Evolution of dosage compensation under sexual selection differs between X and Z chromosomes

Abstract

Complete sex chromosome dosage compensation has more often been observed in XY than ZW species. In this study, using a population genetic model and the chicken transcriptome, we assess whether sexual conflict can account for this difference. Sexual conflict over expression is inevitable when mutation effects are correlated across the sexes, as compensatory mutations in the heterogametic sex lead to hyperexpression in the homogametic sex. Coupled with stronger selection and greater reproductive variance in males, this results in slower and less complete evolution of Z compared with X dosage compensation. Using expression variance as a measure of selection strength, we find that, as predicted by the model, dosage compensation in the chicken is most pronounced in genes that are under strong selection biased towards females. Our study explains the pattern of weak dosage compensation in ZW systems, and suggests that sexual selection plays a major role in shaping sex chromosome dosage compensation.

Figure 1. The evolution of dosage compensation on Z and X chromosomes.

Expected gene expression is shown for males (blue) and females (red) under a very low (ρ=0.1, dotted line), intermediate (ρ=0.5, dashed line) and strong inter-sexual correlation (ρ=0.8, solid line)—(see equations (13) and (14) for dynamics). a,b show equal selection in males and females (S_m=S_f=0.5); c,d show stronger selection in males (S_m=1, S_f=0.1). Evolutionary time refers to the number of generations, ignoring the time taken by successive mutations to fix. Expression is scaled according to the initial degradation z₀ of expression in the heterogametic sex due to the loss of one gene copy, which here is set at z₀=1. Other parameters were also held equal across the two sex chromosome systems (N_eX=N_eZ=1125, μ=0.0003).

Figure 2. Variance in male reproductive success and the evolution of dosage compensation.

Stochastic evolutionary trajectories of male (blue) and female (red) expression for (a) Z-linked and (b) X-linked genes (see equations (11) and (12) for dynamics). Levels of expression are shown for low (η=1, light shade), intermediate (η=3, intermediate shade) or high (η=10, dark shade) degrees of male reproductive variance (the number of successful breeding females is set at 1,000). A sample of 5 trajectories is shown for each parameter value. Variance in heterogametic sex expression for (c) Z-linked and (d) X-linked genes after the end of the simulation is shown as a frequency distribution for 1,000 replicates. Selection is stronger on males than on females (S_m=1, S_f=0.2), inter-sexual correlation is relatively strong (ρ=0.6) and the mutation rate is μ=0.0003.

Figure 3. Selection on gene expression and dosage compensation in the chicken liver.

The figure shows the strength of sexually concordant selection and the measure of male bias in selection strength for liver-expressed genes used in our analysis. Dosage compensated genes (0.8