Sexually antagonistic "zygotic drive" of the sex chromosomes

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.

Figure 1. A green-beard effect mutation (a') causes its bearer to express a distinguishing phenotype (the green-beard ‘tag’ illustrated by green shading) and differentially interact with other individuals by i) helping other tagged individuals (increasing their survival and/or fecundity; solid arrow), and/or ii) harming untagged competitor individuals (dashed arrow).

Figure 2. Summary of how linkage to the sex chromosomes simplifies the requisite multifarious phenotype needed to produce a sexually antagonistic green-beard effects that fuel SA-zygotic drive.

Figure 3. Summary of sexually antagonistic selection in males on the X and Y chromosomes.

Figure 4. Antagonistic coevolution between the X and Y leading to recurrent episodes of SA-zygotic drive.

The autosomes will only evolve to block harmful phenotypes coded by the X and Y when SA-zygotic drive causes the average fitness of the brood to decline.

Figure 5. The dynamics of the average values x and y, variances of x and y, and the average fitness of sons and daughters.

(A) A run with α = 0.4 and μ = 0.00001. (B) A run with α = 0.025 and μ = 0.001. Red depicts x and daughters and blue depicts y and sons.

Figure 6. A pedigree analysis of female homosexuality.

The focal homosexual individual is highlighted in yellow. Relatives expressing elevated rates of homosexuality are shown in red (based on Table 6 of Pattatucci and Hamer (1995) [41]).

Figure 7. Fitness function for α = 0.4 (stronger selection, steeper blue curve), α = 0.1 (moderate selection, green curve), and α = 0.025 (weaker selection, red curve).