Scorpions have evolved a variety of toxins with a plethora of biological targets, but characterizing their evolution has been limited by the lack of a comprehensive phylogenetic hypothesis of scorpion relationships grounded in modern, genome-scale datasets. Disagreements over scorpion higher-level systematics have also incurred challenges to previous interpretations of venom families as ancestral or derived. To redress these gaps, we assessed the phylogenomic relationships of scorpions using the most comprehensive taxonomic sampling to date. We surveyed genomic resources for the incidence of calcins (a type of calcium channel toxin), which were previously known only from 16 scorpion species. Here, we show that calcins are diverse, but phylogenetically restricted only to parvorder Iurida, one of the two basal branches of scorpions. The other branch of scorpions, Buthida, bear the related LKTx toxins (absent in Iurida), but lack calcins entirely. Analysis of sequences and molecular models demonstrates remarkable phylogenetic inertia within both calcins and LKTx genes. These results provide the first synapomorphies (shared derived traits) for the recently redefined clades Buthida and Iurida, constituting the only known case of such traits defined from the morphology of molecules.
Scorpions constitute a charismatic lineage of arthropods and comprise more than 2500 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. To redress this gap, we assembled a phylogenomic data set of 100 scorpion venom gland transcriptomes and 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 the 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-active sodium channel toxins (NaTx) have independently evolved in five lineages within Buthidae. Temporal windows of mammal-targeting toxin origins are correlated with the basal diversification of more »
- Publication Date:
- NSF-PAR ID:
- 10364667
- Journal Name:
- Systematic Biology
- ISSN:
- 1063-5157
- Publisher:
- Oxford University Press
- Sponsoring Org:
- National Science Foundation
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Scorpion toxins are thought to have originated from ancestral housekeeping genes that underwent diversification and neofunctionalization, as a result of positive selection. Our understanding of the evolutionary origin of these peptides is hindered by the patchiness of existing taxonomic sampling. While recent studies have shown phylogenetic inertia in some scorpion toxins at higher systematic levels, evolutionary dynamics of toxins among closely related taxa remain unexplored. In this study, we used new and previously published transcriptomic resources to assess evolutionary relationships of closely related scorpions from the family Hadruridae and their toxins. In addition, we surveyed the incidence of scorpine-like peptides (SLP, a type of potassium channel toxin), which were previously known from 21 scorpion species. We demonstrate that scorpine-like peptides exhibit gene duplications. Our molecular analyses demonstrate that only eight sites of two SLP copies found in scorpions are evolving under positive selection, with more sites evolving under negative selection, in contrast to previous findings. These results show evolutionary conservation in toxin diversity at shallow taxonomic scale.
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Scorpion toxins are thought to have originated from ancestral housekeeping genes that underwent diversification and neofunctionalization, as a result of positive selection. Our understanding of the evolutionary origin of these peptides is hindered by the patchiness of existing taxonomic sampling. While recent studies have shown phylogenetic inertia in some scorpion toxins at higher systematic levels, evolutionary dynamics of toxins among closely related taxa remain unexplored. In this study, we used new and previously published transcriptomic resources to assess evolutionary relationships of closely related scorpions from the family Hadruridae and their toxins. In addition, we surveyed the incidence of scorpine-like peptides (SLP, a type of potassium channel toxin), which were previously known from 21 scorpion species. We demonstrate that scorpine-like peptides exhibit gene duplications. Our molecular analyses demonstrate that only eight sites of two SLP copies found in scorpions are evolving under positive selection, with more sites evolving under negative selection, in contrast to previous findings. These results show evolutionary conservation in toxin diversity at shallow taxonomic scale.
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