Phylogenomics of scorpions reveal a co-diversification of scorpion mammalian predators and mammal-specific sodium channel toxins

Abstract

Scorpions constitute a charismatic lineage of arthropods and comprise more than 2,500 described species. Found throughout various tropical and temperate habitats, these predatory arachnids have a long evolutionary history, with a fossil record that began in the Silurian. While all scorpions are venomous, the asymmetrically diverse family Buthidae harbors nearly half the diversity of extant scorpions, and all but one of the 58 species that are medically significant to humans. Many aspects of scorpion evolutionary history are unclear, such as the relationships of the most toxic genera and their constituent venom peptides. Furthermore, the diversification age of toxins that act specifically on mammalian ion channels have never been inferred. To redress these gaps, we assembled a large-scale phylogenomic dataset of 100 scorpion venom transcriptomes and/or genomes, emphasizing the sampling of highly toxic buthid genera. To infer divergence times of venom gene families, we applied a phylogenomic node dating approach for the species tree in tandem with phylostratigraphic bracketing to estimate minimum ages of mammal-specific toxins. Our analyses establish a robustly supported phylogeny of scorpions, particularly with regard to relationships between medically significant taxa. Analysis of venom gene families shows that mammal-specific sodium channel toxins have independently evolved in five lineages within Buthidae. The temporal windows of mammal-specific toxin origins are contiguous with the basal diversification of major scorpion mammal predators such as carnivores, shrews, bats and rodents. These results suggest an evolutionary arms race model comprised of co-diversification of mammalian predators and NaTx homologs in buthid venom.