Phylogenomics of scorpions reveal contemporaneous diversification of scorpion mammalian predators and mammal-active sodium channel toxins

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. However, the lack of a
densely sampled scorpion phylogeny has hindered broader inferences of the
diversification dynamics of scorpion toxins. As redress, we assembled a
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. Temporal windows of mammal-specific toxin origins are correlated
with the basal diversification of major scorpion mammal predators such as
carnivores, shrews, bats and rodents. These results suggest an
evolutionary model of relatively recent diversification of buthid sodium
channel toxin (NaTx) homologs in response to diversification of scorpion
predators.