Correlation between ontogenetic dietary shifts and venom variation in Australian brown snakes ( Pseudonaja )

Abstract

Venom is a key evolutionary trait, as evidenced by its widespread convergent evolution across the animal kingdom. In an escalating prey-predator arms race, venoms evolve rapidly to guarantee predatory or defensive success. Variation in venom composition is ubiquitous among snakes. Here, we tested variation in venom activity on substrates relevant to blood coagulation among Pseudonaja (brown snake) species, Australian elapids responsible for the majority of medically important human envenomations in Australia. A functional approach was employed to elucidate interspecific variation in venom activity in all nine currently recognised species of Pseudonaja. Fluorometric enzymatic activity assays were performed to test variation in whole venom procoagulant activity among species. Analyses confirmed the previously documented ontogenetic shift from non-coagulopathic venom in juveniles to coagulopathic venom as adults, except for the case of P. modesta, which retains non-coagulopathic venom as an adult. These shifts in venom activity correlate with documented ontogenetic shifts in diet among brown snakes from specialisation on reptilian prey as juveniles (and throughout the life cycle of P. modesta), to a more generalised diet in adults that includes mammals. The results of this study bring to light findings relevant to both clinical and evolutionary toxinology.

Venoms of related mammal-eating species of taipans (Oxyuranus) and brown snakes (Pseudonaja) differ in composition of toxins involved in mammal poisoning

“…Given the down-regulated expression of prothrombinase subunits, there is a possibility that the toxin may be ineffective at subduing squamate reptiles. This is concordant with the lack of prothrombin activation and factor Xa activity by venoms of brown snake juveniles, which also feed on lizards [20,41],…”

“…However, fX and fV expression levels in its venom were extremely low (iBAQ = 0.0035% and 0.0022%, respectively). Their detection indicates that this lizard-eating brown snake apparently has functional genes encoding venom prothrombinase components, but the expression is too low to induce a noticeable procoagulant effect [41,42]. A transcriptomic study on the West Australian P. modesta venom did not find transcripts belonging to fX and recorded low-level expression of fV [38].…”

“…For instance, in our P. textilis venom sample from Queensland (Mackay area), the relative iBAQ proportions were: venom fX = 11.0% and venom fV = 10.6%. A recent study recorded high fX activity of the western brown snake (P. mendgeni) venom, suggesting that high expression of prothrombinase toxins can be expected in this venom as well [41]. Protein families containing toxins known to induce poisoning in mammals are marked with a red X (whether any of the other protein families found in Australian elapid venoms contain mammal-toxic proteins is currently unknown).…”

Comparative Profiling of Three Atheris Snake Venoms: A. squamigera, A. nitschei and A. chlorechis

“…Several components are common to all venoms although with quantitative differences, such as disintegrins, phospholipases and SVMPs, whereas some identified components were species-specific. These differences among species could be the result of diverse factors such as geographic region, ecological factors, prey patterns, evolutionary traits, ontogenetic or individual variability, sexual recombination and other genetic factors as well as age and the storage conditions of a venom sample [3,24].…”

Novelty in three-finger toxin evolution

“…of prey species [69,73,74]. Coupled with the rapid rate of venom evolution, this leads to many snakes evolving toxins that are particularly potent against their specific prey items [20,47,75,76]. Studies of prey specificity across a broad selection of snakes and prey taxa have led to the rule of thumb that small non-enzymatic neurotoxins are particularly useful against diapsid prey (birds and reptiles), while synapsids (mammals) tend to be more susceptible to enzymatic coagulotoxins [18,47,52,76,77].…”