Coevolution takes the sting out of it: Evolutionary biology and mechanisms of toxin resistance in animals

Abstract

Understanding how biotic interactions shape the genomes of the interacting species is a long-sought goal of evolutionary biology that has been hampered by the scarcity of tractable systems in which specific genomic features can be linked to complex phenotypes involved in interspecific interactions. In this review we present the compelling case of evolved resistance to the toxic challenge of venomous or poisonous animals as one such system. Animal venoms and poisons can be comprised of few or of many individual toxins. Here we show that resistance to animal toxins has evolved multiple times across metazoans, although it has been documented more often in phyla that feed on chemically-armed animals than in prey of venomous predators. We review three types of gene-product based resistance: 1) toxin scavenging, where molecules produced by the envenomed organism bind and inactivate the toxins; 2) target-site insensitivity, including landmark cases of convergent changes that make the molecules normally targeted by animal toxins refractory, and; 3) off-target repurposing, where envenomed organisms overcome toxicity by exploiting the function of toxins to alter their physiological effect. We finish by discussing the evolutionary processes that likely played a role in the origin and maintenance of toxin resistance. We conclude that antagonistic interactions involving poisonous or venomous animals are unparalleled models for investigating microevolutionary processes involved in coevolution and linking them to macroevolutionary patterns.

Snake venom potency and yield are associated with prey-evolution, predator metabolism and habitat structure

“…; Arbuckle et al . ). However, whether these cases are taxon specific or form the general rule across all venomous snakes has yet to be tested at a broad taxonomic scale.…”

“…Species are highlighted as silhouettes with colours matching the incapacitation ability scale from (a). (Daltry et al 1996;da Silva & Aird 2001;Mackessy et al 2006;Starkov et al 2007;Barlow et al 2009;Richards et al 2012;Vonk et al 2013;Margres et al 2017), while other examples have either found no such prey-specificity (Williams et al 1988) or cases were the prey species have evolved tolerance towards their predator's venoms (Heatwole & Poran 1995;Biardi et al 2000;Voss 2013;Pomento et al 2016;Arbuckle et al 2017). However, whether these cases are taxon specific or form the general rule across all venomous snakes has yet to be tested at a broad taxonomic scale.…”

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

“…This again suggests a predominant role of diet in driving venom evolution since there is no obvious reason that, for instance, predation risk should typically change greatly following a shift of diet (as would be necessary for inferring a primarily defensive role). However, as striking and informative as these relationships are, coevolution can lead to defensive toxin resistance to snake venom in prey species [24,25], obscuring clear positive relationships between toxicity and natural diet. Moreover, given that the ultimate function of a predatory snake venom is to incapacitate rather than kill prey [26], which may not be mechanistically identical processes, the standard use of lethality as a measure of toxicity blurs the interpretation of such data from an evolutionary ecological perspective to some degree.…”

Snake Venom in Context: Neglected Clades and Concepts

“…Coevolutionary arms races are often invoked to account for diversity in venom composition and activity, as well as the dynamic molecular evolution of toxin genes (e.g., Casewell et al, 2013). On the other hand, interest in the evolution of resistance to venom in both the prey and predators of venomous organisms has also increased recently (after a long history of piecemeal research), highlighted by the publication of two excellent reviews (Holding et al, 2016 andArbuckle et al, 2017) detailing the multiple molecular innovations that confer this resistance. The evolution of chemical weaponry and the reciprocal evolution of resistance may be one of the most important drivers of functional diversity at the molecular level.…”