The Resolution of Sexual Antagonism by Gene Duplication

Abstract

Disruptive selection between males and females can generate sexual antagonism, where alleles improving fitness in one sex reduce fitness in the other. This type of genetic conflict arises because males and females carry nearly identical sets of genes: opposing selection, followed by genetic mixing during reproduction, generates a population genetic ''tug-of-war'' that constrains adaptation in either sex. Recent verbal models suggest that gene duplication and sex-specific cooption of paralogs might resolve sexual antagonism and facilitate evolutionary divergence between the sexes. However, this intuitive proximal solution for sexual dimorphism potentially belies a complex interaction between mutation, genetic drift, and positive selection during duplicate fixation and sex-specific paralog differentiation. The interaction of these processes-within the explicit context of duplication and sexual antagonism-has yet to be formally described by population genetics theory. Here, we develop and analyze models of gene duplication and sex-specific differentiation between paralogs. We show that sexual antagonism can favor the fixation and maintenance of gene duplicates, eventually leading to the evolution of sexually dimorphic genetic architectures for male and female traits. The timescale for these evolutionary transitions is sensitive to a suite of genetic and demographic variables, including allelic dominance, recombination, sex linkage, and population size. Interestingly, we find that female-beneficial duplicates preferentially accumulate on the X chromosome, whereas male-beneficial duplicates are biased toward autosomes, independent of the dominance parameters of sexually antagonistic alleles. Although this result differs from previous models of sexual antagonism, it is consistent with several findings from the empirical genomics literature.

A General Population Genetic Framework for Antagonistic Selection That Accounts for Demography and Recurrent Mutation

“…In population A, equilibrium fitness variation in males and females is given by expressions V m (A) ¼ s m 2 q eq (1 -q eq )/2 and V f (A) ¼ s f 2 q eq (1 -q eq )/2, respectively, with values of q eq from Equation 4b. Suppose that a second population ("population B") has resolved the antagonistic selection by way of gene duplication and sex-specific cooption of the paralogs (e.g., Connallon and Clark 2011). Following duplication, and supposing that the sex-specific selection coefficients do not systematically change, male-deleterious alleles will evolve to a frequency q m 4u/s m and female-deleterious alleles evolve to a frequency q f 4u/s f .…”

Reduced selection and accumulation of deleterious mutations in genes exclusively expressed in men

“…This implies that these genes will be subject to different selection levels in the two sexes, and might even be subject to conflicting selective pressures between the sexes 44 . Hence, it has also been shown in the fruit fly that mutations in genes with sex-biased expression have also sex-biased phenotypic consequences 45 . Another level of selection constraint could stem from the fact that most male gametes do not fertilize any eggs.…”

Inferring the History of Interchromosomal Gene Transposition in Drosophila Using n-Dimensional Parsimony

“…The same patterns of movement are repeated in mammals, with an excess of X-to-autosome gene movements for RNA-based duplicative transpositions (Emerson et al 2004;Potrzebowski et al 2008) and for DNA-based relocations (Moyle et al 2010), but not for DNA-based duplications (Jiang et al 2007;). There are several hypotheses that attempt to explain the excess of Xto-autosome gene traffic, including sexually antagonistic selection (Rice 1984;Wu and Xu 2003;Connallon and Clark 2011), escape from X inactivation (Betrán et al 2002), meiotic drive (Meiklejohn and Tao 2010), and dosage compensation (Bachtrog et al 2010). All of these hypotheses invoke natural selection, differing only in the particular selective agent responsible for driving movement.…”