Abstract
The determination of sex in salmonid fishes is controlled by genetic mechanisms, with males being the heterogametic sex. The master sex-determining gene, the sexually dimorphic gene on the Y chromosome (sdY), is a conserved gene across various salmonid species. Nevertheless, variations in the genomic location of sdY have been observed both within and between species. Furthermore, different studies have reported discordances in the association between the sdY and the phenotypic gender. While some males seem to lack this locus, there have been reports of females carrying sdY. Although the exact reasons behind this discordance remain under investigation, some recent studies have proposed the existence of an autosomal, non-functional copy of sdY as a potential cause. In this study, we confirmed the presence of this autosomal sdY in the SalmoBreed strain of Atlantic salmon using a genoty** platform through a novel approach that allows for high-throughput screening of a large number of individuals. We further characterized the segregation profile of this locus across families and found the ratio of genetically assigned female-to-male progeny to be in accordance with the expected profile of a single autosomal sdY locus. Additionally, our map** efforts localized this locus to chromosome 3 and suggested a putative copy on chromosome 6.
Similar content being viewed by others
Data Availability
Access to the raw genotype data cannot be granted publicly as it is proprietary information of a commercial entity. Inquiries for obtaining the raw genotype data should be directed towards the corresponding author.
References
Alfaqih MA, Brunelli JP, Drew RE, Thorgaard GH (2009) Map** of five candidate sex-determining loci in rainbow trout (Oncorhynchus mykiss). BMC Genet 10:2
Artieri CG, Mitchell LA, Ng SHS et al (2006) Identification of the sex-determining locus of Atlantic salmon (Salmo salar) on chromosome 2. Cytogenet Genome Res 112:152–159
Ayllon F, Solberg MF, Besnier F et al (2020) Autosomal sdY pseudogenes explain discordances between phenotypic sex and DNA marker for sex identification in Atlantic salmon. Frontiers in Genetics 11:544207
Bertho S, Herpin A, Branthonne A et al (2018) The unusual rainbow trout sex determination gene hijacked the canonical vertebrate gonadal differentiation pathway. Proc Natl Acad Sci USA 115:12781–12786
Bertho S, Herpin A, Jouanno E, Yano A, Bobe J, Parrinello H, Journot L et al (2022) A nonfunctional copy of the salmonid sex-determining gene (sdY) is responsible for the “apparent” XY females in Chinook salmon, Oncorhynchus tshawytscha. G3 12:jkab451
Bertho S, Herpin A, Schartl M, Guiguen Y (2021) Lessons from an unusual vertebrate sex-determining gene. Philos Trans R Soc Lond B Biol Sci 376:20200092
Brown MS, Evans BS, Afonso LOB (2020) Publisher correction: discordance for genotypic sex in phenotypic female Atlantic salmon (Salmo salar) is related to a reduced sdY copy number. Sci Rep 10:11966
Cavileer TD, Hunter SS, Olsen J et al (2015) A sex-determining gene (sdY) assay shows discordance between phenotypic and genotypic sex in wild populations of chinook salmon. Trans Am Fish Soc 144:423–430
Chang CC, Chow CC, Tellier LC et al (2015) Second-generation PLINK: rising to the challenge of larger and richer datasets. GigaScience 4:7
Devlin RH, Biagi CA, Smailus DE (2001) Genetic map** of y-chromosomal DNA markers in pacific salmon. Genetica 111:43–58
Duggal P, Gillanders EM, Holmes TN, Bailey-Wilson JE (2008) Establishing an adjusted p-value threshold to control the family-wide type 1 error in genome wide association studies. BMC Genomics 9:516
Eisbrenner WD, Botwright N, Cook M et al (2014) Evidence for multiple sex-determining loci in Tasmanian Atlantic salmon (Salmo salar). Heredity 113:86–92
Faber-Hammond J, Phillips RB, Park LK (2012) The sockeye salmon neo-y chromosome is a fusion between linkage groups orthologous to the coho y chromosome and the long arm of rainbow trout chromosome 2. Cytogenet Genome Res 136:69–74
Faber-Hammond JJ, Phillips RB, Brown KH (2015) Comparative analysis of the shared sex-determination region (SDR) among salmonid fishes. Genome Biol Evol 7:1972–1987
Gao G, Waldbieser GC, Youngblood RC et al (2022) The generation of the first chromosome-level de-novo genome assembly and the development and validation of a 50K SNP array for North American Atlantic salmon). bioRxiv. https://doi.org/10.1101/2022.09.28.509896
Houston RD, Taggart JB, C’ezard T et al (2014) Development and validation of a high density SNP genoty** array for Atlantic salmon (Salmo salar). BMC Genomics 15:90
Kijas J, McWilliam S, Sanchez MN et al (2018) Evolution of sex determination loci in Atlantic salmon. Sci Rep 8:5664
Larson WA, McKinney GJ, Seeb JE, Seeb LW (2016) Identification and characterization of sex-associated loci in sockeye salmon using genoty**-by-sequencing and comparison with a sex-determining assay based on the sdY gene. J Hered 107:559–566
Lien S, Koop BF, Sandve SR et al (2016) The Atlantic salmon genome provides insights into rediploidization. Nature 533:200–205
Lubieniecki KP, Lin S, Cabana EI et al (2015) Genomic instability of the sex-determining locus in Atlantic salmon (Salmo salar). G3 Bethesda Md 5:2513–22
Macqueen DJ, Johnston IA (2014) A well-constrained estimate for the timing of the salmonid whole genome duplication reveals major decoupling from species diversification. Proceedings Biological Sciences 281:20132881
Magerhans A, Hörstgen-Schwark G (2010) Selection experiments to alter the sex ratio in rainbow trout (Oncorhynchus mykiss) by means of temperature treatment. Aquaculture 306:63–67
May B, Johnson KR, Wright JE (1989) Sex linkage in salmonids: evidence from a hybridized genome of brook trout and Arctic charr. Biochem Genet 27:291–301
Moghadam HK, Ferguson MM, Danzmann RG (2007) Linkage variation at the sex-determining locus within Fraser strain Arctic charr Salvelinus alpinus. J Fish Biol 71:294–301
Nagler JJ, Bouma J, Thorgaard GH, Dauble DD (2001) High incidence of a male-specific genetic marker in phenotypic female chinook salmon from the Columbia river. Environ Health Perspect 109:67–69
Nagler JJ, Cavileer T, Steinhorst K, Devlin RH (2003) Determination of genetic sex in chinook salmon (Oncorhynchus tshawytscha) using the male-linked growth hormone pseudogene by real-time PCR. Mar Biotechnol (NY) 6:186–191
Phillips RB, Morasch MR, Park LK et al (2005) Identification of the sex chromosome pair in coho salmon (Oncorhynchus kisutch): Lack of conservation of the sex linkage group with chinook salmon (Oncorhynchus tshawytscha). Cytogenet Genome Res 111:166–170
Phillips RB, DeKoning JJ, Ventura AB et al (2009) Recombination is suppressed over a large region of the rainbow trout Y chromosome. Anim Genet 40:925–932
Phillips RB, Dekoning JJ, Brunelli JP et al (2013) Characterization of the OmyY1 region on the rainbow trout y chromosome. International Journal of Genomics 2013
Podlesnykh AV, Brykov VA, Kukhlevsky AD (2017) Unstable linkage of molecular markers with sex determination gene in pacific salmon (Oncorhynchus spp.). J Hered 108:328–333
Sakamoto T, Danzmann RG, Gharbi K et al (2000) A microsatellite linkage map of rainbow trout (Oncorhynchus mykiss) characterized by large sex-specific differences in recombination rates. Genetics 155:1331–1345
Sham PC, Purcell SM (2014) Statistical power and significance testing in large-scale genetic studies. Nat Rev Genet 15:335–346
Valdivia K, Jouanno E, Volff J-N et al (2014) High temperature increases the masculinization rate of the all-female (XX) rainbow trout “mal” population. PloS one 9
Von Bargen J, Smith CT, Rueth J (2015) Development of a Chinook salmon sex identification SNP assay based on the growth hormone pseudogene. J Fish Wildl Manag 6:213–219
Woram RA, Gharbi K, Sakamoto T et al (2003) Comparative genome analysis of the primary sex-determining locus in salmonid fishes. Genome Res 13:272–280
Yang J, Lee SH, Goddard ME, Visscher PM (2013) Genome-wide complex trait analysis (GCTA): methods, data analyses, and interpretations. Methods in Molecular Biology (clifton, NJ) 1019:215–236
Yano A, Guyomard R, Nicol B et al (2012) An immune-related gene evolved into the master sex-determining gene in rainbow trout, Oncorhynchus mykiss. Current Biology: CB 22:1423–1428
Yano A, Nicol B, Jouanno E, Guiguen Y (2014) Heritable targeted inactivation of the rainbow trout (Oncorhynchus mykiss) master sex-determining gene using zinc-finger nucleases. Mar Biotechnol (NY) 16:243–250
Zhang Q, Nakayama I, Fujiwara A et al (2001) Sex identification by male-specific growth hormone pseudogene (GH-psi) in Oncorhynchus masou complex and a related hybrid. Genetica 111:111–118
Author information
Authors and Affiliations
Contributions
The experiment was designed and conceptualized by all authors. Data collection was supervised and coordinated by Ingunn Thorland, Carlos Lozano, Brede Fanneme and Borghild Hillestad. Arrangement for SNP genoty** was carried out by Brede Fanneme and Borghild Hillestad. Bioinformatics and genomics analysis were performed by Hooman Moghadam, who also drafted the initial version of the manuscript. All authors contributed to the interpretation of the data and to the development of the paper.
Corresponding author
Ethics declarations
Competing Interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Moghadam, H.K., Fannemel, B., Thorland, I. et al. Identification and Genomic Localization of Autosomal sdY Locus in a Population of Atlantic Salmon (Salmo salar). Mar Biotechnol 25, 438–446 (2023). https://doi.org/10.1007/s10126-023-10217-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-023-10217-4