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

Vergara M, Basto MP, Madeira MJ, Gómez-Moliner BJ, Santos-Reis M, Fernandes C, Ruiz-González A - PLoS ONE (2015)

Bottom Line: However, there was significant indication for contemporary genetic structuring, albeit weak, into at least three different subpopulations.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology and Animal Cell Biology, Zoology Laboratory, University of the Basque Country (UPV/EHU), Vitoria-Gasteiz, Spain; Systematics, Biogeography and Population Dynamics Research Group, Lascaray Research Center, University of the Basque Country (UPV/EHU), Vitoria-Gasteiz, Spain.

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.

No MeSH data available.


a) Geographic location of the 252 individuals sequenced for mtDNA in the Iberian Peninsula, which was divided into four regions (NE, NW, SE and SW). Pie charts represent the proportion of the samples with each haplotype in each region. b) Median-joining network of the 252 mtDNA sequences. Each haplotype (H1 to H12) is represented by a different coloured symbol (the same in the map). Grey numbers on the lines connecting haplotypes indicate the position of mutations in the alignment. “n” is the number of sequences in each haplotype. Less frequent haplotypes are represented by a square (n = 1), diamond (n = 2) and triangle (n = 3) to facilitate their identification.
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pone.0134257.g002: a) Geographic location of the 252 individuals sequenced for mtDNA in the Iberian Peninsula, which was divided into four regions (NE, NW, SE and SW). Pie charts represent the proportion of the samples with each haplotype in each region. b) Median-joining network of the 252 mtDNA sequences. Each haplotype (H1 to H12) is represented by a different coloured symbol (the same in the map). Grey numbers on the lines connecting haplotypes indicate the position of mutations in the alignment. “n” is the number of sequences in each haplotype. Less frequent haplotypes are represented by a square (n = 1), diamond (n = 2) and triangle (n = 3) to facilitate their identification.

Mentions: The median-joining network (Fig 2) showed a star-like topology with most haplotypes differing by a single mutation from two common central haplotypes (H1 and H2), themselves also separated by a single substitution. Haplotype H12, found only in two samples from near the eastern Pyrenees, at eight mutational steps from the centre of the network, was the sole exception to this pattern. The network did not suggest any marked phylogeographic structure, with the most common haplotypes (H1: 41.6%; H2: 31.3%) scattered throughout the Iberian Peninsula. However, haplotype frequencies differed notably between regions, with all of them having private haplotypes with the exception of region SW (Fig 2). In the NW, H1 was the most common haplotype (68.5%) followed by H2 (20.4%), H7 (5.6%), the private haplotype H11 (3.7%) and H4 (1.8%). In the NE (Fig 2), H2 was the most frequent haplotype (38.9%), but some private haplotypes were also found in this region (H3, H8 and H10), including the most divergent haplotype H12, rendering the NE region the one with the highest haplotype diversity and haplotypic richness (S3 Table). The SW region, mostly corresponding to western Andalucía and south Portugal, harboured 5 haplotypes, the widespread H1 and H2 (55.9 and 36.8% respectively) plus H5, H7 and H9. Lastly, in the SE region, the analysed samples had haplotypes H1 (38.1%), H5 (33.3%), H9 (9.5%), H2 (4.8%) and the private haplotype H6 (14.3%).


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

Vergara M, Basto MP, Madeira MJ, Gómez-Moliner BJ, Santos-Reis M, Fernandes C, Ruiz-González A - PLoS ONE (2015)

a) Geographic location of the 252 individuals sequenced for mtDNA in the Iberian Peninsula, which was divided into four regions (NE, NW, SE and SW). Pie charts represent the proportion of the samples with each haplotype in each region. b) Median-joining network of the 252 mtDNA sequences. Each haplotype (H1 to H12) is represented by a different coloured symbol (the same in the map). Grey numbers on the lines connecting haplotypes indicate the position of mutations in the alignment. “n” is the number of sequences in each haplotype. Less frequent haplotypes are represented by a square (n = 1), diamond (n = 2) and triangle (n = 3) to facilitate their identification.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4519273&req=5

pone.0134257.g002: a) Geographic location of the 252 individuals sequenced for mtDNA in the Iberian Peninsula, which was divided into four regions (NE, NW, SE and SW). Pie charts represent the proportion of the samples with each haplotype in each region. b) Median-joining network of the 252 mtDNA sequences. Each haplotype (H1 to H12) is represented by a different coloured symbol (the same in the map). Grey numbers on the lines connecting haplotypes indicate the position of mutations in the alignment. “n” is the number of sequences in each haplotype. Less frequent haplotypes are represented by a square (n = 1), diamond (n = 2) and triangle (n = 3) to facilitate their identification.
Mentions: The median-joining network (Fig 2) showed a star-like topology with most haplotypes differing by a single mutation from two common central haplotypes (H1 and H2), themselves also separated by a single substitution. Haplotype H12, found only in two samples from near the eastern Pyrenees, at eight mutational steps from the centre of the network, was the sole exception to this pattern. The network did not suggest any marked phylogeographic structure, with the most common haplotypes (H1: 41.6%; H2: 31.3%) scattered throughout the Iberian Peninsula. However, haplotype frequencies differed notably between regions, with all of them having private haplotypes with the exception of region SW (Fig 2). In the NW, H1 was the most common haplotype (68.5%) followed by H2 (20.4%), H7 (5.6%), the private haplotype H11 (3.7%) and H4 (1.8%). In the NE (Fig 2), H2 was the most frequent haplotype (38.9%), but some private haplotypes were also found in this region (H3, H8 and H10), including the most divergent haplotype H12, rendering the NE region the one with the highest haplotype diversity and haplotypic richness (S3 Table). The SW region, mostly corresponding to western Andalucía and south Portugal, harboured 5 haplotypes, the widespread H1 and H2 (55.9 and 36.8% respectively) plus H5, H7 and H9. Lastly, in the SE region, the analysed samples had haplotypes H1 (38.1%), H5 (33.3%), H9 (9.5%), H2 (4.8%) and the private haplotype H6 (14.3%).

Bottom Line: However, there was significant indication for contemporary genetic structuring, albeit weak, into at least three different subpopulations.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology and Animal Cell Biology, Zoology Laboratory, University of the Basque Country (UPV/EHU), Vitoria-Gasteiz, Spain; Systematics, Biogeography and Population Dynamics Research Group, Lascaray Research Center, University of the Basque Country (UPV/EHU), Vitoria-Gasteiz, Spain.

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.

No MeSH data available.