Abstract
Genomic conflict is perplexing because it causes the fitness of a species to decline rather than improve. Many diverse forms of genomic conflict have been identified, but this extant tally may be incomplete. Here, we show that the unusual characteristics of the sex chromosomes can, in principle, lead to a previously unappreciated form of sexual genomic conflict. The phenomenon occurs because there is selection in the heterogametic sex for sex-linked mutations that harm the sex of offspring that does not carry them, whenever there is competition among siblings. This harmful phenotype can be expressed as an antagonistic green-beard effect that is mediated by epigenetic parental effects, parental investment, and/or interactions among siblings. We call this form of genomic conflict sexually antagonistic “zygotic drive”, because it is functionally equivalent to meiotic drive, except that it operates during the zygotic and postzygotic stages of the life cycle rather than the meiotic and gametic stages. A combination of mathematical modeling and a survey of empirical studies is used to show that sexually antagonistic zygotic drive is feasible, likely to be widespread in nature, and that it can promote a genetic “arms race” between the homo- and heteromorphic sex chromosomes. This new category of genomic conflict has the potential to strongly influence other fundamental evolutionary processes, such as speciation and the degeneration of the Y and W sex chromosomes. It also fosters a new genetic hypothesis for the evolution of enigmatic fitness-reducing traits like the high frequency of spontaneous abortion, sterility, and homosexuality observed in humans.
Highlights
Sex chromosomes are unusual compared to the autosomes for three reasons
Feasibility of Maternal and Paternal SA-GrBd-Effects Consider the expression of the paternal X and Y chromosomes during spermatogenesis at a time when the developing gametes remain functionally diploid, i.e., before the primary spermatogonial cell has divided into haploid spermatids, and while the four developing spermatids derived from each spermatagonial cell remain connected by cytoplasmic bridges that permit RNA, steroid hormones, proteins and other molecules to be exchanged
We explore the fate of mutations located on the X and Y chromosome that code for i) paternal investment (PI) that is skewed toward the sex of offspring that carries them, ii) epigenetic paternal effects that interfere with the ontogeny of the sex of offspring that do not carry them, and iii) competitive sib-sib-interactions that reduce the competitive ability of the sex that does not carry them
Summary
Sex chromosomes are unusual compared to the autosomes for three reasons. Non-recombining sex chromosomes can evolve to become far more dimorphic than autosomes. It has long been recognized that these characteristics can contribute to genetic conflict in the context of meiotic drive, but other forms of potential sex-linked genetic conflict have received relatively little attention (reviewed in [1]). We evaluate the potential for the special characteristics of the sex chromosomes to contribute to a meiotic-drive like process – sexually antagonistic zygotic drive (hereafter, SA-zygotic drive) – that operates due to competition among opposite-sex siblings, rather than gamete types. The phenotypes that fuel this process are sexually antagonistic greenbeard effects (hereafter SA-GrBd-effects) that only operate when there is competition among siblings
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