Sex-dependent dominance maintains migration supergene in rainbow trout

doi:10.1038/s41559-019-1044-6

. 2019 Dec;3(12):1731-1742.

doi: 10.1038/s41559-019-1044-6. Epub 2019 Nov 25.

Sex-dependent dominance maintains migration supergene in rainbow trout

Devon E Pearse^#¹, Nicola J Barson^#², Torfinn Nome², Guangtu Gao³, Matthew A Campbell⁴, Alicia Abadía-Cardoso⁵, Eric C Anderson⁶, David E Rundio⁶, Thomas H Williams⁶, Kerry A Naish⁷, Thomas Moen⁸, Sixin Liu³, Matthew Kent², Michel Moser², David R Minkley⁹, Eric B Rondeau⁹, Marine S O Brieuc⁷, Simen Rød Sandve², Michael R Miller¹⁰, Lucydalila Cedillo¹⁰, Kobi Baruch¹¹, Alvaro G Hernandez¹², Gil Ben-Zvi¹¹, Doron Shem-Tov¹¹, Omer Barad¹¹, Kirill Kuzishchin¹³, John Carlos Garza⁶, Steven T Lindley⁶, Ben F Koop⁹, Gary H Thorgaard¹⁴, Yniv Palti¹⁵, Sigbjørn Lien¹⁶

Affiliations

¹ Fisheries Ecology Division, Southwest Fisheries Science Center, National Marine Fisheries Service, Santa Cruz, CA, USA. devon.pearse@noaa.gov.
² Centre for Integrative Genetics, Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life Sciences, Ås, Norway.
³ National Center for Cool and Cold Water Aquaculture, USDA-ARS, Kearneysville, WV, USA.
⁴ Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA, USA.
⁵ Facultad de Ciencias Marinas, Universidad Autónoma de Baja California, Baja California, Mexico.
⁶ Fisheries Ecology Division, Southwest Fisheries Science Center, National Marine Fisheries Service, Santa Cruz, CA, USA.
⁷ School of Aquatic and Fishery Sciences, University of Washington, WA, Seattle, USA.
⁸ AquaGen, Trondheim, Norway.
⁹ Department of Biology, University of Victoria, Victoria, British Columbia, Canada.
¹⁰ Department of Animal Science, University of California, CA, Davis, USA.
¹¹ NRGene Ltd., Ness-Ziona, Israel.
¹² Roy J. Carver Biotechnology Center, University of Illinois at Urbana-Champaign, IL, Urbana, USA.
¹³ Moscow State University, Moscow, Russian Federation.
¹⁴ School of Biological Sciences and Center for Reproductive Biology, Washington State University, WA, Pullman, USA.
¹⁵ National Center for Cool and Cold Water Aquaculture, USDA-ARS, Kearneysville, WV, USA. yniv.palti@ars.usda.gov.
¹⁶ Centre for Integrative Genetics, Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life Sciences, Ås, Norway. sigbjorn.lien@nmbu.no.

^# Contributed equally.

PMID: 31768021
DOI: 10.1038/s41559-019-1044-6

Sex-dependent dominance maintains migration supergene in rainbow trout

Devon E Pearse et al. Nat Ecol Evol. 2019 Dec.

. 2019 Dec;3(12):1731-1742.

doi: 10.1038/s41559-019-1044-6. Epub 2019 Nov 25.

Authors

Affiliations

¹ Fisheries Ecology Division, Southwest Fisheries Science Center, National Marine Fisheries Service, Santa Cruz, CA, USA. devon.pearse@noaa.gov.
² Centre for Integrative Genetics, Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life Sciences, Ås, Norway.
³ National Center for Cool and Cold Water Aquaculture, USDA-ARS, Kearneysville, WV, USA.
⁴ Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, CA, USA.
⁵ Facultad de Ciencias Marinas, Universidad Autónoma de Baja California, Baja California, Mexico.
⁶ Fisheries Ecology Division, Southwest Fisheries Science Center, National Marine Fisheries Service, Santa Cruz, CA, USA.
⁷ School of Aquatic and Fishery Sciences, University of Washington, WA, Seattle, USA.
⁸ AquaGen, Trondheim, Norway.
⁹ Department of Biology, University of Victoria, Victoria, British Columbia, Canada.
¹⁰ Department of Animal Science, University of California, CA, Davis, USA.
¹¹ NRGene Ltd., Ness-Ziona, Israel.
¹² Roy J. Carver Biotechnology Center, University of Illinois at Urbana-Champaign, IL, Urbana, USA.
¹³ Moscow State University, Moscow, Russian Federation.
¹⁴ School of Biological Sciences and Center for Reproductive Biology, Washington State University, WA, Pullman, USA.
¹⁵ National Center for Cool and Cold Water Aquaculture, USDA-ARS, Kearneysville, WV, USA. yniv.palti@ars.usda.gov.
¹⁶ Centre for Integrative Genetics, Department of Animal and Aquacultural Sciences, Faculty of Biosciences, Norwegian University of Life Sciences, Ås, Norway. sigbjorn.lien@nmbu.no.

^# Contributed equally.

PMID: 31768021
DOI: 10.1038/s41559-019-1044-6

Erratum in

Publisher Correction: Sex-dependent dominance maintains migration supergene in rainbow trout.
Pearse DE, Barson NJ, Nome T, Gao G, Campbell MA, Abadía-Cardoso A, Anderson EC, Rundio DE, Williams TH, Naish KA, Moen T, Liu S, Kent M, Moser M, Minkley DR, Rondeau EB, Brieuc MSO, Sandve SR, Miller MR, Cedillo L, Baruch K, Hernandez AG, Ben-Zvi G, Shem-Tov D, Barad O, Kuzishchin K, Garza JC, Lindley ST, Koop BF, Thorgaard GH, Palti Y, Lien S. Pearse DE, et al. Nat Ecol Evol. 2020 Jan;4(1):170. doi: 10.1038/s41559-019-1076-y. Nat Ecol Evol. 2020. PMID: 31819240

Abstract

Males and females often differ in their fitness optima for shared traits that have a shared genetic basis, leading to sexual conflict. Morphologically differentiated sex chromosomes can resolve this conflict and protect sexually antagonistic variation, but they accumulate deleterious mutations. However, how sexual conflict is resolved in species that lack differentiated sex chromosomes is largely unknown. Here we present a chromosome-anchored genome assembly for rainbow trout (Oncorhynchus mykiss) and characterize a 55-Mb double-inversion supergene that mediates sex-specific migratory tendency through sex-dependent dominance reversal, an alternative mechanism for resolving sexual conflict. The double inversion contains key photosensory, circadian rhythm, adiposity and sex-related genes and displays a latitudinal frequency cline, indicating environmentally dependent selection. Our results show sex-dependent dominance reversal across a large autosomal supergene, a mechanism for sexual conflict resolution capable of protecting sexually antagonistic variation while avoiding the homozygous lethality and deleterious mutations associated with typical heteromorphic sex chromosomes.

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References

1. Connallon, T. The geography of sex-specific selection, local adaptation, and sexual dimorphism. Evolution 69, 2333–2344 (2015). - PubMed
1. Lande, R. Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34, 292–305 (1980). - PubMed
1. Mank, J. E. Population genetics of sexual conflict in the genomic era. Nat. Rev. Genet. 18, 721–730 (2017). - PubMed
1. Barson, N. J. et al. Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon. Nature 528, 405–408 (2015). - PubMed
1. Bachtrog, D. et al. Sex determination: why so many ways of doing it? PLoS Biol. 12, e1001899 (2014). - PubMed - PMC

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[1] Connallon, T. The geography of sex-specific selection, local adaptation, and sexual dimorphism. Evolution 69, 2333–2344 (2015). - PubMed

[2] Connallon, T. The geography of sex-specific selection, local adaptation, and sexual dimorphism. Evolution 69, 2333–2344 (2015). - PubMed

[3] Lande, R. Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34, 292–305 (1980). - PubMed

[4] Lande, R. Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34, 292–305 (1980). - PubMed

[5] Mank, J. E. Population genetics of sexual conflict in the genomic era. Nat. Rev. Genet. 18, 721–730 (2017). - PubMed

[6] Mank, J. E. Population genetics of sexual conflict in the genomic era. Nat. Rev. Genet. 18, 721–730 (2017). - PubMed

[7] Barson, N. J. et al. Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon. Nature 528, 405–408 (2015). - PubMed

[8] Barson, N. J. et al. Sex-dependent dominance at a single locus maintains variation in age at maturity in salmon. Nature 528, 405–408 (2015). - PubMed

[9] Bachtrog, D. et al. Sex determination: why so many ways of doing it? PLoS Biol. 12, e1001899 (2014). - PubMed - PMC

[10] Bachtrog, D. et al. Sex determination: why so many ways of doing it? PLoS Biol. 12, e1001899 (2014). - PubMed - PMC

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Sex-dependent dominance maintains migration supergene in rainbow trout

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Sex-dependent dominance maintains migration supergene in rainbow trout

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