Sperm experience intense and varied selection that dramatically impacts the evolution of sperm quality. Selection acts to ensure that sperm are fertilization-competent and able to overcome the many challenges experienced on their way towards eggs. However, simply being able to fertilize an egg is not enough to ensure male fertility in most species. Owing to the prevalence of female multiple mating throughout the animal kingdom, successful fertilization requires sperm to outcompete rival sperm. In addition, females can actively influence sperm quality, storage or utilization to influence male fertility. This review provides an overview of how these selective forces influence the evolution of sperm quality. After exploring the link between sperm traits and male fertility, we examine how post-mating competition between rival ejaculates influences the evolution of sperm quality. We then describe how complex genetic, social and sexual interactions influence sperm quality, focusing on the importance of seminal fluid and interactions between sperm and the female's reproductive tract. In light of the complexities of selection on sperm traits, greater use of multivariate approaches that incorporate male-male, sperm-sperm and sperm-female interactions to study sperm quality will enhance our understanding of how selection acts on sperm traits and factors influencing male fertility. Because the metric of male reproductive success--fertilization--is the same across the animal kingdom, we argue that information about sperm evolution gained from non-human animals has enormous potential to further our understanding of the factors that impact human fertility.

Sperm velocity is one of the main determinants of the outcome of sperm competition. Since sperm vary considerably in their morphology between and within species, it seems likely that sperm morphology is associated with sperm velocity. Theory predicts that sperm velocity may be increased by enlarged midpiece (energetic component) or flagellum length (kinetic component), or by particular ratios between sperm components, such as between flagellum length and head size. However, such associations have rarely been found in empirical studies. In a comparative framework in passerine birds, we tested these theoretical predictions both across a wide range of species and within a single family, the New World blackbirds (Icteridae). In both study groups, sperm velocity was influenced by sperm morphology in the predicted direction. Consistent with theoretical models, these results show that selection on sperm morphology and velocity are likely to be concomitant evolutionary forces.

Spermatozoa are amongst the most variable cells, and three factors are thought to account for this variation in design: fertilization mode, phylogeny, and postcopulatory sexual selection. In addition, it has long been assumed that a tradeoff exists between sperm size and number, and although postcopulatory sexual selection affects both traits, empirical evidence for a tradeoff has so far been elusive. Our recent theoretical model predicts that the nature of a direct tradeoff between sperm size and number varies with sperm competition mechanism and sperm competition risk. We test these predictions using a comparative approach in two very different taxa with different sperm competition mechanisms: passerine birds (mechanism: simple raffle) and Drosophila fruit flies (sperm displacement). We show that in both groups, males increase their total ejaculate investment with increasing sperm competition risk, but whereas passerine birds allocate disproportionately to sperm number, drosophilids allocate disproportionately to sperm size. This striking difference between the two groups can be at least partly explained by sperm competition mechanisms depending on sperm size relative to the size of the female reproductive tract: in large animals (passerines), sperm numbers are advantageous in sperm competition owing to dilution inside the female tract, whereas in small animals (drosophilids), large sperm are advantageous for physical competition (sperm displacement). Our study provides two important results. First, we provide convincing evidence for the existence of a sperm size–number tradeoff. Second, we show that by considering both sperm competition mechanism and dilution, can we account for variation in sperm size between different taxa.

In contrast to early predictions, it is now widely accepted that males incur substantive costs from ejaculate production. Hence, males are predicted to allocate their reproductive investments, including ejaculate size, relative to the risk of sperm competition and to female quality. The study of sperm allocation, however, has been technically challenging with nonvirgin females because sperm from different males must be discriminated within the female reproductive tract. To date, such investigations have thus largely been restricted to species that transfer sperm in spermatophores or for which females can be fitted with a harness to capture the incoming ejaculate. In this study, we examined sperm allocation using male Drosophila melanogaster that express a fluorescently labeled protein in sperm heads, allowing us to quantify sperm numbers from different males within the female reproductive tract. We found that male D. melanogaster deliver significantly more sperm to mated, large or young females compared with virgins, small or old females, respectively, whereas copulation duration was only significantly longer with large than with small females. These results provide further evidence for costly ejaculate production and consequent prudent allocation of sperm.