Mechanisms underlying the sperm quality advantage in sperm competition and cryptic female choice in Drosophila melanogaster

Contrary to early predictions of sperm competition theory, postcopulatory sexual selection favoring increased investment per sperm (e.g., sperm size, sperm quality) has been demonstrated in numerous organisms. Recent findings reveal that sperm production strategies are highly variable, with males of some species producing relatively few, giant sperm. We empirically demonstrate for Drosophila melanogaster that both sperm quality and sperm quantity independently contribute to competitive male fertilization success. The interaction between sperm quality and quantity suggests an internal positive reinforcement on selection for sperm quality, with selection predicted to intensify as investment per sperm increases and the number of sperm competing declines. The mechanism underlying the sperm quality advantage is elucidated through examination of the relationship between female sperm-storage organ morphology and the differential organization of different length sperm within the organ. Our results exemplify that primary sex cells can bear secondary sexual straits

Sperm death and dumping in Drosophila

Mating with more than one male is the norm for females of many species. In addition to generating competition between the ejaculates of different males, multiple mating may allow females to bias sperm use. In Drosophila melanogaster, the last male to inseminate a female sires approximately 80% of subsequent progeny. Both sperm displacement, where resident sperm are removed from storage by the incoming ejaculate of the copulating male, and sperm incapacitation, where incoming seminal fluids supposedly interfere with resident sperm, have been implicated in this pattern of sperm use. But the idea of incapacitation is problematic because there are no known mechanisms by which an individual could damage rival sperm and not their own. Females also influence the process of sperm use, but exactly how is unclear. Here we show that seminal fluids do not kill rival sperm and that any 'incapacitation' is probably due to sperm ageing during sperm storage. We also show that females release stored sperm from the reproductive tract (sperm dumping) after copulation with a second male and that this requires neither incoming sperm nor seminal fluids. Instead, males may cause stored sperm to be dumped or females may differentially eject sperm from the previous mating

Male × Female Interaction for a Pre-Copulatory Trait, but Not a Post-Copulatory Trait, among Cosmopolitan Populations of Drosophila melanogaster

Sexual coevolution occurs when changes in the phenotype of one sex select for changes in the other sex. We can identify the “footprint” of this coevolution by mating males and females from different populations and testing for a male-female genotype interaction for a trait associated with male (or female) performance. Here we mated male Drosophila melanogaster from five different continents with females from their own and different continents to test for a male-female interaction for mating speed, a pre-copulatory trait, and female reproductive investment, a post-copulatory trait. We found a strong male-female interaction for mating speed, consistent with previous studies using different populations, suggesting that the potential for sexual coevolution for this trait is present in this species. In contrast, we did not detect a male-female interaction for female reproductive investment. Although a male-female interaction for mating speed is compatible with the hypothesis of ongoing sexual coevolution, the nature of our experimental design is unable to exclude alternate explanations. Thus, the evolutionary mechanisms promoting male-female genotype interactions for pre-copulatory mating traits in D. melanogaster warrant further investigation

Sperm Competition, Sperm Numbers and Sperm Quality in Muroid Rodents

Sperm competition favors increases in relative testes mass and production efficiency, and changes in sperm phenotype that result in faster swimming speeds. However, little is known about its effects on traits that contribute to determine the quality of a whole ejaculate (i.e., proportion of motile, viable, morphologically normal and acrosome intact sperm) and that are key determinants of fertilization success. Two competing hypotheses lead to alternative predictions: (a) sperm quantity and quality traits co-evolve under sperm competition because they play complementary roles in determining ejaculate's competitive ability, or (b) energetic constraints force trade-offs between traits depending on their relevance in providing a competitive advantage. We examined relationships between sperm competition levels, sperm quantity, and traits that determine ejaculate quality, in a comparative study of 18 rodent species using phylogenetically controlled analyses. Total sperm numbers were positively correlated to proportions of normal sperm, acrosome integrity and motile sperm; the latter three were also significantly related among themselves, suggesting no trade-offs between traits. In addition, testes mass corrected for body mass (i.e., relative testes mass), showed a strong association with sperm numbers, and positive significant associations with all sperm traits that determine ejaculate quality with the exception of live sperm. An “overall sperm quality” parameter obtained by principal component analysis (which explained 85% of the variance) was more strongly associated with relative testes mass than any individual quality trait. Overall sperm quality was as strongly associated with relative testes mass as sperm numbers. Thus, sperm quality traits improve under sperm competition in an integrated manner suggesting that a combination of all traits is what makes ejaculates more competitive. In evolutionary terms this implies that a complex network of genetic and developmental pathways underlying processes of sperm formation, maturation, transport in the female reproductive tract, and preparation for fertilization must all evolve in concert

Sperm form and function: what do we know about the role of sexual selection?

Sperm morphological variation has attracted considerable interest and generated a wealth of (mostly descriptive) studies over the past three centuries. Yet, apart from biophysical studies linking sperm morphology to swimming velocity, surprisingly little is known about the adaptive significance of sperm form and the selective processes underlying its tremendous diversification throughout the animal kingdom. Here, we first discuss the challenges of examining sperm morphology in an evolutionary context and why our understanding of it is still so poor. Then, we review empirical evidence for how sexual selection theory applies to the evolution of sperm form and function, including putative secondary sexual traits borne by sperm

Data from: Size-dependent ejaculation strategies and reproductive success in the yellow dung fly, Scathophaga stercoraria

Theory predicts that sperm competition will favour the production of larger ejaculates. However, because the benefits of greater reproductive investment are balanced by the costs of spermatogenesis, expenditure should depend on male physiology, mating rate and the relationship between additional investment and fertilization gains. In the yellow dung fly, Scathophagastercoraria, males adopt size-dependent alternative mating tactics that are associated with discrete ecological resources (foraging and oviposition substrates), although males switch between these environments throughout their lives. By copulating on foraging substrate (fruit or flowers), males can bypass intense mate competition that occurs at oviposition sites (cow dung), but as a consequence, must occupy a disfavoured mating role (i.e. face a greater risk that their ejaculate will be displaced from storage prior to fertilization). Small males often mate on foraging substrate, whereas large males mate in this environment only during feeding bouts. Optimal ejaculate expenditure should therefore depend on male size and their current mating role. By measuring copula duration (i.e. ejaculate expenditure) of natural matings and assigning paternity to resulting offspring, we confirmed that copulations on dung sire approximately three times as many offspring as those on foraging substrate. Furthermore, large males reduced copula duration on fruit, as predicted, since this strategy enables greater investment into high-payoff matings on dung. Conversely, small males copulated for shorter durations on dung than on foraging substrate, perhaps to minimize the risk of being displaced from copula by a rival. These patterns of ejaculate expenditure translated into greater offspring production for large males on dung and for small males on fruit. We discuss the possible proximate factors driving these size- and context-dependent patterns of ejaculate allocation by yellow dung fly males. Together, our findings shed light on the allocation strategies and reproductive consequences of alternative mating tactics

Sperm length is not influenced by haploid gene expression in the flies Drosophila melanogaster and Scathophaga stercoraria

Recent theoretical models have postulated a role for haploid–diploid conflict and for kin selection favouring sperm cooperation and altruism in the diversification and specialization of sperm form. A critical assumption of these models—that haploid gene expression contributes to variation in sperm form—has never been demonstrated and remains contentious. By quantifying within-male variation in sperm length using crosses between males and females from populations that had been subjected to divergent experimental selection, we demonstrate that haploid gene expression does not contribute to variation in sperm length in both Drosophila melanogaster and Scathophaga stercoraria. This finding casts doubt on the importance of haploid–diploid conflict and kin selection as evolutionary influences of sperm phenotypes

Gress.Pitnick.AB.data

Raw copula durations for pomace males (m1.cop.dur) and dung males (m2.cop.dur) were recorded in the field, as was ambient temperature (temp1 = temperature during pomace mating, temp2 = temperature during dung mating); Portion of offspring sired by male 1 and 2 (P1 and P2); m1.progeny and m2.progeny represent the absolute number of offspring sired by male 1 and 2 in the subsequent female clutch; male hind tibia length was measured in the lab (m1.ru and m2.ru raw values, m1.htl.mm and m2.htl.mm are divided by 32 to convert to mm); sperm1 and sperm2 are estimates of the number of sperm transferred per ejaculate using known relationships between male htl and sperm transfer rate (0.0018 (htl^3) - 0.003) * 826.8