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Disentangling the genetic effects of refugial isolation and range expansion in a trans-continentally distributed species

Heredity (2018) | Download Citation

Abstract

In wide-ranging taxa with historically dynamic ranges, past allopatric isolation and range expansion can both influence the current structure of genetic diversity. Considering alternate historical scenarios involving expansion from either a single refugium or from multiple refugia can be useful in differentiating the effects of isolation and expansion. Here, we examined patterns of genetic variability in the trans-continentally distributed painted turtle (Chrysemys picta). We utilized an existing phylogeographic dataset for the mitochondrial control region and generated additional data from nine populations for the mitochondrial control region (n = 302) and for eleven nuclear microsatellite loci (n = 247). We created a present-day ecological niche model (ENM) for C. picta and hindcast this model to three reconstructions of historical climate to define three potential scenarios with one, two, or three refugia. Finally, we employed spatially-explicit coalescent simulations and an approximate Bayesian computation (ABC) framework to test which scenario best fit the observed genetic data. Simulations indicated that phylogeographic and multilocus population-level sampling both could differentiate among refugial scenarios, although inferences made using mitochondrial data were less accurate when a longer coalescence time was assumed. Furthermore, all empirical genetic datasets were most consistent with expansion from a single refugium based on ABC. Our results indicate a stronger role for post-glacial range expansion, rather than isolation in allopatric refugia followed by range expansion, in structuring diversity in this species. To distinguish among complex historical scenarios, we recommend explicitly modeling the effects of range expansion and evaluating alternate refugial scenarios for wide-ranging taxa.

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Acknowledgements

Blood and tissue samples were collected under the appropriate permits (IACUC permits from Earlham College and the University of Wisconsin-Madison; Indiana Scientific Purposes license #16-030; Scientific Collecting Permit #135 from the Wisconsin Department of Natural Resources; New York License to Collect and Possess #1757; UBC Animal Care Certificate # A11-0163 and BC Ministry of Environment sampling permit # VI11-71744). The Sackler Institute of Comparative Genomics and George Amato provided lab facilities and materials. Simulations and other computationally intensive analyses were carried out through the CUNY High Performance Computing Core, College of Staten Island, City University of New York. JBI was supported by the Earlham College Summer Research Fund. BNR was supported by a Gerstner Foundation postdoctoral fellowship and the Russ Gilder Graduate School at the American Museum of Natural History. Finally, comments provided by the editorial staff and three anonymous reviewers greatly improved the manuscript, and we thank them for their hard work and insight.

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Affiliations

  1. W.K. Kellogg Biological Station, Michigan State University, Hickory Corners, MI, USA

    • B. N. Reid
  2. American Museum of Natural History, New York, NY, USA

    • B. N. Reid
    •  & C. J. Raxworthy
  3. The Graduate Center, City University of New York, New York, NY, USA

    • J. M. Kass
    •  & S. Wollney
  4. City College of the City University of New York, New York, NY, USA

    • J. M. Kass
  5. City University of New York- College of Staten Island, New York, NY, USA

    • S. Wollney
    • , E. M. Viola
    •  & J. Pantophlet
  6. University of British Columbia-Okanagan, Kelowna, BC, Canada

    • E. L. Jensen
    •  & M. A. Russello
  7. Earlham College, Richmond, IN, USA

    • J. B. Iverson
  8. University of Wisconsin, Madison, WI, USA

    • M. Z. Peery
  9. New York University, New York, NY, USA

    • E. Naro-Maciel

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Correspondence to B. N. Reid.

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https://doi.org/10.1038/s41437-018-0135-5