Recent discoveries of sex chromosome diversity across the tree of life have challenged the canonical model of conserved sex chromosome evolution and evoked new theories on labile sex chromosomes that maintain less differentiation and frequent turnover. However, theories of labile sex chromosome evolution lack direct empirical support due to the paucity of case studies demonstrating ongoing sex chromosome turnover in nature. Two divergent lineages (viz. WL & EL) of nine-spined sticklebacks (Pungitius pungitius) with different sex chromosomes (linkage group [LG] 12 in the EL, unknown in the WL) hybridize in a natural secondary contact zone in the Baltic Sea, providing an opportunity to study ongoing turnover between coexisting sex chromosomes. We first identified an 80 kbp genomic region on LG3 as the sex-determining region (SDR) in the WL using whole-genome resequencing data of family crosses. We then verified this region as the SDR in most other WL populations, and demonstrated a turnover in admixed marine populations where the evolutionarily younger and homomorphic LG3 sex chromosomes replace the older and heteromorphic LG12 sex chromosomes. Our results provide a rare evolutionary snapshot on the process of a turnover, supporting the hypothesis of sex chromosome turnover driven by selection against deleterious mutation load.
Sex chromosome turnover in hybridizing stickleback lineages