selection acting to limit hybridization. Most documented cases of reproductive character displacement involve characters that are poorly understood at the genetic level, and rejecting alternative hypotheses for biogeographic shifts in reproductive traits is often very difficult. In sea urchins, the gamete recognition protein bindin evolves under positive selection when species are broadly sympatric, suggesting character displacement may be operating in this system. We sampled sympatric and allopatric populations of two species in the sea urchin genus Echinometra for variation in bindin and for the mitochondrial cytochrome oxidase I to examine patterns of population differentiation and molecular evolution at a reproductive gene. We found a major shift in bindin alleles between central Pacific (allopatric) and western Pacific (sympatric) populations of E. oblonga. Allopatric populations of E. oblonga are polyphyletic with E. sp. C at bindin, whereas sympatric populations of the two species are reciprocally monophyletic. There is a strong signal of positive selection (P(N)/P(S) = 4.5) in the variable region of the first exon of bindin, which is associated with alleles found in sympatric populations of E. oblonga. These results indicate that there is a strong pattern of reproductive character displacement between E. oblonga and E. sp. C and that the divergence is driven by selection. There is much higher population structure in sympatric populations at the bindin locus than at the neutral mitochondrial locus, but this difference is not seen in allopatric populations. These data suggest a pattern of speciation driven by selection for local gamete coevolution as a result of interactions between sympatric species. Although this pattern is highly suggestive of speciation by reinforcement, further research into hybrid fitness and egg-sperm interactions is required to address this potential mechanism for character displacement.     

Disruptive natural selection predicts divergence between the sexes during adaptive radiation

Evolution of sexual dimorphism in ecologically relevant traits, for example, via resource competition between the sexes, is traditionally envisioned to stall the progress of adaptive radiation. An alternative view is that evolution of ecological sexual dimorphism could in fact play an important positive role by facilitating sex‐specific adaptation. How competition‐driven disruptive selection, ecological sexual dimorphism, and speciation interact during real adaptive radiations is thus a critical and open empirical question. Here, we examine the relationships between these three processes in a clade of salamanders that has recently radiated into divergent niches associated with an aquatic life cycle. We find that morphological divergence between the sexes has occurred in a combination of head shape traits that are under disruptive natural selection within breeding ponds, while divergence among species means has occurred independently of this disruptive selection. Further, we find that adaptation to aquatic life is associated with increased sexual dimorphism across taxa, consistent with the hypothesis of clade‐wide character displacement between the sexes. Our results suggest the evolution of ecological sexual dimorphism may play a key role in niche divergence among nascent species and demonstrate that ecological sexual dimorphism and ecological speciation can and do evolve concurrently in the early stages of adaptive radiation.     

Character displacement as the "best of a bad situation": fitness trade-offs resulting from selection to minimize resource and mate competition

Abstract Character displacement has long been considered a major cause of adaptive diversification. When species compete for resources or mates, character displacement minimizes competition by promoting divergence in phenotypes associated with resource use (ecological character displacement) or mate attraction (reproductive character displacement). In this study, we investigated whether character displacement can also have pleiotropic effects that lead to fitness trade-offs between the benefits of avoiding competition and costs accrued in other fitness components. We show that both reproductive and ecological character displacement have caused spadefoot toads to evolve smaller body size in the presence of a heterospecific competitor. Although this shift in size likely arose as a by-product of character displacement acting to promote divergence between species in mating behavior and larval development, it concomitantly reduces offspring survival, female fecundity, and sexual selection on males. Thus, character displacement may represent the "best of a bad situation" in that it lessens competition, but at a cost. Individuals in sympatry with the displaced phenotype will have higher fitness than those without the displaced trait because they experience reduced competition, but they may have reduced fitness relative to individuals in allopatry. Such a fitness trade-off can limit the conditions under which character displacement evolves and may even increase the risk of "Darwinian extinction" in sympatric populations. Consequently, character displacement may not always promote diversification in the manner that is often expected.     

A MATERNAL EFFECT MEDIATES RAPID POPULATION DIVERGENCE AND CHARACTER DISPLACEMENT IN SPADEFOOT TOADS

Despite long-standing interest in character displacement, little is known of its underlying proximate causes. Here, we explore the role of maternal effects in character displacement. We specifically investigated whether differences in maternal body condition mediate divergence in the expression of resource-use traits between populations of spadefoot toads ( Spea multiplicata ) that occur in sympatry with a heterospecific competitor and those that occur in allopatry. In sympatry, S. multiplicata is forced by its competitor onto a less profitable resource. As a result, sympatric females mature in poorer condition and invest less into offspring. Consequently, their offspring produce a resource-use phenotype that minimizes competition with the other species and that also differs from the phenotype produced in allopatry. These differences in trait expression between allopatry and sympatry disappear once mothers are equilibrated in body condition in the laboratory. Thus, a condition-dependent maternal effect mediates population divergence and character displacement. Such effects potentially buffer populations from extinction (via competitive exclusion) while genetic changes accumulate, which produce divergent traits in the absence of the maternal effect. Maternal effects may therefore often be important in determining the initial direction and rate of evolution during the early stages of character displacement.