Abstract
Atlantic Halibut (Hippoglossus hippoglossus) has a X/Y genetic sex determination system, but the sex determining factor is not known. We produced a high-quality genome assembly from a male and identified parts of chromosome 13 as the Y chromosome due to sequence divergence between sexes and segregation of sex genotypes in pedigrees. Linkage analysis revealed that all chromosomes exhibit heterochiasmy, i.e. male-only and female-only meiotic recombination regions (MRR/FRR). We show that FRR/MRR intervals differ in nucleotide diversity and repeat class content and that this is true also for other Pleuronectidae species. We further show that remnants of a Gypsy-like transposable element insertion on chr13 promotes early male specific expression of gonadal somatic cell derived factor (gsdf). Less than 4.5 MYA, this male-determining element evolved on an autosomal FRR segment featuring pre-existing male meiotic recombination barriers, thereby creating a Y chromosome. Our findings indicate that heterochiasmy may facilitate the evolution of genetic sex determination systems relying on linkage of sexually antagonistic loci to a sex-determining factor.
Highlights
In contrast to the highly conserved mammalian and avian sex determination systems, fish display much more plasticity and turnover of sex chromosomes and sex determination systems, with many already described systems for genetic control of sex being young in comparison to their mammalian and avian counterparts [1]
We show that males have much higher gene activity of the gene gonadal somatic cell derived factor, which is located on the sex chromosomes and has a role in testicular development
Our interpretation is that following an ancient Gypsy element insertion on the autosomal progenitor of chr13, this element degraded and left a remnant long terminal repeat (LTR), which acts as a promoter driving the expression of gsdf ectopically during development of XY individuals, making carriers develop into phenotypic males
Summary
In contrast to the highly conserved mammalian and avian sex determination systems, fish display much more plasticity and turnover of sex chromosomes and sex determination systems, with many already described systems for genetic control of sex being young in comparison to their mammalian and avian counterparts [1]. Several master sex determining (MSD) genes have been described in teleosts, most of which belong to one of three protein families (DMRT, SOX, and TGF-ß and its signaling pathway) [8], and these have originated either from sub- or neofunctionalization of duplicated genes, or by allelic diversification [1]. Exceptions to these protein families are found for salmonids, where sdy is the MSD gene [9] and recently the breast cancer anti-estrogen resistance protein 1 (BCAR1) and bone morphogenetic protein receptor type-1B (bmpr1b) have been reported as MSD genes in catfish (Ictalurus punctatus) [10] and Atlantic herring (Clupea harengus) [11], respectively. A wide range of systems have evolved for genetic control of sex determination in fish and additional complexity is added by environmental variables contributing to sex determination in some species
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