How ecological opportunity drives asymmetric phenotypic diversity in the gartersnakes, watersnakes, and allies (Natricidae:Thamnophiini).

Ecological opportunity promotes rapid evolution as species fill unoccupied niche space and is a common explanation for asymmetric diversity within taxonomic groups. Most studies on ecological opportunity focus on isolated areas such as islands, lakes, and mountaintops. However, ecological opportunity via colonization can occur on continents where lineages pass through a geographical/environmental barrier, resulting in accelerated rates of phenotypic evolution. North American Thamnophiini (gartersnakes, watersnakes, brownsnakes, and swampsnakes) are a clade of colubroid snakes that exhibit high levels of ecological variance and a wide variety of diet preferences inhabiting many disparate biomes. Additionally, Thamnophiini represents an asymmetric radiation where 57% of species diversity is represented by the gartersnakes (Thamnophis). Furthermore, the group is geographically unevenly distributed; apart from Storeria storerioides, Thamnophis is the only genus that naturally occurs west of the Western Continental Divide in North America. As a result, ecological specializations occur independently throughout the clade with convergence in morphology and ecology shared between western and eastern groups. However, it is unclear whether this ecological convergence extends to the underlying skeletal morphology, whose distinct elements can evolve independently and thus reveal the mechanistic basis of morphological adaptation. Morphology of the snake skull has been shown to be influenced by natural history traits such as habitat and diet. Using high-dimensional shape data collected from µCT-scans and a well-resolved phylogeny of Thamnophiini inferred from genomic data, we conducted geometric morphometrics to analyze the tempo and mode of trait evolution of the snake skull, a highly adaptive component of the snake skeleton. We conducted Bayesian phylogenetic comparative methods that explicitly incorporate background rate heterogeneity across the tree to assess the impact of natural history traits, such as diet and habitat, and geography on morphological evolution and convergence. Our results support morphological convergence of skull shape across different ecotypes. Importantly, our results provide evidence that morphological rate is influenced by habitat and geography, with the colonizing western taxa exhibiting higher rates of morphological evolution than eastern taxa. This suggests that a major part of Thamnophiini diversification is strongly influenced by ecological opportunity following the westward expansion of Thamnophis lineages.