Sexual reproduction is widespread in the animal kingdom and sexual evolution has been honored as “the queen of problems in evolutionary biology”. To date, our understanding of sexual evolution is largely biased to animals with heteromorphic sex chromosomes, which formed the classic theory of sex chromosome evolution. Molluscs constitute the second largest, Precambrian-originated animal phylum with a diversity of sexual systems, including simultaneous hermaphroditism, sequential hermaphroditism, strict gonochorism and even parthenogenesis. However, this ideal animal group for studying sexual evolution has long been neglected partly for its uncharacterized homomorphic sex chromosomes and sex-determining genes (SDGs). Our group has been focusing on the ancient bivalve mollusc family of Pectinidae and carried out systematic studies using histology, genomics and regulatome methods. We have traced the gonadal sex differentiation of scallop and accurately determined the molecular sex differentiation prior to morphological sex differentiation. We identified the first characterized 350-Myr homomorphic sex chromosomes (representing the oldest known sex-chromosome in the animal kingdom) and SDGs (e.g., FOXL2) in Mollusca through the large-scale sexual genome sequencing. We report the novel mechanism for "inheritance" turnover of SDGs by regulatory element translocation. The long-term undifferentiation of scallop sex chromosomes were surprisingly found to be potentially sustained by intertwined regulation of reversible sex-biased genes (SBGs). Recently, we have introduced the dwarf surfclam Mulinia lateralis as the mollusc model to further study the bisexual regulatory flexibility by focusing on the molecular regulation between SDGs and SBGs. Our findings provide not only novel insights into the evolution and regulation of ancient homomorphic sex chromosomes, but also guidance for establishing the sex control breeding of scallop.
Novel insights from Mollusca into ancient sex chromosome evolution and sexual regulation