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Allele frequency dynamics in a pedigreed natural population

Nancy Chen, Ivan Juric, Elissa J. Cosgrove, Reed Bowman, John W. Fitzpatrick, Stephan J. Schoech, Andrew G. Clark, and Graham Coop
PNAS February 5, 2019 116 (6) 2158-2164; published ahead of print February 5, 2019 https://doi.org/10.1073/pnas.1813852116
Nancy Chen
aCenter for Population Biology, University of California, Davis, CA 95616;bDepartment of Evolution & Ecology, University of California, Davis, CA 95616;cDepartment of Biology, University of Rochester, Rochester, NY 14627;
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  • ORCID record for Nancy Chen
  • For correspondence: nancy.chen@rochester.edu
Ivan Juric
dDepartment of Quantitative Health Sciences, Lerner Research Institute, Cleveland Clinic Foundation, Cleveland, OH 44195;
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Elissa J. Cosgrove
eDepartment of Molecular Biology & Genetics, Cornell University, Ithaca, NY 14850;
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Reed Bowman
fAvian Ecology Program, Archbold Biological Station, Venus, FL 33960;
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John W. Fitzpatrick
gCornell Lab of Ornithology, Cornell University, Ithaca, NY 14850;
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Stephan J. Schoech
hDepartment of Biological Sciences, University of Memphis, Memphis, TN 38152
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Andrew G. Clark
eDepartment of Molecular Biology & Genetics, Cornell University, Ithaca, NY 14850;
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Graham Coop
aCenter for Population Biology, University of California, Davis, CA 95616;bDepartment of Evolution & Ecology, University of California, Davis, CA 95616;
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  1. Edited by Nils C. Stenseth, University of Oslo, Oslo, Norway, and approved November 19, 2018 (received for review August 10, 2018)

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Significance

Evolution is change in the genetic composition of populations. In nature, individuals reproduce, die, and move among populations, leading to changes in the population frequency of the alleles they carry. Here we study an extensive family tree (pedigree) for an exhaustively sampled natural population of Florida Scrub-Jays to directly characterize the mechanisms underlying how genetic material is transmitted to future generations. We link individual fitness with long-term genetic contributions and quantify the relative roles of evolutionary processes governing allele frequency change. This study clearly illustrates how short-term evolutionary change occurs within a natural population.

Abstract

A central goal of population genetics is to understand how genetic drift, natural selection, and gene flow shape allele frequencies through time. However, the actual processes underlying these changes—variation in individual survival, reproductive success, and movement—are often difficult to quantify. Fully understanding these processes requires the population pedigree, the set of relationships among all individuals in the population through time. Here, we use extensive pedigree and genomic information from a long-studied natural population of Florida Scrub-Jays (Aphelocoma coerulescens) to directly characterize the relative roles of different evolutionary processes in shaping patterns of genetic variation through time. We performed gene dropping simulations to estimate individual genetic contributions to the population and model drift on the known pedigree. We found that observed allele frequency changes are generally well predicted by accounting for the different genetic contributions of founders. Our results show that the genetic contribution of recent immigrants is substantial, with some large allele frequency shifts that otherwise may have been attributed to selection actually due to gene flow. We identified a few SNPs under directional short-term selection after appropriately accounting for gene flow. Using models that account for changes in population size, we partitioned the proportion of variance in allele frequency change through time. Observed allele frequency changes are primarily due to variation in survival and reproductive success, with gene flow making a smaller contribution. This study provides one of the most complete descriptions of short-term evolutionary change in allele frequencies in a natural population to date.

  • population genetics
  • pedigrees
  • fitness
  • gene flow
  • genetic drift

Footnotes

  • ↵1To whom correspondence should be addressed. Email: nancy.chen{at}rochester.edu.
  • Author contributions: N.C., A.G.C., and G.C. designed research; N.C., E.J.C., R.B., J.W.F., and S.J.S. performed research; N.C. and I.J. contributed new reagents/analytic tools; N.C., E.J.C., R.B., J.W.F., and S.J.S. performed data collection; N.C. and G.C. analyzed data; and N.C. and G.C. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: All data and code used in this study can be found at Figshare, 10.6084/m9.figshare.7044368.

  • See Commentary on page 1834.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1813852116/-/DCSupplemental.

Published under the PNAS license.

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Allele frequency dynamics in a pedigreed natural population
Nancy Chen, Ivan Juric, Elissa J. Cosgrove, Reed Bowman, John W. Fitzpatrick, Stephan J. Schoech, Andrew G. Clark, Graham Coop
Proceedings of the National Academy of Sciences Feb 2019, 116 (6) 2158-2164; DOI: 10.1073/pnas.1813852116

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Allele frequency dynamics in a pedigreed natural population
Nancy Chen, Ivan Juric, Elissa J. Cosgrove, Reed Bowman, John W. Fitzpatrick, Stephan J. Schoech, Andrew G. Clark, Graham Coop
Proceedings of the National Academy of Sciences Feb 2019, 116 (6) 2158-2164; DOI: 10.1073/pnas.1813852116
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