Multi-genome comparisons reveal gain-and-loss evolution of anti-Mullerian hormone receptor type 2 as a candidate master sex-determining gene in Percidae

Author:

Kuhl HeinerORCID,Euclide Peter T.ORCID,Klopp ChristopheORCID,Cabau CédricORCID,Zahm MargotORCID,Lopez-Roques CélineORCID,Iampietro CaroleORCID,Kuchly ClaireORCID,Donnadieu CécileORCID,Feron RomainORCID,Parrinello HuguesORCID,Poncet CharlesORCID,Jaffrelo Lydia,Confolent Carole,Wen MingORCID,Herpin AmauryORCID,Jouanno ElodieORCID,Bestin AnastasiaORCID,Haffray PierrickORCID,Morvezen RomainORCID,de Almeida Taina RochaORCID,Lecocq ThomasORCID,Schaerlinger BéréniceORCID,Chardard DominiqueORCID,Żarski DanielORCID,Larson Wesley A.ORCID,Postlethwait John H.ORCID,Timirkhanov SerikORCID,Kloas WernerORCID,Wuertz SvenORCID,Stöck MatthiasORCID,Guiguen YannORCID

Abstract

Abstract Background The Percidae family comprises many fish species of major importance for aquaculture and fisheries. Based on three new chromosome-scale assemblies in Perca fluviatilis, Perca schrenkii, and Sander vitreus along with additional percid fish reference genomes, we provide an evolutionary and comparative genomic analysis of their sex-determination systems. Results We explored the fate of a duplicated anti-Mullerian hormone receptor type-2 gene (amhr2bY), previously suggested to be the master sex-determining (MSD) gene in P. flavescens. Phylogenetically related and structurally similar amhr2 duplicates (amhr2b) were found in P. schrenkii and Sander lucioperca, potentially dating this duplication event to their last common ancestor around 19–27 Mya. In P. fluviatilis and S. vitreus, this amhr2b duplicate has been likely lost while it was subject to amplification in S. lucioperca. Analyses of the amhr2b locus in P. schrenkii suggest that this duplication could be also male-specific as it is in P. flavescens. In P. fluviatilis, a relatively small (100 kb) non-recombinant sex-determining region (SDR) was characterized on chromosome 18 using population-genomics approaches. This SDR is characterized by many male-specific single-nucleotide variations (SNVs) and no large duplication/insertion event, suggesting that P. fluviatilis has a male heterogametic sex-determination system (XX/XY), generated by allelic diversification. This SDR contains six annotated genes, including three (c18h1orf198, hsdl1, tbc1d32) with higher expression in the testis than in the ovary. Conclusions Together, our results provide a new example of the highly dynamic sex chromosome turnover in teleosts and provide new genomic resources for Percidae, including sex-genotyping tools for all three known Perca species.

Funder

Agence Nationale de la Recherche

Deutsche Forschungsgemeinschaft

Leibniz-Institut für Gewässerökologie und Binnenfischerei (IGB) im Forschungsverbund Berlin e.V.

Publisher

Springer Science and Business Media LLC

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