New grant from the State Plan of R&D&i of Excellence. Our understanding of the causes and consequences of sexual conflict is hampered due to a lack of knowledge on a fundamental question: Does sexual conflict underlies the structure of socio-sexual networks and the ability of individuals to shape their social environment? This project will exploit the integration of experimental evolution protocols and evolutionary thinking with social network theory to address this question.
Despite serving the primary objective of ensuring that at least one sperm cell reaches and fertilizes an ovum, the male ejaculate (i.e. spermatozoa and seminal fluid) is a compositionally complex ‘trait’ that can respond phenotypically to subtle changes in conditions. In particular, recent research has shown that environmentally and genetically induced changes to ejaculates can have implications for offspring traits that are independent of the DNA sequence encoded into the sperm’s haploid genome. In this review, we compile evidence from several disciplines and numerous taxonomic systems to reveal the extent of such ejaculate-mediated paternal effects (EMPEs). We consider a number of environmental and genetic factors that have been shown to impact offspring phenotypes via ejaculates, and where possible we highlight the putative mechanistic pathways by which ejaculates can act as conduits for paternal effects. We also highlight how females themselves can influence EMPEs, and in some cases how maternally derived sources of variance may confound attempts to test for EMPEs. Finally, we consider a range of putative evolutionary implications of EMPEs, and suggest a number of potentially useful approaches for exploring these further. Overall our review confirms that EMPEs are both widespread and varied in their effects, although studies reporting their evolutionary effects are still in their infancy.
Mating often bears large costs to females, especially in species with high levels of sexual conflict over mating rates. Given the direct costs to females associated with multiple mating, which include reductions in lifespan and lifetime reproductive success, past research focused on identifying potential indirect benefits (through increases in offspring fitness) that females may accrue. Far less attention has, however, been devoted to understanding how costs of sexual interactions to females may extend across generations. Hence, little is known about the transgenerational implications of variation in mating rates, or the net consequences of maternal sexual activities across generations. Using the seed beetle, Callosobruchus maculatus, a model system for the study of sexual conflict, we investigate the effects of mating with multiple males versus a single male, and tease apart effects due to sexual harassment and those due to mating per se, over three generations. A multigenerational analysis indicated that females that were exposed to ongoing sexual harassment and who also were permitted to mate with multiple males showed no difference in net fitness compared to females that mated just once without ongoing harassment. Intriguingly, however, females that were continually harassed, but permitted to mate just once, suffered a severe decline in net fitness compared to females that were singly (not harassed) or multiply mated (harassed, but potentially gaining benefits via mating with multiple males). Overall, the enhanced fitness in multiply mated compared to harassed females may indicate that multiple mating confers transgenerational benefits. These benefits may counteract, but do not exceed (i.e., we found no difference between singly and multiply mated females), the large transgenerational costs of harassment. Our study highlights the importance of examining transgenerational effects from an inclusive (looking at both indirect benefits but also costs) perspective, and the need to investigate transgenerational effects across several generations if we are to fully understand the consequences of sexual interactions, sexual conflict evolution, and the interplay of sexual conflict and multi-generational costs and benefits.
Sex ratio allocation has important fitness consequences, and theory predicts that parents should adjust offspring sex ratio in cases where the fitness returns of producing male and female offspring vary. The ability of fathers to bias offspring sex ratios has traditionally been dismissed given the expectation of an equal proportion of X- and Y-chromosome-bearing sperm (CBS) in ejaculates due to segregation of sex chromosomes at meiosis. This expectation has been recently refuted. Here we used Peromyscus leucopus to demonstrate that sex ratio is explained by an exclusive effect of the father, and suggest a likely mechanism by which male-driven sex-ratio bias is attained. We identified a male sperm morphological marker that is associated with the mechanism leading to sex ratio bias; differences among males in the sperm nucleus area (a proxy for the sex chromosome that the sperm contains) explain 22% variation in litter sex ratio. We further show the role played by the sperm nucleus area as a mediator in the relationship between individual genetic variation and sex-ratio bias. Fathers with high levels of genetic variation had ejaculates with a higher proportion of sperm with small nuclei area. This, in turn, led to siring a higher proportion of sons (25% increase in sons per 0.1 decrease in the inbreeding coefficient). Our results reveal a plausible mechanism underlying unexplored male-driven sex-ratio biases. We also discuss why this pattern of paternal bias can be adaptive. This research puts to rest the idea that father contribution to sex ratio variation should be disregarded in vertebrates, and will stimulate research on evolutionary constraints to sex ratios—for example, whether fathers and mothers have divergent, coinciding, or neutral sex allocation interests. Finally, these results offer a potential explanation for those intriguing cases in which there are sex ratio biases, such as in humans.