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.     

Positive feedback between ecological and reproductive character displacement in a young avian hybrid zone

Character displacement can reduce costly interspecific interactions between young species. We investigated the mechanisms behind divergence in three key traits-breeding habitat choice, timing of breeding, and plumage coloration-in Ficedula flycatchers. We found that male pied flycatchers became expelled from the preferred deciduous habitat into mixed forest as the superior competitor, collared flycatchers, increased in numbers. The peak in food abundance differs between habitats, and the spatial segregation was paralleled by an increased divergence in timing of breeding between the two species. Male pied flycatchers vary from brown to black with brown coloration being more frequent in sympatry with collared flycatchers, a pattern often proposed to result from selection against hybridization, that is, reinforcement. In contrast to this view, we show that brown male pied flycatchers more often hybridize than black males. Male pied flycatcher plumage coloration influenced the territory obtained in areas of co-occurrence with collared flycatchers, and brown male pied flycatchers experienced higher relative fitness than black males when faced with heterospecific competition. We suggest that allopatric divergence in resource defense ability causes a feedback loop at secondary contact where male pied flycatchers with the most divergent strategy compared to collared flycatchers are favored by selection.     

Reproductive character displacement is not the only possible outcome of reinforcement

We study the form of the clines in a female mating preference and male display trait using simulations of a hybrid zone. Allopatric populations of two species are connected by demes in a stepping stone arrangement. Results show that reproductive character displacement (a pattern of increased prezygotic isolation in sympatry compared with allopatry) may or may not result when there is reinforcement (defined here as the strengthening of prezygotic isolation as a result of selection against hybrids, relative to the amount of prezygotic isolation present when hybrids are not selected against). Further, reproductive character displacement of the preference may or may not occur when it occurs in the male display. We conclude that the absence of reproductive character displacement is not evidence against the operation of reinforcement.     

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

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

Reproductive character displacement and signal ontogeny in a sympatric assemblage of electric fish

The reproductive signals of two or more taxa may diverge in areas of sympatry, due to selection against costly reproductive interference. This divergence, termed reproductive character displacement (RCD), is expected in species-rich assemblages, where interspecific signal partitioning among closely related species is common. However, RCD is usually documented from simple two-taxon cases, via geographical tests for greater divergence of reproductive traits in sympatry than in allopatry. We propose a novel approach to recognizing and understanding RCD in multi-species communities--one that traces the displacement of signals within multivariate signal space during the ontogeny of individual animals. We argue that a case for RCD can be made if the amount of signal displacement between a pair of species after maturation is negatively correlated to distance in signal space before maturation. Our application of this approach, using a dataset of communication signals from a sympatric Amazonian assemblage of the electric fish genus Gymnotus, provides strong evidence for RCD among multiple species. We argue that RCD arose from the costs of heterospecific mismating, but interacted with sexual selection--favoring the evolution of conspicuous male signals that not only serve for mate-choice, but which simultaneously facilitate species recognition.     

Six cryptic species on a single species of host plant: morphometric evidence for possible reproductive character displacement

Abstract 1. Diversification of some highly host‐specific herbivorous insects may occur in allopatry, without shifts in host use. Such allopatric divergence may be accelerated by sexual selection operating on courtship displays. Wing size and shape may affect visual and vibrational courtship displays in tephritid fruit flies. Geometric morphometric methods were used to examine wings of six sympatric cryptic species in the neotropical genus Blepharoneura. All six species feed on flowers of the same species of host (Gurania spinulosa), a neotropical vine in the Cucurbitaceae. Three of the fly species court and mate in close proximity on the host. Thus, courtship behaviours could serve as important reproductive isolating mechanisms. Two sets of hypotheses were tested: (i) species differ in wing shape and wing size; and (ii) species are sexually dimorphic in wing size and wing shape. Wing size differed among a few species, but wing shape differed significantly among all six species. Sexual dimorphism in wing size was found in only one species, but sexual dimorphism in wing shape was found in two of the three species known to court on the same host plant. In the two sexually dimorphic species, wing shape differed among males, but not among females. This suggests that selection for reproductive character displacement might accelerate divergence in wing shape.     

Using genomic data to revisit an early example of reproductive character displacement in Haitian Anolis lizards

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 40 years 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.     

Asymmetrical reproductive character displacement in the house mouse

Our study addressed reproductive character displacement between two subspecies of the house mouse, Mus musculus musculus and Mus musculus domesticus that hybridize in Europe along a zone where selection against hybridization is known to occur. Based on a multi-population approach, we investigated spatial patterns of divergence of mate preference in the two taxa. Mate preference was significantly higher in the contact zone than in allopatry in both subspecies, suggesting that reproductive character displacement occurs. Moreover, patterns of preference were stronger in M. m. musculus than in M. m. domesticus, indicating an asymmetrical divergence between the two. In the context of selection against hybridization, our results may provide empirical support for the hypothesis of reinforcement in a parapatric hybrid zone. We discuss factors that could explain the asymmetrical pattern of divergence and the possible impact of a unimodal structure on the maintenance of premating divergence between the two subspecies.     

Existence of a pattern of reproductive character displacement in Homobasidiomycota but not in Ascomycota

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 character displacement of female,but not male song discrimination in an avian hybrid zone

Divergence of male sexual signals and female preferences for those signals often maintains reproductive boundaries between closely related, co‐occurring species. However, contrasting sources of selection, such as interspecific competition, can lead to weak divergence or even convergence of sexual signals in sympatry. When signals converge, assortative mating can be maintained if the mating preferences of females diverge in sympatry (reproductive character displacement; RCD), but there are few explicit examples. Pied flycatchers (Ficedula hypoleuca) are sympatric with collared flycatchers (F. albicollis) on the Baltic island of Öland, where males from both species compete over nestboxes, their songs converge, and the two species occasionally hybridize. We compare song discrimination of male and female pied flycatchers on Öland and in an allopatric population on the Swedish mainland. Using field choice trials, we show that male pied flycatchers respond similarly to the songs of both species in sympatry and allopatry, while female pied flycatchers express stronger discrimination against heterospecific songs in sympatry than in allopatry. These results are consistent with RCD of song discrimination of female pied flycatchers where they co‐occur with collared flycatchers, which should maintain species assortative mating despite convergence of male sexual signals.     

Frequency dependent natural selection during character displacement in sticklebacks

Abstract We know little about how natural selection on a species is altered when a closely related species consuming similar resources appears in its environment. In a pond experiment with threespine sticklebacks I tested the prediction that divergent natural selection between competitors is frequency-dependent, changing with the distribution of phe-notypes in the environment. Differential growth and survival of phenotypes in a target stickleback population were contrasted between two treatments. In one treatment an offshore zooplankton feeder (the limnetic stickleback species) was added to the same pond as the target. In the other treatment I added the benthic stickleback instead, a species adapted to feeding on invertebrates from sediments and inshore vegetation. The target population was ecologically and morphologically intermediate with phenotypic variance artificially inflated by hybridization. Growth rates of phenotypes within the target population differed between treatments as predicted by character displacement. The impact of adding a second species always fell most heavily on those phenotypes in the target population resembling the added species most closely. However, those individuals in the target population that most resembled the added species did not experience reduced survival. Instead, consistent survival differences between populations suggested the presence of an inshore –offshore gradient in mortality risk. These results provide further support for the hypothesis of character displacement in sympatric sticklebacks. They suggest that displacement along the resource gradient also led to divergence in vulnerability to agents of mortality, probably including predation.     

Infant loss during and after male replacement in gibbons

According to the sexual selection hypothesis, infanticide during resident male replacement is an adaptive strategy that has evolved because the killing of unweaned offspring sired by previous males shortens the inter‐birth intervals of the mothers whose infants are targeted and thereby increases the reproductive fitness of the perpetrator. To test this hypothesis, we describe previously unreported cases of primary male replacement for two gibbon species (Hylobates lar and Nomascus nasutus), and review all other reported cases of primary male replacement in gibbons. Overall, infants were present in nearly half of all cases (16/33, 48%) and of the 18 infants present during replacement, 50% (N = 9) disappeared within 2 months of the event. In four of the five cases where there was sufficient demographic information to identify the likely sire of the subsequent offspring of females that lost infants, the new male was believed to be the sire. Infants were also less likely to die or disappear if the new male and original resident male were possible kin. However, there was no significant difference in the age of infants between those that died or disappeared following replacement and those that survived to weaning (p = .630). Our review of takeover‐related infant loss in gibbons confirms that periods of male instability are risky for unweaned infants and that replacing males benefit from infant loss. Nevertheless, variability in the context of infant loss and difficulties related to data collection in the field make it difficult to test competing hypotheses concerning the mechanisms and functions of infanticide in the small apes.     

Speciation via habitat specialization: the evolution of reproductive isolation as a correlated character

Summary A diverse group of theoretical and empirical studies are integrated into a composite model of sympatric speciation via habitat specialization. It is shown that disruptive selection on a continuous distribution of habitat preference can lead to the evolution of prezygotic reproductive isolation as a correlated character. The form of selection eliminates the major theoretical objections to the process of sympatric speciation. The principal difference between this model and the allopatric model of speciation is that the initial barrier to gene flow between subpopulations is produced by the evolution of gaps in the phenotypic distribution of spatial/temporal habitat use, rather than an extrinsic geographical barrier.     

The evolution of reproductive character displacement conflicts with how sexual selection operates within a species

Processes that affect the evolution of female preferences or male display traits involved in mating decisions in different geographic areas have the potential to result in within-species divergence. This could occur via reinforcement of mate recognition in species using the same traits for species recognition and sexual selection. Sympatric individuals experience reinforcement of female preferences and male display traits, whereas allopatric individuals do not, creating the potential for divergent sexual selection in sympatric and allopatric populations. Sexual selection operates on the cuticular hydrocarbons (CHCs) of Drosophila serrata, and reinforcement on the CHCs of populations sympatric with D. birchii. Here, we manipulate sexual selection in D. serrata populations generated by hybridizing natural sympatric and allopatric populations. Under the influence of sexual selection, male CHCs evolved from an intermediate phenotype to resemble an allopatric phenotype, which was driven by female choice. Additionally, female choice resulted in evolution of an allopatric female preference, so that allopatric males were preferred to sympatric males. Allopatric CHCs and preferences represent a sexual selection optimum via female choice. Sympatric populations display suboptimal phenotypes relative to their allopatric conspecifics. The combination of reinforcement and sexual selection can therefore generate divergence in female preferences and male display traits.     

Sexual conflict and reproductive isolation in flies

Sexual conflict is predicted to generate more rapid reproductive isolation between larger populations. While there is some empirical support for this, the data are inconsistent and, additionally, there has been criticism of some of the evidence. Here we reanalyse two experimental-evolution datasets using an isolation index widely applied in the speciation literature. We find evidence for reproductive isolation through sexual conflict in Sepsis cynipsea, but not in Drosophila melanogaster, and this occurred to a greater degree in larger populations, which is consistent with previous findings.     

Limits to the evolution of assortative mating by female choice under restricted gene flow

The evolution of assortative mating is a key component of the process of speciation with gene flow. Several recent theoretical studies have pointed out, however, that sexual selection which can result from assortative mating may cause it to plateau at an intermediate level; this is primarily owing to search costs of individuals with extreme phenotypes and to assortative preferences developed by individuals with intermediate phenotypes. I explore the limitations of assortative mating further by analysing a simple model in which these factors have been removed. Specifically, I use a haploid two-population model to ask whether the existence of assortative mating is sufficient to drive the further evolution of assortative mating. I find that a weakening in the effective strength of sexual selection with strong assortment leads to the existence of both a peak level of trait differentiation and the evolution of an intermediate level of assortative mating that will cause that peak. This result is robust to the inclusion of local adaptation and different genetic architecture of the trait. The results imply the existence of fundamental limits to the evolution of assortment via sexual selection in this situation, with which other factors, such as search costs, may interact.     

Experimentally induced variation in neuroendocrine processes affects male reproductive behaviour,sperm characteristics and social interactions

While extensive research has focused on how social interactions evolve, the fitness consequences of the neuroendocrine mechanisms underlying these interactions have rarely been documented, especially in the wild. Here, we measure how the neuroendocrine mechanisms underlying male behaviour affect mating success and sperm competition in the ocellated wrasse (Symphodus ocellatus). In this species, males exhibit three alternative reproductive types. “Nesting males” provide parental care, defend territories and form cooperative associations with unrelated “satellites,” who cheat by sneaking fertilizations but help by reducing sperm competition from “sneakers” who do not cooperate or provide care. To measure the fitness consequences of the mechanisms underlying these social interactions, we used “phenotypic engineering” that involved administering an androgen receptor antagonist (flutamide) to wild, free‐living fish. Nesting males treated with flutamide shifted their aggression from sneakers to satellite males and experienced decreased submissiveness by sneaker males (which correlated with decreased nesting male mating success). The preoptic area (POA), a region controlling male reproductive behaviours, exhibited dramatic down‐regulation of androgen receptor (AR) and vasotocin 1a receptor (V1aR) mRNA following experimental manipulation of androgen signalling. We did not find a direct effect of the manipulation on male mating success, paternity or larval production. However, variation in neuroendocrine mechanisms generated by the experimental manipulation was significantly correlated with changes in behaviour and mating success: V1aR expression was negatively correlated with satellite‐directed aggression, and expression of its ligand arginine vasotocin (AVT) was positively correlated with courtship and mating success, thus revealing the potential for sexual selection on these mechanisms.     

Molecular signatures of selection on reproductive character displacement of flower color in Phlox drummondii

Character displacement, which arises when species diverge in sympatry to decrease competition for resources or reproductive interference, has been observed in a wide variety of plants and animals. A classic example of reproductive character displacement, presumed to be caused by reinforcing selection, is flower‐color variation in the native Texas wildflower Phlox drummondii. Here, we use population genetic analyses to investigate molecular signatures of selection on flower‐color variation in this species. First, we quantify patterns of neutral genetic variation across the range of P. drummondii to demonstrate that restricted gene flow and genetic drift cannot explain the pattern of flower‐color divergence in this species. There is evidence of extensive gene flow across populations with different flower colors, suggesting selection caused flower‐color divergence. Second, analysis of sequence variation in the genes underlying this divergence reveals a signature of a selective sweep in one of the two genes, further indicating selection is responsible for divergence in sympatry. The lack of a signature of selection at the second locus does not necessarily indicate a lack of selection on this locus but instead brings attention to the uncertainty in depending on molecular signatures to identify selection.     

Intraspecific variation in sexual isolation in the jewel wasp Nasonia

Abstract.— Divergence in mate recognition systems can lead to reproductive isolation. In this study, we investigate patterns of intraspecific variation that contribute to premating isolation within and between two haplodiploid species, Nasonia vitripennis and N. longicornis . In a broad-scale survey of 17 North American isofemale lines encompassing the two species, we report strong asymmetric sexual isolation between species and a dramatic level of intraspecific variation for mate discrimination between species. A general lack of incipient speciation was found, with the exception of low levels of interpopulational sexual isolation within N. vitripennis . Regression analysis shows that the degree of intraspecific variation for within-species mating frequency is not associated with the degree for between-species mating frequency. Reinforcement or reproductive character displacement may be involved in some of the variation in inter-species premating isolation.