Selective regimes and evolutionary dynamics of Z and W gametologs across an expanded avian neo-sex chromosome

Abstract Sex-chromosome evolution is characterised by Y/W degeneration and its consequences for selection on X/Z-linked recessive mutations in the heterogametic sex, yet how functional constraints modulate the evolutionary dynamics of Z–W gametologs remains poorly resolved. We addressed this question in larks (Alaudidae), a lineage carrying enlarged neo-sex chromosomes with multiple evolutionary strata formed through repeated translocations and successive recombination-suppression events. Using whole-genome sequences of males and females of two Alauda species, we analysed 1,759 Z–W gametologs. We found that W-gene degeneration was governed primarily by evolutionary time and intrinsic gene features: long genes were lost earliest, although this tendency was mitigated by gene essentiality, as indicated by high haploinsufficiency scores. Z-linked genes lacking a functional W counterpart exhibited higher non-synonymous divergence than Z genes retaining a functional W, consistent with selection-driven faster-Z evolution. The strongest signature of purifying selection, comparable to that of pseudoautosomal genes, was observed in haploinsufficient Z-linked genes, which were also more likely to retain W gametologs. Although W genes generally diverged faster, their selection signatures covaried with those of Z and with haploinsufficiency, suggesting partially shared Z–W evolutionary dynamics. Notably, a small subset of W genes showed intensified or positive selection, including several genes associated with putative female-specific functions. Together, our results demonstrate that gene essentiality slows functional divergence on both Z and W, modulates faster-Z dynamics and enables key W genes to remain functional – and potentially advantageous for females – for millions of generations after recombination cessation.