Research ArticleEVOLUTIONARY GENETICS

Whole-genome sequence analysis shows that two endemic species of North American wolf are admixtures of the coyote and gray wolf

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Science Advances  27 Jul 2016:
Vol. 2, no. 7, e1501714
DOI: 10.1126/sciadv.1501714

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  • RE: Response to Sutherland eLetter
    • Bridget vonHoldt, Princeton University
    • Other Contributors:
      • James A. Cahill, University of California Santa Cruz
      • Ilan Gronau, Interdisciplinary Center Herzliya
      • Beth Shapiro, University of California Santa Cruz
      • Jeff Wall, University of California San Francisco
      • Robert Wayne, University of California Los Angeles

    Response to Sutherland’s eLetter

    Bridgett M. vonHoldt, James A. Cahill, Ilan Gronau, Beth Shapiro, Jeff Wall, Robert K. Wayne

    EDITORIAL NOTE: Formal Correction to Follow

    REVISED TABLE

    We reviewed Sutherland's comments (below in italics) carefully and feel that they can be fully addressed by corrections to the appropriate places in the manuscript and Table S1 (see link directly above "REVISED TABLE"). These corrections do not change the underlying results or interpretations, but we feel they resolve all of Sutherland's concerns.

     

    eLetter Responses:

     

    There are several errors in vonHoldt et al. (2016) that would seem worthy of formal correction by the authors, especially given the significant implications of their results for threatened taxa such as the red wolf. These errors include:

     

    1. vonHoldt et al. (2016) indicate that they worked with the genomes of a total of 3 red wolves, one of which apparently derived from a previous study, and two of which were newly sequenced for this study. However, their Table 1 provides an incorrect citation number for the origin of redwolf1, "54", which in the bibliography of the paper is listed as a paper by Lunter and Goodson that has...

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    Competing Interests: None declared.
  • RE: corrections in the text of vonHoldt et al. 2016

    There are several errors in vonHoldt et al. (2016) that would seem worthy of formal correction by the authors, especially given the significant implications of their results for threatened taxa such as the red wolf. These errors include:

    1. vonHoldt et al. (2016) indicate that they worked with the genomes of a total of 3 red wolves, one of which apparently derived from a previous study, and two of which were newly sequenced for this study. However, their Table 1 provides an incorrect citation number for the origin of redwolf1, "54", which in the bibliography of the paper is listed as a paper by Lunter and Goodson that has nothing specific to do with canid genetics. So the origin and identity of redwolf1 remains unclear.

    2. The caption for Table 1 indicates the table shows ancestry proportions, but no ancestry proportions are actually listed.

    3. Looking in Table S1 (in the Supplemental materials), which presents D statistic results for various combinations of species, the three red wolves are no longer referred to as redwolf1, 2, and 3, as they are in the text of the article. Instead, there are only two red wolves referred to in Table S1, "redwolf661" and "redwolf762", even though D statistic results are shown for three red wolves in Figure S3, so presumably such calculations were completed for all three specimens? Interestingly, in another portion of the text (page 7) the authors refer to complete sequenced genomes for...

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    Competing Interests: None declared.
  • RE: A response to Kays
    • Bridgett vonHoldt, Assistant Professor, Princeton University
    • Other Contributors:
      • James Cahill, Graduate student, UC Santa Cruz
      • Ilan Gronau, Professor, Efi Arazi School of Computer Science, Herzliya Interdisciplinary Center
      • Annabel Beichman, Graduate student, UC Los Angeles
      • Kirk E Lohmueller, Assistant Professor, UC Los Angeles
      • John P Pollinger, Staff scientist, UC Los Angeles
      • Jeff Wall, Assistant Professor, UC San Francisco
      • Beth Shapiro, Professor, UC Santa Cruz
      • Robert Wayne, Professor, UC Los Angeles

    Dr. Kays invokes a mitochondrial DNA (mtDNA) capture hypothesis to explain potential discordances between mtDNA haplotype and complete genome sequence data. However, the presence of a divergent mtDNA haplotype is not evidence enough to support the mtDNA capture hypothesis or the existence of a separate species. Caution is warranted when interpreting results from mtDNA sequences as they derive from a single non-recombining locus that only represents matrilineal dynamics and may be affected by natural selection (e.g. 1). It is well known that gene genealogies are highly variable due to the randomness inherent in the coalescent process (e.g. 2-4). In other words, a single demographic model can and will generate very different genealogies. Divergence and recent branches within a genealogy are not surprising and are even expected. Further, this dichotomy becomes more pronounced with large ancestral population sizes (N), as the variance in the time to the most recent common ancestor is of the order N2 (3-5).

    Gray wolves and coyotes are known to have had a large ancestral population size (e.g. effective size 30,000-45,000 for wolves, 6). Therefore, coalescent processes can generate divergent lineages as well as clusters of closely related mtDNA haplotypes. A divergent lineage, if examined in isolation, could be misinterpreted as support for a distinct species if mtDNA sampling was geographically restricted. The divergent and controversial “Algonquin” or eastern wolf (Canis...

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    Competing Interests: None declared.
  • A hypothesis for the disagreement between nuclear and mitochondrial DNA of North American Canis
    • Roland Kays, Scientist, North Carolina Museum of Natural Sciences and North Carolina State University

    The whole-genome analysis of VonHoldt et al. (1) provides the most complete picture to date of North American Canis autosomes, finding no history for long independent, species level evolutionary histories for the red wolf (Canis rufus) or eastern wolf (C. lycaon), suggesting instead that both have a modern origin through hybridization between wolves (C. lupus) and coyotes (C. latrans). This compelling nuclear DNA evidence leaves one mystery yet unsolved - why do many eastern canids have a unique mitochondrial haplotype that does not match extant coyotes or wolves?
    This 'lycaon-type' haplotype was the most compelling evidence used to argue that eastern wolves should be recognized as a unique species (2) because it is similar to coyotes, yet different enough (3%) to suggest ~500K years of divergence between the two. Thus, the eastern wolf was proposed as a sister species to the coyote, evolving into a larger, deer-eating predator in eastern forests. Samples from historic and fossil eastern wolves have likewise returned mtDNA haplotypes similar to this lycaon-type (3) or to coyotes (4, 5), further supporting the coyote sister species hypothesis. Red wolves also have coyote-like mtDNA (6). Thus while the nuclear genome results of VonHoldt et al. (1) support a two species model for North American Canids (C. lupus & latrans), the mtDNA patterns support a three or four species model (adding C. lycaon and/or rufus).

    I suggest that the discordance be...

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    Competing Interests: None declared.