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Abstract Drosophila , long sperm are favoured in sperm competition based on the length of the female's primary sperm storage organ, the seminal receptacle (SR ). This sperm–SR interaction, together with a genetic correlation between the traits, suggests that the coevolution of exaggerated sperm andSR lengths may be driven by Fisherian runaway selection. Here, we explore the costs and benefits of long sperm andSR genotypes, both in the sex that carries them and in the sex that does not. We measured male and female fitness in inbred lines ofDrosophila melanogaster derived from four populations previously selected for long sperm, short sperm, longSR s or shortSR s. We specifically asked: What are the costs and benefits of long sperm in males and longSR s in females? Furthermore, do genotypes that generate long sperm in males or longSR s in females impose a fitness cost on the opposite sex? Answers to these questions will address whether long sperm are an honest indicator of male fitness, male post‐copulatory success is associated with male precopulatory success, female choice benefits females or is costly, and intragenomic conflict could influence evolution of these traits. We found that both sexes have increased longevity in long sperm and longSR genotypes. Males, but not females, from longSR lines had higher fecundity. Our results suggest that sperm–SR coevolution is facilitated by both increased viability and indirect benefits of long sperm andSR s in both sexes. -
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Abstract Post‐copulatory sexual selection is thought to be responsible for much of the extraordinary diversity in sperm morphology across metazoans. However, the extent to which post‐copulatory selection targets sperm morphology versus sperm production is generally unknown. To address this issue, we simultaneously characterized the evolution of sperm morphology (length of the sperm head, midpiece and flagellum) and testis size (a proxy for sperm production) across 26 species of
Anolis lizards, a group in which sperm competition is likely. We found that the length of the sperm midpiece has evolved 2–3 times faster than that of the sperm head or flagellum, suggesting that midpiece size may be the most important aspect of sperm morphology with respect to post‐copulatory sexual selection. However, testis size has evolved faster than any aspect of sperm morphology or body size, supporting the hypothesis that post‐copulatory sexual selection acts more strongly upon sperm production than upon sperm morphology. Likewise, evolutionary increases in testis size, which typically indicate increased sperm competition, are not associated with predictable changes in sperm morphology, suggesting that any effects of post‐copulatory selection on sperm morphology are either weak or variable in direction across anoles. Collectively, our results suggest that sperm production is the primary target of post‐copulatory sexual selection in this lineage. -
Reproductive traits that influence female remating and competitive fertilization rapidly evolve in response to sexual selection and sexual conflict. One such trait, observed across diverse animal taxa, is the formation of a structural plug inside the female reproductive tract (FRT), either during or shortly after mating. In Drosophila melanogaster , male seminal fluid forms a mating plug inside the female bursa, which has been demonstrated to influence sperm entry into storage and latency of female remating. Processing of the plug, including its eventual ejection from the female's reproductive tract, influences the competitive fertilization success of her mates and is mediated by female × male genotypic interactions. However, female contributions to plug formation and processing have received limited attention. Using developmental mutants that lack glandular FRT tissues, we reveal that these tissues are essential for mating plug ejection. We further use proteomics to demonstrate that female glandular proteins, and especially proteolytic enzymes, contribute to mating plug composition and have a widespread impact on plug formation and composition. Together, these phenotypic and molecular data identify female contributions to intersexual interactions that are a potential mechanism of post-copulatory sexual selection.more » « less
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Interactions between sperm and the female reproductive tract (FRT) are critical to reproductive success and yet are poorly understood. Because sperm complete their functional maturation within the FRT, the life history of sperm is likely to include a molecular “hand-off” from males to females. Although such intersexual molecular continuity is likely to be widespread among all internally fertilizing species, the identity and extent of female contributions are largely unknown. We combined semiquantitative proteomics with sex-specific isotopic labeling to catalog the posttesticular life history of the sperm proteome and determine the extent of molecular continuity between male and FRTs. We show that the Drosophila melanogaster sperm proteome undergoes substantial compositional changes after being transferred to the FRT. Multiple seminal fluid proteins initially associate with sperm, but most become undetectable after sperm are stored. Female-derived proteins also begin to associate with sperm immediately after mating, and they comprise nearly 20% of the postmating sperm proteome following 4 d of storage in the FRT. Female-derived proteins that associate with sperm are enriched for processes associated with energy metabolism, suggesting that female contributions support sperm viability during the prolonged period between copulation and fertilization. Our research provides a comprehensive characterization of sperm proteome dynamics and expands our understanding of the critical process of sperm–FRT interactions.more » « less
