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

Lizards usually exhibit frequent turnovers and a much greater diversity of sex determination mechanisms compared to birds and mammals, with the conserved ZW sex chromosomes of anguimorph lizards originating over 115 million years ago a seeming exception. We previously discovered in an anguimorph lizard Varanus acanthurus (Vac) whose entire chrW, but not chrZ is homologous to part of the chr2 by cytogenetic mapping, suggesting its complex history of sex chromosome evolution yet to be elucidated. To address this, we assemble a chromosome-level genome, and provide evidence that the Vac sex chromosome pair has undergone at least two times of recombination loss, producing a pattern of evolutionary strata like that of birds and mammals. Comparison to other lizard genomes date the stepwise propagation of specific retrotransposon subfamilies enriched near the duplicated gene pairs on the chrW and chr2 to the varanid ancestor. These retrotransposons probably have mediated the recruitment and amplification of autosomal genes on the chrW, including members of a large vomeronasal chemosensory receptor gene family V2R. Our results 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.