Changes in sexual signals are greater than changes in ecological traits in a dichromatic group of fishes

Understanding the mechanisms by which phenotypic divergence occurs is central to speciation research. These mechanisms can be revealed by measuring differences in traits that are subject to different selection pressures; greater influence of different types of selection can be inferred from greater divergence in associated traits. Here, we address the potential roles of natural and sexual selection in promoting phenotypic divergence between species of snubnose darters by comparing differences in body shape, an ecologically relevant trait, and male color, a sexual signal. Body shape was measured using geometric morphometrics, and male color was measured using digital photography and visual system‐dependent color values. Differences in male color are larger than differences in body shape across eight allopatric, phylogenetically independent species pairs. While this does not exclude the action of divergent natural selection, our results suggest a relatively more important role for sexual selection in promoting recent divergence in darters. Variation in the relative differences between male color and body shape across species pairs reflects the continuous nature of speciation mechanisms, ranging from ecological speciation to speciation by sexual selection alone.     

Change in sexual signalling traits outruns morphological divergence across an ecological gradient in the post‐glacial radiation of the songbird genus Junco

The relative roles of natural and sexual selection in promoting evolutionary lineage divergence remains controversial and difficult to assess in natural systems. Local adaptation through natural selection is known to play a central role in promoting evolutionary divergence, yet secondary sexual traits can vary widely among species in recent radiations, suggesting that sexual selection may also be important in the early stages of speciation. Here, we compare rates of divergence in ecologically relevant traits (morphology) and sexually selected signalling traits (coloration) relative to neutral structure in genome‐wide molecular markers and examine patterns of variation in sexual dichromatism to explore the roles of natural and sexual selection in the diversification of the songbird genus Junco (Aves: Passerellidae). Juncos include divergent lineages in Central America and several dark‐eyed junco (J. hyemalis) lineages that diversified recently as the group recolonized North America following the last glacial maximum (ca. 18,000 years ago). We found an accelerated rate of divergence in sexually selected characters relative to ecologically relevant traits. Moreover, sexual dichromatism measurements suggested a positive relationship between the degree of colour divergence and the strength of sexual selection when controlling for neutral genetic distance. We also found a positive correlation between dichromatism and latitude, which coincides with the geographic axis of decreasing lineage age in juncos but also with a steep ecological gradient. Finally, we found significant associations between genome‐wide variants linked to functional genes and proxies of both sexual and natural selection. These results suggest that the joint effects of sexual and ecological selection have played a prominent role in the junco radiation.     

The diversification of mate preferences by natural and sexual selection

The evolution of sexual display traits or preferences for them in response to divergent natural selection will alter sexual selection within populations, yet the role of sexual selection in ecological speciation has received little empirical attention. We evolved 12 populations of Drosophila serrata in a two‐way factorial design to investigate the roles of natural and sexual selection in the evolution of female mate preferences for male cuticular hydrocarbons (CHCs). Mate preferences weakened in populations evolving under natural selection alone, implying a cost in the absence of their expression. Comparison of the vectors of linear sexual selection revealed that the populations diverged in the combination of male CHCs that females found most attractive, although this was not significant using a mixed modelling approach. Changes in preference direction tended to evolve when natural and sexual selection were unconstrained, suggesting that both processes may be the key to initial stages of ecological speciation. Determining the generality of this result will require data from various species across a range of novel environments.     

Sexual selection drives rapid divergence in bowerbird display traits

Abstract.— Sexual selection driving display trait divergence has been suggested as a cause of rapid speciation, but there is limited supporting evidence for this from natural populations. Where speciation by sexual selection has occurred in newly diverged populations, we expect that there will be significant differences in female preferences and corresponding male display traits in the absence of substantial genetic and other morphological differentiation. Two allopatric populations of the Vogelkop bowerbird, Amblyornis inornatus , show large, qualitative differences in a suite of display traits including bower structure and decorations. We experimentally demonstrate distinct male decoration color preferences within each population, provide direct evidence of female preferences for divergent decoration and bower traits in the population with more elaborate display, and show that there is minimal genetic differentiation between these populations. These results support the speciation by sexual selection hypothesis and are most consistent with the hypothesis that changes in male display have been driven by divergent female choice.     

Contemporary sexual selection does not explain variation in male display traits among populations

Sexual selection is widely hypothesized to facilitate the evolution of reproductive isolation through divergence in sexual traits and sexual trait preferences among populations. However, direct evidence of divergent sexual selection causing intraspecific trait divergence remains limited. Using the wolf spider Schizocosa crassipes, we characterized patterns of female mate choice within and among geographic locations and related those patterns to geographic variation in male display traits to test whether divergent sexual selection caused by mate choice explains intraspecific trait variation. We found evidence of phenotypic selection on male behavior arising from female mate choice, but no evidence that selection varied among locations. Only those suites of morphological and behavioral traits that did not influence mate choice varied geographically. These results are inconsistent with ongoing divergent sexual selection underlying the observed intraspecific divergence in male display traits. These findings align with theory on the potentially restrictive conditions under which divergent sexual selection may persist, and suggest that long‐term studies capable of detecting periodic or transient divergent sexual selection will be critical to rigorously assess the relative importance of divergent sexual selection in intraspecific trait divergence.     

The role of sexual isolation during rapid ecological divergence: Evidence for a new dimension of isolation in Rhagoletis pomonella

The pace of divergence and likelihood of speciation often depends on how and when different types of reproductive barriers evolve. Questions remain about how reproductive isolation evolves after initial divergence. We tested for the presence of sexual isolation (reduced mating between populations due to divergent mating preferences and traits) in Rhagoletis pomonella flies, a model system for incipient ecological speciation. We measured the strength of sexual isolation between two very recently diverged (~170 generations) sympatric populations, adapted to different host fruits (hawthorn and apple). We found that flies from both populations were more likely to mate within than between populations. Thus, sexual isolation may play an important role in reducing gene flow allowed by early-acting ecological barriers. We also tested how warmer temperatures predicted under climate change could alter sexual isolation and found that sexual isolation was markedly asymmetric under warmer temperatures – apple males and hawthorn females mated randomly while apple females and hawthorn males mated more within populations than between. Our findings provide a window into the early speciation process and the role of sexual isolation after initial ecological divergence, in addition to examining how environmental conditions could shape the likelihood of further divergence.     

Host shifts and signal divergence: mating signals covary with host use in a complex of specialized plant‐feeding insects

A combination of divergent natural and sexual selection is a powerful cause of speciation. This conjunction of evolutionary forces may often occur when divergence is initiated by ecological differences between populations because local adaptation to new resources can lead to changes in sexual selection. The hypothesis that differences in resource use contribute to the evolution of reproductive isolation by altering the nature of sexual selection predicts that: (1) differences in sexual traits, such as signals and preferences, are an important source of reproductive isolation between species using different resources; (2) there are identifiable sources of selection on sexual traits that differ between species using different resources; and (3) signals vary between populations using different resources to a larger extent than between populations using the same resource at different localities. Testing these predictions requires a group of closely‐related species or populations that specialize on different resources and for which the traits involved in mate choice are known. The Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae) are host plant specialists in which speciation is associated with shifts to novel host plants. Mating in this complex is preceded by an exchange of vibrational signals transmitted through host plant stems, and the signal traits important for mate choice have been identified. In the E. binotata complex, previous work has supported the first two predictions: (1) signal differences between species are important in mate recognition and (2) host shifts can alter both the trait values favoured by sexual selection and the evolutionary response to that selection. In the present study, we tested the last prediction by conducting a large‐scale study of mating signal variation within and between the 11 species in the complex. We find that differences in host use are strongly associated with differences in signal traits important for mate recognition. This result supports the hypothesis that hosts shifts have led to speciation in this group in part through their influence on divergence in mate communication systems. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 99 , 60–72.     

Multiple speciation events in an arthropod with divergent evolution in sexual morphology

Sexual selection can facilitate divergent evolution of traits related to mating and consequently promote speciation. Theoretically, independent operation of sexual selection in different populations can lead to divergence of sexual traits among populations and result in allopatric speciation. Here, we show that divergent evolution in sexual morphology affecting mating compatibility (body size and genital morphologies) and speciation have occurred in a lineage of millipedes, the Parafontaria tonominea species complex. In this millipede group, male and female body and genital sizes exhibit marked, correlated divergence among populations, and the diverged morphologies result in mechanical reproductive isolation between sympatric species. The morphological divergence occurred among populations independently and without any correlation with climatic variables, although matching between sexes has been maintained, suggesting that morphological divergence was not a by-product of climatic adaptation. The diverged populations underwent restricted dispersal and secondary contact without hybridization. The extent of morphological difference between sympatric species is variable, as is diversity among allopatric populations; consequently, the species complex appears to contain many species. This millipede case suggests that sexual selection does contribute to species richness via morphological diversification when a lineage of organisms consists of highly divided populations owing to limited dispersal.     

The ecology of sexual conflict: ecologically dependent parallel evolution of male harm and female resistance in Drosophila melanogaster

The prevalence of sexual conflict in nature, along with the potentially stochastic nature of the resulting coevolutionary trajectories, makes it an important driver of phenotypic divergence and speciation that can operate even in the absence of environmental differences. The majority of empirical work investigating sexual conflict's role in population divergence/speciation has therefore been done in uniform environments and any role of ecology has largely been ignored. However, theory suggests that natural selection can constrain phenotypes influenced by sexual conflict. We use replicate populations of Drosophila melanogaster adapted to alternative environments to test how ecology influences the evolution of male effects on female longevity. The extent to which males reduce female longevity, as well as female resistance to such harm, both evolved in association with adaptation to the different environments. Our results demonstrate that ecology plays a central role in shaping patterns of population divergence in traits under sexual conflict.     

The maintenance of phenotypic divergence through sexual selection: An experimental study in barn swallows Hirundo rustica

Previous studies have shown that sexual signals can rapidly diverge among closely related species. However, we lack experimental studies to demonstrate that differences in trait‐associated reproductive performance maintain sexual trait differences between closely related populations, in support for a role of sexual selection in speciation. Populations of Northern Hemisphere distributed barn swallows Hirundo rustica are closely related, yet differ in two plumage‐based traits: ventral color and length of the outermost tail feathers (streamers). Here we provide experimental evidence that manipulations of these traits result in different reproductive consequences in two subspecies of barn swallow: (H. r. erythrogaster in North America and H. r. transitiva in the East Mediterranean). Experimental results in Colorado, USA, demonstrate that males with (1) darkened ventral coloration and (2) shortened streamers gained paternity between two successive reproductive bouts. In contrast, exaggeration of both traits improved reproductive performance within H. r. transitiva in Israel: males with a combination treatment of darkened ventral coloration and elongated streamers gained paternity between two successive reproductive bouts. Collectively, these experimental results fill an important gap in our understanding for how divergent sexual selection maintains phenotype differentiation in closely related populations, an important aspect of the speciation process.     

When can ecological speciation be detected with neutral loci?

It is not yet clear under what conditions empirical studies can reliably detect progress toward ecological speciation through the analysis of allelic variation at neutral loci. We use a simulation approach to investigate the range of parameter space under which such detection is, and is not, likely. We specifically test for the conditions under which divergent natural selection can cause a ‘generalized barrier to gene flow’ that is present across the genome. Our individual‐based numerical simulations focus on how population divergence at neutral loci varies in relation to recombination rate with a selected locus, divergent selection on that locus, migration rate and population size. We specifically test whether genetic differences at neutral markers are greater between populations in different environments than between populations in similar environments. We find that this expected signature of ecological speciation can be detected under part of the parameter space, most consistently when divergent selection is strong and migration is intermediate. By contrast, the expected signature of ecological speciation is not reliably detected when divergent selection is weak or migration is low or high. These findings provide insights into the strengths and weaknesses of using neutral markers to infer ecological speciation in natural systems.     

Speciation is associated with changing ornamentation rather than stronger sexual selection

Although sexual ornamentation mediates reproductive isolation, comparative evidence does not support the hypothesis that stronger sexual selection promotes speciation. Prior analyses have neglected the possibility that decreases in ornamentation may also promote speciation, such that both increases and decreases in the strength of sexual selection and associated changes in ornamentation promote speciation. To test this hypothesis, we studied color ornamentation in one of the largest and fastest avian radiations, the estrildid finches. We show that more ornamented lineages do not speciate more, even though they tend to have faster rates of ornamental evolution, whereas changes in ornamentation (i.e., increases or decreases) are associated with speciation. This indicates that divergence in sexually selected ornamentation, rather than stronger sexual selection, promotes or is otherwise associated with speciation. We also show that gregariousness and investment in reproduction are related to the elaboration of some ornamental traits, suggesting ecological influences on speciation mediated by ornamentation. We conclude that past work focusing specifically on the strength of sexual selection may have greatly underestimated the importance of sexual ornamentation for speciation.     

Divergence of a speciation trait through artificial selection: Insights into constraints,by-product effects and sexual isolation

Speciation and sexual isolation often occur when divergent female mating preferences target male secondary sexual traits. Despite the importance of such male signals, little is known about their evolvability and genetic linkage to other traits during speciation. To answer these questions, we imposed divergent artificial selection for 10 non-overlapping generations on the Inter-Pulse-Interval (IPI) of male courtship songs; which has been previously shown to be a major species recognition trait for females in the Drosophila athabasca species complex. Focusing on one of the species, Drosophila mahican (previously known as EA race), we examined IPI's: (1) rate of divergence, (2) response to selection in different directions, (3) genetic architecture of divergence and (4) by-product effects on other traits that have diverged in the species complex. We found rapid and consistent response for higher IPI but less response to lower IPI; implying asymmetrical constraints. Genetic divergence in IPI differed from natural species in X versus autosome contribution and in dominance, suggesting that evolution may take different paths. Finally, selection on IPI did not alter other components of male songs, or other ecological traits, and did not cause divergence in female preferences, as evidenced by lack of sexual isolation. This suggests that divergence of male courtship song IPI is unconstrained by genetic linkage with other traits in this system. This lack of linkage between male signals and other traits implies that female preferences or ecological selection can co-opt and mould specific male signals for species recognition free of genetic constraints from other traits.     

Parallel evolution of sexual isolation in sticklebacks

Mechanisms of speciation are not well understood, despite decades of study. Recent work has focused on how natural and sexual selection cause sexual isolation. Here, we investigate the roles of divergent natural and sexual selection in the evolution of sexual isolation between sympatric species of threespine sticklebacks. We test the importance of morphological and behavioral traits in conferring sexual isolation and examine to what extent these traits have diverged in parallel between multiple, independently evolved species pairs. We use the patterns of evolution in ecological and mating traits to infer the likely nature of selection on sexual isolation. Strong parallel evolution implicates ecologically based divergent natural and/or sexual selection, whereas arbitrary directionality implicates nonecological sexual selection or drift. In multiple pairs we find that sexual isolation arises in the same way: assortative mating on body size and asymmetric isolation due to male nuptial color. Body size and color have diverged in a strongly parallel manner, similar to ecological traits. The data implicate ecologically based divergent natural and sexual selection as engines of speciation in this group.     

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.     

Female mate choice of male signals is unlikely to promote ecological adaptation in Enchenopa treehoppers (Hemiptera: Membracidae)

A key question in speciation research is how ecological and sexual divergence arise and interact. We tested the hypothesis that mate choice causes local adaptation and ecological divergence using the rationale that the performance~signal trait relationship should parallel the attractiveness~signal trait relationship. We used female fecundity as a measure of ecological performance. We used a species in the Enchenopa binotata treehopper complex, wherein speciation involves adaptation to novel environments and divergence in sexual communication. We used a full‐sibling, split‐family rearing design to estimate genetic correlations (r_G) between fecundity and signal traits, and compared those relationships against population‐level mate preferences for the signal traits. Animal model estimates for r_G between female fecundity and male signal traits overlapped zero—rejecting the hypothesis—but could reflect sample size limitations. The magnitude of r_G correlated with the strength of the mate preferences for the corresponding signal traits, especially for signal frequency, which has the strongest mate preference and the most divergence in the complex. However, signal frequencies favored by the population‐level mate preference are not associated with high fecundity. Therefore, mate preferences do not appear to have been selected to favor high‐performance genotypes. Our findings suggest that ecological and sexual divergence may arise separately, but reinforce each other, during speciation.     

Predation‐associated divergence of male genital morphology in a livebearing fish

Male genital morphology is remarkably diverse across internally fertilizing animals, a phenomenon largely attributed to sexual selection. Ecological differences across environments can alter the context of sexual selection, yet little research has addressed how this may influence the rapid, divergent evolution of male genitalia. Using the model system of Bahamas mosquitofish (Gambusia hubbsi) undergoing ecological speciation across blue holes, we used geometric morphometric methods to test (i) whether male genital shape (the small, approximately 1 mm long, distal tip of the sperm‐transfer organ, the gonopodium) has diverged between populations with and without predatory fish and (ii) whether any observed divergence has a genetic basis. We additionally examined the effects of genetic relatedness and employed model selection to investigate other environmental factors (i.e. interspecific competition, adult sex ratio and resource availability) that could potentially influence genital shape via changes in sexual selection. Predation regime comprised the most important factor associated with male genital divergence in this system, although sex ratio and some aspects of resource availability had suggestive effects. We found consistent, heritable differences in male genital morphology between predation regimes: Bahamas mosquitofish coexisting with predatory fish possessed more elongate genital tips with reduced soft tissue compared with counterparts inhabiting blue holes without predatory fish. We suggest this may reflect selection for greater efficiency of sperm transfer and fertilization during rapid and often forced copulations in high‐predation populations or differences in sexual conflict between predation regimes. Our study highlights the potential importance of ecological variation, particularly predation risk, in indirectly generating genital diversity.     

EVOLUTION OF DIVERGENT FEMALE MATING PREFERENCE IN RESPONSE TO EXPERIMENTAL SEXUAL SELECTION

Sexual selection is predicted to drive the coevolution of mating signals and preferences (mating traits) within populations, and could play a role in speciation if sexual isolation arises due to mating trait divergence between populations. However, few studies have demonstrated that differences in mating traits between populations result from sexual selection alone. Experimental evolution is a promising approach to directly examine the action of sexual selection on mating trait divergence among populations. We manipulated the opportunity for sexual selection (low vs. high) in populations of Drosophila pseudoobscura. Previous studies on these experimental populations have shown that sexual selection manipulation resulted in the divergence between sexual selection treatments of several courtship song parameters, including interpulse interval (IPI) which markedly influences male mating success. Here, we measure female preference for IPI using a playback design to test for preference divergence between the sexual selection treatments after 130 generations of experimental sexual selection. The results suggest that female preference has coevolved with male signal, in opposite directions between the sexual selection treatments, providing direct evidence of the ability of sexual selection to drive the divergent coevolution of mating traits between populations. We discuss the implications in the context sexual selection and speciation.     

Patterns of reproductive isolation within and between two Lygaeus species characterized by sexual conflicts over mating

Theory suggests that, under some circumstances, sexual conflict over mating can lead to divergent sexually antagonistic coevolution among populations for traits associated with mating, and that this can promote reproductive isolation and hence speciation. However, sexual conflict over mating may also select for traits (e.g. male willingness to mate) that enhance gene flow between populations, limiting population divergence. In the present study, we compare pre‐ and post‐mating isolation within and between two species characterized by male–female conflict over mating rate. We quantify sexual isolation among five populations of the seed bug Lygaeus equestris collected from Italy and Sweden, and two replicates of a population of the sister‐species Lygaeus simulans, also collected from Italy. We find no evidence of reproductive isolation amongst populations of L. equestris, suggesting that sexual conflict over mating has not led to population divergence in relevant mating traits in L. equestris. However, there was strong asymmetric pre‐mating isolation between L. equestris and L. simulans: male L. simulans were able to mate successfully with female L. equestris, whereas male L. equestris were largely unable to mate with female L. simulans. We found little evidence for strong post‐mating isolation between the two species, however, with hybrid F₂ offspring being produced. Our results suggest that sexual conflict over mating has not led to population divergence, and indeed perhaps supports the contrary theoretical prediction that male willingness to mate may retard speciation by promoting gene flow.     

Looking for a similar partner: host plants shape mating preferences of herbivorous insects by altering their contact pheromones

The role of phenotypical plasticity in ecological speciation and the evolution of sexual isolation remains largely unknown. We investigated whether or not divergent host plant use in an herbivorous insect causes assortative mating by phenotypically altering traits involved in mate recognition. We found that males of the mustard leaf beetle Phaedon cochleariae preferred to mate with females that were reared on the same plant species to females provided with a different plant species, based on divergent cuticular hydrocarbon profiles that serve as contact pheromones. The cuticular hydrocarbon phenotypes of the beetles were host plant specific and changed within 2 weeks after a shift to a novel host plant species. We suggest that plant-induced phenotypic divergence in mate recognition cues may act as an early barrier to gene flow between herbivorous insect populations on alternative host species, preceding genetic divergence and thus, promoting ecological speciation.