Rapid Radiations and the Race to Redundancy: An Investigation of the Evolution of Australian Elapid Snake Venoms

Jackson, Timothy N. W.; Koludarov, Ivan; Ali, Syed Abid; Dobson, James; Zdenek, Christina N.; Dashevsky, Daniel; Masci, Paul P.; Nouwens, Amanda; Josh, Peter; Goldenberg, Jonathan; Cipriani, Vittoria; Hay, Chris; Hendrikx, Iwan; Dunstan, Nathan; Allen, Luke

doi:10.3390/toxins8110309

Cited by 77 publications

(127 citation statements)

References 63 publications

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“…Many Australian elapids snakes feed on reptilian prey that is inactive/dormant at the time of the snake’s attack, and thus suffocation through lethal lethargy inducing flaccid paralysis is an effective predatory strategy in elapid snakes [56]. Such a predatory strategy is also widely used in a myriad of venomous snakes that lack the apomorphic high-pressure delivery systems [44,47,59,62,130,131,132,134,135,136].…”

Section: Resultsmentioning

confidence: 99%

“…Study of this species increases our knowledge of venom evolution and demonstrates the relevance of studying toxins, proteins unconstrained by endophysiological functions and under extreme selection pressures [56], in order to gain insight into more general patterns of evolution. In addition, the results are of considerable interest to those seeking to understand the mechanisms underlying Na V gating.…”

Section: Resultsmentioning

confidence: 99%

“…Examples include elapids first arriving in Australia when it was a continent largely devoid of snakes other than slow moving pythons and burrowing blind snakes [54]. Subsequent explosive organismal diversification was paralleled by dramatic shifts in venom chemistry even between populations with minimal organismal genetic variation [55,56]. …”

Section: Introductionmentioning

confidence: 99%

“…Venom is a key evolutionary innovation, in myriad lineages, that diversifies in concert with organismal morphological diversification [11,13,14,15,25,26,27,28,29,30,33,34,37,41,43,44,45,46,47,55,56,57,58,59,60,61,62,63]. This mechanical and chemical interrelationship continues throughout the evolutionary history of a venomous lineage.…”

Section: Introductionmentioning

confidence: 99%

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The Snake with the Scorpion’s Sting: Novel Three-Finger Toxin Sodium Channel Activators from the Venom of the Long-Glanded Blue Coral Snake (Calliophis bivirgatus)

Yang

Deuis

Dashevsky

et al. 2016

Toxins

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Millions of years of evolution have fine-tuned the ability of venom peptides to rapidly incapacitate both prey and potential predators. Toxicofera reptiles are characterized by serous-secreting mandibular or maxillary glands with heightened levels of protein expression. These glands are the core anatomical components of the toxicoferan venom system, which exists in myriad points along an evolutionary continuum. Neofunctionalisation of toxins is facilitated by positive selection at functional hotspots on the ancestral protein and venom proteins have undergone dynamic diversification in helodermatid and varanid lizards as well as advanced snakes. A spectacular point on the venom system continuum is the long-glanded blue coral snake (Calliophis bivirgatus), a specialist feeder that preys on fast moving, venomous snakes which have both a high likelihood of prey escape but also represent significant danger to the predator itself. The maxillary venom glands of C. bivirgatus extend one quarter of the snake’s body length and nestle within the rib cavity. Despite the snake’s notoriety its venom has remained largely unstudied. Here we show that the venom uniquely produces spastic paralysis, in contrast to the flaccid paralysis typically produced by neurotoxic snake venoms. The toxin responsible, which we have called calliotoxin (δ-elapitoxin-Cb1a), is a three-finger toxin (3FTx). Calliotoxin shifts the voltage-dependence of NaV1.4 activation to more hyperpolarised potentials, inhibits inactivation, and produces large ramp currents, consistent with its profound effects on contractile force in an isolated skeletal muscle preparation. Voltage-gated sodium channels (NaV) are a particularly attractive pharmacological target as they are involved in almost all physiological processes including action potential generation and conduction. Accordingly, venom peptides that interfere with NaV function provide a key defensive and predatory advantage to a range of invertebrate venomous species including cone snails, scorpions, spiders, and anemones. Enhanced activation or delayed inactivation of sodium channels by toxins is associated with the extremely rapid onset of tetanic/excitatory paralysis in envenomed prey animals. A strong selection pressure exists for the evolution of such toxins where there is a high chance of prey escape. However, despite their prevalence in other venomous species, toxins causing delay of sodium channel inhibition have never previously been described in vertebrate venoms. Here we show that NaV modulators, convergent with those of invertebrates, have evolved in the venom of the long-glanded coral snake. Calliotoxin represents a functionally novel class of 3FTx and a structurally novel class of NaV toxins that will provide significant insights into the pharmacology and physiology of NaV. The toxin represents a remarkable case of functional convergence between invertebrate and vertebrate venom systems in response to similar selection pressures. These results underscore the dynamic evolution of the Toxicofera re...

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The Snake with the Scorpion’s Sting: Novel Three-Finger Toxin Sodium Channel Activators from the Venom of the Long-Glanded Blue Coral Snake (Calliophis bivirgatus)

Yang

Deuis

Dashevsky

et al. 2016

Toxins

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“…CONCLUSION which could also potentially make them subject to higher mutation rates. Unfortunately, no published colubroid snake genome has been able to conclusively resolve the chromosomal location of the 3FTx gene cluster [70,[267][268][269]. BLAST searches between 3FTx containing scaffolds from other assemblies and the C. viridis genome reveal similarity between the 3FTx scaffolds and an unassigned scaffold in the C. viridis (as well as more minor matches to Chromosome 1).…”

Section: Chapter 6 Conclusionmentioning

confidence: 99%

Novelty in three-finger toxin evolution

Dashevsky¹

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Snakes are a striking taxon on many levels and have an indelible place in the collective culture of humanity. This is due to a number of unusual features including their limblessness, ability to ingest large prey, but most importantly their venom. From a biological perspective, snakes are equally fascinating, showing how a simple body plan can be used to great effect in an extremely broad variety of niches. Snakes are globally distributed and ecologically diverse; as a result, since recent research has shown that most snakes are venomous to some degree, their venom is equally diverse. This thesis focuses on one major toxin family: three-finger toxins (3FTx). These toxins can be found in virtually all venomous snake lineages and are often neurotoxic. Since their original recruitment there have been numerous instances of structural and functional innovation within this toxin family. The research in this thesis pertains to several such novel adaptations in snakes of the colubrid and elapid families, many of whose venom is composed primarily of these toxins. Chapter 2 deals with the ancestral version 3FTx and how, in the colubrine genus Boiga, simple mutations in toxins can lead to structural changes, in this case additional cysteines enable the formation of dimeric toxins with increased potency. These novel toxins can, in turn, open up new niches to the snakes which possess those toxins. In B. irregularis they facilitated a destructive invasion event and may have similarly assisted in the spread of an ancestral Boiga since our research shows that several other species possess similar dimeric toxins. This echoes a process that occurred in the ancestor of the elapids where the loss of a pair of cysteines and their disulfide bond was followed by an incredible diversification of these toxins and the snakes that produce them. Chapter 3 explores venom composition and activity of the genus Calliophis, the most basal genus of the elapids. C. bivirgatus and C. intestinalis both possess extremely elongated venom glands and each produce 3FTx with novel sodium channel toxicity. However, the two venoms produce opposite effects from one another. These results suggests some intriguing possibilities about the evolutionary history of these novel traits in Calliophis and the general composition of their venoms inform our understanding of how the venoms of more derived elapids evolved.Chapters 4 and 5 focus on the genus Micrurus. This genus from the Americas is by far the most speciose genus of elapids and belongs to the coral snake clade which is the next branch in the phylogeny of the elapids after Calliophis. The venoms of these snakes all contain a high number of unique 3FTx, though some venoms may be dominated by PLA2 toxins in terms of overall composition. Chapter 4 focuses on the sequence diversity of 3FTx from this genus and the selection regimes under which they operate. This diversity may lay the groundwork for rapid changes in the toxin composition of the venom and accompanying changes in venom activity. Chapter 5 directly ...

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Fang shape varies with ontogeny and sex in the venomous elapid snake Pseudonaja affinis

Cleuren

Patterson

Hocking

et al. 2022

Journal of Morphology

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A predator's preferred prey often changes over the course of its life as it grows from an inexperienced juvenile through to a sexually mature adult. For species with highly specialised feeding strategies, this may require its anatomy to change over the course of its life. The dugite (Pseudonaja affinis, Günther 1872) is a venomous snake from Australia that displays such a diet shift, with juveniles feeding on small reptiles, while adults mainly target mammals. We examined the morphology of fangs across both sexes and throughout ontogeny using geometric morphometrics and cross-sectional sharpness measurements of key functional regions on these teeth. This highlighted key differences in shape that likely relate to the varied properties of their adult and juvenile diet. We found that juveniles display a more robust and blunter fang, which likely relates to feeding on scaly lizard prey, whereas adults have slender fangs with sharper tips, which reflects their diet of softer mammalian prey. There were also dif-

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Rapid Radiations and the Race to Redundancy: An Investigation of the Evolution of Australian Elapid Snake Venoms

Cited by 77 publications

References 63 publications

The Snake with the Scorpion’s Sting: Novel Three-Finger Toxin Sodium Channel Activators from the Venom of the Long-Glanded Blue Coral Snake (Calliophis bivirgatus)

The Snake with the Scorpion’s Sting: Novel Three-Finger Toxin Sodium Channel Activators from the Venom of the Long-Glanded Blue Coral Snake (Calliophis bivirgatus)

Novelty in three-finger toxin evolution

Fang shape varies with ontogeny and sex in the venomous elapid snake Pseudonaja affinis

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