Is Pairing with a Relative Heritable? Estimating Female and Male Genetic Contributions to the Degree of Biparental Inbreeding in Song Sparrows (Melospiza melodia)

Matthew E. Wolak, Jane M. Reid

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13 Citations (Scopus)
3 Downloads (Pure)

Abstract

The degree of inbreeding expressed within populations can profoundly shape evolutionary dynamics. The degree to which individuals inbreed is frequently assumed to evolve in response to selection, for example, resulting from inbreeding depression. Such evolutionary responses require additive genetic variance (VA) in the degree to which individuals inbreed. However, the magnitude of VA in the degree of biparental inbreeding has never been estimated. We devised a quantitative genetic model to estimate sex‐specific VA in the degree to which individuals inbreed while accounting for effects of individuals’ own coefficients of inbreeding and genetic effects stemming from immigration. We applied this model to the degree of inbreeding expressed through social pairing in free‐living song sparrows (Melospiza melodia). Estimates of VA for both sexes appreciably exceeded 0 and the cross‐sex genetic covariance was strongly positive, creating substantial total VA in the degree of inbreeding. Our analyses also revealed inbreeding depression in the degree of inbreeding, such that more inbred individuals paired with closer relatives, and immigrant effects, such that individuals with greater genomic contributions from immigrants paired with more distant relatives. We thereby demonstrate that the degree of biparental inbreeding can show substantial VA in nature and might consequently evolve in response to selection.
Original languageEnglish
Pages (from-to)736-752
Number of pages17
JournalThe American Naturalist
Volume187
Issue number6
Early online date18 Apr 2016
DOIs
Publication statusPublished - Jun 2016

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Passeriformes
inbreeding
song
animal communication
immigration
inbreeding depression
genetic covariance
inbreeding coefficient
quantitative genetics
genetic variance
Melospiza
genomics
gender

Keywords

  • animal model
  • genetic groups
  • inbreeding strategy
  • kinship
  • mating system evolution
  • quantitative genetics

Cite this

@article{c4597329d7a34c7eb29b92af7131e38e,
title = "Is Pairing with a Relative Heritable?: Estimating Female and Male Genetic Contributions to the Degree of Biparental Inbreeding in Song Sparrows (Melospiza melodia)",
abstract = "The degree of inbreeding expressed within populations can profoundly shape evolutionary dynamics. The degree to which individuals inbreed is frequently assumed to evolve in response to selection, for example, resulting from inbreeding depression. Such evolutionary responses require additive genetic variance (VA) in the degree to which individuals inbreed. However, the magnitude of VA in the degree of biparental inbreeding has never been estimated. We devised a quantitative genetic model to estimate sex‐specific VA in the degree to which individuals inbreed while accounting for effects of individuals’ own coefficients of inbreeding and genetic effects stemming from immigration. We applied this model to the degree of inbreeding expressed through social pairing in free‐living song sparrows (Melospiza melodia). Estimates of VA for both sexes appreciably exceeded 0 and the cross‐sex genetic covariance was strongly positive, creating substantial total VA in the degree of inbreeding. Our analyses also revealed inbreeding depression in the degree of inbreeding, such that more inbred individuals paired with closer relatives, and immigrant effects, such that individuals with greater genomic contributions from immigrants paired with more distant relatives. We thereby demonstrate that the degree of biparental inbreeding can show substantial VA in nature and might consequently evolve in response to selection.",
keywords = "animal model, genetic groups, inbreeding strategy, kinship, mating system evolution, quantitative genetics",
author = "Wolak, {Matthew E.} and Reid, {Jane M.}",
note = "Acknowledgments We thank the Tsawout and Tseycum First Nation bands for access to Mandarte, P. Arcese and everyone who contributed to the long‐term data collection, and the European Research Council and Royal Society for funding. We thank P. Bijma, J. D. Hadfield, L. F. Keller, and E. Postma for illuminating discussions. In addition, R. Bonduriansky, L. E. B. Kruuk, and an anonymous reviewer provided insightful comments that improved the manuscript.",
year = "2016",
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T2 - Estimating Female and Male Genetic Contributions to the Degree of Biparental Inbreeding in Song Sparrows (Melospiza melodia)

AU - Wolak, Matthew E.

AU - Reid, Jane M.

N1 - Acknowledgments We thank the Tsawout and Tseycum First Nation bands for access to Mandarte, P. Arcese and everyone who contributed to the long‐term data collection, and the European Research Council and Royal Society for funding. We thank P. Bijma, J. D. Hadfield, L. F. Keller, and E. Postma for illuminating discussions. In addition, R. Bonduriansky, L. E. B. Kruuk, and an anonymous reviewer provided insightful comments that improved the manuscript.

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N2 - The degree of inbreeding expressed within populations can profoundly shape evolutionary dynamics. The degree to which individuals inbreed is frequently assumed to evolve in response to selection, for example, resulting from inbreeding depression. Such evolutionary responses require additive genetic variance (VA) in the degree to which individuals inbreed. However, the magnitude of VA in the degree of biparental inbreeding has never been estimated. We devised a quantitative genetic model to estimate sex‐specific VA in the degree to which individuals inbreed while accounting for effects of individuals’ own coefficients of inbreeding and genetic effects stemming from immigration. We applied this model to the degree of inbreeding expressed through social pairing in free‐living song sparrows (Melospiza melodia). Estimates of VA for both sexes appreciably exceeded 0 and the cross‐sex genetic covariance was strongly positive, creating substantial total VA in the degree of inbreeding. Our analyses also revealed inbreeding depression in the degree of inbreeding, such that more inbred individuals paired with closer relatives, and immigrant effects, such that individuals with greater genomic contributions from immigrants paired with more distant relatives. We thereby demonstrate that the degree of biparental inbreeding can show substantial VA in nature and might consequently evolve in response to selection.

AB - The degree of inbreeding expressed within populations can profoundly shape evolutionary dynamics. The degree to which individuals inbreed is frequently assumed to evolve in response to selection, for example, resulting from inbreeding depression. Such evolutionary responses require additive genetic variance (VA) in the degree to which individuals inbreed. However, the magnitude of VA in the degree of biparental inbreeding has never been estimated. We devised a quantitative genetic model to estimate sex‐specific VA in the degree to which individuals inbreed while accounting for effects of individuals’ own coefficients of inbreeding and genetic effects stemming from immigration. We applied this model to the degree of inbreeding expressed through social pairing in free‐living song sparrows (Melospiza melodia). Estimates of VA for both sexes appreciably exceeded 0 and the cross‐sex genetic covariance was strongly positive, creating substantial total VA in the degree of inbreeding. Our analyses also revealed inbreeding depression in the degree of inbreeding, such that more inbred individuals paired with closer relatives, and immigrant effects, such that individuals with greater genomic contributions from immigrants paired with more distant relatives. We thereby demonstrate that the degree of biparental inbreeding can show substantial VA in nature and might consequently evolve in response to selection.

KW - animal model

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KW - inbreeding strategy

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U2 - 10.1086/686198

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