Ejaculate-mediated paternal effects: evidence, mechanisms and evolutionary implications

Abstract

Despite serving the primary objective of ensuring that at least one sperm cell reaches and fertilises 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.

Nongenetic paternal effects via seminal fluid

“…The strong nongenetic paternal effects on offspring phenotype that we have documented raise general questions around the validity of quantitative genetic designs, such as the full‐sib half‐sib design, that ascribe sire effects to additive genetic variance (Banta and Richards ; Evans et al. ). They also hold important implications for our understanding of evolutionary processes.…”

“…There is growing evidence that nongenetic paternal effects on offspring can be mediated by the ejaculate (Evans et al. ). The ejaculate consists of both sperm and seminal fluid fractions, both of which can affect offspring phenotype by mechanisms that are independent of the DNA carried in the sperm nucleus.…”

“…Although recent discussions have recognized the necessity to consider nongenetic paternal effects in estimating paternal genetic effects (Banta and Richards ), the magnitude of the potential problem has not yet been examined formally (Evans et al. ).…”

Temperature as a modulator of sexual selection

“…Second, because temperature affects a host of physiological mechanisms with consequences that may spill over to subsequent generations via paternal effects or the transmission of epigenetic marks. Paternal germline epigenetic changes that are environmentally triggered are increasingly recognised as modulators of sperm function (Jenkins et al, 2017;Stuppia et al, 2015) but also, remarkably, as sources of variance in the offspring phenotype (Miller, Brinkworth & Iles, 2010;Wang, Liu & Sun, 2017;Jenkins et al, 2017;Stuppia et al, 2015;Donkin & Barres, 2018;Evans et al, 2019). In the nematode Caenorhabditis elegans, for instance, temperature variation induces multigenerational inheritance of gene expression through both oocytes and sperm (Klosin et al, 2017).…”

“…Demonstrating such long-lasting epigenetic memory of parental temperature experiences, and at the same time unravelling the underlying mechanisms, is challenging and has been seldom achieved (Klosin et al, 2017). Nonetheless, there are reasons to suspect that temperatureinduced transmission of epigenetic marks affecting sperm and offspring phenotypes may be common (Evans et al, 2019). In most systems, we ignore whether cross-generational effects driven by paternal environment are driven by epigenetic mechanisms or mediated by other factors (e.g.…”