Phylogenomic analyses resolve relationships among garter snakes (Thamnophis: Natricinae: Colubridae) and elucidate biogeographic history and morphological evolution

Garter snakes (Thamnophis) are a successful group of natricines endemic to North America. They have become important natural models for ecological and evolutionary research, yet prior efforts to resolve phylogenetic relationships have resulted in conflicting topologies and weak support for certain relationships. Here, we use genomic data generated with a reduced representation double-digest RADseq approach to reassess evolutionary relationships across Thamnophis. We then use the resulting phylogeny to better understand how biogeography and feeding ecology have influenced lineage diversification and morphological evolution. We recovered highly congruent and strongly supported topologies from maximum likelihood and Bayesian analyses, but some discordance with a multispecies coalescent approach. All phylogenomic estimates split Thamnophis into two clades largely defined by northern and southern North American species. Divergence time estimates and biogeographic analyses indicate a mid-Miocene origin of Thamnophis in Mexico. In addition, historic vicariant events thought to explain biogeographic patterns in other lineages (e.g., Isthmus of Tehuantepec, Rocky Mountain Range, and Trans-Mexican Volcanic Belt) appear to have influenced patterns of diversification in Thamnophis as well. Analyses of morphological traits associated with feeding ecology showed moderate to strong phylogenetic signal. Nevertheless, phylogenetic ANOVA suggested significant differences in certain cranial morphologies between aquatic specialists and garter snakes that are terrestrial-aquatic generalists, independent of evolutionary history. Our new estimate of Thamnophis phylogeny yields an improved understanding of the biogeographic history and morphological evolution of garter snakes, and provides a robust framework for future research on these snakes.

Automated summary

Garter snakes of the Thamnophis genus in North America were studied using genomic data to understand their evolutionary relationships, biogeography, and morphological evolution. The analysis revealed two main clades of Thamnophis, with divergence estimated to have occurred in mid-Miocene in Mexico. Historic vicariant events and feeding ecology were found to influence the diversification patterns in these snakes. The study also showed that certain cranial morphologies were significantly different between aquatic specialists and terrestrial-aquatic generalists. The findings provide a better understanding of the evolutionary history and morphological evolution of garter snakes and lay the groundwork for future research.