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.
Highlights
Sex chromosomes play a significant role in key evolutionary processes such as speciation and adaptation (Charlesworth et al 1987; Vicoso and Charlesworth 2006)
If the rate of evolution is taken to be the speed at which allele frequencies change over time, it is possible for other factors such as increased genetic drift or the decreased efficacy of purifying selection to contribute to a faster rate of evolution on the Z chromosome
The scripts used in the analysis can be found on https://github.com/henryjuho/ hayes_et_al. On both types of chromosomes, the level of divergence was significantly lower at 0-fold sites than the putatively neutral sites (4-fold and ancestral repeats; bootstrapping P < 0.05; fig. 1a), indicating that 0-fold sites have been subject to evolutionary constraints and purifying selection
Summary
Sex chromosomes play a significant role in key evolutionary processes such as speciation and adaptation (Charlesworth et al 1987; Vicoso and Charlesworth 2006). It reduces the effective population size (Ne) of the Z chromosome (NeZ) to 3=4 of that of the autosomes (NeA), which could increase the amount of genetic drift (Charlesworth 2009; Ellegren 2009). This could result in relaxed purifying selection on deleterious mutations and accelerated rates of fixation of mildly deleterious mutations on the Z chromosome (Vicoso and Charlesworth 2006; Charlesworth 2009)
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