Conspecific sperm precedence is reinforced, but postcopulatory sexual selection weakened, in sympatric populations of Drosophila.
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ABSTRACT:
SUBMITTER: Castillo DM
PROVIDER: S-EPMC6452082 | biostudies-literature | 2019 Mar
REPOSITORIES: biostudies-literature
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Project description:Negative interspecific mating interactions, known as reproductive interference, can hamper species coexistence in a local patch and promote niche partitioning or geographical segregation of closely related species. Conspecific sperm precedence (CSP), which occurs when females that have mated with both conspecific and heterospecific males preferentially use conspecific sperm for fertilization, might contribute to species coexistence by mitigating the costs of interspecific mating and hybridization. We discussed whether two species exhibiting CSP can coexist in a local environment in the presence of reproductive interference. First, using a behaviorally explicit mathematical model, we demonstrated that two species characterized by negative mating interactions are unlikely to coexist because the costs of reproductive interference, such as loss of mating opportunity with conspecific partners, are inevitably incurred when individuals of both species are present. Second, we experimentally examined differences in mating activity and preference in two Harmonia ladybird species known to exhibit CSP. These behavioral differences may lead to local extinction of H. yedoensis because of reproductive interference by H. axyridis. This prediction is consistent with field observations that H. axyridis uses various food sources and habitats whereas H. yedoensis is confined to a less preferred prey item and a pine tree habitat. Finally, by a comparative approach, we observed that niche partitioning or parapatric distribution, but not sympatric coexistence in the same habitat, is maintained between species with CSP belonging to a wide range of taxa, including vertebrates and invertebrates living in aquatic or terrestrial environments. Taken together, it is possible that reproductive interference may destabilize local coexistence even in closely related species that exhibit CSP.
| S-EPMC7920778 | biostudies-literature
Project description:BackgroundThe evolutionary role of postcopulatory sexual selection in shaping male reproductive traits, including sperm morphology, is well documented in several taxa. However, previous studies have focused almost exclusively on the influence of sperm competition on variation among species. In this study we tested the hypothesis that intraspecific variation in sperm morphology is driven by the level of postcopulatory sexual selection in passerine birds.Methodology/findingsUsing two proxy measures of sperm competition level, (i) relative testes size and (ii) extrapair paternity level, we found strong evidence that intermale variation in sperm morphology is negatively associated with the degree of postcopulatory sexual selection, independently of phylogeny.Conclusions/significanceOur results show that the role of postcopulatory sexual selection in the evolution of sperm morphology extends to an intraspecific level, reducing the variation towards what might be a species-specific 'optimum' sperm phenotype. This finding suggests that while postcopulatory selection is generally directional (e.g., favouring longer sperm) across avian species, it also acts as a stabilising evolutionary force within species under intense selection, resulting in reduced variation in sperm morphology traits. We discuss some potential evolutionary mechanisms for this pattern.
| S-EPMC1855076 | biostudies-literature
Project description:Drosophila pseudoobscura females that co-occur with sister species D. persimilis show elevated fertilization by conspecific sperm when they mate with both a heterospecific and a conspecific male. This phenomenon, known as conspecific sperm precedence (CSP), has evolved as a mechanism to avoid maladaptive hybridization with D. persimilis. In this study, we assessed pericopulatory (during mating) and postcopulatory (after mating) traits in crosses with sympatric or allopatric D. pseudoobscura females and conspecific or heterospecific males to evaluate potential mechanisms of CSP in this system. We observed shorter copulation duration in crosses with sympatric females, but found no difference in quantity of sperm transferred or female reproductive tract toxicity between sympatry and allopatry. Our data show some support for the hypothesis that parasperm, a short, sterile sperm morph, can protect fertile eusperm from the D. pseudoobscura female reproductive tract, though it is unclear how this might affect patterns of sperm use in sympatry vs. allopatry. Overall, these results suggest that copulation duration could potentially contribute to the elevated CSP observed in sympatry.
| S-EPMC10889848 | biostudies-literature
Project description:In some species, sperm form coordinated groups that are hypothesized to improve their swimming performance in competitive contexts or to navigate through the viscous fluids of the female reproductive tract. Here we investigate sperm aggregation across closely related species of Peromyscus mice that naturally vary by mating system to test the predictions that sperm aggregates 1) are faster than solitary sperm in species that females mate multiply to aid cells in sperm competition, and 2) outperform solitary sperm cells in viscous environments. We find significant variation in the size of sperm aggregates, which negatively associates with relative testis mass, a proxy for sperm competition risk, suggesting that postcopulatory sexual selection has a stabilizing effect on sperm group size. Moreover, our results show that sperm aggregates are faster than solitary sperm in some, but not all, species, and this can vary by fluid viscosity. Of the two species that produce the largest and most frequent groups, we find that sperm aggregates from the promiscuous P. maniculatus are faster than solitary sperm in every experimentally viscous environment but aggregation provides no such kinematic advantage under these same conditions for the monogamous P. polionotus. The reduced performance of P. polionotus aggregates is associated with less efficient aggregate geometry and the inclusion of immotile or morphological abnormal sperm. Our cross-species comparison yields insight into the evolution of sperm social behaviors, provides evidence of extensive variation in the Peromyscus lineage, and reveals that differences in sperm aggregate quality associate with postcopulatory sexual selection.
| S-EPMC8857933 | biostudies-literature
Project description:BACKGROUND:Male - female incompatibilities can be critical in keeping species as separate and discrete units. Premating incompatibilities and postzygotic hybrid sterility/inviability have been widely studied as isolating barriers between species. In recent years, a number of studies have brought attention to postmating prezygotic barriers arising from male - male competition and male - female interactions. Yet little is known about the genetic basis of postmating prezygotic isolation barriers between species. RESULTS:Using D. simulans lines with mapped introgressions of D. mauritiana into their third chromosome, we find at least two D. mauritiana introgressions causing male breakdown in competitive paternity success. Eighty one genes within the mapped introgressed regions were identified as broad-sense candidates on the basis of male reproductive tract expression and male-related function. The list of candidates was narrowed down to five genes based on differences in male reproductive tract expression between D. simulans and D. mauritiana. Another ten genes were confirmed as candidates using evidence of adaptive gene coding sequence diversification in the D. simulans and/or D. mauritiana lineage. Our results show a complex genetic basis for conspecific sperm precedence, with evidence of gene interactions between at least two third chromosome loci. Pleiotropy is also evident from correlation between conspecific sperm precedence and female induced fecundity and the identification of candidate genes that might exert an effect through genetic conflict and immunity. CONCLUSIONS:We identified at least two loci responsible for conspecific sperm precedence. A third of candidate genes within these two loci are located in the 89B cytogenetic position, highlighting a possible major role for this chromosome position during the evolution of species specific adaptations to postmating prezygotic reproductive challenges.
| S-EPMC2864193 | biostudies-literature
Project description:Despite limitations on offspring production, almost all multicellular species use sex to reproduce. Sex gives rise to sexual selection, a widespread force operating through competition and choice within reproduction, however, it remains unclear whether sexual selection is beneficial for total lineage fitness, or if it acts as a constraint. Sexual selection could be a positive force because of selection on improved individual condition and purging of mutation load, summing into lineages with superior fitness. On the other hand, sexual selection could negate potential net fitness through the actions of sexual conflict, or because of tensions between investment in sexually selected and naturally selected traits. Here, we explore these ideas using a multigenerational invasion challenge to measure consequences of sexual selection for the overall net fitness of a lineage. After applying experimental evolution under strong versus weak regimes of sexual selection for 77 generations with the flour beetle Tribolium castaneum, we measured the overall ability of introductions from either regime to invade into conspecific competitor populations across eight generations. Results showed that populations from stronger sexual selection backgrounds had superior net fitness, invading more rapidly and completely than counterparts from weak sexual selection backgrounds. Despite comprising only 10% of each population at the start of the invasion experiment, colonizations from strong sexual selection histories eventually achieved near-total introgression, almost completely eliminating the original competitor genotype. Population genetic simulations using the design and parameters of our experiment indicate that this invasion superiority could be explained if strong sexual selection had improved both juvenile and adult fitness, in both sexes. Using a combination of empirical and modeling approaches, our findings therefore reveal positive and wide-reaching impacts of sexual selection for net population fitness when facing the broad challenge of invading competitor populations across multiple generations.
| S-EPMC6145403 | biostudies-literature
Project description:The extreme morphological variability of the baculum across mammals is thought to be the result of sexual selection (particularly, high levels of postcopulatory selection). However, the evolutionary trajectory of the mammalian baculum is little studied and evidence for the adaptive function of the baculum has so far been elusive. Here, we use Markov chain Monte Carlo methods implemented in a Bayesian phylogenetic framework to reconstruct baculum evolution across the mammalian class and investigate the rate of baculum length evolution within the primate order. We then test the effects of testes mass (postcopulatory sexual selection), polygamy, seasonal breeding and intromission duration on the baculum in primates and carnivores. The ancestral mammal did not have a baculum, but both ancestral primates and carnivores did. No relationship was found between testes mass and baculum length in either primates or carnivores. Intromission duration correlated with baculum presence over the course of primate evolution, and prolonged intromission predicts significantly longer bacula in extant primates and carnivores. Both polygamous and seasonal breeding systems predict significantly longer bacula in primates. These results suggest the baculum plays an important role in facilitating reproductive strategies in populations with high levels of postcopulatory sexual selection.
| S-EPMC5204150 | biostudies-literature
Project description:Recent theory has suggested that sympatric speciation can occur quite easily when individuals that are ecologically similar mate assortatively. Although many of these models have assumed that individuals have equal mating success, in nature rare phenotypes may often suffer decreased mating success. Consequently, assortative mating may often generate stabilizing sexual selection. We show that this effect can substantially impede sympatric speciation. Our results emphasize the need for data on the strength of the stabilizing component of selection generated by mating in natural populations.
| S-EPMC1691651 | biostudies-literature
Project description:When females mate to multiple males, the last male to mate fathers the majority of progeny. When males of different species inseminate a female, the sperm of the male conspecific to the female is favored in fertilization in a process known as conspecific sperm precedence (CSP). A large number of studies in Drosophila have assayed the genetic basis of sperm competition, with a main focus on D. melanogaster and accessory gland protein genes. Only a few studies have attempted to disentangle the genetic basis of CSP between related species of Drosophila. Although there is no a priori reason to believe that genes influencing intraspecific sperm competitive ability might also mediate conspecific sperm precedence, no study has addressed the question. Here, we test a group of candidate CSP genes between D. simulans and D. mauritiana for their effect on sperm competition in D. melanogaster. The use of P-element insertion lines identified CG14891 gene disruption as the only one causing a significant decrease in second male paternity success relative to wild-type and ebony tester males. The gene disruption affected both sperm displacement and the sperm fertilizing ability. Out of five genes tested using RNA interference, only gene knockdown of CG6864(Mst89B) [corrected] significantly reduced the male's ability to father progeny when second to mate. Our results suggest that CG14891 and CG6468 might have been co-opted from an intraspecies gene function (i.e., sperm competition) into an interspecies avoidance phenotype (i.e., CSP). Alternatively, the dual role of these genes could be a consequence of their pleiotropic roles.
| S-EPMC4169163 | biostudies-other
Project description:It is widely acknowledged that in most species sexual selection continues after mating. Although it is generally accepted that females play an important role in generating paternity biases (i.e. cryptic female choice, CFC), we lack a quantitative understanding of the relative importance of female-controlled processes in influencing variance in male reproductive fitness. Here, we address this question experimentally using the guppy Poecilia reticulata, a polyandrous fish in which pre- and postcopulatory sexual selection jointly determine male reproductive fitness. We used a paired design to quantify patterns of paternity for pairs of rival males across two mating contexts, one in which the female retained full control over double (natural) matings and one where sperm from the same two males were artificially inseminated into the female. We then compared the relative paternity share for a given pair of males across both contexts, enabling us to test the key prediction that patterns of paternity will depend on the extent to which females retain behavioural control over matings. As predicted, we found stronger paternity biases when females retained full control over mating compared with when artificial insemination (AI) was used. Concomitantly, we show that the opportunity for postcopulatory sexual selection (standardized variance in male reproductive success) was greater when females retained control over double matings compared with when AI was used. Finally, we show that the paternity success of individual males exhibited higher repeatability across successive brood cycles when females retained behavioural control of matings compared with when AI was used. Collectively, these findings underscore the critical role that females play in determining the outcome of sexual selection and to our knowledge provide the first experimental evidence that behaviourally moderated components of CFC increase the opportunity for sexual selection.
| S-EPMC6191706 | biostudies-literature