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Population genomic data reveal extreme geographic subdivision and novel conservation actions for the declining foothill yellow-legged frog

Heredityvolume 121pages112125 (2018) | Download Citation

Abstract

Genomic data have the potential to inform high resolution landscape genetic and biological conservation studies that go far beyond recent mitochondrial and microsatellite analyses. We characterize the relationships of populations of the foothill yellow-legged frog, Rana boylii, a declining, “sentinel” species for stream ecosystems throughout its range in California and Oregon. We generated RADseq data and applied phylogenetic methods, hierarchical Bayesian clustering, PCA and population differentiation with admixture analyses to characterize spatial genetic structure across the species range. To facilitate direct comparison with previous analyses, we included many localities and individuals from our earlier work based on mitochondrial DNA. The results are striking, and emphasize the power of our landscape genomic approach. We recovered five extremely differentiated primary clades that indicate that R. boylii may be the most genetically differentiated anuran yet studied. Our results provide better resolution and more spatially consistent patterns than our earlier work, confirming the increased resolving power of genomic data compared to single-locus studies. Genomic structure is not equal across the species distribution. Approximately half the range of R. boylii consists of a single, relatively uniform population, while Sierra Nevada and coastal California clades are deeply, hierarchically substructured with biogeographic breaks observed in other codistributed taxa. Our results indicate that clades should serve as management units for R. boylii rather than previously suggested watershed boundaries, and that the near-extinct population from southwestern California is particularly diverged, exhibits the lowest genetic diversity, and is a critical conservation target for species recovery.

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Acknowledgements

We thank Amy Lind, the Museum of Vertebrate Zoology, University of California, Berkeley, and the Department of Herpetology at the California Academy of Sciences for providing samples, Erin Toffelmier and Genevieve Mount for laboratory assistance, and Phil Spinks for conversations regarding analyses. This work used the Vincent J. Coates Genomics Sequencing Laboratory at UC Berkeley, supported by NIH S10 Instrumentation Grants S10RR029668 and S10RR027303, and the Comet cluster at the San Diego Supercomputing Center—an XSEDE resource (Towns et al. 2014), supported by NSF ACI-1548562. EMM and HBS are supported by NSF-DEB 1257648 and grants from the US Fish and Wildlife Service and the US Bureau of Reclamation. MG was supported by a grant from The Scientific and Technological Council of Turkey (TUBITAK).

Author contributions

EMM analyzed the data and wrote the initial draft manuscript, MG collected the data and edited the manuscript, and HBS developed the initial project and edited the manuscript.

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Affiliations

  1. Department of Ecology and Evolutionary Biology, La Kretz Center for California Conservation Science, and Institute of the Environment and Sustainability, University of California, Los Angeles, CA, USA

    • Evan McCartney-Melstad
    • , Müge Gidiş
    •  & H. Bradley Shaffer
  2. Kütahya School of Health, Dumlupınar University, Kütahya, Turkey

    • Müge Gidiş

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The authors declare that they have no conflict of interest.

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Correspondence to Evan McCartney-Melstad.

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https://doi.org/10.1038/s41437-018-0097-7

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