Ancient homomorphy of molluscan sex chromosomes sustained by reversible sex-biased genes and sex determiner translocation.

Abstract

Contrary to classic theory prediction, sex-chromosome homomorphy is prevalent in the animal kingdom but it is unclear how ancient homomorphic sex chromosomes avoid chromosome-scale degeneration. Molluscs constitute the second largest, Precambrian-originated animal phylum and have ancient, uncharacterized homomorphic sex chromosomes. Here, we profile eight genomes of the bivalve mollusc family of Pectinidae in a phylogenetic context and show 350 million years sex-chromosome homomorphy, which is the oldest known sex-chromosome homomorphy in the animal kingdom, far exceeding the ages of well-known heteromorphic sex chromosomes such as 130-200 million years in mammals, birds and flies. The long-term undifferentiation of molluscan sex chromosomes is potentially sustained by the unexpected intertwined regulation of reversible sex-biased genes, together with the lack of sexual dimorphism and occasional sex chromosome turnover. The pleiotropic constraint of regulation of reversible sex-biased genes is widely present in ancient homomorphic sex chromosomes and might be resolved in heteromorphic sex chromosomes through gene duplication followed by subfunctionalization. The evolutionary dynamics of sex chromosomes suggest a mechanism for 'inheritance' turnover of sex-determining genes that is mediated by translocation of a sex-determining enhancer. On the basis of these findings, we propose an evolutionary model for the long-term preservation of homomorphic sex chromosomes.