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

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.

Landscape effects on the contemporary genetic structure of Ruffed Grouse (Bonasa umbellus) populations

“…As such, we should no longer assume that dispersal distance and distribution are the only factors driving dispersal patterns, and that IBR is only likely to affect species at small scales. This adds to the growing body of work highlighting the importance of evaluating the role of environmental variables in population genetic structuring (McRae & Beier, 2007;Vergara et al, 2015). It also underscores the need for more landscape genetic studies focusing on broadly distributed taxa because they may be experiencing genetic isolation regardless of their relatively ubiquitous distributions.…”

Assessment of spatial genetic structure to identify populations at risk for infection of an emerging epizootic disease

“…By treating allele frequencies as correlated across related clusters as opposed to independently distributed, spatially explicit clustering is more likely to represent the true underlying structure of continuously distributed populations (Guillot, 2008). Thus, clustering methods accounting for genetic autocorrelation are likely to have increased power to detect cryptic subpopulation structure and may outperform other clustering and edge detection methods in identifying features associated with genetic discontinuities (Safner et al, 2011; Vergara et al, 2015). While gene flow may be widespread in continuously distributed populations, disease prevalence rates can vary spatially even with minute deviations from genetic panmixia (Blanchong et al, 2008).…”

Genetic analysis of Turkish martens: Do two species of the genus Martes occur in Anatolia?

“…() and Vergara et al. () found two dominant haplotypes represented in their samples of stone marten from Bulgaria and the Iberian Peninsula, respectively. Similarly, we found two primary haplotypes (MFO1 and MFO2) represented in the Turkish samples and sequences included in our study.…”

“…Vergara et al. () analysed 252 samples of M. foina from the Iberian Peninsula (Portugal and Spain) using of four mitochondrial genes/regions (including the 3′ half of the CytB gene) comprising 621 bp and 23 microsatellite loci. For the mitochondrial sequence data, they found 12 haplotypes, with a haplotype diversity of 0.705 and a nucleotide diversity of 0.00169.…”

“…This hypothesis is consistent with previous suggestions relating to the origin of some populations of the European stone marten. For example, some authors have suggested that the stone marten is a Holocene immigrant that colonized Europe from South‐West Asia following the expansion of Neolithic farming cultures from the Near East (Anderson, ; Sommer & Benecke, ; Vergara et al., ). Taking into consideration the current distribution and star‐shaped network of stone marten haplotypes, both Tajima's D and mismatch distribution analyses showed signatures consistent with a rapid population expansion (Figure ; Table ).…”