The complex genetic architecture of male mate choice evolution between Drosophila species.
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ABSTRACT:
SUBMITTER: Shahandeh MP
PROVIDER: S-EPMC7239879 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Mate discrimination is a key mechanism restricting gene flow between species. While studied extensively with respect to female mate choice, mechanisms of male mate choice between species are far less studied. Thus, we have little knowledge of the relative frequency, importance, or overall contribution of male mate discrimination to reproductive isolation. In the present study, we estimated the relative contributions of male and female choice to reproductive isolation between Drosophila simulans and D. sechellia, and show that male mate discrimination accounts for the majority of the current isolation between these species. We further demonstrate that males discriminate based on female cuticular hydrocarbon pheromones, and collect evidence supporting the hypothesis that male mate discrimination may alleviate the costs associated with heterospecific courtship and mating. Our findings highlight the potentially significant contribution of male mate choice to the formation of reproductive isolating barriers, and thus the speciation process.
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Project description:An increasing number of empirical studies in animals have demonstrated male mate choice. However, little is known about the evolution of postpairing male choice, specifically which occurs by differential allocation of male parental care in response to female signals. We use a population genetic model to examine whether such postpairing male mate choice can evolve when males face a trade-off between parental care and extra-pair copulations (EPCs). Specifically, we assume that males allocate more effort to providing parental care when mated to preferred (signaling) females, but they are then unable to allocate additional effort to seek EPCs. We find that both male preference and female signaling can evolve in this situation, under certain conditions. First, this evolution requires a relatively large difference in parental investment between males mated to preferred versus nonpreferred females. Second, whether male choice and female signaling alleles become fixed in a population versus cycle in their frequencies depends on the additional fecundity benefits from EPCs that are gained by choosy males. Third, less costly female signals enable both signaling and choice alleles to evolve under more relaxed conditions. Our results also provide a new insight into the evolution of sexual conflict over parental care.
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Project description:Models of sexual conflict over mating, including conflict over indirect benefits of mate choice, have generally presumed that female resistance to male coercion must involve direct confrontation, which can lead to sexually antagonistic coevolutionary arms-races. We built a quantitative model examining the largely ignored possibility that females may evolve new, additional mate preferences for new male traits that undermine male capacity to coerce. Thus, females may "remodel" the coercive capacity of the male phenotype in order to enhance their own sexual autonomy-a novel alternative mechanism by which females may avoid arms-races. We demonstrate that evolutionary "remodeling" is possible, in spite of costs to males, because females that prefer males with protective, autonomy-enhancing traits (traits correlated with lower coercion effectiveness) are likelier to gain indirect benefits of having attractive mates. Our analysis reveals new possibilities for the evolution of systems of sexual conflict over indirect benefits, showing that autonomy-enhancing male traits can act as a "public good," benefiting all females regardless of mating preferences, leading to oscillatory dynamics; and that preferences for more protective male traits will often be favored relative to preferences for less protective traits, potentially leading to an evolutionary "snowball" of expanding sexual autonomy.
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Project description:Secondary contact between formerly isolated populations may result in hybrid breakdown, in which untested allelic combinations in hybrids are maladaptive and limit genetic exchange. Studying early-stage reproductive isolation may yield key insights into the genetic architectures and evolutionary forces underlying the first steps toward speciation. Here, we leverage the recent worldwide expansion of Drosophila melanogaster to test for hybrid breakdown between populations that diverged within the last 13,000 years. We found clear evidence for hybrid breakdown in male reproduction, but not female reproduction or viability, supporting the prediction that hybrid breakdown affects the heterogametic sex first. The frequency of non-reproducing F2 males varied among different crosses involving the same southern African and European populations, as did the qualitative effect of cross direction, implying a genetically variable basis of hybrid breakdown and a role for uniparentally inherited factors. The levels of breakdown observed in F2 males were not recapitulated in backcrossed individuals, consistent with the existence of incompatibilities with at least three partners. Thus, some of the very first steps toward reproductive isolation could involve incompatibilities with complex and variable genetic architectures. Collectively, our findings emphasize this system's potential for future studies on the genetic and organismal basis of early-stage reproductive isolation.
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Project description:Male eagerness to mate is a central paradigm of sexual selection theory. However, limited sperm supplies mean that male sexual restraint might sometimes be favored under promiscuous mating. Here, we demonstrate dynamic plasticity in male mating effort when females are encountered sequentially under varying sperm competition risk. Rather than showing consistent eagerness to mate, male house mice (Mus musculus domesticus) instead tailor their mating effort according to likely reproductive payoffs. They are significantly less likely to mate when sperm competition is certain and potential reproductive payoffs low, but dramatically increase investment if they do choose to mate under such circumstances. By contrast, male mice are significantly more likely to mate in situations simulating extra-territorial copulations, where future risk of competition is high but so too are potential reproductive rewards. Differential mating propensity appears to be the primary mechanism by which male house mice allocate sperm adaptively under sperm competition risk because we find no evidence for facultative adjustment of sperm numbers per ejaculate or ejaculation frequency in response to female-related cues. We conclude that sequential male mate choice under sperm competition risk could be a widespread but often unappreciated mechanism of strategic sperm allocation.
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Project description:Male songbirds use song to advertise their attractiveness as potential mates, and the properties of those songs have a powerful influence on female mate preferences. One idea is that males may exert themselves maximally in each song performance, consistent with female evaluation and formation of mate preferences being the primary contributors to mate choice. Alternatively, males may modulate their song behaviour to different degrees in the presence of different females, consistent with both male and female mate preferences contributing to mutual mate choice. Here we consider whether male Bengalese finches, Lonchura striata domestica, express mate preferences at the level of individual females, and whether those preferences are manifest as changes in song behaviour that are sufficient to influence female mate choice. We tested this idea by recording songs performed by individual unmated males during a series of 1 h interactions with each of many unmated females. Across recording sessions, males systematically varied both the quantity and the quality of the songs that they performed to different females. Males also varied their song properties throughout the course of each interaction, and behavioural tests using female birds revealed that songs performed at the onset of each interaction were significantly more attractive than songs performed by the same male later during the same interaction. This demonstration of context-specific variation in the properties of male reproductive signals and a role for that variation in shaping female mate preference reveals that male mate preferences play an important role in mutual mate choice in this species. Because these birds thrive so well in the laboratory and are so amenable to observation and experimentation across generations, these results yield a new model system that may prove especially advantageous in disentangling the role of male and female mate preferences in shaping mutual mate choice and its long-term benefits or consequences.
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Project description:Epistasis and pleiotropy feature prominently in the genetic architecture of quantitative traits but are difficult to assess in outbred populations. We performed a diallel cross among coisogenic Drosophila P-element mutations associated with hyperaggressive behavior and showed extensive epistatic and pleiotropic effects on aggression, brain morphology, and genome-wide transcript abundance in head tissues. Epistatic interactions were often of greater magnitude than homozygous effects, and the topology of epistatic networks varied among these phenotypes. The transcriptional signatures of homozygous and double heterozygous genotypes derived from the six mutations imply a large mutational target for aggressive behavior and point to evolutionarily conserved genetic mechanisms and neural signaling pathways affecting this universal fitness trait.
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Project description:BackgroundDespite its important implications in behavioural and evolutionary ecology, male mate choice has been poorly studied, and the relative contribution of personality and morphological traits remains largely unknown. We used standard two-choice mating trials to explore whether two personality traits (i.e., shyness and activity) and/or body size of both sexes affect mate choice in male mosquitofish Gambusia affinis. In the first set of trials involving 40 males, we tested whether males would prefer larger females and whether the preference would be affected by males' body length and personality traits, and females' activity level. In the second set of trials (using another 40 males), we tested whether males would prefer more active females and whether the preference would be affected by males' body length and personality traits.ResultsBoth shyness and activity in males were significantly repeatable and constituted a behavioural syndrome. No overall directional preference for large (or small) females with the same activity levels was detected because larger males preferred larger females and smaller males chose smaller females. Males' strength of preference for larger females was also positively correlated with the activity level of larger females but negatively with the activity level of smaller females. Males spent more time associating with active females regardless of their body lengths, indicating males' selection was more influenced by female activity level than body size. Males' preference for inactive females was enhanced when females became active. There was no convincing evidence for the effect of males' personality traits or body length on their preferences for females' activity level.ConclusionsOur study supports the importance of body size in male mate choice but highlights that personality traits may outweigh body size preferences when males choose mating partners.
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Project description:The M and S molecular forms of Anopheles gambiae s.s. have been considered incipient species for more than ten years, yet the mechanism underlying assortative mating of these incipient species has remained elusive. The discovery of the importance of harmonic convergence of wing beat frequency in mosquito mating and its relation to wing size have laid the foundation for exploring phenotypic divergence in wing size of wild populations of the two forms. In this study, wings from field collected mosquitoes were measured for wing length and wing width from two parts of the sympatric distribution, which differ with respect to the strength of assortative mating. In Mali, where assortative mating is strong, as evidenced by low rates of hybridization, mean wing lengths and wing widths were significantly larger than those from Guinea-Bissau. In addition, mean wing widths in Mali were significantly different between molecular forms. In Guinea-Bissau, assortative mating appears comparatively reduced and wing lengths and widths did not differ significantly between molecular forms. The data presented in this study support the hypothesis that wing beat frequency may mediate assortative mating in the incipient species of A. gambiae and represent the first documentation of a morphological difference between the M and S molecular forms.
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Project description:Mate choice plays a fundamental role in speciation, yet we know little about the molecular mechanisms that underpin this crucial decision-making process. Stickleback fish differentially adapted to limnetic and benthic habitats are reproductively isolated and females of each species use different male traits to evaluate prospective partners and reject heterospecific males. Here, we integrate behavioral data from a mate choice experiment with gene expression profiles from the brains of females actively deciding whether to mate. We find substantial gene expression variation between limnetic and benthic females, regardless of behavioral context, suggesting general divergence in constitutive gene expression patterns, corresponding to their genetic differentiation. Intriguingly, female gene co-expression modules covary with male display traits but in opposing directions for sympatric populations of the two species, suggesting male displays elicit a dynamic neurogenomic response that reflects known differences in female preferences. Furthermore, we confirm the role of numerous candidate genes previously implicated in female mate choice in other species, suggesting that evolutionary tinkering with these conserved molecular processes underlies divergent mate preferences and sexual isolation. Taken together, our study adds important new insights to our understanding of the molecular processes underlying female decision-making critical for generating sexual isolation and speciation.
2024-05-07 | GSE263554 | GEO