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

Adaptive radiation is a common explanation for asymmetric diversity within
taxonomic groups. Adaptive radiation is often initiated by ecological
opportunity which promotes rapid evolution as species fill unoccupied
niche space. 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 if this
ecological convergence extends to skeletal morphological traits, which are
key for understanding ecological 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, genome-scale 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.