Elsevier

Biological Conservation

Volume 155, October 2012, Pages 186-192
Biological Conservation

Perspective
Conservation genomics in perspective: A holistic approach to understanding Canis evolution in North America

https://doi.org/10.1016/j.biocon.2012.05.017 Get rights and content

Abstract

The use of genome-wide single nucleotide polymorphisms (SNPs) in wildlife conservation is growing rapidly and promises to revolutionize the field of population genetics. However, genomic data should not be interpreted in isolation of other biological and complementary genetic data. Here, we used recently published genome-wide SNP data from Canis species in combination with data from more traditional genetic markers and evidence from non-genetic fields to show how a broader frame of reference is important for interpretation of genomic data. We conducted a principal components analysis (PCA) and phylogenetic analysis of 48 K SNP data to show that a three-species model of Canis evolution in North America is not rejected by the data and deserves further investigation with more representative samples from Algonquin Park. We also demonstrate how a holistic perspective provides a more complete picture of evolutionary processes underlying diversification and speciation events in the genus Canis. Overall, we highlight the importance of careful examination and synthesis of all lines of evidence for the implementation of effective conservation policies for endangered species.

Highlights

► We re-analyze 48 K SNP data to test the eastern wolf (C. lycaon) hypothesis. ► We use a holistic approach to understand Canis evolution in North America. ► We conclude that the C. lycaon hypothesis cannot be rejected by the data. ► Wolves from Algonquin Provincial Park represent a North American evolved wolf.► Biased assumptions and narrow scientific perspective hinder conservation efforts.

Introduction

The use of genome-wide single nucleotide polymorphisms (SNPs) in assessing population structure in wildlife species has seen a marked increase in recent years. SNPs are an attractive marker for evolutionary studies because they occur throughout the genome, they are bi-parentally inherited, they follow a relatively simple and well-defined pattern of mutation, genotypes are easily standardized across laboratories, and high-throughput technology allows thousands of loci to be analyzed for a relatively low cost (Morin et al., 2004). They should not, however, be viewed as an indiscriminate replacement for other molecular markers in the population genetics toolkit because SNPs may not be “unconditionally superior to more traditional approaches” in all circumstances (Schlötterer, 2004), particularly when sampling is inadequate and/or metadata is insufficient or misinterpreted such that erroneous conclusions are drawn.

In a recent volume of Genome Research, vonHoldt et al. (2011) analyzed 48,036 SNPs in wolves, coyotes, and dogs to develop a better understanding of admixture in wild canid populations. The paper provides an extensive amount of genomic data that contributes significantly to the field of canine genetics. The data do not, however, support the authors’ conclusion of a two-species model of Canis evolution in North America that relegates a third species, the eastern wolf (Canis lycaon) (referred to as “Great Lakes wolf” by the authors), to the product of hybridization between gray wolves (C. lupus) and coyotes (C. latrans). The incorrect conclusions drawn by the authors contribute to the perceived lack of consensus regarding wolf taxonomy that has led the United States Fish and Wildlife Service (USFWS) to retract its original recognition of the eastern wolf as a distinct species, C. lycaon (US Fish, 2011a, US Fish, 2011b) and continue to treat it as a gray wolf subspecies (C. lupus lycaon) (USFWS, 2012), despite the lack of scientific evidence to support it as such. Here, we re-analyzed different subgroups of the 48 K SNP data and interpret the results within a broader genetic and ecological context. We conclude that a three-species model of Canis evolution that includes C. lycaon as a distinct North American evolved wolf is not rejected by the data and therefore deserves further investigation. Moreover, we demonstrate that the data presented by vonHoldt et al. (2011) are misconstrued due to flawed assumptions that bias the interpretation on various analytical levels, and because the authors fail to interpret their findings within the context of ecology, natural history, the fossil record, and other genetic markers.

Section snippets

Methods

We provide a critique of the methods, results, and conclusions of vonHoldt et al. (2011) and highlight points that need to be more fully considered in the interpretation of the data presented by the authors. To provide further insight into the evolutionary history of the Canis genus, we performed novel analyses on the SNP data presented in vonHoldt et al. (2011). We conducted a centred, unscaled principal components analysis (PCA) implemented in the adegenet package (Jombart and Ahmed, 2011) of

Sample selection and ancestry assignment

First, wolves from the Great Lakes region contain both gray wolf and eastern wolf genes (Wheeldon and White, 2009, Fain et al., 2010) but they are not representative of the historic eastern wolf that has been proposed as sharing a common evolutionary history in North America alongside coyotes (Wilson et al., 2000). Previous work on mitochondrial DNA (mtDNA) (Wilson et al., 2000, Grewal et al., 2004), Y-chromosome DNA (Wilson et al., in press), and microsatellite loci (Rutledge et al., 2010a)

Conclusions

Based on the genetic data in combination with a broader scientific perspective, the C. lycaon hypothesis cannot be rejected. We conclude, therefore, that the biases introduced by vonHoldt et al. (2011) through the methodological design of the species datasets grouped for analyses (i.e. gray wolves and coyotes), along with the limited sample size of representative eastern wolves from Algonquin Provincial Park, and the unresolved issues associated with SNP analyses and ascertainment bias, render

Note

Though not important for the purposes of this commentary, a correction to the text of vonHoldt et al. (2011) is that the reference to samples from the 400 to 500-year-old site described in Rutledge et al. (2010c) are from southern Ontario, not from Quebec.

Acknowledgments

Thank you to Bridgett vonHoldt and her collaborators for supplying the 48 K SNP dataset (from vonHoldt et al. 2011).

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