[Herpetology / Evolution • 2016] Historical Contingency in a Multigene Family Facilitates Adaptive Evolution of Toxin Resistance

An international research team led by Virginia Tech discovered how snakes evolved the ability to eat extremely toxic species.

photo: Richard Greene

Highlights

• Toxin resistance in sensory neurons evolved in reptiles before the origin of snakes

• Resistant motor neurons evolved four times in snakes that eat amphibians

• Coevolutionary arms races with toxic prey were facilitated by resistant nerves

Summary

Novel adaptations must originate and function within an already established genome. As a result, the ability of a species to adapt to new environmental challenges is predicted to be highly contingent on the evolutionary history of its lineage. Despite a growing appreciation of the importance of historical contingency in the adaptive evolution of single proteins, we know surprisingly little about its role in shaping complex adaptations that require evolutionary change in multiple genes. One such adaptation, extreme resistance to tetrodotoxin (TTX), has arisen in several species of snakes through coevolutionary arms races with toxic amphibian prey, which select for TTX-resistant voltage-gated sodium channels (Nav). Here, we show that the relatively recent origins of extreme toxin resistance, which involve the skeletal muscle channel Nav1.4, were facilitated by ancient evolutionary changes in two other members of the same gene family. A substitution conferring TTX resistance to Nav1.7, a channel found in small peripheral neurons, arose in lizards ∼170 million years ago (mya) and was present in the common ancestor of all snakes. A second channel found in larger myelinated neurons, Nav1.6, subsequently evolved resistance in four different snake lineages beginning ∼38 mya. Extreme TTX resistance has evolved at least five times within the past 12 million years via changes in Nav1.4, but only within lineages that previously evolved resistant Nav1.6 and Nav1.7. Our results show that adaptive protein evolution may be contingent upon enabling substitutions elsewhere in the genome, in this case, in paralogs of the same gene family.

Santa Cruz Garter Snake Thamnophus atratus & Rough-skinned Newt Taricha granulosa.

pbase.com/inaturalist

Joel W. McGlothlin, Megan E. Kobiela, Chris R. Feldman, Todd A. Castoe, Shana L. Geffeney, Charles T. Hanifin, Gabriela Toledo, Freek J. Vonk, Michael K. Richardson, Edmund D. Brodie Jr., Michael E. Pfrender, Edmund D. Brodie III. 2016. Historical Contingency in a Multigene Family Facilitates Adaptive Evolution of Toxin Resistance. Current Biology.  In Press.  DOI:  10.1016/j.cub.2016.04.056 

How an evolutionary arms race with snakes turned newts super toxic http://wpo.st/ASoe1

Snakes and newts have been locked in an evolutionary arms race since before they even existed. http://www.theatlantic.com/science/archive/2016/06/the-very-long-war-between-snakes-and-newts/486311/

[Herpetology / Evolution • 2009] A Central Role for Venom in Predation by Varanus komodoensis (Komodo Dragon) and the Extinct Giant Varanus (Megalania) priscus

Fig. 2. Anatomical investigation of the Varanus komodoensis venom system. (A) Magnetic resonance imaging of the V. komodoensis head showing the protein-secreting mandibular venom gland, with the 6 compartments colored in alternating red and pink (C1–C6), and the mucus-secreting infralabial gland in yellow (L).
(B) Longitudinal MRI section showing the large duct emerging separately from each compartment of the mandibular venom gland and threading between the mucus lobes of the infralabial gland to terminate between successive teeth (black oval areas).
(C) Transverse MRI section showing the large central lumen of the mandibular venom gland and individual lobes of the labial gland.
(D) Transverse histology of Masson’s Trichromestained section showing the intratubular lumina of the mandibular venom gland that feed into the large central lumen.
(E) Transverse histology of Masson’s Trichrome-stained section of a mucus infralabial gland showing numerous tightly packed internal lobules (note that the 6 large dark folds are histology artifacts).

Abstract

The predatory ecology of Varanus komodoensis (Komodo Dragon) has been a subject of long-standing interest and considerable conjecture. Here, we investigate the roles and potential interplay between cranial mechanics, toxic bacteria, and venom. Our analyses point to the presence of a sophisticated combined-arsenal killing apparatus. We find that the lightweight skull is relatively poorly adapted to generate high bite forces but better adapted to resist high pulling loads. We reject the popular notion regarding toxic bacteria utilization. Instead, we demonstrate that the effects of deep wounds inflicted are potentiated through venom with toxic activities including anticoagulation and shock induction. Anatomical comparisons of V. komodoensis with V. (Megalania) priscus fossils suggest that the closely related extinct giant was the largest venomous animal to have ever lived.

Keywods: evolution, phylogeny, squamate, protein, toxin

http://phenomena.nationalgeographic.com/2009/05/18/venomous-komodo-dragons-kill-prey-with-wound-and-poison-tactics/

Fry, B., Wroe, S., Teeuwisse, W., van Osch, M., Moreno, K., Ingle, J., McHenry, C., Ferrara, T., Clausen, P., Scheib, H., Winter, K., Greisman, L., Roelants, K., van der Weerd, L., Clemente, C., Giannakis, E., Hodgson, W., Luz, S., Martelli, P., Krishnasamy, K., Kochva, E., Kwok, H., Scanlon, D., Karas, J., Citron, D., Goldstein, E., Mcnaughtan, J., & Norman, J. 2009. A Central Role for Venom in Predation by Varanus komodoensis (Komodo Dragon) and the Extinct Giant Varanus (Megalania) priscus. Proceedings of the National Academy of Sciences 

DOI: 10.1073/pnas.0810883106