Assembly and analysis of Sinipercidae fish sex chromosomes reveals that a supergene drives sex chromosome origin and turnover.

Abstract

The sex chromosomes of fish are usually homomorphic and recently derived, making them an ideal model to understand the origin and evolution of sex chromosomes in vertebrates. Here, combined Pacbio, Hi-C, and Illumina sequencing of the male mandarin fish (Siniperca chuatsi) genome enabled the assembly of a high-quality chromosome-level genome, including highly resolved X and Y chromosome assemblies. Genome wide association study (GWAS) and coverage information analysis revealed a 2.0 Mbp sex determining region (SDR). A Y-specific duplication of the anti-Müllerian hormone (amh) gene, amhy, was identified that encoded a truncated AMH protein. Loss of function and overexpression experiments demonstrated that amhy may act as a male sex-determining gene (SDG). GWAS led to the identification of a common sex chromosome (Chr24) and SDG (amhy) in S. scherzeri, while another sex chromosome (Chr11) was identified in Coreoperca whiteheadi. Interestingly, completely conserved protein coding sequences of amhy were commonly identified in male S. chuatsi, S. scherzeri, and S. knerii. These results support a classic model for the origin and evolution of early sex chromosomes and suggest that amhy is a super SDG that can drive the origin and turnover of sex chromosome in vertebrates.