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Taxonomic and conservation implications of population genetic admixture, mito-nuclear discordance, and male-biased dispersal of a large endangered snake, Drymarchon couperi - PubMed

  • ️Tue Jan 01 2019

Taxonomic and conservation implications of population genetic admixture, mito-nuclear discordance, and male-biased dispersal of a large endangered snake, Drymarchon couperi

Brian Folt et al. PLoS One. 2019.

Abstract

Accurate species delimitation and description are necessary to guide effective conservation of imperiled species, and this synergy is maximized when multiple data sources are used to delimit species. We illustrate this point by examining Drymarchon couperi (Eastern Indigo Snake), a large, federally-protected species in North America that was recently divided into two species based on gene sequence data from three loci and heuristic morphological assessment. Here, we re-evaluate the two-species hypothesis for D. couperi by evaluating both population genetic and gene sequence data. Our analyses of 14 microsatellite markers revealed 6-8 genetic population clusters with significant admixture, particularly across the contact zone between the two hypothesized species. Phylogenetic analyses of gene sequence data with maximum-likelihood methods suggested discordance between mitochondrial and nuclear markers and provided phylogenetic support for one species rather than two. For these reasons, we place Drymarchon kolpobasileus into synonymy with D. couperi. We suggest inconsistent patterns between mitochondrial and nuclear DNA are driven by high dispersal of males relative to females. We advocate for species delimitation exercises that evaluate admixture and gene flow in addition to phylogenetic analyses, particularly when the latter reveal monophyletic lineages. This is particularly important for taxa, such as squamates, that exhibit strong sex-biased dispersal. Problems associated with over-delimitation of species richness can become particularly acute for threatened and endangered species, because of high costs to conservation when taxonomy demands protection of more individual species than are supported by accumulating data.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Bar plots of population clustering estimated through the Bayesian clustering algorithm Structure with K = 8 for specimens of Drymarchon couperi (Eastern Indigo Snake).

The y-axis is the proportion of individual ancestry for each cluster; in the x-axis, number represents county where sample was collected. County names for each number are shown in S5 Table. Some counties (e.g., 12–26) are overlapping on the x-axis due to small sample size per cluster.

Fig 2
Fig 2

Maps of Drymarchon couperi (sensu lato) sampling sites represented as (A) pie charts of percent ancestry within population clusters identified by Structure analyses with K = 8 populations, and (B) cluster membership from the Geneland analysis with K = 6 populations. For both panels, percent ancestry and/or cluster membership was assigned given the number of populations K that received the highest support during analyses. The black dashed lines indicates the boundary between the Atlantic and Gulf lineages from [26]. For panel (A), colors are as in Fig 1.

Fig 3
Fig 3

Spatially lagged scores for each sample from the first (A) and second (B) axes of a spatial principle components analysis (sPCA). Samples with more extreme values/colors are more genetically differentiated. Atlantic lineage samples [26] are displayed using circles while Gulf lineage samples are displayed using squares; the black dashed lines indicates the boundary between the Atlantic and Gulf lineages.

Fig 4
Fig 4. Plots of pairwise genetic distance (1—proportion of shared alleles) against Euclidean distance (km) showing positive isolation by distance.

Solid lines show the predicted pattern of isolation by distance from a linear mixed-effects model with maximum-likelihood population effects (MLPEs; [64]). (A) Pairwise distances within Atlantic lineage samples; (B) pairwise distances within Atlantic lineage samples (gray circles) and among samples from both Atlantic and Gulf lineages (white circles); (C) pairwise distances within Gulf lineage samples; (D) pairwise distances within Gulf lineage samples (gray circles) and among samples from both Atlantic and Gulf lineages (white circles).

Fig 5
Fig 5. Maximum-likelihood phylogeny of Eastern Indigo Snakes (Drymarchon couperi) and outgroups inferred from sequence data from the mitochondrial loci cytochrome b and ND4.

Indigo snake samples are labeled by hypothetical lineage, state, county, and sample numbers from [26]. Colors: blue = Atlantic lineage, orange = Gulf lineage. Bootstrap support is listed for major nodes.

Fig 6
Fig 6. Maximum-likelihood phylogeny of Eastern Indigo Snakes (Drymarchon couperi) and outgroups inferred from sequence data from the nuclear gene neurotrophin-3 (NT3).

Indigo snake samples are labeled by hypothetical lineage, state, county, and sample numbers from [26]. Colors: blue = Atlantic lineage, orange = Gulf lineage. Bootstrap support is listed for major nodes.

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Grants and funding

We thank the Alabama Department of Conservation and Natural Resources, Auburn University College of Science and Mathematics, Orianne Society, and U.S. Fish and Wildlife Service for funding that made this study possible. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.