Gene traffic mediated by transposable elements shaped the dynamic evolution of ancient sex chromosomes of varanid lizard

Lizards exhibit rapid turnovers and a much greater diversity of sex determination mechanisms compared to birds and eutherians. This makes the conserved ZW sex chromosomes of anguimorph lizards originated over 115 million years ago a seeming exception. We recently discovered in an anguimorph lizard Varanus acanthurus (Vac) that its entire W chromosome (chrW), but not chrZ is homologous to part of the chr2 by cytogenetic mapping, suggesting a complex history of its sex chromosome evolution yet to be elucidated. To address this, we assembled a chromosome-level genome, and provided evidence that the Vac sex chromosome pair had undergone at least three times of recombination suppression, forming a similar pattern of evolutionary strata to that of birds or mammals. We identified the putative sex-determining genes in the oldest evolutionary stratum that had first lost recombination. Comparison to other lizard genomes dated the stepwise propagation of specific retrotransposon subfamilies shared by chrW and chr2 to the varanid ancestor. These retrotransposons are also enriched near the duplicated genes shared by the two chromosomes and probably mediated the recruitment of many autosomal genes that rejuvenated the degenerating chrW, including members of a large vomeronasal chemosensory receptor gene family V2R. Our results challenge the canonical model of sex chromosome evolution, and suggest that the W or Y chromosome as a refugium of repetitive elements, may recurrently recruit short-lived functional genes responsible for sexual dimorphisms during its long-term course of degeneration.