Abstract
Centipedes are among the most ancient groups of venomous predatory arthropods. Extant species belong to five orders, but our understanding of the composition and evolution of centipede venoms is based almost exclusively on one order, Scolopendromorpha. To gain a broader and less biased understanding we performed a comparative proteotranscriptomic analysis of centipede venoms from all five orders, including the first venom profiles for the orders Lithobiomorpha, Craterostigmomorpha, and Geophilomorpha. Our results reveal an astonishing structural diversity of venom components, with 93 phylogenetically distinct protein and peptide families. Proteomically-annotated gene trees of these putative toxin families show that centipede venom composition is highly dynamic across macroevolutionary timescales, with numerous gene duplications as well as functional recruitments and losses of toxin gene families. Strikingly, not a single family is found in the venoms of representatives of all five orders, with 67 families being unique for single orders. Ancestral state reconstructions reveal that centipede venom originated as a simple cocktail comprising just four toxin families, with very little compositional evolution happening during the approximately 50 My before the living orders had diverged. Venom complexity then increased in parallel within the orders, with scolopendromorphs evolving particularly complex venoms. Our results show that even venoms composed of toxins evolving under the strong constraint of negative selection can have striking evolutionary plasticity on the compositional level. We show that the functional recruitments and losses of toxin families that shape centipede venom arsenals are not concentrated early in their evolutionary history, but happen frequently throughout.
Highlights
Venom is one of nature’s most frequently evolved adaptations
Various mechanisms can be involved in toxin recruitment and evolution, including recruitment of single-copy nontoxin genes, changes in the location and level of gene expression, gene duplication followed by positive selection to facilitate functional diversification, gene or domain duplication combined with concerted evolution to increase effective expression levels, negative selection to conserve the function of ecologically important toxins, and functional loss of toxins through transcriptional and translational downregulation, which can lead to pseudogenization or complete loss of toxin genes (Moran et al 2008; Fry et al 2009; Casewell et al 2013; Hargreaves et al 2014; Reyes-Velasco et al 2015; Sunagar and Moran 2015; Madio et al 2018; Laxme et al 2019)
We reconstructed the macroevolutionary history of functional recruitments and losses of toxin families from centipede venom proteomes, using parsimony-based character state optimizations informed by our phylogenetic analyses of toxin gene families. We used both DELTRAN (Delayed Transformation) and ACCTRAN (Accelerated Transformation) optimization to reconstruct the evolution of venom composition, but we focused our main discussions around the latter because it presents a conservative estimate of the extent to which centipede venom complexity evolved in parallel within the five orders, while maximizing the amount of early compositional evolution that is inferred along shared ancestral lineages
Summary
Venom is one of nature’s most frequently evolved adaptations. A conservative estimate suggests it has evolved more than 80 times in the animal kingdom to play important roles in predation, defense, blood feeding, and other functions (Fry et al 2009; Casewell et al 2013; Jenner and Undheim 2017). Venoms are typically complex cocktails of bioactive molecules, commonly referred to as toxins that disrupt normal physiological functioning of envenomated victims Most of these toxins are proteins and peptides, which are thought to have mainly evolved through the functional recruitment of physiological components into venom, where they can evolve new roles and functions as toxins (Casewell et al 2013). These mechanisms of toxin recruitment, maintenance, diversification, and loss drive the macroevolution of venom on a compositional level
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