Genomic origins and evolution of neo-sex chromosomes in Pacific Island birds

The standard model of sex chromosome evolution is based on ancient XY or ZW systems. Young neo-sex chromosomes that form via the translocation of autosomal material to preexisting sex chromosomes provide materials to study early events in sex chromosome evolution. Neo-sex chromosomes are taxonomically widespread but, until recently, appeared to be rare in female-heterogametic taxa, including birds. Here, we report on the comparative evolutionary genomics of newly discovered neo-Z and neo-W sex chromosomes in two Pacific Island birds, the honeyeater species, Myzomela tristrami and M. cardinalis. Our results show that 19 to 21 Mya, ~85% of chr5, an autosome, translocated to the pseudoautosomal region (PAR) of an ancestral sex chromosome (Z or W) and rapidly recombined onto its heterolog, leaving the remainder of chr5 to segregate as a remnant autosome. A large inversion then established a nonrecombining (NR) neo-W region and a neo-PAR. The accumulation of at least seven additional inversions created interspersed blocks of ancestral and neo-W sequence, without expanding the NR region. The neo-W experienced mass invasion by endogenous retrovirus repeats, a reduced efficacy of selection, and functional degeneration. Many of our observations are consistent with predictions of the standard model, whereas others highlight idiosyncrasies of neo-sex chromosomes that arise via translocation of autosomal sequence to ancestral sex chromosomes. We speculate, in particular, that the repository of retrotransposons on the ancestral W may have been an accelerant in the evolution of neo-W structure, content, and functional degeneration.