Selfish genes and sexual selection: the impact of genomic parasites on host reproduction

Abstract

Selfish genetic elements (SGEs) such as replicating mobile elements, segregation distorters and maternally inherited endosymbionts, bias their transmission success relative to the rest of the genome to increase in representation in subsequent generations. As such, they generate conflict with the rest of the genome. Such intragenomic conflict is also a hallmark of sexually antagonistic (SA) alleles, which are shared genes between the sexes but that have opposing fitness effects when expressed in males and females. However, whilst both SGEs and SA alleles are recognized as common and potent sources of genomic conflict, the realization that SGEs can also generate sexually antagonistic selection and contribute to sexual conflict in addition to generate sexual selection is largely overlooked. Here, I show that SGEs frequently generate sex-specific selection and outline how SGEs that are associated with compromised male fertility can shape female mating patterns, play a key role in the dynamics of sex-determination systems and likely be an important source of sexually antagonistic genetic variation. Given the prevalence of SGEs, their contribution to sexual conflict is likely to be greatly overlooked.

Selfish genetic elements and male fertility

“…Post-copulatory mechanisms offer another mitigation route for females. The importance of polyandry, when females mate with multiple males, when at risk of mating with an SGEcarrying male has received much attention [5,50]. Polyandry is favoured because SGE-carrying males can be at a disadvantage when competing against other males' undamaged ejaculates owing to the production of fewer sperm or sperm with lower vigour [52] and multiple studies across taxa have demonstrated SGE-carrying males to be inferior spermcompetitors (e.g.…”

“…4 2nd male only transferred seminal fluids and not sperm, an estimate of 0.125 is therefore extrapolated from SR males producing 25% as many offspring as ST males when exposed to the seminal fluid of a 2nd male. 5 Paternity estimated from competition of sex ratio and standard males against an inferior tester mutant strain, potentially causing an underestimated P1 and overestimated P2. royalsocietypublishing.org/journal/rstb Phil.…”

“…SGEs involving sperm manipulation confer direct fitness costs to males that carry them; therefore, we expect females to mitigate against mating to such 'inferior' males [4][5][6]. A simple strategy is pre-copulatory mate choice to avoid mating with SGE males entirely.…”

“…A simple strategy is pre-copulatory mate choice to avoid mating with SGE males entirely. However, evidence for direct mate choice is remarkably scarce, with only a few good examples of discrimination against SGE-carrying males whereas most studies find no such evidence (for review see [5,50]; figure 1). However, SGEs can be costly to a male's fitness in a variety of ways and, as a result, any female choice for high-fitness males might generally select against SGE-carrying low-fitness males [51].…”

“…As a result, spermatogenesis through to fertilization can be viewed as a series of arenas that are vulnerable to the activities of SGEs. The actions of SGEs in sperm have far-reaching impacts, killing sperm and zygotes, changing the physiology and mating behaviour of males and females, and have perhaps influenced the evolution of some of the deep structures of spermatogenesis ( [4][5][6]; figure 1).…”