Utah State University and Butantan Institute scientists publish evolutionary findings in 'iScience.'
IMAGE: A MAGNIFIED IMAGE OF THE MOUTH OF A RINGED CAECILIAN, SIPHONOPS ANNULATUS, REVEALS SNAKE-LIKE DENTAL GLANDS. RESEARCHERS FROM BRAZIL'S BUTANTAN INSTITUTE AND UTAH STATE UNIVERSITY SAY THE GLANDS COULD INDICATE... view more
CREDIT: BUTANTAN INSTITUTE, BRAZIL
LOGAN, UTAH, USA - Utah State University biologist Edmund 'Butch' Brodie, Jr. and colleagues from São Paulo's Butantan Institute report the first known evidence of oral venom glands in amphibians. Their research, supported by the Brazilian National Council for Scientific and Technological Development, appears in the July 3, 2020, issue of iScience.
"We think of amphibians - frogs, toads and the like -- as basically harmless," says Brodie, emeritus professor in USU's Department of Biology. "We know a number of amphibians store nasty, poisonous secretions in their skin to deter predators. But to learn at least one can inflict injury from its mouth is extraordinary."
Brodie and his colleagues discovered the oral glands in a family of caecilians, serpent-like creatures related to frogs and salamanders. Neither snakes nor worms, caecilians are found in tropical climates of Africa, Asian and the Americas. Some are aquatic and some, like the ringed caecilian (Siphonops annulatus) studied by Brodie's team, live in burrows of their own making.
In 2018, the team reported the species secreted substances from skin glands at both ends of its snake-like body. Concentrated at the head and extending the length of the body, the creature emits a mucous-like lubricant that enables it to quickly dive underground to escape predators. At the tail, caecilians have glands armed with a toxin, which acts as a last line of chemical defense, blocking a hastily burrowed tunnel from hungry hunters.
"What we didn't know is these caecilians have tiny fluid-filled glands in the upper and lower jaw, with long ducts that open at the base of each of their spoon-shaped teeth," Brodie says.
His research colleague Pedro Luiz Mailho-Fontana, who studied with Brodie as a visiting graduate student at USU's Logan campus in 2015, noticed the never-before-described oral glands. Using embryonic analysis, Mailho-Fontana, first author of the paper, discovered the glands - called "dental glands" - originated from a different tissue than the slime and poison glands found in the caecilian's skin.
"The poisonous skin glands form from the epidermis, but these oral glands develop from the dental tissue, and this is the same developmental origin we find in the venom glands of reptiles," he says.
The researchers surmise caecilians, equipped with no limbs and only a mouth for hunting, activate their oral glands when they bite down on prey, including worms, termites, frogs and lizards.
The team doesn't yet know the biochemical composition of the fluid held in the oral glands.
"If we can verify the secretions are toxic, these glands could indicate an early evolutionary design of oral venom organs," Brodie says. "They may have evolved in caecilians earlier than in snakes."
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First evidence of snake-like venom glands found in amphibians
IMAGE: THIS IMAGE SHOWS A GENERAL VIEW OF THE RINGED CAECILIAN, SIPHONOPS ANNULATUS. view more
CREDIT: CARLOS JARED
Caecilians are limbless amphibians that, to the untrained eye, can be easily mistaken for snakes. Though caecilians are only distantly related to their reptilian cousins, researchers in a study appearing July 3 in the journal iScience describe specialized glands found along the teeth of the ringed caecilian (Siphonops annulatus), which have the same biological origin and possibly similar function to the venom glands of snakes. If further research can confirm that the glands contain venom, caecilians may represent the oldest land-dwelling vertebrate animal with oral venom glands.
Caecilians are peculiar creatures, being nearly blind and using a combination of facial tentacles and slime to navigate their underground tunnels. "These animals produce two types of secretions--one is found mostly in the tail that is poisonous, while the head produces a mucus to help with crawling through the earth," says senior author Carlos Jared, a biologist and Director of the Structural Biology Lab at the Butantan Institute in São Paulo. "Because caecilians are one of the least-studied vertebrates, their biology is a black box full of surprises."
"It is while examining the mucous glands of the ringed caecilian that I stumbled upon a never before described set of glands closer to the teeth," says first author Pedro Luiz Mailho-Fontana, a post-doctoral student in the Structural Biology Lab at the Butantan Institute.
What Mailho-Fontana found were a series of small fluid-filled glands in the upper and lower jaw, with long ducts that opened at the base of each tooth. Using embryonic analysis, he found that these oral glands originated from a different tissue than the slime and poison glands found in the caecilian's skin. "The poisonous skin glands of the ringed caecilian form from the epidermis, but these oral glands develop from the dental tissue, and this is the same developmental origin we find in the venom glands of reptiles," says Mailho-Fontana. This marks the first time glands of this kind have been found in an amphibian.
Researchers suspect that the ringed caecilian may use the secretions from these snake-like oral glands to incapacitate its prey. "Since caecilians have no arms or legs, the mouth is the only tool they have to hunt," says co-author Marta Maria Antoniazzi, an evolutionary biologist at the Butantan Institute. "We believe they activate their oral glands the moment they bite down, and specialized biomolecules are incorporated into their secretions.
A preliminary chemical analysis of the oral gland secretions of the ringed caecilian found high activity of phospholipase A2, a common protein found in the toxins of venomous animals. "The phospholipase A2 protein is uncommon in non-venomous species, but we do find it in the venom of bees, wasps, and many kinds of reptiles," says Mailho-Fontana. In fact, the biological activity of phospholipase A2 found in the ringed caecilian was higher than what is found in some rattlesnakes. Still, more biochemical analysis is needed to confirm whether the glandular secretions are toxic.
If future work can verify the secretions are toxic, caecilian oral glands could indicate an early evolutionary design of oral venom organs. "Unlike snakes which have few glands with a large bank of venom, the ringed caecilian has many small glands with minor amounts of fluid. Perhaps caecilians represent a more primitive form of venom gland evolution. Snakes appeared in the Cretaceous probably 100 million years ago, but caecilians are far older, being roughly 250 million years old," Jared says.
Very few groups of land-dwelling vertebrates have serpent-like bodies, and this research suggests there might be a connection between a limbless body plan and the evolution of a venomous bite. "For snakes and caecilians, the head is the sole unit to explore the environment, to fight, to eat, and to kill," says Antoniazzi. "One theory is that perhaps these necessities encourage the evolution of venom in limbless animals."
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This work was supported by the National Council for Scientific and Technological Development (CNPq), São Paulo Research Foundation (FAPESP), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brazil (CAPES).
iScience, Mailho-Fontana et al.: "Morphological Evidence for an Oral Venom System in Caecilian Amphibians" https://www.cell.com/iscience/fulltext/S2589-0042(20)30419-3
iScience (@iScience_CP) is an open-access journal from Cell Press that provides a platform for original research and interdisciplinary thinking in the life, physical, and earth sciences. The primary criterion for publication in iScience is a significant contribution to a relevant field combined with robust results and underlying methodology. Visit: http://www.
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