A Study of Faster-Z Evolution in the Great Tit (Parus major)

Abstract

Sex chromosomes contribute substantially to key evolutionary processes such as speciation and adaptation. Several theories suggest that evolution could occur more rapidly on sex chromosomes, but currently our understanding of whether and how this occurs is limited. Here, we present an analysis of the great tit (Parus major) genome, aiming to detect signals of faster-Z evolution. We find mixed evidence of faster divergence on the Z chromosome than autosomes, with significantly higher divergence being found in ancestral repeats, but not at 4- or 0-fold degenerate sites. Interestingly, some 4-fold sites appear to be selectively constrained, which may mislead analyses that use these sites as the neutral reference (e.g., dN/dS). Consistent with other studies in birds, the mutation rate is significantly higher in males than females, and the long-term Z-to-autosome effective population size ratio is only 0.5, significantly lower than the expected value of 0.75. These are indicative of male-driven evolution and high variance in male reproductive success, respectively. We find no evidence for an increased efficacy of positive selection on the Z chromosome. In contrast, the Z chromosome in great tits appears to be affected by increased genetic drift, which has led to detectable signals of weakened intensity of purifying selection. These results provide further evidence that the Z chromosome often has a low effective population size, and that this has important consequences for its evolution. They also highlight the importance of considering multiple factors that can affect the rate of evolution and effective population sizes of sex chromosomes.

Keywords: Z chromosome; effective population size; genetic drift; positive selection; sex chromosomes.

Fig. 1.

—Comparing divergence levels between the Z chromosome (blue) and the autosomes (orange) for (a) different regions of interest, (b) 0-fold versus 4-fold changes (d₀/d₄), and (c) 0-fold changes compared with changes in ancestral repeats (d₀/d_AR). Error bars show 95% CIs.

Fig. 2.

—Nucleotide diversity (a) and Tajima’s D (b) for different regions of the genome on both the Z chromosome (blue) and the autosomes (orange). Error bars show 95% CIs.