Phylogeography and lineage-specific patterns of genetic diversity and molecular evolution in a group of North American skinks

Abstract

Geography influences the evolutionary trajectory of species by mediating opportunities for hybridization, gene flow, demographic shifts and adaptation. We sought to understand how geography and introgression can generate species‐specific patterns of genetic diversity by examining phylogeographical relationships in the North American skink species Plestiodon multivirgatus and P. tetragrammus (Squamata: Scincidae). Using a multilocus dataset (three mitochondrial genes, four nuclear genes; a total of 3455 bp) we discovered mito‐nuclear discordance, consistent with mtDNA introgression. We further tested for evidence of species‐wide mtDNA introgression by using comparisons of genetic diversity, selection tests and extended Bayesian skyline analyses. Our findings suggest that P. multivirgatus acquired its mitochondrial genome from P. tetragrammus after their initial divergence. This putative species‐wide mitochondrial capture was further evidenced by statistically indistinguishable substitution rates between mtDNA and nDNA in P. multivirgatus. This rate discrepancy was observed in P. multivirgatus but not P. tetragrammus, which has important implications for studies that combine mtDNA and nDNA sequences when inferring time since divergence between taxa. Our findings suggest that by facilitating opportunities for interspecific introgression, geography can alter the course of molecular evolution between recently diverged lineages.

Testing the geographical dimensions of genetic diversity following range expansion in a North American snake

“…The range and demographic expansion patterns we observed in T. gracilis largely conform to the predominant phylogeographical pattern observed for vertebrates in central North America (Burbrink et al, 2016), including other snakes (Cox & Chippindale, 2014;McKelvy & Burbrink, 2017), lizards (Moseley et al, 2015), amphibians (Lemmon et al, 2007;Fontenot et al, 2011;Streicher et al, 2012), birds (Ball et al, 1988;Bouzat et al, 1998;Johnson, 2008) and mammals (Riddle & Honeycutt, 1990;Demastes et al, 2002). This shared pattern among diverse taxonomic groups suggests that many terrestrial taxa in this region have recently expanded northwards across the Great Plains, and many have a resulting legacy of depleted genetic variation in the northern segments of their distributions.…”

“…We found that only a subset of mitochondrial and nuclear variation in T. gracilis is present across the large northern swathe of their geographical range, and this is a pattern that has been found in many other taxa (e.g. Fontenot et al, 2011;Streicher et al, 2012;Moseley et al, 2015). The historical contingencies of range expansion and contraction have perhaps increased the potential of southern populations for adaptation to natural and human-mediated alterations in climate and habitat in the terrestrial fauna of central North America.…”

“…In this study, the Balcones escarpment separates most of the clades found north (Northeast) and south of this barrier (Live Oak and South Texas), although one clade spans this barrier (Northwestern clade). The Balcones Escarpment has been found to delimit mitochondrial clades in snakes (Burbrink, 2002;Castoe et al, 2007), lizards (Moseley et al, 2015) and mammals (Riddle, 1995;Andersen & Light, 2012), but not frogs (Mulcahy & Mendelson, 2000;Lemmon et al, 2007;Streicher et al, 2012). Interestingly, the Balcones Escarpment does not represent an abrupt physical barrier to dispersal, and habitat transitions above and below the escarpment are relatively subtle.…”

“…Range expansion can lead to low levels of genetic diversity at range fronts and therefore has the potential to create widespread, genetically homogeneous groups of individuals (Excoffier et al, 2009). Crucially, understanding how range expansion and contraction can impact genetic diversity has important implications for delimiting species (Streicher et al, 2012(Streicher et al, , 2016, detecting introgression (Moseley et al, 2015) and predicting evolutionary responses to ecological change (Pearson & Dawson, 2003).…”

“…We studied genetic diversity across the geographical range of the North American flat-headed snake, Tantilla gracilis. This small, semifossorial snake is found throughout the south-central USA west of the Mississippi River and north of Mexico (Dixon, 2000;Werler & Dixon, 2000;Ernst & Ernst, 2003;Lemos-Espinal et al, 2004), a region where many animal species exhibit the molecular signature of recent range and population expansion (Hamilton et al, 2011;Streicher et al, 2012;Moseley et al, 2015;Burbrink et al, 2016), including snakes (Cox & Chippindale, 2014;Ruane et al, 2015;Streicher et al, 2016;McKelvy & Burbrink, 2017). We combined range-wide geographical sampling, multilocus molecular phylogenetics and analyses of molecular diversity to study genetic variation in the flat-headed snake, which has probably been influenced by both refugial dynamics and range expansion.…”