Males that exhibit alternative reproductive tactics (ARTs) often differ in the risk of sperm competition and the energetic trade-offs they experience. The resulting patterns of selection could lead to between-tactic differences in ejaculate traits. Despite extensive research on male ARTs, there is no comprehensive review of whether and what differences in sperm traits exist between male ARTs. We review existing theory on ejaculate evolution relevant to ARTs and then conduct a comprehensive vote-counting review of the empirical data comparing sperm traits between males adopting ARTs. Despite the general expectation that sneaker males should produce sperm that are more competitive (e.g. higher quality or performance), we find that existing theory does not predict explicitly how males adopting ARTs should differ in sperm traits. The majority of studies find no significant difference in sperm performance traits between dominant and sneaker males. However, when there is a difference, sneaker males tend to have higher sperm performance trait values than dominant males. We propose ways that future theoretical and empirical research can improve our understanding of the evolution of ejaculate traits in ARTs. We then highlight how studying ejaculate traits in species with ARTs will improve our broader knowledge of ejaculate evolution. This article is part of the theme issue ‘Fifty years of sperm competition’.

In contrast to sexual selection on traits that affect interactions between the sexes before mating, little theoretical research has focused on the coevolution of postmating traits via cryptic female choice (when females bias fertilization toward specific males). We used simulation models to ask (a) whether and, if so, how nondirectional cryptic female choice (female-by-male interactions in fertilization success) causes deviations from models that focus exclusively on male-mediated postmating processes, and (b) how the risk of sperm competition, the strength of cryptic female choice, and tradeoffs between sperm number and sperm traits interact to influence the coevolutionary dynamics between cryptic female choice and sperm traits. We found that incorporating cryptic female choice can result in males investing much less in their ejaculates than predicted by models with sperm competition only. We also found that cryptic female choice resulted in the evolution of genetic correlations between cryptic female choice and sperm traits, even when the strength of cryptic female choice was weak, and the risk of sperm competition was low. This suggests that cryptic female choice may be important even in systems with low multiple mating. These genetic correlations increased with the risk of sperm competition and as the strength of cryptic female choice increased. When the strength of cryptic female choice and risk of sperm competition was high, extreme codivergence of sperm traits and cryptic female choice preference occurred even when the sperm trait traded off with sperm number. We also found that male traits lagged behind the evolution of female traits; this lag decreased with increasing strength of cryptic female choice and risk of sperm competition. Overall, our results suggest that cryptic female choice deserves more attention theoretically and may be driving trait evolution in ways just beginning to be explored.

Given that sperm production can be costly, theory predicts that males should optimally adjust the quantity and/or quality of their sperm in response to their social environment to maximize their paternity success. Although experiments demonstrate that males can alter their ejaculates in response to manipulations of the social environment and studies show that ejaculate traits covary with social environment across populations, it is unknown whether individual variation in sperm traits corresponds to natural variation found within wild populations. Using an island population of brown anole lizards (Anolis sagrei), we tested the prediction that sperm traits (sperm count, sperm morphology, sperm velocity) respond to natural variation in the risk of sperm competition, as inferred from the local density and operational sex ratio (OSR) of conspecifics. We found that males living in high-density areas of the island produced relatively larger sperm midpieces, smaller sperm heads, and lower sperm counts. Sperm traits were unrelated to OSR after accounting for the covariance between OSR and density. Our findings broaden the implications of sperm competition theory to intrapopulation social environment variation by showing that sperm count and sperm morphology vary with fine-scale differences in density within a single wild population.

Sperm competition is a widespread phenomenon that shapes male reproductive success. Ejaculates present many potential targets for postcopulatory selection (e.g., sperm morphology, count, and velocity), which are often highly correlated and potentially subject to complex multivariate selection. Although multivariate selection on ejaculate traits has been observed in laboratory experiments, it is unclear whether selection is similarly complex in wild populations, where individuals mate frequently over longer periods of time. We measured univariate and multivariate selection on sperm morphology, sperm count, and sperm velocity in a wild population of brown anole lizards (Anolis sagrei). We conducted a mark-recapture study with genetic parentage assignment to estimate individual reproductive success. We found significant negative directional selection and negative quadratic selection on sperm count, but we did not detect directional or quadratic selection on any other sperm traits, nor did we detect correlational selection on any trait combinations. Our results may reflect pressure on males to produce many small ejaculates and mate frequently over a six-month reproductive season. This study is the first to measure multivariate selection on sperm traits in a wild population and provides an interesting contrast to experimental studies of external fertilizers, which have found complex multivariate selection on sperm phenotypes.

Understanding the thermal sensitivity of reproductive interactions is crucial given global warming. Previous studies have almost exclusively focused on interactions before mating, even though important interactions between the sexes also occur after mating (e.g. gamete interactions), which are likely also affected by temperature. Thus, it remains unknown how temperature affects the influence of female reproductive fluid on sperm performance, thereby altering female control over fertilization (cryptic female choice). This gap limits our understanding of how sexual selection changes with seasonal temperature fluctuations and temperatures outside the range of historical norms. We tested how temperatures relevant to current conditions and climate change projections influence the mechanisms underlying cryptic female choice in a marine fish, Symphodus ocellatus . Under typical, cooler thermal conditions, female reproductive fluid enhances sperm velocity and biases fertilization dynamics to favour preferred, dominant males over sneaker males. We find that warmer temperatures decrease female influence on sperm velocity, especially for dominant males. This results in dominant males having slower sperm than sneaker males at warmer temperatures, reducing the expected paternity of preferred, dominant males. Our results highlight that considering the thermal sensitivity of female–male interactions that occur after mating will be essential for understanding how seasonal variation and climate change can influence fertility, reproduction and sexual selection. Read the free Plain Language Summary for this article on the Journal blog.