Broad geographic sampling reveals the shared basis and environmental correlates of seasonal adaptation in Drosophila

  1. Heather E Machado  Is a corresponding author
  2. Alan Bergland  Is a corresponding author
  3. Ryan W Taylor
  4. Susanne Tilk
  5. Emily Behrman
  6. Kelly Dyer
  7. Daniel K Fabian
  8. Thomas Flatt
  9. Josefa González
  10. Talia L Karasov
  11. Bernard Y Kim
  12. Iryna Kozeretska
  13. Brian P Lazzaro
  14. Thomas Merritt
  15. John E Pool
  16. Katherine O'Brien
  17. Subhash Rajpurohit
  18. Paula R Roy
  19. Stephen W Schaeffer
  20. Svitlana Serga
  21. Paul Schmidt  Is a corresponding author
  22. Dmitri A Petrov
  1. Wellcome Sanger Institute, United Kingdom
  2. University of Virginia, United States
  3. Stanford University, United States
  4. University of Pennsylvania, United States
  5. University of Georgia, United States
  6. University of Cambridge, United Kingdom
  7. University of Fribourg, Switzerland
  8. Institute of Evolutionary Biology, CSIC- Universitat Pompeu Fabra, Spain
  9. University of Utah, United States
  10. Taras Shevchenko National Univ Kyiv, Ukraine
  11. Cornell University, United States
  12. Laurentian University, Canada
  13. University of Wisconsin-Madison, United States
  14. University of Kansas, United States
  15. The Pennsylvania State University, United States
  16. Taras Shevchenko National University of Kyiv, Ukraine

Abstract

To advance our understanding of adaptation to temporally varying selection pressures, we identified signatures of seasonal adaptation occurring in parallel among Drosophila melanogaster populations. Specifically, we estimated allele frequencies genome-wide from flies sampled early and late in the growing season from 20 widely dispersed populations. We identified parallel seasonal allele frequency shifts across North America and Europe, demonstrating that seasonal adaptation is a general phenomenon of temperate fly populations. Seasonally fluctuating polymorphisms are enriched in large chromosomal inversions and we find a broad concordance between seasonal and spatial allele frequency change. The direction of allele frequency change at seasonally variable polymorphisms can be predicted by weather conditions in the weeks prior to sampling, linking the environment and the genomic response to selection. Our results suggest that fluctuating selection is an important evolutionary force affecting patterns of genetic variation in Drosophila.

Data availability

- All raw sequence data have been deposited to the NCBI short read archive (SRA; BioProject Accession #PRJNA308584; accession numbers for each sample can be found in Supplemental Table 1).- Code to conduct these analyses, primary results files, and code to reproduce the figures are available at https://github.com/machadoheather/dmel_seasonal_RTEC.- VCF files with the raw allele frequencies per population and a R-data file of allele frequencies and effective sample sizes (Nc; compatible with scripts) are available on DataDryad (https://datadryad.org/stash/dataset/doi:10.5061/dryad.4r7b826).

The following data sets were generated

Article and author information

Author details

  1. Heather E Machado

    CASM, Wellcome Sanger Institute, Hinxton, United Kingdom
    For correspondence
    heather.machado@sanger.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1523-3937
  2. Alan Bergland

    Department of Biology, University of Virginia, Charlottesville, United States
    For correspondence
    aob2x@virginia.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7145-7575
  3. Ryan W Taylor

    Department of Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9003-6378
  4. Susanne Tilk

    Department of Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9156-9360
  5. Emily Behrman

    Dept. of Biology, University of Pennsylvania, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2472-9635
  6. Kelly Dyer

    University of Georgia, Athens, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Daniel K Fabian

    Centre for Pathogen Evolution, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Thomas Flatt

    Department of Biology, University of Fribourg, Fribourg, Switzerland
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5990-1503
  9. Josefa González

    Institute of Evolutionary Biology, CSIC- Universitat Pompeu Fabra, Barcelona, Spain
    Competing interests
    The authors declare that no competing interests exist.
  10. Talia L Karasov

    Department of Biology, University of Utah, Salt Lake City, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Bernard Y Kim

    Department of Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5025-1292
  12. Iryna Kozeretska

    General and Medical Genetics Dept, Taras Shevchenko National Univ Kyiv, Kyiv, Ukraine
    Competing interests
    The authors declare that no competing interests exist.
  13. Brian P Lazzaro

    Department of Entomology, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.
  14. Thomas Merritt

    Department of Chemistry & Biochemistry, Laurentian University, Sudbury, Canada
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4795-7534
  15. John E Pool

    Laboratory of Genetics, University of Wisconsin-Madison, Madison, United States
    Competing interests
    The authors declare that no competing interests exist.
  16. Katherine O'Brien

    Department of Biology, University of Pennsylvania, Columbus, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4660-0338
  17. Subhash Rajpurohit

    Dept. of Biology, University of Pennsylvania, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
  18. Paula R Roy

    Department of Ecology and Evolutionary Biology, University of Kansas, Lawrence, United States
    Competing interests
    The authors declare that no competing interests exist.
  19. Stephen W Schaeffer

    Department of Biology, The Pennsylvania State University, University Park, United States
    Competing interests
    The authors declare that no competing interests exist.
  20. Svitlana Serga

    Taras Shevchenko National University of Kyiv, Taras Shevchenko National University of Kyiv, Kyiv, Ukraine
    Competing interests
    The authors declare that no competing interests exist.
  21. Paul Schmidt

    Dept. of Biology, University of Pennsylvania, Philadelphia, United States
    For correspondence
    schmidtp@upenn.edu
    Competing interests
    The authors declare that no competing interests exist.
  22. Dmitri A Petrov

    Department of Biology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3664-9130

Funding

NIH Office of the Director (R01GM100366)

  • Dmitri A Petrov

NIH Office of the Director (R35GM118165)

  • Dmitri A Petrov

NIH Office of the Director (R01GM100366,R01GM137430)

  • Alan Bergland

NIH Office of the Director (F32GM097837,R35GM119686)

  • Alan Bergland

European Commission (H2020-ERC-2014-CoG-647900)

  • Josefa González

Natural Sciences and Engineering Research Council of Canada (RGPIN-2018-05551)

  • Thomas Merritt

Canada Research Chairs (950-230113)

  • Thomas Merritt

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Magnus Nordborg, Austrian Academy of Sciences, Austria

Version history

  1. Received: February 16, 2021
  2. Accepted: June 21, 2021
  3. Accepted Manuscript published: June 22, 2021 (version 1)
  4. Version of Record published: July 1, 2021 (version 2)

Copyright

© 2021, Machado et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Heather E Machado
  2. Alan Bergland
  3. Ryan W Taylor
  4. Susanne Tilk
  5. Emily Behrman
  6. Kelly Dyer
  7. Daniel K Fabian
  8. Thomas Flatt
  9. Josefa González
  10. Talia L Karasov
  11. Bernard Y Kim
  12. Iryna Kozeretska
  13. Brian P Lazzaro
  14. Thomas Merritt
  15. John E Pool
  16. Katherine O'Brien
  17. Subhash Rajpurohit
  18. Paula R Roy
  19. Stephen W Schaeffer
  20. Svitlana Serga
  21. Paul Schmidt
  22. Dmitri A Petrov
(2021)
Broad geographic sampling reveals the shared basis and environmental correlates of seasonal adaptation in Drosophila
eLife 10:e67577.
https://doi.org/10.7554/eLife.67577

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https://doi.org/10.7554/eLife.67577

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