Phylogenetically diverse diets favor more complex venoms in North American pitvipers

Abstract

The role of natural selection in the evolution of trait complexity can be characterized by testing hypothesized links between complex forms and their functions across species. Predatory venoms are composed of multiple proteins that collectively function to incapacitate prey. Venom complexity fluctuates over evolutionary timescales, with apparent increases and decreases in complexity, and yet the causes of this variation are unclear. We tested alternative hypotheses linking venom complexity and ecological sources of selection from diet in the largest clade of front-fanged venomous snakes in North America: the rattlesnakes, copperheads, cantils, and cottonmouths. We generated independent transcriptomic and proteomic measures of venom complexity and collated several natural history studies to quantify dietary variation. We then constructed genome-scale phylogenies for these snakes for comparative analyses. Strikingly, prey phylogenetic diversity was more strongly correlated to venom complexity than was overall prey species diversity, specifically implicating prey species’ divergence, rather than the number of lineages alone, in the evolution of complexity. Prey phylogenetic diversity further predicted transcriptomic complexity of three of the four largest gene families in viper venom, showing that complexity evolution is a concerted response among many independent gene families. We suggest that the phylogenetic diversity of prey measures functionally relevant divergence in the targets of venom, a claim supported by sequence diversity in the coagulation cascade targets of venom. Our results support the general concept that the diversity of species in an ecological community is more important than their overall number in determining evolutionary patterns in predator trait complexity.

Snake Venom

“…Geographic location and varied diet have led to the development of more and more complex venom. Being generalized feeders, many species of snake have a larger repertoire of proteins in their venom that affect individual prey animal species differently [6]. Honing the composition, mechanism of delivery, dosage and action of venom remains one of nature's greater success stories to date.…”

“…The dietary preferences of the snake can magnify the change in venom. The snake can produce a potent mixture that can affect different prey animals uniquely [6]. There is no efficient antivenin generated against sea snakes.…”

Venom Gene Sequence Diversity and Expression Jointly Shape Diet Adaptation in Pitvipers

“…This genomic architecture means the evolution of venom genes and the pathway from genotype to a complex phenotype can be investigated in multiple gene families across a set of venomous species. These features make venom an exceptional system for examining how complex adaptive phenotypes are assembled and evolve, and for understanding the impact of phenotypic complexity on ecological function ( Holding, Drabeck, et al 2016 ; Sunagar et al 2016 ; Arbuckle 2020 ; Giorgianni et al 2020 ; Zancolli and Casewell 2020 ; Holding et al 2021 ).…”

Combined Molecular and Elemental Mass Spectrometry Approaches for Absolute Quantification of Proteomes: Application to the Venomics Characterization of the Two Species of Desert Black Cobras, Walterinnesia aegyptia and Walterinnesia morgani

“… 23 Hence, identifying the specific pressures that tailored the composition and bioactivities of venoms across snake clades may have implications for the clinical treatment of human envenomings. 24 − 27 …”