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

Kuhl H. Euclide P.T. Klopp C. Cabau C. Zahm M. Lopez-Roques C. Iampietro C. Kuchly C. Donnadieu C. Feron R. Parrinello H. Poncet C. Jaffrelo L. Confolent C. Wen M. Herpin A. Jouanno E. Bestin A. Haffray P. Morvezen R. de Almeida T.R. Lecocq T. Schaerlinger B. Chardard D. Żarski D. Larson W.A. Postlethwait J.H. Timirkhanov S. Kloas W. Wuertz S. Stöck M. Guiguen Y.
December 2024 BioMed Central Ltd

BMC Biology
2024 #22 Issue 1

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.

Genome , Perches , Pikeperches , Sex chromosomes , Sex-determination

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Leibniz-Institute of Freshwater Ecology and Inland Fisheries – IGB (Forschungsverbund Berlin), Müggelseedamm 301/310, Berlin, D-12587, Germany
Department of Forestry and Natural Resources

Sigenae, Plateforme Bioinformatique, Genotoul, BioinfoMics, UR875 Biométrie et Intelligence Artificielle, INRAE, Castanet-Tolosan, France
Sigenae, GenPhySE, Université de Toulouse, INRAE, ENVT, Castanet-Tolosan, France
INRAE, US 1426, GeT-PlaGe, Genotoul, Castanet-Tolosan, France
Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland
Swiss Institute of Bioinformatics, Lausanne, Switzerland
Montpellier GenomiX (MGX), c/o Institut de Génomique Fonctionnelle, 141 rue de la Cardonille, Montpellier Cedex 05, 34094, France
GDEC Gentyane, INRAE, Université Clermont Auvergne, Clermont-Ferrand, France
INRAE, LPGP, Rennes, 35000, France
State Key Laboratory of Developmental Biology of Freshwater Fish, College of Life Science, Hunan Normal University, Changsha, China
SYSAAF, Station INRAE-LPGP, Campus de Beaulieu, Rennes Cedex, 35042, France
University of Lorraine, INRAE, L2A, Nancy, France
Department of Gamete and Embryo Biology, Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, ul. Tuwima 10, 10-748, Olsztyn, Poland
National Oceanographic and Atmospheric Administration, National Marine Fisheries Service, Alaska Fisheries Science Center, 17109 Point Lena Loop Road, Auke Bay LaboratoriesJuneau, 99801, AK, United States
Institute of Neuroscience, University of Oregon, Eugene, 97403, OR, United States
Sea Biology LLP, Almaty, Kazakhstan

Leibniz-Institute of Freshwater Ecology and Inland Fisheries – IGB (Forschungsverbund Berlin)
Department of Forestry and Natural Resources

Sigenae
Sigenae
INRAE
Department of Ecology and Evolution
Swiss Institute of Bioinformatics
Montpellier GenomiX (MGX)
GDEC Gentyane
INRAE
State Key Laboratory of Developmental Biology of Freshwater Fish
SYSAAF
University of Lorraine
Department of Gamete and Embryo Biology
National Oceanographic and Atmospheric Administration
Institute of Neuroscience
Sea Biology LLP

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