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Sex differentiation in grayling (Salmonidae) goes through an all-male stage and is delayed in genetic males who instead grow faster

Diane Maitre, Oliver M. Selmoni, Anshu Uppal, Lucas Marques da Cunha, Laetitia G. E. Wilkins, Julien Roux, Kenyon B. Mobley, Susanne Knörr, Marc Robinson-Rechavi, View ORCID ProfileClaus Wedekind
doi: https://doi.org/10.1101/135194
Diane Maitre
1Department of Ecology and Evolution, Biophore, University of Lausanne, 1015 Lausanne, Switzerland
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Oliver M. Selmoni
1Department of Ecology and Evolution, Biophore, University of Lausanne, 1015 Lausanne, Switzerland
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Anshu Uppal
1Department of Ecology and Evolution, Biophore, University of Lausanne, 1015 Lausanne, Switzerland
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Lucas Marques da Cunha
1Department of Ecology and Evolution, Biophore, University of Lausanne, 1015 Lausanne, Switzerland
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Laetitia G. E. Wilkins
1Department of Ecology and Evolution, Biophore, University of Lausanne, 1015 Lausanne, Switzerland
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Julien Roux
1Department of Ecology and Evolution, Biophore, University of Lausanne, 1015 Lausanne, Switzerland
2Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland
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Kenyon B. Mobley
1Department of Ecology and Evolution, Biophore, University of Lausanne, 1015 Lausanne, Switzerland
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Susanne Knörr
3Aquatic Ecology and Toxicology Group, Center of Organismic Studies, University of Heidelberg, Heidelberg, Germany
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Marc Robinson-Rechavi
1Department of Ecology and Evolution, Biophore, University of Lausanne, 1015 Lausanne, Switzerland
2Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland
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Claus Wedekind
1Department of Ecology and Evolution, Biophore, University of Lausanne, 1015 Lausanne, Switzerland
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  • ORCID record for Claus Wedekind
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Abstract

Fish can be threatened by distorted sex ratios that arise during sex differentiation. It is therefore important to understand sex determination and differentiation, especially in river-dwelling fish that are often exposed to environmental factors that may interfere with sex differentiation. However, sex differentiation is not sufficiently understood in keystone taxa such as the Thymallinae, one of the three salmonid subfamilies. Here we study a wild grayling (Thymallus thymallus) population that suffers from distorted sex ratios. We found sex determination in the wild and in captivity to be genetic and linked to the sdY locus. We therefore studied sex-specific gene expression in embryos and early larvae that were bred and raised under different experimental conditions, and we studied gonadal morphology in five monthly samples taken after hatching. Significant sex-specific changes in gene expression (affecting about 25,000 genes) started around hatching. Gonads were still undifferentiated three weeks after hatching, but about half of the fish showed immature testes around seven weeks after hatching. Over the next few months, this phenotype was mostly replaced by the “testis-to-ovary” or “ovaries” phenotypes. The gonads of the remaining fish, i.e. approximately half of the fish in each sampling period, remained undifferentiated until six months after fertilization. Genetic sexing of the last two samples revealed that fish with undifferentiated gonads were all males, who, by that time, were on average larger than the genetic females (verified in 8-months old juveniles raised in another experiment). Only 12% of the genetic males showed testicular tissue six months after fertilization. We conclude that sex differentiation starts around hatching, goes through an all-male stage for both sexes (which represents a rare case of “undifferentiated” gonochoristic species that usually go through an all-female stage), and is delayed in males who, instead of developing their gonads, grow faster than females during these juvenile stages.

Author contribution MRR and CW initiated the project. DM, OS, AU, LMC, LW, and CW sampled the adult fish, did the experimental in vitro fertilizations, and prepared the embryos for experimental rearing in the laboratory. All further manipulations on the embryos and the larvae were done by DM, OS, AU, LMC, and LW. The RNA-seq data were analyzed by OS, JR, and MRR, the histological analyses were done by DM, supervised by SK, and the molecular genetic sexing was performed by DM, OS, AU, and KBM. DM, OS, and CW performed the remaining statistical analyses and wrote the first version of the manuscript that was then critically revised by all other authors.

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Posted May 08, 2017.
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Sex differentiation in grayling (Salmonidae) goes through an all-male stage and is delayed in genetic males who instead grow faster
Diane Maitre, Oliver M. Selmoni, Anshu Uppal, Lucas Marques da Cunha, Laetitia G. E. Wilkins, Julien Roux, Kenyon B. Mobley, Susanne Knörr, Marc Robinson-Rechavi, Claus Wedekind
bioRxiv 135194; doi: https://doi.org/10.1101/135194
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Sex differentiation in grayling (Salmonidae) goes through an all-male stage and is delayed in genetic males who instead grow faster
Diane Maitre, Oliver M. Selmoni, Anshu Uppal, Lucas Marques da Cunha, Laetitia G. E. Wilkins, Julien Roux, Kenyon B. Mobley, Susanne Knörr, Marc Robinson-Rechavi, Claus Wedekind
bioRxiv 135194; doi: https://doi.org/10.1101/135194

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