Inferring Population Genetic Structure in Widely and Continuously Distributed Carnivores: The Stone Marten (Martes foina) as a Case Study

PLoS One. 2015 Jul 29;10(7):e0134257. doi: 10.1371/journal.pone.0134257. eCollection 2015.

Abstract

The stone marten is a widely distributed mustelid in the Palaearctic region that exhibits variable habitat preferences in different parts of its range. The species is a Holocene immigrant from southwest Asia which, according to fossil remains, followed the expansion of the Neolithic farming cultures into Europe and possibly colonized the Iberian Peninsula during the Early Neolithic (ca. 7,000 years BP). However, the population genetic structure and historical biogeography of this generalist carnivore remains essentially unknown. In this study we have combined mitochondrial DNA (mtDNA) sequencing (621 bp) and microsatellite genotyping (23 polymorphic markers) to infer the population genetic structure of the stone marten within the Iberian Peninsula. The mtDNA data revealed low haplotype and nucleotide diversities and a lack of phylogeographic structure, most likely due to a recent colonization of the Iberian Peninsula by a few mtDNA lineages during the Early Neolithic. The microsatellite data set was analysed with a) spatial and non-spatial Bayesian individual-based clustering (IBC) approaches (STRUCTURE, TESS, BAPS and GENELAND), and b) multivariate methods [discriminant analysis of principal components (DAPC) and spatial principal component analysis (sPCA)]. Additionally, because isolation by distance (IBD) is a common spatial genetic pattern in mobile and continuously distributed species and it may represent a challenge to the performance of the above methods, the microsatellite data set was tested for its presence. Overall, the genetic structure of the stone marten in the Iberian Peninsula was characterized by a NE-SW spatial pattern of IBD, and this may explain the observed disagreement between clustering solutions obtained by the different IBC methods. However, there was significant indication for contemporary genetic structuring, albeit weak, into at least three different subpopulations. The detected subdivision could be attributed to the influence of the rivers Ebro, Tagus and Guadiana, suggesting that main watercourses in the Iberian Peninsula may act as semi-permeable barriers to gene flow in stone martens. To our knowledge, this is the first phylogeographic and population genetic study of the species at a broad regional scale. We also wanted to make the case for the importance and benefits of using and comparing multiple different clustering and multivariate methods in spatial genetic analyses of mobile and continuously distributed species.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bayes Theorem
  • Cluster Analysis
  • DNA, Mitochondrial / genetics
  • Europe
  • Fossils
  • Gene Flow / genetics
  • Genetic Variation / genetics
  • Genetics, Population / methods
  • Haplotypes / genetics
  • Microsatellite Repeats / genetics
  • Mustelidae / genetics*
  • Phylogeography / methods
  • Principal Component Analysis / methods
  • Sequence Analysis, DNA / methods

Substances

  • DNA, Mitochondrial

Grants and funding

This study has been partially funded by the Basque Government through the Research group on ‘‘Systematics, Biogeography and Population Dynamics’’ (Ref. IT317-10; GIC10/76; IT575-13). MV (Ref: RBFI-2012-446) and ARG (Ref: DKR-2012-64) were supported by a PhD and post-doctoral fellowships awarded by the Dept. of Education, Universities and Research of the Basque Government. MPB and CF acknowledge financial support from Fundação para a Ciência e Tecnologia through the PhD fellowship SFRH/BD/38410/2007, the Ciência 2007 contract C2007-UL-342-CBA1, and the research project PTDC/BIA-BEC/101511/2008. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.