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. In this study, we first identify an 80 kbp genomic region on LG3 as the sex-determining region (SDR) using whole-genome resequencing data of family crosses of a WL population. We then verify this region as the SDR in most other WL populations and demonstrate a potentially ongoing sex chromosome turnover in admixed marine populations where the evolutionarily younger and homomorphic LG3 sex chromosome replaces the older and heteromorphic LG12 sex chromosome. The results provide a rare glimpse of sex chromosome turnover in the wild and indicate the possible existence of additional yet undiscovered sex chromosome diversity in Pungitius sticklebacks.

SLRfinder: A method to detect candidate sex‐linked regions with linkage disequilibrium clustering

“…LG3:17260000-17340000; Yi et al, 2024) in the Western European lineage (WL). Both lineages have the XX/XY sex determination.…”

“…Both lineages have the XX/XY sex determination. In addition, two UK populations have unidentified sex chromosomes, and a hybrid Polish population was identified with both types of sex chromosomes ( 10LG3-determined males and 1 LG12-determined male; Yi et al, 2024). The WGS data of nine-spined sticklebacks were published in a previous study (Feng et al, 2022) and available on ENA (project PRJEB39599).…”

“…To assess the statistical power of SLRfinder, we first applied it to To test the effects of sex ratios, we used the previously identified genetic sexes of nine-spined sticklebacks (Yi et al, 2024) and only included the seven WL populations and the 24 EL populations that have at least four individuals per sex. We kept the same total number of individuals (n = 28 in WL, n = 96 in EL) and modified sex ratios by randomly selecting two individuals per sex per population (even sex ratio), or one individual from one sex and three from the other in each population (sex ratios 1:3 or 3:1).…”

“…Early studies in mammals and birds have demonstrated highly conserved and heteromorphic (i.e., having different morphologies) sex chromosomes with conserved sex-determining genes and degenerated Y or W chromosomes (Cortez et al, 2014). On the contrary, accumulating studies have found less conserved but much more labile sex chromosomes that may be different between closely related lineages in fish, amphibians, reptiles and some invertebrates (Dufresnes et al, 2015;Furman et al, 2020;Hearn et al, 2022;Jeffries et al, 2018;Myosho et al, 2012;Ogata et al, 2021;Tree of Sex Consortium, 2014;Vicoso, 2019;Yi et al, 2024). These labile sex chromosomes tend to be homomorphic (i.e., sex chromosomes having indistinguishable morphologies) and are featured by little or no degeneration, low inter-sex differentiation, variable sex-determining genes and sex-linked regions (SLRs) restricted to narrow genomic regions.…”

“…This method does not require known phenotypic sexes, but it assumes that only X/Z scaffolds are assembled in the reference genome, which is practically the same as requiring a reference genome of the homogametic sex. In addition, these available methods are mostly based on sequencing depth (RADSex and SATC) or depth and heterozygosity (PSASS, FindZX), but many studies have shown that depth may not differ between sexes on labile sex chromosomes that are homomorphic and have narrow SLRs (Jeffries et al, 2022;Yi et al, 2024). Therefore, new methods are needed to help identify labile sex chromosomes in non-model species.…”