Experimental sexual selection reveals rapid divergence in male and female reproductive transcriptomes and their interactions

Mating causes substantial changes in females, altering male and female reproductive fitness. Some postmating effects are hypothesized to be at least partially mediated by gene expression changes, driven by postcopulatory sexual selection, which results in population divergence of reproductive proteins that could generate reproductive isolation. However, understanding of the direct role of sexual selection on gene expression divergence along with the subsequent molecular mismatches that could occur between diverging populations is limited. Here, we analyze gene expression divergence following over 150 generations of experimental evolution in which Drosophila pseudoobscura evolved under either elevated polyandry or enforced monogamy. We find that sexual selection rapidly impacted sex-, tissue-, and mating-specific responses, and not always in the predicted direction. Postmating female responses are either unique to each sexual selection treatment or exhibit asymmetric non-congruence, in which monogamy females upregulate and polyandry females downregulate the same genes following mating. This substantial population divergence of gene expression also gives rise to either unique or mismatched gene expression patterns in crosses between treatments. Many of these genes are involved in immune and stress responses, and non-congruent responses are particularly prevalent in the female reproductive tract, the main arena for postcopulatory sexual selection. In summary, we show that sexual selection has pervasive impacts on gene expression divergence acting both differentially between reproductive tissues of the same sex and asymmetrically in postmating female responses, and this divergence is highest in the female reproductive tract, the main arena for postcopulatory sexual selection.

Imminent risk of predation reduces the relative strength of postcopulatory sexual selection in the guppy

Fifty years of research on sperm competition has led to a very good understanding of the interspecific variation in sperm production traits. The reasons why this variation is often very large within populations have been less investigated. We suggest that the interaction between fluctuating environmental conditions and polyandry is a key phenomenon explaining such variation. We focus here on imminent predation risk (IPR). IPR impacts significantly several aspects of prey behaviour and reproduction, and it is expected to influence the operation of sexual selection before and after mating. We estimated the effect of IPR on the male opportunity for pre- and postcopulatory sexual selection in guppies ( Poecilia reticulata ), a livebearing fish where females prefer colourful males and mate multiply. We used a repeated-measures design, in which males were allowed to mate with different females either under IPR or in a predator-free condition. We found that IPR increased the total opportunity for sexual selection and reduced the relative contribution of postcopulatory sexual selection to male reproductive success. IPR is inherently variable and our results suggest that interspecific reproductive interference by predators may contribute towards maintaining the variation in sperm production within populations. This article is part of the theme issue ‘Fifty years of sperm competition'.

Within-population sperm competition intensity does not predict asymmetry in conpopulation sperm precedence

Postcopulatory sexual selection can generate evolutionary arms races between the sexes resulting in the rapid coevolution of reproductive phenotypes. As traits affecting fertilization success diverge between populations, postmating prezygotic (PMPZ) barriers to gene flow may evolve. Conspecific sperm precedence is a form of PMPZ isolation thought to evolve early during speciation yet has mostly been studied between species. Here , we show conpopulation sperm precedence (CpSP) between Drosophila montana populations. Using Pool-seq genomic data we estimate divergence times and ask whether PMPZ isolation evolved in the face of gene flow. We find models incorporating gene flow fit the data best indicating populations experienced considerable gene flow during divergence. We find CpSP is asymmetric and mirrors asymmetry in non-competitive PMPZ isolation, suggesting these phenomena have a shared mechanism. However, we show asymmetry is unrelated to the strength of postcopulatory sexual selection acting within populations. We tested whether overlapping foreign and coevolved ejaculates within the female reproductive tract altered fertilization success but found no effect. Our results show that neither time since divergence nor sperm competitiveness predicts the strength of PMPZ isolation. We suggest that instead cryptic female choice or mutation-order divergence may drive divergence of postcopulatory phenotypes resulting in PMPZ isolation. This article is part of the theme issue ‘Fifty years of sperm competition’.

The Drosophila seminal proteome and its role in postcopulatory sexual selection

Postcopulatory sexual selection (PCSS), comprised of sperm competition and cryptic female choice, has emerged as a widespread evolutionary force among polyandrous animals. There is abundant evidence that PCSS can shape the evolution of sperm. However, sperm are not the whole story: they are accompanied by seminal fluid substances that play many roles, including influencing PCSS. Foremost among seminal fluid models is Drosophila melanogaster , which displays ubiquitous polyandry, and exhibits intraspecific variation in a number of seminal fluid proteins (Sfps) that appear to modulate paternity share. Here, we first consolidate current information on the identities of D. melanogaster Sfps. Comparing between D. melanogaster and human seminal proteomes, we find evidence of similarities between many protein classes and individual proteins, including some D. melanogaster Sfp genes linked to PCSS, suggesting evolutionary conservation of broad-scale functions. We then review experimental evidence for the functions of D. melanogaster Sfps in PCSS and sexual conflict. We identify gaps in our current knowledge and areas for future research, including an enhanced identification of PCSS-related Sfps, their interactions with rival sperm and with females, the role of qualitative changes in Sfps and mechanisms of ejaculate tailoring. This article is part of the theme issue ‘Fifty years of sperm competition’.

Postcopulatory sexual selection and the evolution of shape complexity in the carnivoran baculum

The baculum is an enigmatic bone within the mammalian glans penis, and the driving forces behind its often bizarre shape have captivated evolutionary biologists for over a century. Hypotheses for the function of the baculum include aiding in intromission, stimulating females and assisting with prolonged mating. Previous attempts to test these hypotheses have focused on the gross size of the baculum and have failed to reach a consensus. We conducted three-dimensional imaging and apply a new method to quantify three-dimensional shape complexity in the carnivoran baculum. We show that socially monogamous species are evolving towards complex-shaped bacula, whereas group-living species are evolving towards simple bacula. Overall three-dimensional baculum shape complexity is not related to relative testes mass, but tip complexity is higher in induced ovulators and species engaging in prolonged copulation. Our study provides evidence of postcopulatory sexual selection pressures driving three-dimensional shape complexity in the carnivore baculum.

The importance of pre- and postcopulatory sexual selection promoting adaptation to increasing temperatures

Global temperatures are increasing rapidly affecting species globally. Understanding if and how different species can adapt fast enough to keep up with increasing temperatures is of vital importance. One mechanism that can accelerate adaptation and promote evolutionary rescue is sexual selection. Two different mechanisms by which sexual selection can facilitate adaptation are pre- and postcopulatory sexual selection. However, the relative effects of these different forms of sexual selection in promoting adaptation are unknown. Here, we present the results from an experimental study in which we exposed fruit flies Drosophila melanogaster to either no mate choice or 1 of 2 different sexual selection regimes (pre- and postcopulatory sexual selection) for 6 generations, under different thermal regimes. Populations showed evidence of thermal adaptation under precopulatory sexual selection, but this effect was not detected in the postcopulatory sexual selection and the no choice mating regime. We further demonstrate that sexual dimorphism decreased when flies evolved under increasing temperatures, consistent with recent theory predicting more sexually concordant selection under environmental stress. Our results suggest an important role for precopulatory sexual selection in promoting thermal adaptation and evolutionary rescue.