Genetics and evidence for balancing selection of a sex-linked colour polymorphism in a songbird

Kang Wook Kim; Benjamin C. Jackson; Hanyuan Zhang; David P. L. Toews; Scott A. Taylor; Emma I. Greig; Irby J. Lovette; Mengning M. Liu; Angus Davison; Simon C. Griffith; Kai Zeng; Terry Burke

doi:10.1038/s41467-019-09806-6

Genetics and evidence for balancing selection of a sex-linked colour polymorphism in a songbird

Kang Wook Kim^*, Benjamin C. Jackson, Hanyuan Zhang, David P. L. Toews, Scott A. Taylor, Emma I. Greig, Irby J. Lovette, Mengning M. Liu, Angus Davison, Simon C. Griffith, Kai Zeng, Terry Burke

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

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Abstract

Colour polymorphisms play a key role in sexual selection and speciation, yet the mechanisms that generate and maintain them are not fully understood. Here, we use genomic and transcriptomic tools to identify the precise genetic architecture and evolutionary history of a sex-linked colour polymorphism in the Gouldian finch Erythrura gouldiae that is also accompanied by remarkable differences in behaviour and physiology. We find that differences in colour are associated with an ~72-kbp region of the Z chromosome in a putative regulatory region for follistatin, an antagonist of the TGF-β superfamily genes. The region is highly differentiated between morphs, unlike the rest of the genome, yet we find no evidence that an inversion is involved in maintaining the distinct haplotypes. Coalescent simulations confirm that there is elevated nucleotide diversity and an excess of intermediate frequency alleles at this locus. We conclude that this pleiotropic colour polymorphism is most probably maintained by balancing selection.

Original language	English
Article number	1852
Pages (from-to)	1-11
Number of pages	11
Journal	Nature Communications
Volume	10
Issue number	1
DOIs	https://doi.org/10.1038/s41467-019-09806-6
Publication status	Published - 23 Apr 2019

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Copyright the Author(s) 2019. Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher.

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Publisher version (open access)Final published version, 1.54 MBLicence: CC BY

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title = "Genetics and evidence for balancing selection of a sex-linked colour polymorphism in a songbird",

abstract = "Colour polymorphisms play a key role in sexual selection and speciation, yet the mechanisms that generate and maintain them are not fully understood. Here, we use genomic and transcriptomic tools to identify the precise genetic architecture and evolutionary history of a sex-linked colour polymorphism in the Gouldian finch Erythrura gouldiae that is also accompanied by remarkable differences in behaviour and physiology. We find that differences in colour are associated with an ~72-kbp region of the Z chromosome in a putative regulatory region for follistatin, an antagonist of the TGF-β superfamily genes. The region is highly differentiated between morphs, unlike the rest of the genome, yet we find no evidence that an inversion is involved in maintaining the distinct haplotypes. Coalescent simulations confirm that there is elevated nucleotide diversity and an excess of intermediate frequency alleles at this locus. We conclude that this pleiotropic colour polymorphism is most probably maintained by balancing selection.",

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AU - Kim, Kang Wook

AU - Jackson, Benjamin C.

AU - Zhang, Hanyuan

AU - Toews, David P. L.

AU - Taylor, Scott A.

AU - Greig, Emma I.

AU - Lovette, Irby J.

AU - Liu, Mengning M.

AU - Davison, Angus

AU - Griffith, Simon C.

AU - Zeng, Kai

AU - Burke, Terry

N1 - Copyright the Author(s) 2019. Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher.

PY - 2019/4/23

Y1 - 2019/4/23

N2 - Colour polymorphisms play a key role in sexual selection and speciation, yet the mechanisms that generate and maintain them are not fully understood. Here, we use genomic and transcriptomic tools to identify the precise genetic architecture and evolutionary history of a sex-linked colour polymorphism in the Gouldian finch Erythrura gouldiae that is also accompanied by remarkable differences in behaviour and physiology. We find that differences in colour are associated with an ~72-kbp region of the Z chromosome in a putative regulatory region for follistatin, an antagonist of the TGF-β superfamily genes. The region is highly differentiated between morphs, unlike the rest of the genome, yet we find no evidence that an inversion is involved in maintaining the distinct haplotypes. Coalescent simulations confirm that there is elevated nucleotide diversity and an excess of intermediate frequency alleles at this locus. We conclude that this pleiotropic colour polymorphism is most probably maintained by balancing selection.

AB - Colour polymorphisms play a key role in sexual selection and speciation, yet the mechanisms that generate and maintain them are not fully understood. Here, we use genomic and transcriptomic tools to identify the precise genetic architecture and evolutionary history of a sex-linked colour polymorphism in the Gouldian finch Erythrura gouldiae that is also accompanied by remarkable differences in behaviour and physiology. We find that differences in colour are associated with an ~72-kbp region of the Z chromosome in a putative regulatory region for follistatin, an antagonist of the TGF-β superfamily genes. The region is highly differentiated between morphs, unlike the rest of the genome, yet we find no evidence that an inversion is involved in maintaining the distinct haplotypes. Coalescent simulations confirm that there is elevated nucleotide diversity and an excess of intermediate frequency alleles at this locus. We conclude that this pleiotropic colour polymorphism is most probably maintained by balancing selection.

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Genetics and evidence for balancing selection of a sex-linked colour polymorphism in a songbird

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The danger within: assessing the threats to an endangered finch from genetic incompatibility, limited dispersal and effective population size

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Genetics and evidence for balancing selection of a sex-linked colour polymorphism in a songbird

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The danger within: assessing the threats to an endangered finch from genetic incompatibility, limited dispersal and effective population size

Cite this