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      Mismatches between the genetic and phenotypic sex in the wild Kou population of Nile tilapia Oreochromis niloticus

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          Abstract

          Sex determination and sex chromosomes can be very diverse between teleost species. The group of tilapias shows a polymorphism in sex determination not only between closely related species but also between domestic strains within a species. In the Nile tilapia, the major effect genes and therefore the Y chromosome have been located on either linkage group 1 (LG1) or LG23 depending on the strains. In a Japanese strain, the sex determinant of LG23 (the amhY gene) has been identified as a duplicated amh (anti-Müllerian hormone) gene, with its gametolog found on the X chromosome ( amhX). AmhY is located in tandem with the amhΔY gene (a truncated form) on the Y chromosome. X and Y chromosome markers based on the amh genes have been validated only on a few domestic strains but not in wild populations. Here, we used four of these markers in order to examine (1) the possible variation in sex determination of a wild population of Nile tilapia living in Lake Kou (Burkina Faso), (2) putative polymorphisms for these amh copies and (3) the existence of sex reversed individuals in the wild. Our genotyping of 91 wild Kou individuals with the amh sex-diagnostic markers of LG23 showed that while phenotypic females were all XX, phenotypic males were either XY or XX. Progeny testing of eight of these XX males revealed that one of these males consistently sired all-female progenies, suggesting that it is a wild sex reversed male (which could result from high temperature effects). The other XX males gave balanced sex ratios, suggesting that sex is controlled by another locus (possibly on another LG) which may be epistatically dominant over the LG23 locus. Finally, identification of unexpected amh genotypes was found for two individuals. They produced either balanced or female-biased sex ratios, depending on the breeder with whom they were crossed, suggesting possible recombination between the X and the Y chromosomes.

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          Most cited references43

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          DMY is a Y-specific DM-domain gene required for male development in the medaka fish.

          Although the sex-determining gene Sry has been identified in mammals, no comparable genes have been found in non-mammalian vertebrates. Here, we used recombinant breakpoint analysis to restrict the sex-determining region in medaka fish (Oryzias latipes) to a 530-kilobase (kb) stretch of the Y chromosome. Deletion analysis of the Y chromosome of a congenic XY female further shortened the region to 250 kb. Shotgun sequencing of this region predicted 27 genes. Three of these genes were expressed during sexual differentiation. However, only the DM-related PG17 was Y specific; we thus named it DMY. Two naturally occurring mutations establish DMY's critical role in male development. The first heritable mutant--a single insertion in exon 3 and the subsequent truncation of DMY--resulted in all XY female offspring. Similarly, the second XY mutant female showed reduced DMY expression with a high proportion of XY female offspring. During normal development, DMY is expressed only in somatic cells of XY gonads. These findings strongly suggest that the sex-specific DMY is required for testicular development and is a prime candidate for the medaka sex-determining gene.
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            Sex chromosome specialization and degeneration in mammals.

            Sex chromosomes--particularly the human Y--have been a source of fascination for decades because of their unique transmission patterns and their peculiar cytology. The outpouring of genomic data confirms that their atypical structure and gene composition break the rules of genome organization, function, and evolution. The X has been shaped by dosage differences to have a biased gene content and to be subject to inactivation in females. The Y chromosome seems to be a product of a perverse evolutionary process that does not select the fittest Y, which may cause its degradation and ultimate extinction.
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              Tracing the emergence of a novel sex-determining gene in medaka, Oryzias luzonensis.

              Three sex-determining (SD) genes, SRY (mammals), Dmy (medaka), and DM-W (Xenopus laevis), have been identified to date in vertebrates. However, how and why a new sex-determining gene appears remains unknown, as do the switching mechanisms of the master sex-determining gene. Here, we used positional cloning to search for the sex-determining gene in Oryzias luzonensis and found that GsdfY (gonadal soma derived growth factor on the Y chromosome) has replaced Dmy as the master sex-determining gene in this species. We found that GsdfY showed high expression specifically in males during sex differentiation. Furthermore, the presence of a genomic fragment that included GsdfY converts XX individuals into fertile XX males. Luciferase assays demonstrated that the upstream sequence of GsdfY contributes to the male-specific high expression. Gsdf is downstream of Dmy in the sex-determining cascade of O. latipes, suggesting that emergence of the Dmy-independent Gsdf allele led to the appearance of this novel sex-determining gene in O. luzonensis.
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                Author and article information

                Contributors
                Journal
                PeerJ
                PeerJ
                peerj
                peerj
                PeerJ
                PeerJ Inc. (San Diego, USA )
                2167-8359
                18 September 2019
                2019
                : 7
                : e7709
                Affiliations
                [1 ]Unité de recherche aquaculture et biodiversité aquatique/Laboratoire d’études et de recherche sur les ressources naturelles et sciences de l’environnement, Université Nazi BONI , Bobo-Dioulasso, Burkina Faso
                [2 ]Institut de l’environnement et de recherches agricoles, Centre national de la recherche scientifique et technologique , Bobo-Dioulasso, Burkina Faso
                [3 ]Centre international de recherche-développement sur l’élevage en zone subhumide , Bobo-Dioulasso, Burkina Faso
                [4 ]ISEM, Université de Montpellier, CNRS, IRD, EPHE , Montpellier, France
                [5 ]UMR ISEM, CIRAD , Montpellier, France
                Article
                7709
                10.7717/peerj.7709
                6754722
                8a54acca-ffc3-4b7a-8d0a-2166e3a23b85
                ©2019 Sissao et al.

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.

                History
                : 20 March 2019
                : 20 August 2019
                Funding
                Funded by: UEMOA
                Funded by: PROGEVAL
                Funded by: WECARD/UEMOA
                Funded by: CLIMSEX
                Funded by: ANR project
                Award ID: ANR-15-CE02-0012
                This work was supported by the following projects: “Improved Fish Seed” funded by UEMOA, PROGEVAL funded by WECARD/UEMOA and CLIMSEX funded by ANR project N° ANR-15-CE02-0012. There was no additional external funding received for this study The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Aquaculture, Fisheries and Fish Science
                Biodiversity
                Ecology
                Genetics

                nile tilapia,sex determination,sex-reversal,sex chromosomes,wild population

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