Phylogenomics and Biogeography of North American Trechine Cave Beetles (Coleoptera: Carabidae) Inferred from Ultraconserved Elements.

Cave trechine beetles (Coleoptera: Carabidae: Trechini) are members of cave communities globally and important models for understanding the colonization of caves, adaptation to cave life, and the diversification of cave-adapted lineages. In eastern North America, cave trechines are the most species-rich group of terrestrial troglobionts, hypothesized to comprise over 150 taxa in six genera with no closely related extant surface members. Previous studies have hypothesized that the Pleistocene climate change was a major driver of cave colonization and diversification in the temperate terrestrial cave fauna in this region. However, our time-calibrated molecular phylogeny resulting from the analysis of 16,794 bases from 68 Ultraconserved Elements (UCEs) loci for 45 species of this clade supports an alternative hypothesis whereby cave colonization of the surface ancestor of eastern North American cave trechines likely began in the early Miocene in the Appalachians Ridge and Valley (APP) and dispersed into the Interior Low Plateau (ILP) in an east to west manner beginning 17.0 Mya. The APP served as a cradle for diversification and as a bridge linking the southern Appalachians and Interior Low Plateau enabling the dispersal and subsequent diversification of these cave beetles. Major clades in our time-calibrated phylogeny attained their present-day geographic distributions by the early Miocene followed by multiple additional episodes of cave colonization and diversification occurring throughout the Pliocene and Pleistocene. The genera Neaphanops, Darlingtonea, Nelsonites, and Ameroduvalius were nested within the speciose genus Pseudanophthalmus supporting the hypothesis that these taxa are derived Pseudanophthalmus. Moreover, while several morphologically-defined species groups of Pseudanophthalmus are monophyletic, others were not recovered, warranting future taxonomic and systematic research. The molecular systematics and biogeography of these unique trechine cave beetles offer a model for other comparative evolutionary and ecological studies of troglobionts to further our understanding of factors driving speciation and biogeographic patterns.