Faster-Z in Leptidea

The faster-Z/X hypothesis predicts that sex-linked genes should diverge faster than autosomal genes and may therefore play important roles in speciation. However, studies across different lineages have shown mixed support for this effect, a variation that has been explained by various evolutionary mechanisms. So far, most analyses have focused on systems with old and well differentiated sex chromosomes, but less is known about divergence of more recently acquired neo-sex chromosomes. In the female heterogametic order Lepidoptera (moths and butterflies), fusions between the ancestral Z chromosome and autosomes are relatively frequent, but the evolutionary dynamics of neo Z-linked genes have not been explored in detail. Here, we analysed the faster-Z effect in Leptidea sinapis, a butterfly with an exceptionally reorganized genome and three Z chromosomes. We show that the neo-Z chromosomes have been acquired in a stepwise fashion, resulting in distinct strata of differentiation and masculinization. While Z-linked divergence generally seems to have been driven by adaptive processes, the relative effects of selection and drift showed a temporal trend where selection has been more prevalent for genes located on older Z linked regions, causing increased divergence of Z-linked genes with female-biased expression. In contrast, the intensity of selection on genes located on the most recently acquired neo-Z chromosome (Z3) appears to have been hampered by the presence of gametologs on the largely intact, homologous neo-W chromosome. However, the intermediately aged neo-Z chromosome (Z2), which is completely differentiated from W gametologs, showed less evolutionary constraint than the ancestral Z, resulting in particularly fast evolution. Our results therefore support that neo-sex chromosomes can constitute temporary hot-spots of adaptation and divergence. The underlying dynamics are likely causally linked to shifts in selective constraints, evolution of gene expression and the degeneration of W-linked gametologs which gradually expose Z-linked genes to selection.