Integration of phylogenomics and molecular modeling reveals lineage-specific diversification of toxins in scorpions.

Carlos E Santibáñez-López,Nathaniel Rush,Daniel A Janies,John Williams,Prashant P Sharma,Ricardo Kriebel,Jesús A Ballesteros,Zachary Witter

doi:10.7717/peerj.5902

Carlos E Santibáñez-López, Nathaniel Rush + Show 6 more

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https://doi.org/10.7717/peerj.5902

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Abstract

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.

Highlights

Scorpions are an iconic group of arachnids that are central to investigations of arthropod terrestrialization, morphological stasis, and diversification of body plans (Kjellesvig-Waering, 1986; Jeram, 1998; Sharma et al, 2014; Waddington, Rudkin & Dunlop, 2015)
Within parvorder Buthida, a clade comprised of Chaerilidae + Pseudochactidae was recovered as the sister group of Buthidae
This ancestral peptide subsequently diversified into LKTx and calcins, in the two lineages originating from the basal split in scorpions

Summary

Introduction

Scorpions are an iconic group of arachnids that are central to investigations of arthropod terrestrialization, morphological stasis, and diversification of body plans (Kjellesvig-Waering, 1986; Jeram, 1998; Sharma et al, 2014; Waddington, Rudkin & Dunlop, 2015). The origin of toxins in animal venom has been inferred to be the result of recruitment of paralogs of ancestral housekeeping genes, followed by diversification and neofunctionalization, a process driven by positive selection (Juarez et al, 2008; Fry et al, 2009; Rokyta et al, 2011; Wong & Belov, 2012; Haney et al, 2016; Dowell et al, 2016). While novel peptides often preserve the same molecular scaffold of their ancestral protein, key changes in functional residues, mostly in surface-exposed sites, acquire newly derived biological activities (Fry et al, 2009; Casewell et al, 2013). Two peptides with statistically insignificant sequence similarity can adopt the same scaffold (Orengo, Jones & Thornton, 1994), resulting in evolutionary convergence in fold structures, and rendering inference of homology non-trivial

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