Recent immigrants alter the quantitative genetic architecture of paternity in song sparrows

Jane M. Reid*, Peter Arcese

*Corresponding author for this work

Research output: Contribution to journalArticle

Abstract

Quantifying additive genetic variances and cross-sex covariances in reproductive traits, and identifying processes that shape and maintain such (co)variances, is central to understanding the evolutionary dynamics of reproductive systems. Gene flow resulting from among-population dispersal could substantially alter additive genetic variances and covariances in key traits in recipient populations, thereby altering forms of sexual conflict, indirect selection and evolutionary responses. However, the degree to which genes imported by immigrants do in fact affect quantitative genetic architectures of key reproductive traits and outcomes is rarely explicitly quantified. We applied structured quantitative genetic analyses to multi-year pedigree, pairing and paternity data from free-living song sparrows (Melospiza melodia) to quantify the differences in mean breeding values for major sex-specific reproductive traits, specifically female extra-pair reproduction and male paternity loss, between recent immigrants and the previously existing population. We thereby quantify effects of natural immigration on the means, variances and cross-sex covariance in total additive genetic values for extra-pair paternity arising within the complex socially monogamous but genetically polygynandrous reproductive system. Recent immigrants had lower mean breeding values for male paternity loss, and somewhat lower values for female extra-pair reproduction, than the local recipient population, and would therefore increase the emerging degree of reproductive fidelity of social pairings. Furthermore, immigration increased the variances in total additive genetic values for these traits, but decreased the magnitudes of the negative cross-sex genetic covariation and correlation below those evident in the existing population. Immigration thereby increased the total additive genetic variance but could decrease the magnitude of indirect selection acting on sex-specific contributions to paternity outcomes. These results demonstrate that dispersal and resulting immigration and gene flow can substantially affect quantitative genetic architectures of complex local reproductive systems, implying that comprehensive theoretical and empirical efforts to understand mating system dynamics will need to incorporate spatial population processes.
Original languageEnglish
JournalEvolution Letters
Publication statusAccepted/In press - 19 Jan 2020

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Passeriformes
quantitative genetics
paternity
immigration
animal communication
reproductive system
reproductive traits
genetic variance
gender
breeding value
gene flow
genetic covariance
mating systems
pedigree

Keywords

  • cross-sex genetic correlation
  • dispersal
  • extra-pair paternity
  • gene flow
  • genetic groups
  • immigration
  • indirect genetic effects
  • mating system
  • polyandry
  • quantitative genetics
  • sexual conflict
  • sexual selection

Cite this

Recent immigrants alter the quantitative genetic architecture of paternity in song sparrows. / Reid, Jane M.; Arcese, Peter.

In: Evolution Letters, 19.01.2020.

Research output: Contribution to journalArticle

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abstract = "Quantifying additive genetic variances and cross-sex covariances in reproductive traits, and identifying processes that shape and maintain such (co)variances, is central to understanding the evolutionary dynamics of reproductive systems. Gene flow resulting from among-population dispersal could substantially alter additive genetic variances and covariances in key traits in recipient populations, thereby altering forms of sexual conflict, indirect selection and evolutionary responses. However, the degree to which genes imported by immigrants do in fact affect quantitative genetic architectures of key reproductive traits and outcomes is rarely explicitly quantified. We applied structured quantitative genetic analyses to multi-year pedigree, pairing and paternity data from free-living song sparrows (Melospiza melodia) to quantify the differences in mean breeding values for major sex-specific reproductive traits, specifically female extra-pair reproduction and male paternity loss, between recent immigrants and the previously existing population. We thereby quantify effects of natural immigration on the means, variances and cross-sex covariance in total additive genetic values for extra-pair paternity arising within the complex socially monogamous but genetically polygynandrous reproductive system. Recent immigrants had lower mean breeding values for male paternity loss, and somewhat lower values for female extra-pair reproduction, than the local recipient population, and would therefore increase the emerging degree of reproductive fidelity of social pairings. Furthermore, immigration increased the variances in total additive genetic values for these traits, but decreased the magnitudes of the negative cross-sex genetic covariation and correlation below those evident in the existing population. Immigration thereby increased the total additive genetic variance but could decrease the magnitude of indirect selection acting on sex-specific contributions to paternity outcomes. These results demonstrate that dispersal and resulting immigration and gene flow can substantially affect quantitative genetic architectures of complex local reproductive systems, implying that comprehensive theoretical and empirical efforts to understand mating system dynamics will need to incorporate spatial population processes.",
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note = "Acknowledgements We thank the Tsawout and Tseycum First Nations Bands for allowing access to Mandarte, everyone who contributed to long-term data collection, the European Research Council, NSERC (Canada) and the Swiss National Science Foundation for funding, Pirmin Nietlisbach, Glauco Camenisch and Lukas Keller for their extensive work on the song sparrow pedigree, and Matthew Wolak for his enthusiastic comments. The authors declare no conflicts of interest.",
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N1 - Acknowledgements We thank the Tsawout and Tseycum First Nations Bands for allowing access to Mandarte, everyone who contributed to long-term data collection, the European Research Council, NSERC (Canada) and the Swiss National Science Foundation for funding, Pirmin Nietlisbach, Glauco Camenisch and Lukas Keller for their extensive work on the song sparrow pedigree, and Matthew Wolak for his enthusiastic comments. The authors declare no conflicts of interest.

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N2 - Quantifying additive genetic variances and cross-sex covariances in reproductive traits, and identifying processes that shape and maintain such (co)variances, is central to understanding the evolutionary dynamics of reproductive systems. Gene flow resulting from among-population dispersal could substantially alter additive genetic variances and covariances in key traits in recipient populations, thereby altering forms of sexual conflict, indirect selection and evolutionary responses. However, the degree to which genes imported by immigrants do in fact affect quantitative genetic architectures of key reproductive traits and outcomes is rarely explicitly quantified. We applied structured quantitative genetic analyses to multi-year pedigree, pairing and paternity data from free-living song sparrows (Melospiza melodia) to quantify the differences in mean breeding values for major sex-specific reproductive traits, specifically female extra-pair reproduction and male paternity loss, between recent immigrants and the previously existing population. We thereby quantify effects of natural immigration on the means, variances and cross-sex covariance in total additive genetic values for extra-pair paternity arising within the complex socially monogamous but genetically polygynandrous reproductive system. Recent immigrants had lower mean breeding values for male paternity loss, and somewhat lower values for female extra-pair reproduction, than the local recipient population, and would therefore increase the emerging degree of reproductive fidelity of social pairings. Furthermore, immigration increased the variances in total additive genetic values for these traits, but decreased the magnitudes of the negative cross-sex genetic covariation and correlation below those evident in the existing population. Immigration thereby increased the total additive genetic variance but could decrease the magnitude of indirect selection acting on sex-specific contributions to paternity outcomes. These results demonstrate that dispersal and resulting immigration and gene flow can substantially affect quantitative genetic architectures of complex local reproductive systems, implying that comprehensive theoretical and empirical efforts to understand mating system dynamics will need to incorporate spatial population processes.

AB - Quantifying additive genetic variances and cross-sex covariances in reproductive traits, and identifying processes that shape and maintain such (co)variances, is central to understanding the evolutionary dynamics of reproductive systems. Gene flow resulting from among-population dispersal could substantially alter additive genetic variances and covariances in key traits in recipient populations, thereby altering forms of sexual conflict, indirect selection and evolutionary responses. However, the degree to which genes imported by immigrants do in fact affect quantitative genetic architectures of key reproductive traits and outcomes is rarely explicitly quantified. We applied structured quantitative genetic analyses to multi-year pedigree, pairing and paternity data from free-living song sparrows (Melospiza melodia) to quantify the differences in mean breeding values for major sex-specific reproductive traits, specifically female extra-pair reproduction and male paternity loss, between recent immigrants and the previously existing population. We thereby quantify effects of natural immigration on the means, variances and cross-sex covariance in total additive genetic values for extra-pair paternity arising within the complex socially monogamous but genetically polygynandrous reproductive system. Recent immigrants had lower mean breeding values for male paternity loss, and somewhat lower values for female extra-pair reproduction, than the local recipient population, and would therefore increase the emerging degree of reproductive fidelity of social pairings. Furthermore, immigration increased the variances in total additive genetic values for these traits, but decreased the magnitudes of the negative cross-sex genetic covariation and correlation below those evident in the existing population. Immigration thereby increased the total additive genetic variance but could decrease the magnitude of indirect selection acting on sex-specific contributions to paternity outcomes. These results demonstrate that dispersal and resulting immigration and gene flow can substantially affect quantitative genetic architectures of complex local reproductive systems, implying that comprehensive theoretical and empirical efforts to understand mating system dynamics will need to incorporate spatial population processes.

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KW - indirect genetic effects

KW - mating system

KW - polyandry

KW - quantitative genetics

KW - sexual conflict

KW - sexual selection

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JF - Evolution Letters

SN - 2056-3744

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