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ARS Home » Northeast Area » Leetown, West Virginia » Cool and Cold Water Aquaculture Research » Research » Publications at this Location » Publication #360217
Research Project: Integrated Research Approaches for Improving Production Efficiency in Salmonids

Location: Cool and Cold Water Aquaculture Research

Title: Sex-dependent dominance maintains migration supergene in rainbow trout

Author
item PEARSE, DEVON - National Marine Fish Services
item BARSON, NICOLA - Centre For Integrative Genetics (CIGENE)
item NOME, TORFINN - Centre For Integrative Genetics (CIGENE)
item Gao, Guangtu
item CAMPBELL, MATTHEW - National Marine Fish Services
item ABADIA-CARDOSO, ALICIA - National Marine Fish Services
item ANDERSON, ERIC - National Marine Fish Services
item RUNDIO, DAVID - National Marine Fish Services
item WILLIAMS, THOMAS - National Marine Fish Services
item NAISH, KERRY - University Of Washington
item MOEN, THOMAS - Aquagen
item Liu, Sixin
item MATTHEW, KENT - Centre For Integrative Genetics (CIGENE)
item MINKLEY, DAVID - University Of Victoria
item RONDEAU, ERIC - University Of Victoria
item BRIEUC, MARINE - University Of Washington
item SANDYE, SIMEN ROD - Centre For Integrative Genetics (CIGENE)
item MILLER, MICHAEL - University Of California, Davis
item CEDILLO, LUCYDALILA - University Of California, Davis
item BARUCH, KOBI - Nrgene
item HERNANDEZ, ALVARO - University Of Illinois
item BEN-ZVI, GIL - Nrgene
item SHEM-TOV, DORON - Nrgene
item BARAD, OMER - Nrgene
item KUZISHCHIN, KIRILL - Moscow State University
item GARZA, JOHN CARLOS - National Marine Fish Services
item LINDLEY, STEVEN - National Marine Fish Services
item KOOP, BEN - University Of Victoria
item THORGAARD, GARY - Washington State University
item Palti, Yniv
item LIEN, SIGBJORN - Centre For Integrative Genetics (CIGENE)

Submitted to: Nature Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/23/2019
Publication Date: 12/4/2019
Publication URL: https://handle.nal.usda.gov/10113/6829260
Citation: Pearse, D.E., Barson, N.J., Nome, T., Gao, G., Campbell, M.A., Abadia-Cardoso, A., Anderson, E.C., Rundio, D.E., Williams, T.H., Naish, K.A., Moen, T., Liu, S., Matthew, K., Minkley, D.R., Rondeau, E.B., Brieuc, M.S., Sandye, S., Miller, M.R., Cedillo, L., Baruch, K., Hernandez, A.G., Ben-Zvi, G., Shem-Tov, D., Barad, O., Kuzishchin, K., Garza, J., Lindley, S.T., Koop, B.F., Thorgaard, G.H., Palti, Y., Lien, S. 2019. Sex-dependent dominance maintains migration supergene in rainbow trout. Nature Ecology and Evolution. 3:1731–1742. https://doi.org/10.1038/s41559-019-1044-6.
DOI: https://doi.org/10.1038/s41559-019-1044-6

Interpretive Summary: A high-quality reference physical genome map is important for facilitating meaningful genetic analyses and enhancing research on the physiology of the organism or species. In an effort to improve the rainbow trout reference genome assembly, we used recent improvements in DNA sequencing technology and sophisticated new bioinformatics pipelines to generate a new reference genome assembly for rainbow trout. Approximately 88% of the new assembly sequences are aligned within chromosomes to generate contiguous chromosome sequences. The new reference genome and the annotation of protein coding genes are now available to the research community for browsing and analyses through the NIH National Center for Biotechnology Information (NCBI) Online interactive databases. The new rainbow trout genome assembly and chromosome sequences provide major improvements for rainbow trout aquaculture genetics research, and for all aspects of research aimed at better understanding of the biology of this economically- and scientifically-important fish. In this scientific report we specifically highlight a very large region on chromosome 5 of the rainbow trout genome that behaves like a super-gene through tight linkage of multiple protein coding genes. This super-gene may contribute to variation in life history traits that affect adaptation of native trout populations in the wild. One such trait is the tendency of migration to the ocean in young adults, where females with heterozygous genotype for this super-gene tend to migrate to the ocean while males tend to remain in their native freshwater birthplace. This unique genetic mechanism for resolving sexual conflict caused by different fitness needs for males and females is reported here for the first time and is thought to have played a major role in the evolution of this species.

Technical Abstract: Traits with different fitness optima in males and females cause sexual conflict when they have a shared genetic basis. Heteromorphic sex chromosomes can resolve this conflict and protect sexually antagonistic polymorphisms but accumulate deleterious mutations. However, many taxa lack differentiated sex chromosomes, and how sexual conflict is resolved in these species is largely unknown. Here we present a chromosome-anchored genome assembly for rainbow trout (Oncorhynchus mykiss) and characterize a 56 Mb double-inversion supergene that mediates sex-specific migration through sex-dependent dominance, a mechanism that reduces sexual conflict. The double-inversion contains key photosensory, circadian rhythm, adiposity, and sexual differentiation genes and displays frequency clines associated with latitude and temperature, revealing environmental dependence. Our results constitute the first example of sex-dependent dominance across a large autosomal supergene, a novel mechanism for sexual conflict resolution capable of protecting polygenic sexually antagonistic variation while avoiding the homozygous lethality and deleterious mutation load of heteromorphic sex chromosomes.