Sex-dependent dominance maintains migration supergene in rainbow trout

Devon E. Pearse; Nicola J. Barson; Torfinn Nome; Guangtu Gao; Matthew A. Campbell; Alicia Abadía-Cardoso; Eric C. Anderson; David E. Rundio; Thomas H. Williams; Kerry A. Naish; Thomas Moen; Sixin Liu; Matthew Kent; Michel Moser; David R. Minkley; Eric B. Rondeau; Marine S.O. Brieuc; Simen Rød Sandve; Michael R. Miller; Lucydalila Cedillo; Kobi Baruch; Alvaro G. Hernandez; Gil Ben-Zvi; Doron Shem-Tov; Omer Barad; Kirill Kuzishchin; John Carlos Garza; Steven T. Lindley; Ben F. Koop; Gary H. Thorgaard; Yniv Palti; Sigbjørn Lien

doi:10.1038/s41559-019-1044-6

Sex-dependent dominance maintains migration supergene in rainbow trout

Devon E. Pearse, Nicola J. Barson, Torfinn Nome, Guangtu Gao, Matthew A. Campbell, Alicia Abadía-Cardoso, Eric C. Anderson, David E. Rundio, Thomas H. Williams, Kerry A. Naish, Thomas Moen, Sixin Liu, Matthew Kent, Michel Moser, David R. Minkley, Eric B. Rondeau, Marine S.O. Brieuc, Simen Rød Sandve, Michael R. Miller, Lucydalila CedilloKobi Baruch, Alvaro G. Hernandez, Gil Ben-Zvi, Doron Shem-Tov, Omer Barad, Kirill Kuzishchin, John Carlos Garza, Steven T. Lindley, Ben F. Koop, Gary H. Thorgaard, Yniv Palti, Sigbjørn Lien

Biotechnology Center

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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.

Original language	English (US)
Pages (from-to)	1731-1742
Number of pages	12
Journal	Nature Ecology and Evolution
Volume	3
Issue number	12
DOIs	https://doi.org/10.1038/s41559-019-1044-6
State	Published - Dec 1 2019

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Ecology

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10.1038/s41559-019-1044-6

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Pearse, D. E., Barson, N. J., Nome, T., Gao, G., Campbell, M. A., Abadía-Cardoso, A., Anderson, E. C., Rundio, D. E., Williams, T. H., Naish, K. A., Moen, T., Liu, S., Kent, M., Moser, M., Minkley, D. R., Rondeau, E. B., Brieuc, M. S. O., Sandve, S. R., Miller, M. R., ... Lien, S. (2019). Sex-dependent dominance maintains migration supergene in rainbow trout. Nature Ecology and Evolution, 3(12), 1731-1742. https://doi.org/10.1038/s41559-019-1044-6

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 2019, 'Sex-dependent dominance maintains migration supergene in rainbow trout', Nature Ecology and Evolution, vol. 3, no. 12, pp. 1731-1742. https://doi.org/10.1038/s41559-019-1044-6

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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.",

author = "Pearse, {Devon E.} and Barson, {Nicola J.} and Torfinn Nome and Guangtu Gao and Campbell, {Matthew A.} and Alicia Abad{\'i}a-Cardoso and Anderson, {Eric C.} and Rundio, {David E.} and Williams, {Thomas H.} and Naish, {Kerry A.} and Thomas Moen and Sixin Liu and Matthew Kent and Michel Moser and Minkley, {David R.} and Rondeau, {Eric B.} and Brieuc, {Marine S.O.} and Sandve, {Simen R{\o}d} and Miller, {Michael R.} and Lucydalila Cedillo and Kobi Baruch and Hernandez, {Alvaro G.} and Gil Ben-Zvi and Doron Shem-Tov and Omer Barad and Kirill Kuzishchin and Garza, {John Carlos} and Lindley, {Steven T.} and Koop, {Ben F.} and Thorgaard, {Gary H.} and Yniv Palti and Sigbj{\o}rn Lien",

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AU - Pearse, Devon E.

AU - Barson, Nicola J.

AU - Nome, Torfinn

AU - Gao, Guangtu

AU - Campbell, Matthew A.

AU - Abadía-Cardoso, Alicia

AU - Anderson, Eric C.

AU - Rundio, David E.

AU - Williams, Thomas H.

AU - Naish, Kerry A.

AU - Moen, Thomas

AU - Liu, Sixin

AU - Kent, Matthew

AU - Moser, Michel

AU - Minkley, David R.

AU - Rondeau, Eric B.

AU - Brieuc, Marine S.O.

AU - Sandve, Simen Rød

AU - Miller, Michael R.

AU - Cedillo, Lucydalila

AU - Baruch, Kobi

AU - Hernandez, Alvaro G.

AU - Ben-Zvi, Gil

AU - Shem-Tov, Doron

AU - Barad, Omer

AU - Kuzishchin, Kirill

AU - Garza, John Carlos

AU - Lindley, Steven T.

AU - Koop, Ben F.

AU - Thorgaard, Gary H.

AU - Palti, Yniv

AU - Lien, Sigbjørn

PY - 2019/12/1

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N2 - 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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Sex-dependent dominance maintains migration supergene in rainbow trout

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