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.     

Divergent adaptation promotes reproductive isolation among experimental populations of the filamentous fungus <Emphasis Type="Italic">Neurospora</Emphasis>

Background  

An open, focal issue in evolutionary biology is how reproductive isolation and speciation are initiated; elucidation of mechanisms with empirical evidence has lagged behind theory. Under ecological speciation, reproductive isolation between populations is predicted to evolve incidentally as a by-product of adaptation to divergent environments. The increased genetic diversity associated with interspecific hybridization has also been theorized to promote the development of reproductive isolation among independent populations. Using the fungal model Neurospora, we founded experimental lineages from both intra- and interspecific crosses, and evolved them in one of two sub-optimal, selective environments. We then measured the influence that initial genetic diversity and the direction of selection (parallel versus divergent) had on the evolution of reproductive isolation.     

Ecological speciation

Ecological processes are central to the formation of new species when barriers to gene flow (reproductive isolation) evolve between populations as a result of ecologically‐based divergent selection. Although laboratory and field studies provide evidence that ‘ecological speciation’ can occur, our understanding of the details of the process is incomplete. Here we review ecological speciation by considering its constituent components: an ecological source of divergent selection, a form of reproductive isolation, and a genetic mechanism linking the two. Sources of divergent selection include differences in environment or niche, certain forms of sexual selection, and the ecological interaction of populations. We explore the evidence for the contribution of each to ecological speciation. Forms of reproductive isolation are diverse and we discuss the likelihood that each may be involved in ecological speciation. Divergent selection on genes affecting ecological traits can be transmitted directly (via pleiotropy) or indirectly (via linkage disequilibrium) to genes causing reproductive isolation and we explore the consequences of both. Along with these components, we also discuss the geography and the genetic basis of ecological speciation. Throughout, we provide examples from nature, critically evaluate their quality, and highlight areas where more work is required.     

Ecological speciation in Gambusia fishes

Although theory indicates that natural selection can facilitate speciation as a by-product, demonstrating ongoing speciation via this by-product mechanism in nature has proven difficult. We examined morphological, molecular, and behavioral data to investigate ecology's role in incipient speciation for a post-Pleistocene radiation of Bahamas mosquitofish (Gambusia hubbsi) inhabiting blue holes. We show that adaptation to divergent predator regimes is driving ecological speciation as a by-product. Divergence in body shape, coupled with assortative mating for body shape, produces reproductive isolation that is twice as strong between populations inhabiting different predator regimes than between populations that evolved in similar ecological environments. Gathering analogous data on reproductive isolation at the interspecific level in the genus, we find that this mechanism of speciation may have been historically prevalent in Gambusia. These results suggest that speciation in nature can result as a by-product of divergence in ecologically important traits, producing interspecific patterns that persist long after speciation events have completed.     

生态物种形成及其研究进展

物种形成是基本的进化过程, 也是生物多样性形成的基础。自然选择可以导致新物种的产生。生态物种形成是指以生态为基础的歧化选择使不同群体分化产生生殖隔离的物种形成过程。本文首先回顾了生态物种形成的研究历史, 并详细介绍了生态物种形成的3个要素, 即歧化选择的来源、生殖隔离的形式以及关联歧化选择与生殖隔离的遗传机制。歧化选择的来源主要包括不同的环境或生态位、不同形式的性选择, 以及群体间的相互作用。生殖隔离的形式多种多样, 我们总结了合子前和合子后隔离的遗传学机制以及在生态物种形成中起到的作用。控制适应性性状的基因与导致生殖隔离的基因可以通过基因多效性或连锁不平衡相互关联起来。借助于第二代测序技术, 研究者可以对生态物种形成的遗传学与基因组学基础进行研究。此外, 本文还总结了生态物种形成领域最新的研究进展, 包括平行进化的全基因组基础, 以及基因流影响群体分化的理论基础。通过归纳比较由下至上和由上至下这两种不同的研究思路, 作者认为这两种思路的结合可以为生态物种形成基因的筛选提供更有力也更精确的方法。同时, 作者还提出生态物种形成的研究应该基于更好的表型描述以及更完整的基因组信息, 研究的物种也应该具有更广泛的代表性。     

Sexual dimorphism and speciation on two ecological coins: patterns from nature and theoretical predictions

Adaptive divergence of phenotypes, such as sexual dimorphism or adaptive speciation, can result from disruptive selection via competition for limited resources. Theory indicates that speciation and sexual dimorphism can result from identical ecological conditions, but co-occurrence is unlikely because whichever evolves first should dissipate the disruptive selection necessary to drive evolution of the other. Here, we consider ecological conditions in which disruptive selection can act along multiple ecological axes. Speciation in lake populations of threespine sticklebacks (Gasterosteus aculeatus) has been attributed to disruptive selection due to competition for resources. Head shape in sticklebacks is thought to reflect adaptation to different resource acquisition strategies. We measure sexual dimorphism and species variation in head shape and body size in stickleback populations in two lakes in British Columbia, Canada. We find that sexual dimorphism in head shape is greater than interspecific differences. Using a numerical simulation model that contains two axes of ecological variation, we show that speciation and sexual dimorphism can readily co-occur when the effects of loci underlying sexually dimorphic traits are orthogonal to those underlying sexually selected traits.     

Mutation‐order divergence by sexual selection: diversification of sexual signals in similar environments as a first step in speciation

The origin of species remains a central question, and recent research focuses on the role of ecological differences in promoting speciation. Ecological differences create opportunities for divergent selection (i.e. ‘ecological’ speciation), a Darwinian hypothesis that hardly requires justification. In contrast, ‘mutation‐order’ speciation proposes that, instead of adapting to different environments, populations find different ways to adapt to similar environments, implying that speciation does not require ecological differences. This distinction is critical as it provides an alternative hypothesis to the prevailing view that ecological differences drive speciation. Speciation by sexual selection lies at the centre of debates about the importance of ecological differences in promoting speciation; here, we present verbal and mathematical models of mutation‐order divergence by sexual selection. We develop three general cases and provide a two‐locus population genetic model for each. Results indicate that alternative secondary sexual traits can fix in populations that initially experience similar natural and sexual selection and that divergent traits and preferences can remain stable in the face of low gene flow. This stable divergence can facilitate subsequent divergence that completes or reinforces speciation. We argue that a mutation‐order process could explain widespread diversity in secondary sexual traits among closely related, allopatric species.     

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.     

Variation in Body Shape across Species and Populations in a Radiation of Diaptomid Copepods

Inter and intra-population variation in morphological traits, such as body size and shape, provides important insights into the ecological importance of individual natural populations. The radiation of Diaptomid species (~400 species) has apparently produced little morphological differentiation other than those in secondary sexual characteristics, suggesting sexual, rather than ecological, selection has driven speciation. This evolutionary history suggests that species, and conspecific populations, would be ecologically redundant but recent work found contrasting ecosystem effects among both species and populations. This study provides the first quantification of shape variation among species, populations, and/or sexes (beyond taxonomic illustrations and body size measurements) to gain insight into the ecological differentiation of Diaptomids. Here we quantify the shape of five Diaptomid species (family Diaptomidae) from four populations each, using morphometric landmarks on the prosome, urosome, and antennae. We partition morphological variation among species, populations, and sexes, and test for phenotype-by-environment correlations to reveal possible functional consequences of shape variation. We found that intraspecific variation was 18-35% as large as interspecific variation across all measured traits. Interspecific variation in body size and relative antennae length, the two traits showing significant sexual dimorphism, were correlated with lake size and geographic location suggesting some niche differentiation between species. Observed relationships between intraspecific morphological variation and the environment suggest that divergent selection in contrasting lakes might contribute to shape differences among local populations, but confirming this requires further analyses. Our results show that although Diaptomid species differ in their reproductive traits, they also differ in other morphological traits that might indicate ecological differences among species and populations.     

Non-ecological speciation, niche conservatism and thermal adaptation: how are they connected?

During the last decade, the ecological theory of adaptive radiation, and its corollary ??ecological speciation??, has been a major research theme in evolutionary biology. Briefly, this theory states that speciation is mainly or largely the result of divergent selection, arising from niche differences between populations or incipient species. Reproductive isolation evolves either as a result of direct selection on mate preferences (e.g. reinforcement), or as a correlated response to divergent selection (??by-product speciation??). Although there are now many tentative examples of ecological speciation, I argue that ecology??s role in speciation might have been overemphasised and that non-ecological and non-adaptive alternatives should be considered more seriously. Specifically, populations and species of many organisms often show strong evidence of niche conservatism, yet are often highly reproductively isolated from each other. This challenges niche-based ecological speciation and reveals partial decoupling between ecology and reproductive isolation. Furthermore, reproductive isolation might often evolve in allopatry before ecological differentiation between taxa or possibly through learning and antagonistic sexual interactions, either in allopatry or sympatry. Here I discuss recent theoretical and empirical work in this area, with some emphasis on odonates (dragonflies and damselflies) and suggest some future avenues of research. A main message from this paper is that the ecology of species differences is not the same as ecological speciation, just like the genetics of species differences does not equate to the genetics of speciation.     

Mate preference across the speciation continuum in a clade of mimetic butterflies

Premating behavioral isolation is increasingly recognized as an important part of ecological speciation, where divergent natural selection causes the evolution of reproductive barriers. A number of studies have now demonstrated that traits under divergent natural selection also affect mate preferences. However, studies of single species pairs only capture a snapshot of the speciation process, making it difficult to assess the role of mate preferences throughout the entire process. Heliconius butterflies are well known for their brightly colored mimetic warning patterns, and previous studies have shown that these patterns are also used as mate recognition cues. Here, we present mate preference data for four pairs of sister taxa, representing different stages of divergence, which together allow us to compare diverging mate preferences across the continuum of Heliconius speciation. Using a novel Bayesian approach, our results support a model of ecological speciation in which strong premating isolation arises early, but continues to increase throughout the continuum from polymorphic populations through to "good," sympatric ecologically divergent species.     

Ecological speciation in sympatric palms: 1. Gene expression,selection and pleiotropy

Ecological speciation requires divergent selection, reproductive isolation and a genetic mechanism to link the two. We examined the role of gene expression and coding sequence evolution in this process using two species of Howea palms that have diverged sympatrically on Lord Howe Island, Australia. These palms are associated with distinct soil types and have displaced flowering times, representing an ideal candidate for ecological speciation. We generated large amounts of RNA‐Seq data from multiple individuals and tissue types collected on the island from each of the two species. We found that differentially expressed loci as well as those with divergent coding sequences between Howea species were associated with known ecological and phenotypic differences, including response to salinity, drought, pH and flowering time. From these loci, we identified potential ‘ecological speciation genes’ and further validate their effect on flowering time by knocking out orthologous loci in a model plant species. Finally, we put forward six plausible ecological speciation loci, providing support for the hypothesis that pleiotropy could help to overcome the antagonism between selection and recombination during speciation with gene flow.     

Experimental evidence that competition between stickleback species favours adaptive character divergence

The ecological character displacement hypothesis assumes that the effects of interspecific resource competition cause divergent selection to favour phenotypes that exploit non-shared resources. This model predicts that interspecific competition declines with increased divergence. Direct tests of this decline are rare despite much comparative evidence for character displacement. We tested this prediction using a pair of divergent brook sticklebacks. Brook sticklebacks sympatric with ninespine sticklebacks have diverged from local allopatric brook populations, and so the two types of brook sticklebacks potentially represent pre- and post-displacement forms. We used enclosures placed in a lake to compare short-term fitness (growth) of sympatric (post-displacement) and allopatric (pre-displacement) brook forms in the presence and absence of ninespine sticklebacks. Brook sticklebacks grew less in the presence vs. absence of ninespine sticklebacks, indicating that interspecific competition occurred. As expected, allopatric brook forms had lower growth than sympatric forms when ninespine sticklebacks were present. This result suggests that ecological character displacement has occurred.     

Social selection parapatry in Afrotropical sunbirds

The extent of range overlap of incipient and recent species depends on the type and magnitude of phenotypic divergence that separates them, and the consequences of phenotypic divergence on their interactions. Signal divergence by social selection likely initiates many speciation events, but may yield niche‐conserved lineages predisposed to limit each others’ ranges via ecological competition. Here, we examine this neglected aspect of social selection speciation theory in relation to the discovery of a nonecotonal species border between sunbirds. We find that Nectarinia moreaui and Nectarinia fuelleborni meet in a ～6 km wide contact zone, as estimated by molecular cline analysis. These species exploit similar bioclimatic niches, but sing highly divergent learned songs, consistent with divergence by social selection. Cline analyses suggest that within‐species stabilizing social selection on song‐learning predispositions maintains species differences in song despite both hybridization and cultural transmission. We conclude that ecological competition between moreaui and fuelleborni contributes to the stabilization of the species border, but that ecological competition acts in conjunction with reproductive interference. The evolutionary maintenance of learned song differences in a hybrid zone recommend this study system for future studies on the mechanisms of learned song divergence and its role in speciation.     

Quantifying Reproductive Barriers in a Sympatric Pair of Darter Species

Quantifying and comparing the strengths of different reproductive barriers between diverging lineages is especially useful for determining the evolutionary mechanisms driving speciation. Etheostoma barrenense and Etheostoma zonale are closely related sympatric species of darters that are sexually dimorphic and exhibit clear differences in male nuptial coloration. Prior studies demonstrated that these species exhibit complete behavioral isolation, and that both intraspecific and interspecific variation in male coloration play a role in female choice, all consistent with speciation by sexual selection on male nuptial color. Remaining unclear, however, is whether behavioral isolation is the strongest reproductive barrier between these species or, alternatively, whether additional reproductive barriers are equally strong, which could implicate mechanisms other than sexual selection in speciation. Here, we compare the relative strengths of multiple reproductive barriers between the two focal species, measuring: (1) ecological isolation, (2) gametic incompatibility, (3) hybrid inviability, (4) conspecific sperm precedence, and comparing these measures to a previously estimated strength of behavioral isolation. We find that behavioral isolation is the strongest reproductive barrier measured to date and suggest it may be the only barrier that has evolved to completion. This result provides additional empirical evidence for speciation driven by sexual selection and provides insight into the maintenance of sympatric species in nature.     

Reproductive Isolation of Hybrid Populations Driven by Genetic Incompatibilities

Despite its role in homogenizing populations, hybridization has also been proposed as a means to generate new species. The conceptual basis for this idea is that hybridization can result in novel phenotypes through recombination between the parental genomes, allowing a hybrid population to occupy ecological niches unavailable to parental species. Here we present an alternative model of the evolution of reproductive isolation in hybrid populations that occurs as a simple consequence of selection against genetic incompatibilities. Unlike previous models of hybrid speciation, our model does not incorporate inbreeding, or assume that hybrids have an ecological or reproductive fitness advantage relative to parental populations. We show that reproductive isolation between hybrids and parental species can evolve frequently and rapidly under this model, even in the presence of substantial ongoing immigration from parental species and strong selection against hybrids. An interesting prediction of our model is that replicate hybrid populations formed from the same pair of parental species can evolve reproductive isolation from each other. This non-adaptive process can therefore generate patterns of species diversity and relatedness that resemble an adaptive radiation. Intriguingly, several known hybrid species exhibit patterns of reproductive isolation consistent with the predictions of our model.     

Male competition fitness landscapes predict both forward and reverse speciation

Speciation is facilitated when selection generates a rugged fitness landscape such that populations occupy different peaks separated by valleys. Competition for food resources is a strong ecological force that can generate such divergent selection. However, it is unclear whether intrasexual competition over resources that provide mating opportunities can generate rugged fitness landscapes that foster speciation. Here we use highly variable male F2 hybrids of benthic and limnetic threespine sticklebacks, Gasterosteus aculeatus Linnaeus, 1758, to quantify the male competition fitness landscape. We find that disruptive sexual selection generates two fitness peaks corresponding closely to the male phenotypes of the two parental species, favouring divergence. Most surprisingly, an additional region of high fitness favours novel hybrid phenotypes that correspond to those observed in a recent case of reverse speciation after anthropogenic disturbance. Our results reveal that sexual selection through male competition plays an integral role in both forward and reverse speciation.     

Divergence in coloration and ecological speciation in the Anolis marmoratus species complex

Adaptive divergence in coloration is expected to produce reproductive isolation in species that use colourful signals in mate choice and species recognition. Indeed, many adaptive radiations are characterized by differentiation in colourful signals, suggesting that divergent selection acting on coloration may be an important component of speciation. Populations in the Anolis marmoratus species complex from the Caribbean island of Guadeloupe display striking divergence in the colour and pattern of adult males that occurs over small geographic distances, suggesting strong divergent selection. Here we test the hypothesis that divergence in coloration results in reduced gene flow among populations. We quantify variation in adult male coloration across a habitat gradient between mesic and xeric habitats, use a multilocus coalescent approach to infer historical demographic parameters of divergence, and examine gene flow and population structure using microsatellite variation. We find that colour variation evolved without geographic isolation and in the face of gene flow, consistent with strong divergent selection and that both ecological and sexual selection are implicated. However, we find no significant differentiation at microsatellite loci across populations, suggesting little reproductive isolation and high levels of contemporary gene exchange. Strong divergent selection on loci affecting coloration probably maintains clinal phenotypic variation despite high gene flow at neutral loci, supporting the notion of a porous genome in which adaptive portions of the genome remain fixed whereas neutral portions are homogenized by gene flow and recombination. We discuss the impact of these findings for studies of colour evolution and ecological speciation.     

Interspecific competition promotes habitat and morphological divergence in a secondary contact zone between two hybridizing songbirds

Interspecific competition is assumed to play an important role in the ecological differentiation of species and speciation. However, empirical evidence for competition's role in speciation remains surprisingly scarce. Here, we studied the role of interspecific competition in the ecological differentiation and speciation of two closely related songbird species, the Common Nightingale (Luscinia megarhynchos) and the Thrush Nightingale (Luscinia luscinia). Both species are insectivorous and ecologically very similar. They hybridize in a secondary contact zone, which is a mosaic of sites where both species co‐occur (syntopy) and sites where only one species is present (allotopy). We analysed fine‐scale habitat data for both species in both syntopic and allotopic sites and looked for associations between habitat use and bill morphology, which have been previously shown to be more divergent in sympatry than in allopatry. We found that the two nightingale species differ in habitat use in allotopic sites, where L. megarhynchos occurred in drier habitats and at slightly higher elevations, but not in syntopic sites. Birds from allotopic sites also showed higher interspecific divergence in relative bill size compared to birds from syntopic sites. Finally, we found an association between bill morphology and elevation. Our results are consistent with the view that interspecific competition in nightingales has resulted in partial habitat segregation in sympatry and that the habitat‐specific food supply has in turn very likely led to bill size divergence. Such ecological divergence may enhance prezygotic as well as extrinsic postzygotic isolation and thus accelerate the completion of the speciation process.     

Evidence for sympatric speciation by host shift in the sea

The genetic divergence and evolution of new species within the geographic range of a single population (sympatric speciation) contrasts with the well-established doctrine that speciation occurs when populations become geographically isolated (allopatric speciation). Although there is considerable theoretical support for sympatric speciation, this mode of diversification remains controversial, at least in part because there are few well-supported examples. We use a combination of molecular, ecological, and biogeographical data to build a case for sympatric speciation by host shift in a new species of coral-dwelling fish (genus Gobiodon). We propose that competition for preferred coral habitats drives host shifts in Gobiodon and that the high diversity of corals provides the source of novel, unoccupied habitats. Disruptive selection in conjunction with strong host fidelity could promote rapid reproductive isolation and ultimately lead to species divergence. Our hypothesis is analogous to sympatric speciation by host shift in phytophagous insects except that we propose a primary role for intraspecific competition in the process of speciation. The fundamental similarity between these fishes and insects is a specialized and intimate relationship with their hosts that makes them ideal candidates for speciation by host shift.