The evolutionary dynamics of sexually antagonistic mutations in pseudoautosomal regions of sex chromosomes

Abstract

Sex chromosomes can evolve gene contents that differ from the rest of the genome, as well as larger sex differences in gene expression compared with autosomes. This probably occurs because fully sex-linked beneficial mutations substitute at different rates from autosomal ones, especially when fitness effects are sexually antagonistic (SA). The evolutionary properties of genes located in the recombining pseudoautosomal region (PAR) of a sex chromosome have not previously been modeled in detail. Such PAR genes differ from classical sex-linked genes by having two alleles at a locus in both sexes; in contrast to autosomal genes, however, variants can become associated with gender. The evolutionary fates of PAR genes may therefore differ from those of either autosomal or fully sex-linked genes. Here, we model their evolutionary dynamics by deriving expressions for the selective advantages of PAR gene mutations under different conditions. We show that, unless selection is very strong, the probability of invasion of a population by an SA mutation is usually similar to that of an autosomal mutation, unless there is close linkage to the sex-determining region. Most PAR genes should thus evolve similarly to autosomal rather than sex-linked genes, unless recombination is very rare in the PAR.

Keywords: Gene expression; pseudoautosomal region; recombination; sex chromosomes; sexual antagonism.

Figure 1

The genetic model. The figure shows an XY sex chromosome pair with a gene (indicated by a short vertical gray line) in the PAR, at a genetic map distance of r from the male-determining, or male-specific region.

Figure 2

Results for the invasion of a population by male-benefit alleles. The y-axis shows the net strength of selection (σ, see text), and the x-axis is the frequency of recombination with the fully sex-linked region; and the r = ½ case represents autosomal loci. The parameters are defined in Table 1. The figure shows examples of the s = 0.1 and 0.01 cases, with h = 0.5. Results are shown for two values of the parameter c (0.5 and 2), where c < 1 corresponds to stronger selection in males than females and c > 1 to stronger selection in females. In the former situation, the mutant allele can invade with any r value; in the latter situation, invasion occurs only if r is below a threshold value (see text). Small dots are the values from equation (A4), large squares are from equation (2), and crosses from equation (4).

Figure 3

Results for the invasion of a population by male-benefit alleles in a situation when s = 0.01, h = 0.5, and c = 1, so that |1 – h(1 + c)| >> s, the condition for the validity of equation (2), is not met. Small dots are the values from equation (A4), crosses are from equation (1), and squares from equation (2).

Figure 4

Results for the invasion of a population by female-benefit alleles. The figure is organised and labeled as in Figure 2, but the two values of the c parameter are 0.75 and 2, because with c = 0.5 the mutant never invades. Small dots are the values from equation (A4), crosses are from equation (8), and squares from equation (6).