Morphological Evidence for an Oral Venom System in Caecilian Amphibians

Abstract

Summary Amphibians are known for their skin rich in glands containing toxins employed in passive chemical defense against predators, different from, for example, snakes that have active chemical defense, injecting their venom into the prey. Caecilians (Amphibia, Gymnophiona) are snake-shaped animals with fossorial habits, considered one of the least known vertebrate groups. We show here that amphibian caecilians, including species from the basal groups, besides having cutaneous poisonous glands as other amphibians do, possess specific glands at the base of the teeth that produce enzymes commonly found in venoms. Our analysis of the origin of these glands shows that they originate from the same tissue that gives rise to teeth, similar to the venom glands in reptiles. We speculate that caecilians might have independently developed mechanisms of production and injection of toxins early in their evolutionary history.

An ancient, conserved gene regulatory network led to the rise of oral venom systems

“…The high similarity between venom and salivary secretions in solenodon seems to confirm the saliva to venom path of toxin recruitment (39). Intriguingly, a recent report on caecilian venom detected fibrinogenolytic activity (63), which is also consistent with the presence of kallikreins (64). It appears that the ancestral salivary GRN's composition predisposes the evolution of envenomation strategies based on hypotensive shock via kallikrein injection.…”

Differences between poison and venom: An attempt at an integrative biological approach

“…As in the other amphibian orders (Anura and Caudata), they are characterised by the presence of cutaneous poison and mucous glands in the whole body. In a recent study carried out with caecilian amphibians, we have shown in the entire group the existence of a different type of gland located in a row along the upper and lower jaws, clearly connected to the base of the teeth through glandular ducts (Mailho-Fontana et al, 2020). The embryological analysis demonstrated that such glands originate from the same tissue that gives origin to the snake venom glands.…”

“…When a caecilian bites a prey to feed, an intense sticky secretion is released around the lips. This secretion has shown to contain not only mucus to facilitate swallowing but also bioactive compounds, such as phospholipase A 2 enzymes, which are common in venoms of several animals, including snakes, bees and wasps (Mailho-Fontana et al, 2020). As caecilians date from the Jurassic period, around 250 million years ago (Pyron, 2011;San Mauro, 2010), it is possible to infer that their dental glands constitute an adaptive convergence with those of snakes, that appeared some 150 million years after, in the Middle Jurassic-Lower Cretaceous (Caldwell et al, 2015).…”

Morphology of the Cutaneous Poison and Mucous Glands in Amphibians with Particular Emphasis on Caecilians (Siphonops annulatus)

“…The cutaneous secretion from the poison and mucous glands is understudied among caecilians. In recent decades, our group has been studying the biology and behaviour of Siphonops annulatus, particularly in relation to the defence and reproductive behaviour in the field and in captivity [11,17,37,44]. The cacao plantation, located in the south of the State of Bahia (Brazil), where the species is abundant, maintains the original environmental conditions of the Atlantic Rainforest, since cacao trees are planted in the shade of the large original trees (plantation modality known as "cabruca") [37].…”