Ecological divergence and the history of gene flow in the Nearctic milksnakes (Lampropeltis triangulum complex)

Many phylogeographic studies on species with large ranges have found genetic-geographic structure associated with changes in habitat and physical barriers to gene flow. These studies may conclude absence of population structure, lineage structure that indicates unique species have been discovered, or suggest more research is needed prior to delimitation. Comparative risks of delimiting species incorrectly or failing to delimit species are usually not weighed and a more detailed return to these problems with more data often does not occur. With genomic data and better modeling capabilities we can more clearly delimit species by understanding causes of speciation with respect to biogeography and migration between lineages, the location of hybrid zones in relationship to the ecology of parental lineages, and differential introgression of genes between taxa. Here we examine the origins of three Nearctic milksnakes (Lampropeltis elapsoides, L. triangulum, and L. gentilis) using genomic-scale data to better understand the diversification of these taxa previously delimited based on a smaller genetic dataset. Methods that reject pure isolation by distance in favor of environmentally driven reduction in gene flow clearly indicate that all three lineages should continue to be recognized as unique species. These results underscore conspicuous environmental changes that occur between the sister-taxa forming due to changes in habitat from the Great Plains (GP) to the forested regions of the Eastern Nearctic (ENA). This area has been recognized for turnover of reptile and amphibian species but with few phylogeographic studies examining environmental-genetic structure in this region. We show that the two species meeting at the GP/ENA, L. triangulum and L. gentilis, likely formed in the mid-Pleistocene and have maintained partial reproductive isolation over much of this time, exchanging fewer than one migrant/generation, and formed a hybrid zone with differential introgression of loci. We also show that when L. triangulum and L. gentilis are each in contact with the much older L. elapsoides, some limited gene flow has occurred. We conclude that phylogenetic reticulation in this genus, and likely for many other taxa, is common across throughout time. Furthermore, the application of the biological species concept to the whole genome will give rise to grave misunderstandings of the complexities of how species form and remain unique even in the face of gene flow.