Coevolution of diet and prey-specific venom activity supports the role of selection in snake venom evolution

Abstract

The processes that drive the evolution of snake venom variability, particularly the role of diet, have been a topic of intense recent research interest. Here, we test whether extensive variation in venom composition in the medically important viper genus Echis is associated with shifts in diet. Examination of stomach and hindgut contents revealed extreme variation between the major clades of Echis in the proportion of arthropod prey consumed. The toxicity (median lethal dose, LD 50 ) of representative Echis venoms to a natural scorpion prey species was found to be strongly associated with the degree of arthropod feeding. Mapping the results onto a novel Echis phylogeny generated from nuclear and mitochondrial sequence data revealed two independent instances of coevolution of venom toxicity and diet. Unlike venom LD 50 , the speed with which venoms incapacitated and killed scorpions was not associated with the degree of arthropod feeding. The prey-specific venom toxicity of arthropod-feeding Echis may thus be adaptive primarily by reducing venom expenditure. Overall, our results provide strong evidence that variation in snake venom composition results from adaptive evolution driven by natural selection for different diets, and underscores the need for a multi-faceted, integrative approach to the study of the causes of venom evolution.

Medically important differences in snake venom composition are dictated by distinct postgenomic mechanisms

“…4A). Contrastingly, the Echis venoms show significant interspecific variation in their lethality to (i) scorpions, where all, apart from E. coloratus, are more potent than the venom of B. arietans to this prey species (20) (Fig. 4B) and (ii) locusts, to which E. p. leakeyi venom is significantly more toxic than venoms from the other Echis species and from B. arietans (25) (Fig.…”

“…1). These species were selected based on their medical importance in Africa and our previous descriptions of interspecific variation in venom composition, dietary preference, and prey lethality (12,20,25,26). We used our previously constructed and assembled venom gland transcriptomes for the four Echis species (26,27) and prepared venom gland trancriptomes for B. arietans and C. cerastes by using identical protocols.…”

“…Because relevant genome information was lacking, we reconciled the resulting gene trees to the previously described species tree (20,29,30) to reconstruct the timing of gene duplication events and to predict the number of untranscribed (or pseudogenic) gene loci. Such reconciliation approaches have successfully been used elsewhere, including with venom toxins, to predict the number of genes housed in a genome in the absence of genomic information (31)(32)(33).…”

“…The result of these processes is a complex suite of toxins that act synergistically to cause rapid prey death. Consequently, it has been hypothesized that variation in venom composition is the result of adaptation in response to dietary selection pressures (1,9,11,20).…”

Effects of geographical heterogeneity in species interactions on the evolution of venom genes

“…This phenomenon is also probably demonstrated by other venomous taxa. For example, snakes employ different envenomation strategies towards different prey [60], and prey species differ in their responses to venoms of different snakes [61,62] and spiders [63]. The positive relationship may be widely represented at other predation phenotypes, and especially those that are rapidly evolving.…”