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Abstract
Whole-genome duplication and genome compaction are thought to have played important roles in teleost fish evolution. Ayu (or sweetfish), Plecoglossus altivelis, belongs to the superorder Stomiati, order Osmeriformes. Stomiati is phylogenetically classified as sister taxa of Neoteleostei. Thus, ayu holds an important position in the fish tree of life. Although ayu is economically important for the food industry and recreational fishing in Japan, few genomic resources are available for this species. To address this problem, we produced a draft genome sequence of ayu by whole-genome shotgun sequencing and constructed linkage maps using a genotyping-by-sequencing approach. Syntenic analyses of ayu and other teleost fish provided information about chromosomal rearrangements during the divergence of Stomiati, Protacanthopterygii and Neoteleostei. The size of the ayu genome indicates that genome compaction occurred after the divergence of the family Osmeridae. Ayu has an XX/XY sex-determination system for which we identified sex-associated loci by a genome-wide association study by genotyping-by-sequencing and whole-genome resequencing using wild populations. Genome-wide association mapping using wild ayu populations revealed three sex-linked scaffolds (total, 2.03 Mb). Comparison of whole-genome resequencing mapping coverage between males and females identified male-specific regions in sex-linked scaffolds. A duplicate copy of the anti-Müllerian hormone type-II receptor gene (amhr2bY) was found within these male-specific regions, distinct from the autosomal copy of amhr2. Expression of the Y-linked amhr2 gene was male-specific in sox9b-positive somatic cells surrounding germ cells in undifferentiated gonads, whereas autosomal amhr2 transcripts were detected in somatic cells in sexually undifferentiated gonads of both genetic males and females. Loss-of-function mutation for amhr2bY induced male to female sex reversal. Taken together with the known role of Amh and Amhr2 in sex differentiation, these results indicate that the paralog of amhr2 on the ayu Y chromosome determines genetic sex, and the male-specific amh-amhr2 pathway is critical for testicular differentiation in ayu.
Highlights
Gonadal sex determination, the process that initiates the development of the testis or ovary from the gonadal primordium, is a universal feature in vertebrate development
Ayu belongs to the superorder Stomiati and the order Osmeriformes
Association mapping revealed a duplicate copy of the anti-Mullerian hormone type-II receptor gene located within a male-specific region
Summary
The process that initiates the development of the testis or ovary from the gonadal primordium, is a universal feature in vertebrate development. Sex-determining genes are highly diverse among vertebrates, especially among teleost fishes [3]. Dmrt1bY/dmy, gsdfY, and sox have all been identified as sex-determining genes in Oryzias fishes [4–7]; and the immune-related gene sdY determines sex in salmonids [8]. In Seriola fishes, sex is most likely determined by female-specific synthesis of estrogens by hsd17b1, encoded by a gene located on the W chromosome [9]. The Y-linked duplicate of amhr is a strong candidate for the sex-determining gene [14]. Sex-determination genes seem to evolve frequently from genes that function in gonadal sex differentiation pathways, there are exceptions, like in salmonids [11]
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