Coevolution of Snake Venom Toxic Activities and Diet: Evidence that Ecological Generalism Favours Toxicological Diversity

Abstract

Snake venom evolution is typically considered to be predominantly driven by diet-related selection pressures. Most evidence for this is based on lethality to prey and non-prey species and on the identification of prey specific toxins. Since the broad toxicological activities (e.g., neurotoxicity, coagulotoxicity, etc.) sit at the interface between molecular toxinology and lethality, these classes of activity may act as a key mediator in coevolutionary interactions between snakes and their prey. Indeed, some recent work has suggested that variation in these functional activities may be related to diet as well, but previous studies have been limited in geographic and/or taxonomic scope. In this paper, we take a phylogenetic comparative approach to investigate relationships between diet and toxicological activity classes on a global scale across caenophidian snakes, using the clinically oriented database at toxinology.com. We generally find little support for specific prey types selecting for particular toxicological effects except that reptile-feeders are more likely to be neurotoxic. We find some support for endothermic prey (with higher metabolic rates) influencing toxic activities, but differently from previous suggestions in the literature. More broadly, we find strong support for a general effect of increased diversity of prey on the diversity of toxicological effects of snake venom. Hence, we provide evidence that selection pressures on the toxicological activities of snake venom has largely been driven by prey diversity rather than specific types of prey. These results complement and extend previous work to suggest that specific matching of venom characteristics to prey may occur at the molecular level and translate into venom lethality, but the functional link between those two is not constrained to a particular toxicological route.

Diet Breadth Mediates the Prey Specificity of Venom Potency in Snakes

“…Hence, the phylogenetic diversity of the diet of the Olive sea snake (Aipysurus laevis), which primarily feeds on fish, is higher in our analysis than the diet of the Common death adder (Acanthophis antarcticus), which feeds on mammals, reptiles, birds and amphibians [9,50]. This potential importance of prey physiological disparity has been highlighted as an explanation for the comparatively simple venoms of sea snakes when compared to their more generalist feeding terrestrial counterparts [47] and for the increased toxicological diversity of venoms associated with species with more taxonomically diverse diets [48]. Furthermore, in Micrurus coral snakes [39] and in Black widow spiders [51], venoms have also been found to show compositional structures defined along the taxonomic grouping of their prey.…”

“…Such a pattern is observed in the lack of complexity in sea snake venoms, which primarily feed on fish, when compared to snakes with more generalist diets [9,29]. Furthermore, in a more recent comparative analysis, the toxicological diversity of snake venoms was found to be higher in species with a more generalist diet [48]. Similarly, in cone snails, venom complexity is found to increase with diet breadth, suggesting that the relationship between diet breadth and venom complexity may be a general pattern found across venomous taxonomic groups [18,28].…”

“…For example, venoms have been found to have substantially different potencies even when tested on prey with similar physiologies [52]. Furthermore, while broader diet breadth has been found to be associated with more complex venoms in both cone snails [28] and snakes [48], associations between specific taxonomic prey groups and particular molecular or toxicological aspects of venoms have been either absent or weak. Hence, while diverse diets are associated with more complex venoms the mechanistic pathways these venoms achieve such diverse functionality is still not clear.…”

A brief review on the natural history, venomics and the medical importance of bushmaster (Lachesis) pit viper snakes

“…A corollary of this fortunate circumstance is that antivenoms generated against venom mixtures containing any Lachesis spp. venom may exhibit paraspecific protection against ( Daltry et al, 1996 ; Davies and Arbuckle, 2019 ) the toxic activities of venoms from any other congeneric species ( Madrigal et al, 2017 ).…”

“…Hence, functional evolution of venoms is intimately linked to the ecology and dietary habits of the venomous organisms. A still small but increasing number of studies support the idea that snake venom evolution is driven by diet-related selection pressures leading to local adaptations ( Barlow et al, 2009 ; Barua and Mikheyev, 2019 ; Daltry et al, 1996 ; Davies and Arbuckle, 2019 ; Jackson et al, 2004 ; Smiley-Walters et al, 2019 ). Consequently, the changes in toxic characteristics of venom that ocurr during the development of L. stenophrys ( Madrigal et al, 2012 ), should be rationalized in the context of its use by the venomous predator.…”