The origin, evolution, and translocation of sex chromosomes in Silurus catfish mediated by transposons.

Abstract

Background: Sex chromosome (SC) evolution is a longstanding topic of focus in evolutionary biology. Teleosts often exhibit rapid turnover of SCs and sex-determining (SD) genes, alongside a diverse range of SC differentiation mechanisms.

Results: On the basis of new chromosome-scale assemblies of three Silurus species (S. microdorsalis, S. glanis, and S. lanzhouensis) and two outgroup species (Pterocryptis cochinchinensis and Kryptopterus bicirrhis), along with our previous assemblies of S. meridionalis and S. asotus, we traced the evolution of SC in the Silurus genus (Siluriformes), following the fate of the known SD gene amhr2y. Phylogenetic analysis showed that amhr2y occurred at least before the divergence of Pterocryptis, Kryptopterus, and Silurus and lost in P. cochinchinensis and K. bicirrhis. Chr24 has become the SC in the ancestor of five Silurus species due to the duplication-and-translocation of amhr2 mediated by LTR transposon. Then, a proto Y was formed and maintained with a shared 60 kb male-specific region of the Y chromosome (MSY) by transposable elements (TEs) expansion and gene gathering. Due to the continuous TEs accumulation, genes other than amhr2y in MSYs have degenerated or been lost, while non-recombinant regions continue to expend, forming MSYs of different sizes in different Silurus species (from 320 to 550 kb). Two turnover events, one homologous (from the left arm to the right arm of Chr24) and one nonhomologous (from Chr24 to Chr5), occurring among five Silurus species were possibly mediated by hAT and Helitron transposons.

Conclusions: Our results on the dynamic evolutionary trajectory of SD gene amhr2y, MSYs, and SCs in Silurus catfish indicated the variability and diversity of fish SCs and confirmed that frequent turnover is an important way to maintain the homology and low differentiation of fish SCs.