Pattern Of Reproductive Character Displacement Research Articles

An experimental test of the evolutionary consequences of sympatry in Drosophila subquinaria.

Prezygotic isolation is often stronger between sympatric as opposed to allopatric taxa, but the underlying cause can be difficult to infer from comparative studies alone. Experimental evolution, where evolutionary responses to treatments manipulating the presence/absence of heterospecific individuals are tracked, can provide a powerful complementary approach. We used experimental evolution to investigate a naturally occurring pattern of reproductive character displacement in the mushroom-feeding fly, Drosophila subquinaria. In nature, female D. subquinaria from populations sympatric with the closely related Drosophila recens discriminate more strongly against heterospecific males than do females from allopatric populations. Starting with 16 replicate allopatric populations of D. subquinaria, we manipulated the presence/absence of D. recens during mating (experimental sympatry vs. control) and, when present, we allowed hybrids to live or kill them each generation. Across 12 generations, heterospecific offspring production from no-choice mating trials between D. subquinaria females and D. recens males declined in both experimental sympatry treatments relative to the control, suggesting increased sexual isolation. Male cuticular hydrocarbon profiles also evolved, but only in the hybrids killed treatment. Our results strongly imply that the existing reproductive character displacement in wild D. subquinaria populations was an evolutionary response to selection arising from secondary contact with D. recens.

Reproductive Character Displacement Drives Diversification of Male Courtship Songs in Drosophila.

AbstractMale secondary sexual traits are one of the most striking and diverse features of the animal kingdom. While these traits are often thought to evolve via sexual selection, many questions remain about their patterns of diversification and their role in speciation. To address these questions, I performed a comparative study of precopulatory male courtship songs of 119 Drosophila species across 10 distinct species groups. I related song divergence to genetic distances, geographic relationships, and sexual isolation between species. On the basis of pairwise Euclidean song distances, species groups typically retained their phylogenetic signal while species within groups diverged five times more in sympatry relative to allopatry, producing a pattern of reproductive character displacement. This occurred despite similar genetic distances in allopatry and sympatry, was exaggerated among younger species pairs, and was driven primarily by the parameter interpulse interval. While sexual isolation in sympatry was high even with low song divergence, these variables were correlated with each other and with increased divergence of female mating preferences in sympatry. The widespread pattern of character displacement implies that allopatric divergence due to processes like sexual selection are very slow relative to sympatric processes such as reinforcement and reproductive interference in driving song diversification across Drosophila.

Are assortative mating and genital divergence driven by reinforcement?

The evolution of assortative mating is a key part of the speciation process. Stronger assortment, or greater divergence in mating traits, between species pairs with overlapping ranges is commonly observed, but possible causes of this pattern of reproductive character displacement are difficult to distinguish. We use a multidisciplinary approach to provide a rare example where it is possible to distinguish among hypotheses concerning the evolution of reproductive character displacement. We build on an earlier comparative analysis that illustrated a strong pattern of greater divergence in penis form between pairs of sister species with overlapping ranges than between allopatric sister‐species pairs, in a large clade of marine gastropods (Littorinidae). We investigate both assortative mating and divergence in male genitalia in one of the sister‐species pairs, discriminating among three contrasting processes each of which can generate a pattern of reproductive character displacement: reinforcement, reproductive interference and the Templeton effect. We demonstrate reproductive character displacement in assortative mating, but not in genital form between this pair of sister species and use demographic models to distinguish among the different processes. Our results support a model with no gene flow since secondary contact and thus favor reproductive interference as the cause of reproductive character displacement for mate choice, rather than reinforcement. High gene flow within species argues against the Templeton effect. Secondary contact appears to have had little impact on genital divergence.

Call variability, stereotypy and relationships in syntopy of tetraploid common lesser escuerzo (Anura: Genus Odontophrynus)

We studied patterns of the geographic variation of mating calls of the common lesser escuerzo Odontophrynus americanus including populations living in syntopy with the closely related O. cordobae and adjacent allopatric populations. The dominant frequency, pulse rate, call duration and pulses/call showed the lowest intra-individual variation (CV<3%). The discriminant function analysis (DFA) assigned 88% of all calls to the correct individual, indicating that the advertisement calls of O. americanus are individually distinctive. Call duration, pulses per call and the dominant frequency were likely related to individual distinctiveness. Pulse rate and pulse temporal parameters related consistently showed the lowest values of CVb/CVw ratio and could be considered key properties for species recognition in O. americanus. We found a greater call divergence between species in syntopy than in allopatry in terms of the pulse rate and particularly the interpulse interval. These results appear to be consistent with a pattern of reproductive character displacement. Further studies testing female selectivity should be essential to evaluate whether acoustic differences observed between syntopic and allopatric populations are biologically significant and if there are differences in selectivity between such areas.

Reproductive character displacement of female mate preferences for male cuticular hydrocarbons in Drosophila subquinaria.

Several lines of evidence implicate sexual isolation in both initiating and completing the speciation process. Although its existence is straightforward to demonstrate, understanding the evolution of sexual isolation requires identifying the underlying phenotypes responsible so that we can determine how these have diverged. Here, we study geographic variation in female mate preferences for male sexual displays in the fly Drosophila subquinaria. Female D. subquinaria that are sympatric with its sister species D. recens discriminate strongly against both D. recens and allopatric conspecific males, whereas females from allopatric populations do not. Furthermore, female mate preferences target at least in part a suite of cuticular hydrocarbons (CHCs) in males and geographic variation in CHCs mirrors the pattern of mate discrimination. In this study, we quantify female mate preferences for male CHCs from populations that span the geographic range of D. subquinaria. We find that the direction of linear sexual selection varies significantly between populations that are sympatric versus allopatric with D. recens in a pattern of reproductive character displacement. Differences in preference partially align with existing differences in CHCs and patterns of sexual isolation, although discrepancies remain that suggest the involvement of additional traits and/or more complex, nonlinear preference functions.

Origins of female genital diversity: Predation risk and lock-and-key explain rapid divergence during an adaptive radiation.

The study of male genital diversity has long overshadowed evolutionary inquiry of female genitalia, despite its nontrivial diversity. Here, we identify four nonmutually exclusive mechanisms that could lead to genital divergence in females, and potentially generate patterns of correlated male-female genital evolution: (1) ecological variation alters the context of sexual selection ("ecology hypothesis"), (2) sexually antagonistic selection ("sexual-conflict hypothesis"), (3) female preferences for male genitalia mediated by female genital traits ("female-choice hypothesis"), and (4) selection against inter-population mating ("lock-and-key hypothesis"). We performed an empirical investigation of all four hypotheses using the model system of Bahamas mosquitofish inhabiting blue holes that vary in predation risk. We found unequivocal support for the ecology hypothesis, with females exhibiting a smaller genital opening in blue holes containing piscivorous fish. This is consistent with stronger postmating female choice/conflict when predators are present, but greater premating female choice in their absence. Our results additionally supported the lock-and-key hypothesis, uncovering a pattern of reproductive character displacement for genital shape. We found no support for the sexual conflict or female choice hypotheses. Our results demonstrate a strong role for ecology in generating female genital diversity, and suggest that lock-and-key may provide a viable cause of female genital diversification.

Reproductive character displacement of epicuticular compounds and their contribution to mate choice in Drosophila subquinaria and Drosophila recens.

Interactions between species can alter selection on sexual displays used in mate choice within species. Here we study the epicuticular pheromones of two Drosophila species that overlap partially in geographic range and are incompletely reproductively isolated. Drosophila subquinaria shows a pattern of reproductive character displacement against Drosophila recens, and partial behavioral isolation between conspecific sympatric versus allopatric populations, whereas D. recens shows no such variation in mate choice. First, using manipulative perfuming experiments, we show that females use pheromones as signals for mate discrimination both between species and among populations of D. subquinaria. Second, we show that patterns of variation in epicuticular compounds, both across populations and between species, are consistent with those previously shown for mating probabilities: pheromone compositions differ between populations of D. subquinaria that are allopatric versus sympatric with D. recens, but are similar across populations of D. recens regardless of overlap with D. subquinaria. We also identify differences in pheromone composition among allopatric regions of D. subquinaria. In sum, our results suggest that epicuticular compounds are key signals used by females during mate recognition, and that these traits have diverged among D. subquinaria populations in response to reinforcing selection generated by the presence of D. recens.

No reproductive character displacement in male advertisement signals of Hyla japonica in relation to the sympatric H. suweonensis

Reproductive interaction between closely related taxa may leave a distinctive signature in which populations of interacting taxa are more dissimilar in sympatry than in allopatry. An ideal condition for such a pattern of reproductive character displacement (RCD) may occur when a population has limited gene flow and experiences strong selection pressure, exerted by an interacting taxon in areas of sympatry. In Korea, there are two closely related treefrog species: Hyla japonica, which is distributed widely throughout the country, and Hyla suweonensis, which occurs sympatrically in a narrow strip of western coastal plains. H. suweonensis is only found within the distribution of H. japonica. These two species have a similar single-note call structure. Here, we tested the possibility of RCD in H. japonica by examining geographic variation in advertisement calls. Although means of temporal and spectral characters were significantly different between the two species, sympatric populations of H. japonica and H. suweonensis overlapped in distributions of most characters. Furthermore, allopatric and sympatric H. japonica populations did not differ in all call characters. Weak genetic differentiation between sympatric and allopatric populations of H. japonica implied either substantial gene flow or recent genetic isolation. Possible explanations for no RCD in male advertisement calls of H. japonica include a difference in fine temporal characteristics between the two species, migration between sympatric and allopatric localities in H. japonica, RCD in female preferences in H. japonica, and weak selection pressure by H. suweonensis.

Epicuticular Compounds of Drosophila subquinaria and D. recens: Identification, Quantification, and Their Role in Female Mate Choice

The epicuticle of various Drosophila species consists of long-chain cuticular hydrocarbons (CHCs) and their derivatives that play a role in waterproofing and a dynamic means of chemical communication. Here, via gas chromatography and mass spectrometry, we identified and quantified the epicuticular composition of D. recens and D. subquinaria, two closely related species that show a pattern of reproductive character displacement in nature. Twenty-four compounds were identified with the most abundant, 11-cis-Vaccenyl acetate, present only in males of each species. Also exclusive to males were five tri-acylglycerides. The 18 remaining compounds were CHCs, all shared between the sexes and species. These CHCs were composed of odd carbon numbers (C29, C31, C33, and C35), with an increase in structural isomers in the C33 and C35 groups. Saturated hydrocarbons comprise only methyl-branched alkanes and were found only in the C29 and C31 groups. Alkenes were the least prevalent, with alkadienes dominating the chromatographic landscape in the longer chain lengths. Sexual dimorphism was extensive with 6/8 of the logcontrast CHCs differing significantly in relative concentration between males and females in D. recens and D. subquinaria, respectively. Males of the two species also differed significantly in relative concentration of six CHCs, while females differed in none. Female-choice mating trials revealed directional sexual selection on male CHCs in a population of each species, consistent with female mate preferences for these traits. The sexual selection vectors differed significantly in multivariate trait space, suggesting that different pheromone blends determine male attractiveness in each species.

Using genomic data to revisit an early example of reproductive character displacement inHaitianAnolislizards

The pattern of reproductive character displacement (RCD)-in which traits associated with reproductive isolation are more different where two species occur together than where they occur in isolation-is frequently attributed to reinforcement, a process during which natural selection acting against maladaptive mating events leads to enhanced prezygotic isolation between species or incipient species. One of the first studies of RCD to include molecular genetic data was described 40years ago in a complex of Haitian trunk anole lizards using a small number of allozyme loci. In this example, Anolis caudalis appears to experience divergence in the color and pattern of an extensible throat fan, or dewlap, in areas of contact with closely related species at the northern and southern limits of its range. However, this case study has been largely overlooked for decades; meanwhile, explanations for geographic variation in dewlap color and pattern have focused primarily on adaptation to local signalling environments. We reinvestigate this example using amplified fragment length polymorphism (AFLP) genome scans, mtDNA sequence data, information on dewlap phenotypes and GIS data on environmental variation to test the hypothesis of RCD generated by reinforcement in Haitian trunk anoles. Together, our phenotypic and genetic results are consistent with RCD at the southern and northern limits of the range of A.caudalis. We evaluate the evidence for reinforcement as the explanation for RCD in Haitian trunk anoles, consider alternative explanations and provide suggestions for future work on the relationship between dewlap variation and speciation in Haitian trunk anoles.

INTRASPECIFIC REPRODUCTIVE CHARACTER DISPLACEMENT IN A POLYMORPHIC POISON DART FROG, DENDROBATES PUMILIO

Divergence in male mating signals and associated female preferences is often an important step in the process of speciation. Reproductive character displacement, the pattern of greater divergence of male signals and/or female preference in sympatry than in allopatry, has been observed in a variety of taxa with different degrees of postzygotic isolation. A number of selective processes, including reinforcement, have been proposed to cause such a pattern. Cases in which reproductive character displacement occurs among intraspecific variants are especially informative for understanding how selection acting within a species can lead to the evolution of reproductive barriers and speciation. This study tested the hypothesis that female strawberry poison dart frogs (Dendrobates pumilio) in polymorphic populations of the Bocas del Toro archipelago of Panama show stronger mating discrimination than do females from monomorphic populations, exhibiting an intraspecific pattern of reproductive character displacement. Our results contribute important insights into understanding selection's role in generating the striking diversity of Bocas del Toro's D. pumilio and provide a snapshot of what could be the early stages of reproductive isolation and speciation.

Speciation via species interactions: the divergence of mating traits within species

A species may overlap with a mosaic of species across its geographic range. Many types of species interaction cause selection on mating traits, but their role in generating within-species divergence has been neglected. The pattern of reproductive character displacement (RCD) has been classically attributed to reinforcement, a process driven by selection against hybridisation. Recent reinforcement research shows that sexual isolation can result between displaced and non-displaced populations. We argue that RCD (and hence potentially speciation) among populations can be generated by a variety of fundamental species interactions beyond reinforcement. We unify these interactions under one process of mating trait divergence and speciation ('RCD speciation'). This process can occur in many geographic settings. Because selection is acting directly on mating traits, rapid speciation can result involving little differentiation in other traits. This pattern of diversification is seen in many groups and regions, and has previously been attributed to sexual selection alone.

Asymmetry in Reproductive Character Displacement

ABSTRACT : A commonly held view in studies of character displacement is that character states of both species are shifted in areas of sympatry. This view has been confirmed in an overwhelming number of cases for ecolo-gical character displacement. Excluding species pairs in which one of the two interacting species is found only within the distribution of the other species and species displaying gynogenesis, the pattern of reproductive character displacement is asymmetrical in that the shift in character states between areas of symaptry and allopatry occurs in only one of the two interacting species. Hypotheses for the reasons behind this asymmetry in reproductive character displacement include (1) homogenization by gene flow, (2) other mechanisms of repro-ductive isolation, and (3) sufficient reproductive isolation being provided by one of the interacting species exhi-biting a pattern of reproductive character displacement. Because reproductive isolation can be achieved by diver-gence at any point in a sequence of premating reproductive behaviors and postmating developments, it is necessary to understand the mechanisms of reproductive isolation of two interacting taxa in areas of sympatry and allopatry and to analyze the relative contributions of potential factors to reproductive isolation to disentangle hypotheses for the patterns of asymmetry.

Existence of a pattern of reproductive character displacement inHomobasidiomycotabut not inAscomycota

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

Reproductive Asynchrony and the Divergence of Hawaiian Crickets

AbstractAsynchrony in reproductive behavior may contribute to reproductive isolation among sympatric species. While the 38 cryptic species of the genus Laupala are primarily distinguished on the basis of variation in pulse rate of male calling songs, additional phenotypes, such as asynchrony in reproductive behavior, may contribute to reproductive isolation in this genus. Here we document similarities and differences in the diel timing of two reproductive behaviors, male singing activity and insemination events. Asynchrony in the diel timing of male singing behavior was observed between two sympatric species, Laupala cerasina and Laupala paranigra, in the field. An interpopulational comparison within L. cerasina did not reveal variation in diel behavior patterns of singing between two locations. Asynchrony in the timing of copulation and sperm transfer between L. cerasina and L. paranigra was documented in the laboratory. The observed pattern of asynchrony in both the field and laboratory could have arisen in a number of ways. One possibility is that species diverged in sympatry because of interspecific interactions, producing a pattern of reproductive character displacement. Alternatively, the observed asynchrony in reproductive behavior may have played a role in the process of community assembly within this recently diverged cricket genus. The presence of interspecific variation and the absence of intraspecific variation revealed by our study do not support a pattern of reproductive character displacement for diel reproductive behavior, suggesting that the differences seen between species were not caused by recent species interactions.

Reinforcement of mate preference among hybridizingHeliconiusbutterflies

Recent models of mate preference evolution suggest that direct selection on alleles at preference loci and correlated evolution of preference with locally adapted mating cues are more likely to drive the evolution of assortative mate preference than reinforcement. Mate preference evolution in mimetic Heliconius butterflies has been attributed to all three forms of selection, but here we show that reinforcement has been critical. By examining geographical variation in assortative mating and male mate preference among seven populations of three hybridizing Heliconius species from Costa Rica, we found pronounced character displacement of preference such that sexual isolation was enhanced in areas of interspecific contact. Of the different explanations for the evolution of assortative mate preference, only reinforcement is dependent on interspecific contact in this system. Thus, the observed pattern of reproductive character displacement of mate preference is best explained as a product of indirect selection generated by natural selection against nonmimetic hybrids.

Natural selection and divergence in mate preference during speciation

Sexual isolation can evolve due to natural selection against hybrids (reinforcement). However, many different forms of hybrid dysfunction, and selective processes that do not involve hybrids, can contribute to the evolution of sexual isolation. Here we review how different selective processes affect the evolution of sexual isolation, describe approaches for distinguishing among them, and assess how they contribute to variation in sexual isolation among populations of Timema cristinae stick-insects. Pairs of allopatric populations of T. cristinae living on different host-plant species exhibit greater sexual isolation than those on the same host, indicating that some sexual isolation has evolved due to host adaptation. Sexual isolation is strongest in regions where populations on different hosts are in geographic contact, a pattern of reproductive character displacement that is indicative of reinforcement. Ecological costs to hybridization do occur but traits under ecological selection (predation) do not co-vary strongly with the probability of between-population mating such that selection on ecological traits is not predicted to produce a strong correlated evolutionary response in mate preference. Moreover, F1 hybrid egg inviability is lacking and the factors contributing to reproductive character displacement require further study. Finally, we show that sexual isolation involves, at least in part, olfactory communication. Our results illustrate how understanding of the evolution of sexual isolation can be enhanced by isolating the roles of diverse ecological and evolutionary processes.

Geographic Variation and Positive Selection on M7 Lysin, an Acrosomal Sperm Protein in Mussels (Mytilus spp.)

Successful fertilization in free-spawning marine organisms depends on the interactions between genes expressed on the surfaces of eggs and sperm. Positive selection frequently characterizes the molecular evolution of such genes, raising the possibility that some common deterministic process drives the evolution of gamete recognition genes and may even be important for understanding the evolution of prezygotic isolation and speciation in the marine realm. One hypothesis is that gamete recognition genes are subject to selection for prezygotic isolation, namely, reinforcement. In a previous study, positive selection on the gene coding for the acrosomal sperm protein M7 lysin was demonstrated among allopatric populations of mussels in the Mytilus edulis species group (M. edulis, Mytilus galloprovincialis, and Mytilus trossulus). Here, we expand sampling to include M7 lysin haplotypes from populations where mussel species are sympatric and hybridize to determine whether there is a pattern of reproductive character displacement (RCD), which would be consistent with reinforcement driving selection on this gene. We do not detect a strong pattern of RCD; neither are there unique haplotypes in sympatry nor is there consistently greater population structure in comparisons involving sympatric populations. One distinct group of haplotypes, however, is strongly affected by natural selection, and this group of haplotypes is found within M. galloprovincialis populations throughout the Northern Hemisphere concurrent with haplotypes common to M. galloprovincialis and M. edulis. We suggest that balancing selection, perhaps resulting from sexual conflicts between sperm and eggs, maintains old allelic diversity within M. galloprovincialis.

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.

Genetic constraints on the evolution of mate recognition under natural selection.

Field populations of Drosophila serrata display reproductive character displacement in cuticular hydrocarbons (CHCs) when sympatric with Drosophila birchii. We have previously shown that the naturally occurring pattern of reproductive character displacement can be experimentally replicated by exposing field allopatric populations of D. serrata to experimental sympatry with D. birchii. Here, we tested whether the repeated evolution of reproductive character displacement in natural and experimental populations was a consequence of genetic constraints on the evolution of CHCs. The genetic variance-covariance (G) matrices for CHCs were determined for populations of D. serrata that had evolved in either the presence or absence of D. birchii under field and experimental conditions. Natural selection on mate recognition under both field and experimental sympatric conditions increased the genetic variance in CHCs consistent with a response to selection based on rare alleles. A close association between G eigenstructure and the eigenstructure of the phenotypic divergence (D) matrix in natural and experimental populations suggested that G matrix eigenstructure may have determined the direction in which reproductive character displacement evolved during the reinforcement of mate recognition.