Monsters and dragons: Venomous lizards

When we think about venomous animals most people think about the same ones. Usually, we think about spiders, scorpions and snakes, despite knowing there are also venomous amphibians, fishes and mammals. Even if snakes are the best known venomous reptiles, in time we have learned that they are not the only group that present venomous glands and that many other reptiles also have the capacity of injecting venom. In this entry we’ll get to know the least known venomous saurians and we’ll try to explain their relationship with snakes.

EVOLUTION OF VENOM IN REPTILES

Everybody is familiar with the toxic abilities of snakes. Traditionally it was believed that venom evolved independently in the different groups of venomous snakes (colubrids, elapids and viperids) and in a lizard family (the helodermatids). Yet this vision has changed over the years and with the discovery of other species of venomous squamates.

The venom of many animals is used for both antivenom development and pharmacological research of analgesics and other medicines. Photo of the extraction of venom from a saw-scaled viper (Echis carinatus), by Kalyan Varma (Image under a GNU license).

Currently, it’s been shown that there are different species of saurian which present glands and organs capable of injecting venom, along with many other species with genetic material related to venom production (even if most aren’t venomous). This occurs, for example, in many apparently non-venomous snakes and lizards that retain genetic material related to the synthesis of venom. This has caused many scientists to group these reptiles under a common clade called Toxicofera, “those who bear toxins”.

This new clade includes the different squamosal taxa, which are believed to have had a venomous common ancestor. These groups are:

• Ophidia: Ophidians, snakes.

Indian wolf snake (Lycodon aulicus), example of an ophidian. Photo by Shantanu Kuveskar.

• Iguania: Iguanas, agamas and chameleons.

Brown basilisk (Basiliscus vittatus), example of an iguanian. Photo by Steve Harbula.

• Anguimorpha: Monitors, slow worms and others.

Earless monitor lizard (Lanthanotus borneensis), example of an anguimorph. Photo by Kulbelbolka.

Even though most current iguanians and anguimorphs don’t present venom, the Toxicofera theory proposes that many species would have lost their capacity to inject venom secondarily. Below we’ll present some of the lesser known venomous saurians.

MONSTERS OF THE NEW WORLD

The most famous venomous lizards are the anguimorphs of the Helodermatidae family. From their discovery it was known that these lizards where venomous, as they present a pair of venomous glands in their lower jaws and various pairs of grooved teeth similar to those of venomous snakes with which they inject venom.

Helodermatid skull, in which we can see the sharp teeth with which they inject their venom. Image from Heloderma.net.

The helodermatis are carnivorous animals which feed on small mammals, birds, wall lizards, amphibians, invertebrates, eggs and carrion. Considering its generalist diet and that their prey are pretty defenceless, it is thought that venom evolved in these reptiles as a predator deterrent method, not as a hunting strategy.

Photo by Walknboston of a Gila monster (Heloderma suspectum), in which we can see its black and yellow coloration, with which it warns its predators about its toxicity (aposematic coloration).

The Gila monster and the beaded lizard (Heloderma horridum) are slow animals which aren’t really dangerous to human beings. Yet their raising popularity as exotic pets has ended with some bite cases. The bite of a Gila monster causes some serious and burning pain, local edema, weakness, dizziness and nausea. Even if heavy bleeding is usually associated with bites, this isn’t due to some sort of anticoagulant substance but to the helodermatid’s sharp teeth and to the fact that to inject the venom they must chew their aggressor strongly , causing deep lacerations.

THE BEARDED DRAGON

The saurians of the genus Pogona are iguanians of the Agamidae family. These Australian reptiles are known as bearded dragons for the spines that they present on their throats. Even though they are adapted to live in arid places, the environmental temperature can affect the sex of their offspring.

Photo of an eastern bearded dragon in which we can see its yellow coloured mouth. Could it be that this coloration is indicating anything? Photo by Matt.

Bearded dragons are inoffensive animals, but there’s one species with a secret weapon. The eastern bearded dragon (Pogona barbata) is a venomous lizard but, while the rest of venomous reptiles only have one pair of venomous glands, the eastern bearded dragon has two pairs: two in its upper jaw and two in its lower jaw.

Transversal section of the mouth of an eastern bearded dragon, in which we can see the incipient venomous glands both in its upper jaw (mxivg) and its lower jaw (mnivg). Image extracted from Fry, Vidal et al.

The venom they produce isn’t really strong (in human beings it only causes a minor swelling) and the glands are considered vestigial. Yet, the Toxicofera theory argues that the glands of the bearded dragon show us the primitive form which the first toxicoferan reptile would have presented, with two pairs of venom glands instead of a single pair like most current venomous reptiles.

THE BIG MONITORS

Everyone has heard about monitor lizards (anguimorphs of the Varanidae family). There are hundreds of documentaries about the Komodo dragon in which we are told that these animals have so many bacteria in their mouths that their bites inflict an infection, deadly enough to kill an adult bull. Yet recent studies have shown that the monitor’s poor buccal hygiene is not what causes the death of their victims.

Perente or perentie (Varanus giganteus) a typical varanid, with long neck, strong legs, active metabolism and developed senses. Photo by Bernard Dupont.

Even if there are three frugivorous species, the rest are obligate carnivores. It has always been said that the mouth’s bacteria of the monitors is what causes the death of their prey, even if there isn’t any studies which prove it. In fact, in many studies it has been seen that the monitor’s saliva isn’t very different from that of other herbivorous reptiles.

Photo in which we see the feared monitor’s saliva, specifically from an Asian water  monitor (Varanus salvator). Image by Lip Kee.

In a study, it was demonstrated that various species of monitor lizards present venom glands in their lower jaws. These glands are among the most complex venomous glands known of all reptiles. In the case of the Komodo dragon, these are compound glands with a larger posterior compartment and five smaller anterior compartments. These compartments have ducts that carry the venom between the teeth.

Even if varanids are closely related to snakes (they share, for example, a bifid tongue), these don’t present the snakes’ characteristic grooves in their teeth. This is due to the fact that instead of injecting the venom directly, monitor lizards use their serrated teeth to open a deep wound in their prey, through which the venom will enter the organism.

Skull of megalania (Varanus priscus) in which we can see the teeth without gooves. This extinct monitor with more than 5 metres long, was the largest venomous animal known. Photo by Steven G. Johnson.

The utility of the venom for the predatory monitors is also supported by the large quantities of venom that they produce. In constrictor snakes that don’t utilise venom, the genes which codify the synthesis of venom are atrophied because of the great amount of energy required to produce it. Monitors, instead, secrete lots of venom with the slightest stimulation of their glands. This venom contains anticoagulant compounds which prevent the wound to close and also produces a cardiovascular shock in the animal by lowering the blood pressure.

A group of Komodo dragons (Varanus komodoensis) feeding on a recently killed pig. Image extracted from Bull, Jessop et al.

Even if we still don’t know for sure if the common ancestor of all these animals was venomous, nor if venom appeared independently in the different families, the relationship between the different members of the clade Toxicofera has been supported by posterior phylogenetic analyses. What we know is that venom is an extremely powerful weapon in the struggle for survival and that, even if snakes are the most numerous venomous reptiles, many other squamate species have been benefiting from the use of toxins, both for self-defence and to subjugate their prey.

REFERENCES

The following sources have been used during the elaboration of this entry:

• Halliday & Adler (2007). La gran enciclopedia de los Anfibios y Reptiles. Editorial Libsa.
• http://www.nature.com/nature/journal/v439/n7076/full/nature04328.html
• http://www.sciencedirect.com/science/article/pii/S0041010114003353
• http://www.leidenuniv.nl/en/researcharchive/index.php3-c=134.htm
• http://www.heloderma.net/en/heloderma.html
• http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0011097
• https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2690028/
• Cover image by Rocío Corzo.

Reptiles and mammals: same origin, different stories

Did mammals evolve from reptiles? The truth is they didn’t. Reptiles and mammals both have independent evolutionary histories that separated soon after the apparition of the so-called amniotic egg, which allowed the babies of these animals to be born outside of water. Previously, we talked about the origin of vertebrates and about how they managed to get out of the sea to start walking on land for the first time. In this entry we’ll explain how the ancestors of reptiles and mammals, the AMNIOTES, became independent of the aquatic medium and became the dominant land animals.

THE AMNIOTIC EGG

The characteristic that unites reptiles and mammals in the same group is the amniotic egg. While amphibian eggs are relatively small and only have one inner membrane, the eggs of amniotes are much bigger and present various membranes protecting the embryo and keeping it in an aqueous medium. The outer layer is the eggshell which, apart from offering physical protection to the embryo, prevents water loss and its porosity allows gas interchange. Beneath the eggshell we can find the next membranes:

Diagram of a crocodile egg: 1. eggshell 2. yolk sac 3. yolk (nutrients) 4. vessels 5. amnion 6. chorion 7. air 8. alantois 9. albumin (white of the egg) 10. amniotic sac 11. embryo 12. amniotic fluid. Image by Amelia P.

• Chorion: The first inner membrane, which offers protection and, together with the amnion, forms the amniotic sac. Also, being in contact with the eggshell, it participates in gas interchange, bringing oxygen from the outside to the embryo and carbon dioxide from the embryo to the outside.
• Amnion: Membrane that surrounds the embryo and constitutes a part of the amniotic sac. It offers an aqueous medium for the embryo and connects it with the yolk sac (a structure that brings food and that is also found in fish and amphibians).
• Allantois: The third layer, it is used as a storage for nitrogen waste products, and together with the chorion, helps in gas interchange.

Diagram of an amphibian egg: 1. jelly capsule 2. vitelline membrane 3. perivitelline fluid 4. yolk 5. embryo. Image by Separe3g.

All these different kinds of membranes eliminate the need amphibians had of laying their eggs in water. Also, unlike amphibians, amniotes don’t go through a gilled larval stage, but are instead born as miniature adults, with lungs and legs (at least those that have them). All these made the first amniotes completely independent of the aquatic medium.

AMNIOTE ORIGINS

The first amniotes evolved around 312 million years ago from reptiliomorph tetrapods. At the end of the Carboniferous period lots of tropical forests where the great primitive amphibians lived disappeared, leaving a colder and drier climate. This ended with many of the big amphibians of that time, allowing the amniotes to occupy new habitats.

Reconstruction of Solenodonsaurus janenschi, one of the candidates in being the first amniote, which lived around 320-305 million years ago in what is now the Czech Republic. Reconstruction by Dmitry Bogdanov.

CHARACTERISTICS

These early amniotes had a series of characteristics that set them apart from their semiaquatic ancestors:

• Horny claws (amphibians don’t have claws) and keratinized skin that prevents water loss.
• Bigger large intestine and higher density of renal tubules to increase water reabsorption.
• Specialized lacrimal glands and a third membrane in the eye (nictitating membrane) which keep the eye wet.
• Larger lungs.
• Loss of the lateral line (sensory organ present in fish and amphibians).

The skeleton and musculature also evolved offering better mobility and agility on a terrestrial medium. The first amniotes presented ribs that encircled their body converging at the sternum, making their inner organs more secure, and a series of muscular receptors offered them better agility and coordination during locomotion.

AMNIOTE SKULLS

Traditionally, the different amniotes were classified based on the structure of their cranium. The characteristic used to classify them was the presence of temporal openings (fenestrae), by which we have three groups:

• Anapsids (“no arches”): No temporal openings (turtles).

Diagram of an anapsid skull, by Preto(m).

• Synapsids (“fused arches”): With only one temporal opening (mammals).

Diagram of a synapsid skull, by Preto(m).

• Diapsids (“two arches”): With two temporal openings (reptiles, including birds).

Diagram of a diapsid skull, by Preto(m).

Previously it was believed that the first amniotes presented an anapsid skull (without openings, like turtles) and that subsequently they separated into synapsids and diapsids (the temporal openings formed “arches” that offered new anchor points for the jaw’s musculature). Yet, it has been discovered that this three-group classification is not valid.

Even though we still believe that the first amniotes were anapsid, it is currently known that these, soon after their apparition, separated into two different lineages: the synapsids (clade Synapsida) and the sauropsids (clade Sauropsida).

SYNAPSIDA

This lineage includes mammals and their amniote ancestors. Even though the first synapsids like Archaeothyris looked externally like lizards, they were more closely related to mammals, as they shared one temporal fenestrae where the jaw muscles passed through.

Drawing of the skull of Archaeothyris, which is thougth to be one of the first synapsids that lived around 306 million years ago in Nova Scotia. Drawing by Gretarsson.

The ancestors of mammals were previously known as “mammal-like reptiles”, as it was thought that mammals had evolved from primitive reptiles. Currently it’s accepted that synapsids form a different lineage independent of reptiles, and that they share a series of evolutionary trends that makes them closer to modern mammals: the apparition of different kinds of teeth, a mandible made of one single bone, the vertical posture of their limbs, etc…

Reconstruction of Dimetrodon grandis, one of the better known synapsids, from about 280 million years ago. Reconstruction by Dmitry Bogdanov.

Even though most modern mammals don’t lay eggs and give birth to live offspring, all groups maintain the amniote’s three characteristic membranes (amnion, chorion and allantois) during embryonic development.

SAUROPSIDA

Sauropsids include current reptiles and their amniote ancestors. Currently, in many scientific papers the word “sauropsid” is used instead of “reptile” when discussing phylogenies, as the sauropsids also includes birds. The first sauropsids were probably anapsids, and soon after their appearance they separated into two groups: the Parareptilia which conserved anapsid skull, and the Eureptilia which include the diapsids (current reptiles and birds).

Evolutionary tree of current vertebrates, in which green color marks the groups previously included inside reptiles. As you can see, the traditional conception of "reptile" includes the ancestors of mammals and excludes birds. Image by Petter Bøckman.

Diapsids are currently the most diversified group of land vertebrates. They diversified greatly in the late Permian period (about 254 million years ago), just before the Mesozoic (the Age of Reptiles). These can be divided into two main groups: the Lepidsaurs and the Archosaurs, both with representatives in our days.

LEPIDOSAURIA: SMALL AND PLENTIFUL

Lepidosaurs (literally “reptiles with scales”) appeared in the early Triassic (around 247 million years ago) and, even if most of them didn’t grow to big sizes, they are currently the largest group of non-avian reptiles. These are characterized by presenting a transversal cloacal slit, by having overlapping scales and shedding their skin whole or in patches and by other skeletal characters.

Shed skin of a rat snake. Photo by Mylittlefinger.

The current lepidosaurs belong to one of two different orders:

• Order Rhynchocephalia: That includes the two species of tuatara. Currently endangered, they are considered living fossils because they present skulls and characteristics similar to the Mesozoic diapsids.

Photo of a tuatara (Sphenodon punctatus), by Tim Vickers.

• Order Squamata: Current squamates include iguanas, chameleons, geckoes, skinks, snakes and other legless lizards. With more than 9000 living species, squamates are a large group with a wide array of adaptations and survival strategies.

Photos of some squamates, from left to right and from top to bottom: Green iguana (Iguana iguana, by Cary Bass), king cobra (Ophiophaga Hannah, by Michael Allen Smith), Mexican mole lizard (Bipes biporus, by Marlin Harms) and Indian chameleon (Chamaeleo zeylanicus, by Shantanu Kuveskar).

ARCHOSAURIA: ANCIENT KINGS

Archosaurs (literally “ruling reptiles”) were the dominant group of land animals during the Mesozoic. These conquered all possible habitats until the extinction of most groups at the end of the Cretaceous period. Some of the extinct groups were the pseudosuchians (relatives of modern crocodiles, order Crocodylia), the pterosaurs (large flying reptiles) and the dinosaurs (excepting birds, clade Aves).

Drawing of the skull of the dinosaur Massospondylus in which we can see the different characteristic openings of diapsid archosaurs. Image by Steveoc 86.

As you see, both groups of modern archosaurs couldn’t be more different. Yet, crocodiles and birds share a common ancestor, and they are both more closely related with each other than with the rest of reptiles.

Photo of two species of modern arcosaurs: a Nile crocodile (Crocodylus niloticus) and a yellow-billed stork (Mycteria ibis). Photo by Tom Tarrant.

AND WHAT ABOUT TURTLES?

Turtles (order Testudines) have always been a group difficult to classify. Turtles are the only living amniotes with an anapsid skull, without any post-ocular opening. That’s why previously they had been classified as descendants of primitive amniotes (clade Anapsida, currently disused) or as primitive anapsid sauropsids (inside the Parareptilia clade)

Skeleton of the extinct tortoise Meiolania platyceps which lived in New Caledonia until 3000 years ago. In this photo it can be seen the compact cranium without openings. Photo by Fanny Schertzer.

Recent molecular studies have revealed that turtles are actually diapsids that lost their temporal openings secondarily. What still divides the scientific community is if testudines are more closely related to Lepidosauromorphs (lepidosaurs and their ancestors) or to Archosauromorphs (archosaurs and their ancestors).

Individual leopard tortoise (Stigmochelys pardalis) from Tanzania. Photo by Charles J. Sharp.

As you have seen, the evolution of amniotes is an extremely complex matter. We hope that with this entry some concepts have been clarified:

1. Mammals (synapsids) come from an evolutionary lineage different from that of reptiles (sauropsids).
2. Sauropsids include traditional reptiles (lepidosaurs, archosaurs and turtes) and birds (inside archosaurs).
3. There’s still so much to investigate about the placement of turtles (testudines) in the evolutionary tree of sauropsids.

Modified diagram about the evolutionary relationships of the different amniote groups.

REFERENCES

During the elaboration of this entry the following sources have been consulted:

• Cover image by Henri Pidoux.
• Halliday & Adler (2007). La gran enciclopedia de los Anfibios y Reptiles. Editorial Libsa.
• Hickman, Roberts, Keen, Larson, l’Anson & Eisenhour (2009). Principios integrales de Zoología (decimocuarta edición). Mc Graw Hill.
• http://www.biologyreference.com/A-Ar/Amniote-Egg.html
• http://www.ucmp.berkeley.edu/vertebrates/tetrapods/amniota.html
• http://tolweb.org/Amniota
• http://onlinelibrary.wiley.com/doi/10.1111/j.1095-8312.1979.tb00027.x/abstract
• https://courses.candelalearning.com/osbiosec/chapter/29-4-reptiles/