Sex chromosome turnover in hybridizing stickleback lineages

Abstract

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 undergo 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) using whole-genome resequencing data of family crosses. We then verified this region as the SDR in most other WL populations and demonstrated an ongoing sex chromosome turnover in admixed marine populations where the evolutionarily younger and homomorphic LG3 sex chromosomes replace the older and heteromorphic LG12 sex chromosomes. The results provide a rare glimpse of ongoing sex chromosome turnover and indicate possible existence of additional but yet undiscovered sex chromosome diversity in Pungitius sticklebacks. TeaserEvolutionarily young sex chromosomes replace the older ones in the hybrid zone of European Pungitius stickleback lineages.