Coalescent Species Delimitation in Milksnakes (Genus Lampropeltis) and Impacts on Phylogenetic Comparative Analyses

Abstract

Both gene-tree discordance and unrecognized diversity are sources of error for accurate estimation of species trees, and can affect downstream diversification analyses by obscuring the correct number of nodes, their density, and the lengths of the branches subtending them. Although the theoretical impact of gene-tree discordance on evolutionary analyses has been examined previously, the effect of unsampled and cryptic diversity has not. Here, we examine how delimitation of previously unrecognized diversity in the milksnake (Lampropeltis triangulum) and use of a species-tree approach affects both estimation of the Lampropeltis phylogeny and comparative analyses with respect to the timing of diversification. Coalescent species delimitation indicates that L. triangulum is not monophyletic and that there are multiple species of milksnake, which increases the known species diversity in the genus Lampropeltis by 40%. Both genealogical and temporal discordance occurs between gene trees and the species tree, with evidence that mitochondrial DNA (mtDNA) introgression is a main factor. This discordance is further manifested in the preferred models of diversification, where the concatenated gene tree strongly supports an early burst of speciation during the Miocene, in contrast to species-tree estimates where diversification follows a birth-death model and speciation occurs mostly in the Pliocene and Pleistocene. This study highlights the crucial interaction among coalescent-based phylogeography and species delimitation, systematics, and species diversification analyses.

Independent Demographic Responses to Climate Change among Temperate and Tropical Milksnakes (Colubridae: Genus Lampropeltis)

“…abnorma , and L . micropholis , following the revised taxonomy of Ruane et al [62] and using GenBank sequences from accession series KF214996–KF216452. These six taxa, with an abundance of populations previously sampled, have extensive distributions throughout the Nearctic and portions of Neotropics (Figs 1 and 2).…”

“…micropholis ( n = 16), rangeing from Western/Central Mexico to Ecuador (see S1 Table in supporting information for details of samples). All six species originated between 1.1 and 3.6 Ma [62] and so would have experienced Late Pleistocene climate change. For L .…”

“…micropholis , the same three genes were used; additional nuclear loci were available for the tropical taxa as well and so we also included the protein coding genes NT3 and PRLR, the introns SPTBN intron 1, Vimenton intron 5, NAV intron 5, and Z-chromosome GAD intron 15, and the anonymous loci 2CL3, 2CL4, and LATCL (S2 Table). Nuclear loci heterozygosities were previously resolved with PHASE v2.1.1 [72] in Ruane et al [62], and so we used the most probable pair of resulting alleles for analyses.…”

“…A recent study demonstrated that diversity within Lampropeltis , specifically within milksnakes, was underestimated, indicating that the former single species of milksnake, L . triangulum , is composed of seven taxa distributed in North, Central, and South America [62]. Therefore, we propose to examine the effects of Quaternary climate change on six closely related taxa that are found in both Nearctic (N = 3 species) and Neotropical (N = 3 species) regions.…”

Post-molecular systematics and the future of phylogenetics

“…The information contained in a dated phylogeny generally reduces to n -1 node ages and 2(n -1) branch lengths, which are subject to numerous upstream biases of phylogenetic and temporal inference that can strongly affect the results of comparative methods [65][66][67]. Then, we demand from this graph information on speciation, extinction, ancestral states, ancestral areas, links between traits or areas and diversification process, community assembly processes, phylogenetically informed regressions and ANOVAs, etc.…”