Squamata

(Lizards and snakes)

Class Reptilia

Order Squamata

Number of families About 42

Number of genera, species About 1,880 genera; 7,200 species

Evolution and systematics

Squamates are the most diverse living clade of reptiles, including about 1,440 genera and 4,450 species of lizards plus 440 genera and 2,750 species of snakes. Although snakes are commonly considered to constitute their own group, they clearly have descended from lizards and are merely limbless lizards. Squamates exhibit more than 70 shared derived traits, which indicate that they are descendants of a common ancestor, forming a large natural monophyletic group. (Snakes and lizards once were classified as different suborders, but since snakes are embedded within lizards, this classification is no longer tenable under the monophyletic standard of modern phylogenetic systematics.)

Sister group

The sister group to squamates is Rhynchocephalia, represented today by only two species of tuatara (Sphenodon) from New Zealand. Superficially, tuatara resemble lizards, in that they have a dorsal crest of scales. They possess two temporal arches (the "diapsid" condition), however, making their skulls quite rigid. They do not have copulatory organs. In tuatara the lower jaw articulates directly with the upper skull, resulting in a narrow gape and slow jaw movements. Tuatara are visual ambush predators that eat large prey, which they pick up with their sticky and fleshy tongues ("lingual prehension"). Because these traits are shared with basal lizards, they are probably ancestral states.

Streptostyly and Jacobson's organ

In all squamates, the lower temporal arch has been lost, and the lower jaw hinges on the quadrate bone, which hangs down from the cranium, a situation known as "streptostyly." This hanging jaw setup provides a mechanical advantage that results in faster jaw opening and closure, a wider gape, and a stronger bite, presumably greatly enhancing prey capture and feeding. All lizards and snakes also have a pair of eversible copulatory organs (hemipenes) at the base of their tails. Another novel and important feature of squamates is a vomeronasal olfactory organ (Jacobson's organ) in the palate, separate from the nasal capsule. Thus, squamates possess three chemosensory systems: (1) taste buds on their tongues, (2) nasal smelling of volatile airborne scents, and (3) vomeronasal analysis of heavy non-airborne chemicals picked up by the tongue and transferred into the Jacobson's organ in the roof of the mouth, where the signal is processed.

Vomerolfaction ability differs greatly among squamates, remaining relatively undeveloped in some basal groups but becoming acutely sensitive in more derived groups, such as varanids and snakes. Ancestral squamates were ambush predators that detected prey by movement using visual cues and had relatively low activity levels and poorly developed chemosensory systems. The large clade Iguania retained these ancestral features, whereas in the more advanced Scleroglossa a suite of derived characteristics developed. Ancestral scleroglossans captured and manipulated prey with their jaws (jaw prehension), thus freeing the tongue to evolve along other lines and facilitating the evolution of sensitive vomerolfaction. Active foraging and higher activity levels were further consequences. They also possessed the combined abilities to flex the skull (mesokinesis), and discriminate prey based on chemical cues, ultimately producing more than 20 remaining families of other lizards plus all snakes (13–18 families), making up 80% of all squamates. Most snakes are entirely legless, and no living snake has functional legs (although a fossil did), eardrums, or movable eyelids. Many other lizards, especially burrowers, also have become limbless and lost their eardrums and eyelids.

Fossil record and biogeography

Squamate history dates back at least to the early Jurrasic, if not the late Triassic. Squamata is the sister taxon to Rhynchocephalia, together making up Lepidosauria. About 200 million years ago (mya), before true lizards existed, one lineage of lepidosaurs gave rise to the ancestor of squamates. No fossils of this common ancestor ("stem group") of all squamates are known. It must have existed during the Upper Triassic to the Lower Jurassic, about 200–250 million mya, but a 50-million-year gap in the fossil record precludes exact dating. Most squamate fossils are considerably more recent. Much of early squamate evolution occurred during the Jurassic and Cretaceous on the supercontinent of Pangaea. Diversification of arthropods during the Jurassic provided a literal banquet for terrestrial vertebrates that could find and capture them. Five late Jurassic (about 150 mya) fossil lizards represent ancient extinct lineages. They are scattered across the squamate phylogenetic tree, indicating that early diversification into major clades (Iguania, Gekkota, Scincomorpha, and Anguimorpha) had taken place by the end of the Jurassic. These early lineages gave rise to the currently recognized 23–24 lizard families and 13–18 snake families.

Squamate evolution is intertwined intimately with continental drift. Some squamate families appear to be of Gondwanan origin, but others arose in the Northern Hemisphere and subsequently dispersed to southern continents. Australia's snakelike pygopodids arose from diplodactylid geckos within the island continent. Four lizard groups reached Australia and underwent extensive adaptive radiations. Some groups, such as skinks and varanids, became more speciose there than they are today in their probable ancestral source areas.

When the northern Laurasian plate separated from the southern Gondwanan plate in the mid-Jurassic, two isolated landmasses were formed. Gondwana presumably held primitive iguanians and gekkotans, whereas Laurasia must have contained ancestral eublepharid geckos, scincomorphans, and anguimorphans. When Gondwana broke apart, its iguanians and gekkotans became isolated on the three large southern landmasses, Africa (agamids, chameleons, and gekkonids), South America (iguanids and sphaerodactyline geckos), and the Australian region (agamids and diplodactylid geckos).

Gekkonids and skinks dispersed widely and became virtually cosmopolitan. Both crossed oceans by rafting and moving across land bridges. Other groups either remained confined to the landmass of origin (cordylids, corytophanines, crotaphytines, diplodactylids, gymnophthalmids, helodermatids, hoplocercines, lanthanotids, leiocephalines, leiosaurines, liolaemines, oplurines, phrynosomatines, pygopodids, sphaerodactylines, tropidurines, and xantusiids) or exhibited a more limited dispersal (agamids, anguids, chamaeleonids, iguanids, lacertids, teiids, and varanids). Exactly when and how snakes diversified and colonized the continents remains poorly understood, but within snakes, scleroglossan evolution produced groups as diverse as fossorial (adapted to digging) burrowers that live in social-insect colonies (scolecophidians) and sea snakes that inhabit the world's warm oceans (Hydrophiinae).

Snakes are arboreal, terrestrial, and aquatic and are top predators in almost all natural communities.

Phylogenetic relationships and number of families

A basal split in squamate phylogeny produced Iguania (99 genera and approximately 1,230 species), which retained ancestral traits (visual ambush predators with lingual prehension and poorly developed vomerolfaction), and Scleroglossa (almost 6,000 species), which adopted innovative new methods of finding and eating prey as well as acutely sensitive vomerolfaction and hydrostatic (operated by liquid pressures) forked tongues. Scleroglossa includes dibamids, amphisabaenians, and snakes, but their exact affinities within Scleroglossa remain uncertain. Remaining scleroglossans, in turn, bifurcated into two large clades, Gekkota and Autarchoglossa. Gekkota (about 1,000 species) evolved elliptical pupils and the ability to operate at low temperatures, allowing nocturnal activity. They use their tongues to clean their lips and eye spectacles. Geckos took to the night, where they found a cornucopia of nocturnal arthropods. (Some geckos have reverted to a diurnal way of life.) The largest and most advanced clade, Autarchoglossa (about 4,800 species), is composed of two smaller sister clades, Scincomorpha (seven families of lizards, with about 1,800 species) and Anguimorpha (five lizard families plus 15–18 snake families, with a total of more than 3,000 species). Members of the three clades, Iguania, Gekkota, and Autarchoglossa, differ considerably in morphologic features, physiological characteristics, behavior, life histories, and ecological niches, especially in foraging mode.

Iguanians are sit-and-wait ambush foragers that catch mobile prey as they move past their hunting stations. Most autarchoglossans are more active, foraging widely and searching for prey; as a result, they have access to sedentary and hidden prey items that are unavailable to iguanians. Active foraging is more expensive than ambush foraging, both in terms of energy expended and exposure to predators, but the returns are greater in calories obtained per unit time. Autarchoglossans have evolved flexible joints in their muzzles and skulls (mesokinesis and cranial kinesis), further improving their ability to capture and subdue large and agile prey.

Snake phylogeny has not yet been resolved, but three major groups are recognized: blindsnakes, primitive snakes, and advanced snakes. Blindsnakes (Scolecophidia) include three families (Anomalepididae, Leptotyphlopidae, and Typhlopidae). These are specialized burrowers and are considered sister to all other snakes (Alethinophidia), which are organized into four superfamilies (Anilioidea, Booidea, Acrochordoidea, and Colubroidea). Anilioids and booids are considered primitive snakes. As an indication of their lizard origin, boas and pythons still possess vestigial remnants of hind limbs, called "anal claws," which indicate that they are basal members of the ophidian clade. Colubroids, the most diverse snakes, are more advanced. Higher snakes are called Macrostomata, which includes boids, pythons, acrochordids, and the most advanced of all snakes, colubrids, viperids, and elapids. The vast majority of snakes are colubrids.

Physical characteristics

Squamates are ectotherms, obtaining their bodily heat from the external environment rather than generating it metabolically in the manner of endotherms (birds and mammals). Ectothermy is sometimes seen as a disadvantage, and lay people often erroneously refer to snakes and lizards as "cold-blooded." Snakes and lizards regulate their body temperatures behaviorally. When it is cold, they actively bask and seek out warm microclimates. When it is too hot, they look for shade and cooler places. When they are active, many squamates have body temperatures just as high as those of birds and mammals. In fact, ectothermy has real advantages over endothermy, especially in warm, dry, unproductive environments, such as deserts and semiarid regions. Ectotherms enjoy a low-energy lifestyle that endotherms can only envy. The food consumed by a 0.17-oz (5 g) bird in a single day will last a 0.17-oz squamate a month. An unproductive habitat, where endotherms cannot exist, will support viable populations of ectotherms. Snakes can go for many months, or even an entire year, without feeding, simply by allowing the body temperature to drop. The economic lifestyle offered by ectothermy enables squamates to thrive and persist during droughts and periods of resource shortages, which a high-energy endotherm simply could not tolerate.

Morphologic features

All lizards and snakes shed their skins at least once each year. Before shedding, a new inner layer of skin forms and separates from the outermost layer of older skin, which appears pale. Eye spectacles of snakes become cloudy. Snakes hook their lip scales on an immobile object and crawl out of their skins, leaving them behind intact and inside out. Sometimes, a snake can be identified to a species from its shed skin. Most lizards shed their skins in patches.

Most lizards have fracture planes in the caudal vertebrae, which facilitate tail loss. Some can even autotomize their own tails voluntarily. Tail loss often allows a lizard to escape from a would-be predator. In such species, tails are regenerated rapidly, although the regrown tail is never as perfect as the original tail. Regenerated tails do not have bony vertebrae but rather a cartilaginous rod. A few lizards and all snakes do not have such fracture planes and cannot regenerate a tail if it is broken off.

Lizard toes have evolved along many different pathways. Adhesive toe lamellae evolved independently in anoles, geckos, and skinks; improved climbing ability; and led to an arboreal lifestyle. Gecko foot hairs, apparently overdesigned by orders of magnitude, exploit intermolecular Van der Waals forces (the subatomic analogue of gravitational forces) to provide powerful purchase even on very smooth surfaces. (Some geckos can run up a pane of glass.) Similarly, independent acquisition of fringed toe scales in several families (e.g., Iguanidae, Teiidae, Scincidae, and Gerhosauridae) increased traction on soft sands and enhanced climbing ability, even enabling some lizards to run across water.

The highly successful Chamaeleonidae (about 130 species) set their own direction in lizard evolution, taking lingual feeding and sit-and-wait ambush foraging to their logical extremes. Ballistic tongues allow chameleons to capture prey more than a body length away without moving, and having their toes bound together (zygodactly) permits them to hang on to and balance on thin branches to exploit arboreal habitats. Prehensile tails facilitate climbing and are used as a fifth leg. Independently moving, turret-like eyes allow chameleons to look all around without even moving their heads. By capturing their prey without moving, staying completely concealed in vegetation, chameleons have eliminated the riskiest aspect of sit-and-wait ambush foraging—pursuit movements.

Jaw prehension of prey freed the tongue from its role in prey capture, permitting it to evolve to become a specialized chemical sampler, carrying non-airborne chemical particles into the mouth to be received and deciphered by the vomeronasal system. The vomeronasal system was present in squamate ancestors, but it remained relatively rudimentary in most iguanians. In scleroglossans, the foretongue became specialized for protrusion and for picking up and transporting chemical signals, and the skull became less robust and more flexible than in iguanians. The temporal region is less broad, owing to reduction or loss of the upper temporal bar. Additional points of potential flexibility arose in scleroglossan skulls, a condition known as "cranial kinesis," or mesokinesis. This allows the muzzle and upper jaw to flex upward and downward, making the jaws more efficient in capture and

manipulation of agile prey. Such jaws bend and better conform to prey, enhancing feeding success.

This combination of skull and chemosensory modifications gave scleroglossans access to microhabitats and prey previously unavailable to iguanians and predisposed them to higher activity levels. For example, an ability to detect and discriminate prey chemically gave scleroglossans access to prey that could not be detected visually. No longer limited to prey moving across their field of vision, squamates could now find highly cryptic invertebrates and vertebrates living in crevices, in the ground, or in water. Remaining in one place for long periods of time has a low-energy payoff compared with searching actively through the habitat for hidden and sedentary prey. Active or wide foraging provided these lizards with a competitive advantage and selected for higher levels of activity. Moving about searching for prey is energetically costly and also increases the risk of exposure to potential predators. Alert behavior and rapid response to predators evolved to enable increased activity levels. Widely foraging scleroglossans find and consume more prey calories per unit time than do iguanians. Gekkota evade both competition and predation by being nocturnal, whereas Autarchoglossa evade potential diurnal predators by being exceedingly alert and agile. Elongation of the body and increased jaw flexibility permitted varanoid lizards to swallow large prey and set the stage for the evolution of snakes.

Snakes carried cranial kinesis to an even higher level than did their lizard ancestors, evolving numerous flexible joints in their skulls. Liberation of the mandibular symphysis (the tendons connecting the two lower jaws) set off snake evolution. Unlike lizards, most snakes also have independent movement of bones on the left and right sides of their skulls. Coupled with streptostyly, these adaptations allow snakes to swallow exceedingly large prey. Snake skulls have diversified widely. Snakes lost both temporal arches and apertures, permitting greater independent movements of the head bones. Many snakes have highly flexible jaws and snouts with many joints and considerable cranial kinesis. The musculature of a snake's head is quite complex, allowing for independent movements of cranial bones. When swallowing large prey, snakes "walk" their way down a prey item, first opening one side of their jaws, extending the jawbones forward, biting down, and then repeating the process on the other side.

Owing to lack of limbs, snake diversity is restricted by morphologic features. Nevertheless, snakes have accomplished some rather spectacular things. Some snakes (Dipsas) pull snails out of their shells. Snail-eating lizards (Dracaena) crush snail shells with molariform teeth. Many lizards are termite specialists. Some, such as certain geckos, catch termites at night when they are active above ground. Others, such as lacertids and teiids, break into termite tunnels during the day. Still others, such as some fossorial skinks, find termites in tunnels and termitaria below ground. All termite-specialized snakes find termites below ground, and many actually spend most of their lives inside termitaria.

Skulls of burrowing snakes are secondarily compacted. Two major sister clades of snakes are Scolecophidia (blindsnakes in the families Leptotyphlopidae, Typhlopidae, and Anomalepididae) and Alethinophidia (all others). Blindsnakes have solid, blunt, and nearly toothless skulls. Considerable variation exists in scolecophidian skulls. Leptotyphlopids manipulate and transport prey with their mandibles (lower jaw), whereas typhlopids and, presumably, anomalepidids rake prey into their mouths with teeth in the upper jaw by rapidly protracting and retracting their maxillae. Mouths of other snakes (Alethinophidia) are filled with dozens of sharp recurved teeth arrayed along several different bones. Snake maxillae vary widely and are movable: hollow hypodermic fangs attached to these bones in viperids swing through almost a full 90° from the folded back, closed-mouth position to the fully erect, stabbing position.

To understand the origin of snakes, one must examine snakelike lizards. Burrowing lizards have small appendages or no limbs at all. They also have no external ear openings, and their eyes often are capped over with a clear spectacle. Ancestral snakes probably were fossorial. Snake eyes have been rebuilt after degenerating during an extensive subterranean existence. All other tetrapods focus by changing the lens curvature using muscles within the eye, but snakes have no such muscles and focus instead by moving the lens back and forth with another set of muscles in the iris.

A rare autarchoglossan lizard from Borneo known as the earless monitor (Lanthanotus) has been identified as a likely candidate for the position of sister group to snakes. Lanthanotus are cylindrical, long-tailed lizards with long necks and short legs. Like snakes, they have a hinge in the lower jaw and no external ear opening. They have forked tongues and tails that do not regenerate, and they shed their skins in one piece, just like snakes. Lanthanotus is the only anguimorphan lizard with a clear brille in the lower eyelid, which could be a precursor to the spectacle of snakes. Other snakelike traits of Lanthanotus include a solidly encased brain, loss of the upper temporal arch, and teeth on the palatine and pterygoid bones.

If snake ancestors were subterranean, ancestors of snakes were the most successful among many scleroglossans that experimented with fossoriality. Considering the many times limblessness has arisen in autarchoglossans, why did evolution of limblessness in varanoids set off such an extensive adaptive radiation as that seen in snakes? Varanoid lizards share a combination of characteristics that opened up a unique opportunity for them, compared with other subterranean lizards. Possession of a forked tongue allowed for keen chemosensory discrimination of prey and detection of airborne chemical signals as well as the ability to follow chemical trails by using the deeply forked tongue as an edge detector. Because fossorial lizards tend to be relatively small, a fossorial varanoid (ancestral snake) would probably be small as well. A fossorial varanoid encountering termites could determine what they were and feed on them, and it could trace their chemical trail back to the colony. Other fossorial autarchoglossans might be able to identify termites, but the lack of forked tongues would inhibit their ability to trace prey to the nest.

Evolution of a body small enough to allow movement through termite passageways, along with a correspondingly small head, would permit access to a rich food resource base. Extreme elongation of the trunk is restricted primarily to subterranean autarchoglossans, but none has taken it to the extremes that snakes did. Limbless or nearly limbless terrestrial scleroglossans (Ophisaurus and pygopodids) have relatively truncated bodies compared with most snakes. Locomotion through existing passageways would favor a concertina-like movement, which in turn would select for longer bodies (as opposed to longer tails) in these snake ancestors. This set of traits describes fairly accurately the three primitive snake families Typhlopidae, Leptotyphlopidae, and Anomalepididae. Elongation of the body most likely preadapted these reptiles for a return to the surface, where a banquet of large vertebrate prey (amphibians, lizards, birds, and mammals) had diversified. Once on the surface, these snake ancestors underwent selection for increased ability to ingest large prey and evolved larger body sizes. They also evolved a loose mandibular symphysis, which allows the two lower jawbones to spread apart, facilitating ingestion of large prey.

Two evolutionary innovations contributed to the success of snakes above ground, efficient locomotion and their highly derived feeding mechanism. An elongated and very flexible body provides much more trunk control over locomotion. Limbed tetrapods expend considerable energy working against gravity to move their own body mass up and down with each step. Across lizard species, the net cost of locomotion (per gram) decreases linearly with increased body mass. The energetic cost of snake locomotion is much more variable. Snakes using concertina locomotion expend more energy than similarly sized lizards, whereas others, who use sidewinding locomotion, expend much less. Snakes can move quite rapidly, and, using an S-shaped loop in the neck, they can strike quickly to capture prey. After returning to the surface, not only could snakes eat large prey relative to their body and head diameter, they also could move their highly flexible bodies around in a manner that few elongated lizards could. Any crevice, hole, or passageway into which they could get their heads was accessible. Increased numbers of vertebrae and associated musculature facilitated swimming, climbing, and other types of locomotion that were either poorly developed or nonexistent in lizards: rectilinear, concertina, sidewinding, and lateral undulation.

Size

Snakes and lizards vary widely in size, from diminutive to gigantic. The smallest lizards, such as the Australian skink Menetia, are among the smallest of terrestrial vertebrates. Neonates have a snout-vent length of only 0.4 in (10 mm) and weigh less than 0.0035 oz (0.1 g), and adults have a snout-vent length of 1 in (25 mm) and a weight of 0.01 oz (0.3 g). Contrast these tiny skinks with Komodo dragons (Varanus komodoensis), at 5 ft (1.5 m) in snout-vent length with a weight of up to 154 lb (70 kg). The largest living squamate is the South American green anaconda (Eunectes murinus), with a snout-vent length of over 30 ft (10 m) and a weight of more than 330 lb (150 kg). Reticulated pythons are almost as large but not as massive. Both constrictors kill and swallow extremely large prey.

General body form

The ancestral condition was that of a tetrapod with four limbs, each with five toes. Reduced limbs and leglessness have arisen repeatedly among squamates, especially in skinks. Except for some pythons and boas, which possess rudimentary vestigial remnants of hind limbs, all snakes are completely limbless. Elongation of the body or tail generally accompanies limb reduction, as it facilitates locomotion without limbs.

Fossoriality has arisen independently many times among scleroglossans. Chemosensory abilities and narrowing of the skull through loss of the temporal arches preadapted scleroglossan clades to burrowing. Chemoreception allowed them to find and pursue prey underground and also to eliminate potentially noxious prey from their diets, opening up yet another adaptive zone. Ultimately, species in nine scleroglossan families (Pygopodidae, Scincidae, Dibamidae, Amphisbaenidae, Trogonophidae, Rhineuridae, Bipedidae, Gymnopthalmidae,

and Anguidae), and snakes in several families, took maximum advantage of a new underground world. Scleroglossans with strikingly similar body plans swim through sand, burrow in tropical soils, and haunt the nests of social insects.

Coloration

Lizards come in a wide variety of colors, including red, orange, yellow, green, blue, indigo, and violet. Most match the color of substrates on which they live, offering camouflage, which confers some degree of protection from predators. Snakes are equally colorful, with some, such as coral snakes (Micrurus), being warningly colored with bright bands of red, yellow, and black.

Distribution

Snakes and lizards are found everywhere in the world, except at very high latitudes, on cold mountaintops, and in the Arctic and Antarctic. At high latitudes and elevations, temperature becomes a limiting factor for animals that rely on external heat sources (ectotherms). Nevertheless, many lizards and snakes have evolved adaptations, such as viviparity (bearing live young), that facilitate living in cold environments.

Biogeography

Throughout the world, most lizard assemblages contain mixtures of iguanians, gekkotans, and autarchoglossans. More diverse squamate faunas tend to have proportionately greater numbers of species of autarchoglossans, whereas less diverse faunas have relatively more iguanians. In assemblages with a substantial number of autarchoglossans, most of the iguanian and gekkotan fauna is arboreal, saxicolous (lives among rocks), nocturnal, or active in the shade. In contrast, where squamate assemblages lack or have few autarchoglossans, such as in North American deserts and high-elevation habitats in South America, iguanians occupy many microhabitats held by autarchoglossans in mixed assemblages elsewhere. Iguanians and gekkotans probably have been displaced by autarchoglossans throughout their evolutionary history, explaining much of their current ecological and geographical distribution. At the same time, the set of traits that provides autarchoglossans with a competitive advantage throughout the world may constrain their ability to persist in the environments and microhabitats dominated by iguanians and gekkotans.

Gekkotan and autarchoglossan lizards are more species rich in the Old World (30% and 51–52%, respectively) than in the New World (16–19% and 31–33%, respectively). Iguanians display the opposite pattern, with considerably fewer species in the Old World (18–19%) than in the New World (49–51%). In the New World, Amazonia and Venezuela have high percentages of autarchoglossans (mostly teiids and gymnophthalmids) and a low percentage of iguanians. Iguanians outnumber scleroglossans in the Caribbean and Central America, and they dominate in Argentina, where there is little scleroglossan diversity, probably because warm seasons are too short to maintain rich autarchoglossan faunas. In the Old World, autarchoglossans are somewhat impoverished in Madagascar, where iguanians and gekkotans are relatively diverse. In South Africa cordylids have reverted to sit-and-wait foraging, possibly owing to a lack of other diurnal sit-and-wait ambush foragers (e.g., agamids) and competition with other actively foraging lizards (scincids, gerrhosaurids, and varanids). Regional trends are even more pronounced at a local level when lizards from particular study sites are considered. Iguania constitute 74% of the saurofauna at twelve New World desert study sites in the Great Basin, Mojave, and Sonoran deserts, but only 8% and 18% at Old World desert study sites in Africa and Australia, respectively.

Habitat

Most natural habitats, including tropical and subtropical islands, support a diversity of squamates. Squamates are terrestrial, arboreal, fossorial, saxicolous, aquatic (both freshwater and marine), diurnal, crepuscular (active at twilight), and nocturnal. They live in deserts, grasslands, chaparral, thornscrub, savannas, forests, and rainforests. Their body plans and lifestyles predispose them to being especially diverse in open, warm, semiarid areas.

Behavior

The shift in feeding behavior from catching prey with the tongue to jaw prehension had numerous ramifications, ultimately leading to the scleroglossan suite of innovations: enhanced chemosensory ability, active foraging, high active body temperatures, selection of high-payoff food, an enhanced ability to find hidden and sedentary prey, and an improved capacity to capture agile prey. As sit-and-wait ambush foragers, iguanians find mobile prey visually. High numbers of ants, insect larvae, grasshoppers, spiders, beetles, and other hymenopterans in their diets suggest that they sample somewhat randomly among arthropods in their immediate microenvironments. Dietary specialization on ants has occurred several times among iguanians, and, in a few cases, entire clades were generated. For example, all species of horned lizards in the North American iguanian genus Phrynosoma are ant specialists, suggesting that ant specialization evolved early in the evolutionary history of this clade and was carried through to all present day descendants.

Many insect larvae, eusocial termites, and other nonmobile arthropods escaped detection by iguanians but could not evade scleroglossans. Access to these resources allowed explosive diversification within the Scleroglossa. In contrast to iguanians, scleroglossans are active foragers (with a few exceptions) with keen chemosensory systems that can add nonmobile prey to their diets. Use of chemical cues by scleroglossans to discriminate prey also facilitates avoidance of noxious prey items. Dietary differences between Iguania and Scleroglossa are subtle, but some abundant prey (ants, other hymenopterans, and beetles) eaten by iguanians are underrepresented in scleroglossan diets. These prey often contain noxious chemicals (particularly alkaloids) and may be discriminated against based on chemical signals detectable by scleroglossans but not by most iguanians. Because alkaloids are metabolic toxins, avoidance of them may have opened up new metabolic opportunities for scleroglossans, allowing for higher activity levels as well as prolonged activity at high body temperatures.

Just as iguanians took lingual feeding to its logical end point, autarchoglossans took jaw prehension and chemoreception to their logical extremes in varanid lizards and snakes. Having evolved superior chemosensory abilities, autarchoglossans became fierce competitors and awesome predators of their more primitive relatives, iguanians and gekkotans. Many gekkotans escaped from autarchoglossans and other diurnal predators by becoming nocturnal. Switching to a nighttime existence, geckos found an unexploited virtual cornucopia of nocturnal insects, such as crickets, moths, and spiders. To avoid autarchoglossans, iguanians became arboreal, shifted to shady microhabitats, or moved up into colder habitats at higher elevations. Some became herbivorous and evolved large body size (iguanines and leiolepidines).

Herbivory evolved several times within Iguania, producing the subfamilies Iguaninae and Liolaeminae within Iguanidae and the subfamily Leiolepidinae within Agamidae. Most of these herbivores are larger in body size compared with their carnivorous relatives. Herbivory either released these iguanians from body size constraints associated with reliance on arthropod prey or drove the evolution of large body size, perhaps as an antipredator tactic—these are the largest iguanians. These herbivorous lizards shifted their foraging behavior, becoming grazers, and enhanced their chemosensory abilities, using the tongue-vomeronasal system to detect chemical signals. Numerous other correlates of herbivory developed, including an enlarged fermentation chamber in the gut and use of microorganisms for digestion of cellulose.

Other iguanians diversified, maintaining rudimentary vomerolfaction, relatively small size, crypsis, sit-and-wait foraging, and relatively low activity levels while subsisting on a wide variety of arthropods. Most insectivorous iguanians eat some ants, and ant specialization has occurred several times. Herbivory also has evolved several times within Scleroglossa, with similar results. Avoidance of plants containing noxious chemicals could have been a driving force behind evolution of chemosensory food discrimination in these lizards. Remaining scleroglossans were dominated by carnivorous, actively foraging clades, although numerous evolutionary reversals took place. Cordylids and some snakes, for example, armed with the scleroglossan arsenal of innovations, reverted to ambush foraging. Evolutionary reversals in diet and foraging modes occurred in cordylids and xenosaurids, along with the associated loss of ability to discriminate prey chemically. Such reversion back to sit-and-wait ambush foraging demonstrates the attractiveness of low-energy requirements and camouflage offered by the iguanian lifestyle.

Like their ancestors, snakes rely heavily on chemosensory cues to locate prey. Not all snakes are active foragers, however; boas, pythons, and vipers have reverted to the iguanian sit-and-wait mode of ambush foraging but armed with a keen chemosensory ability. Two snake subfamilies have evolved infrared receptors ("pits") wired to the optical receptor region of their brains, allowing them virtually to "see" endothermic prey in the dark. Similarly to other snakes, these predatory snakes exploit their sophisticated vomeronasal chemosensory system to locate scent trails and find ideal sites for ambush attacks.

Many snakes are larger than most lizards, and many are dietary specialists. Most eat various vertebrate prey, including fishes, amphibians, lizards, birds, mammals, and even other snakes. Like most lizards, a few snakes consume arthropods, including ants, termites, spiders, centipedes, and scorpions. Some snakes have specialized in other invertebrates, such as earthworms, slugs, and snails. Snake skull morphologic characteristics and dentitions have evolved along many different pathways, each presumably adapting its bearer to efficient exploitation of its own particular prey. Diets of various species of snakes are restricted to amphibian and reptilian eggs, avian eggs, snails, frogs, toads, lizards, other snakes, birds, and mammals. Many snakes will not eat anything outside their own particular prey category. As examples, hognosed snakes (Heterodon) eat only toads, mussuranas (Clelia) eat mostly other snakes, and several snake species (Liophidium, Scaphiodontophis, and Sibynophis) feed almost exclusively on scincid lizards.

Skinks have bony plates called osteoderms embedded within their scales, which overlap in the manner of shingles on a roof, providing a sort of armor. Most have smooth scales and are difficult to grasp and hold on to, especially when they are squirming. Nevertheless, some species of snakes have specialized in skinks as prey items. Several of these skink specialists have evolved hinged teeth that fold back when they encounter an osteoderm but ratchet upright between scales, offering a firm purchase. One clade of gekkotan lizards, Pygopodidae, has converged on the limbless snake body plan. Pygopodids are known as flap-footed lizards because they have no forelimbs and greatly reduced hind limbs. Two species in one genus of pygopodids, Lialis, feed largely on skinks and have independently evolved hinged teeth.

Many snakes kill their prey by constriction, which requires short vertebrae; heavy, supple bodies; and slow movements. Very fast snakes, such as cobras and racers, have elongated vertebrae with musculature extending considerable distances between vertebrae; such snakes are slender and not as supple and seldom can constrict their prey. Another potent solution

to prey capture, used by about 20% of snakes (the inspiration for the hypodermic needle), is envenomation, which has evolved repeatedly among snakes. Some snake venoms are actually powerful protein enzymes, which begin digesting a prey item even before the snake swallows it. Injecting venom into a large and potentially dangerous prey and then releasing it to run away and die elsewhere protects a snake from being injured by its prey. Using their keen vomeronasal sensory systems, snakes can follow the trail left by the departing envenomated prey with considerable accuracy to find the dead and partially digested food item. Snakes, monitor lizards, and large teiids use their hydrostatic, long, forked tongues as edge detectors to follow scent trails.

Rear-fanged snakes (opistoglyphs) are thought to have a primitive condition—their fangs are too far back in their mouths for efficient delivery of venom. Such snakes have to chew to inject venom. The family Elapidae, which includes coral snakes and cobras, has permanently erect short fangs (proteroglyph) in the front of the mouth; they also must chew to inject venom. Vipers and pitvipers have by far the most efficient means of injecting venom deep into their prey. They have long, hollow front fangs attached to the maxillary bone, which hinges backward when a snake closes its mouth but swings forward as the mouth is opened. Fangs in such solenoglyph snakes swing through an arc of 90° from the resting position to the fully erect stabbing position. With use, fangs fall out and are ingested while embedded in prey items, but they are replaced quickly. (A venomous solenoglyph snake has a set of replacement fangs in the roof of its mouth.)

Reproductive biology

The ancestral condition was egg laying, but live bearing has arisen repeatedly among squamates in at least nine different families of lizards as well as among many snakes—many times within some genera. Nearly 20% of all lizard species are viviparous, representing at least 56 independent origins. At least 35 additional origins exist among snakes. In a few species, some populations are oviparous, and others are viviparous. Viviparity arises via egg retention. A female that can "hold" her eggs can bask, warming them and enhancing development as well as protecting them from nest predators. Live bearing and egg retention have allowed squamates to invade cooler regions and to live at higher elevations and higher latitudes. Live bearing allowed transcontinental migrations of some squamates across cold, high-latitude land bridges. Examples include New World natricine snakes and Boinae, among others. Several oviparous squamates (some anguids, skinks, and a few snakes) "guard" or attend nests, protecting developing eggs; a few, including skinks in the genus Eumeces and snakes in the subfamily Pythoninae, enhance development by providing water or heat to developing eggs.

Within Iguania, viviparity clearly arose in connection with invasion of cold habitats. Iguanian eggs simply are held in the oviducts until they hatch and neonates are laid or extruded (ovoviviparity). The most complex known squamate placenta is found in the South American skink, Mabuya heathi. Within scleroglossans, viviparity has not arisen in teiids, varanids, or helodermatids, and it occurs in only one species of lacertid. An ability to seek out good nest sites, thereby increasing juvenile survivorship, could be an alternative to viviparity. Carrying offspring for long periods of time, as is necessary in viviparous species, probably increases predation risk to females, because gravid females burdened with embryos cannot run as fast or escape as well. Nearly all cordylids are viviparous, as are many anguids and skinks. Cordylids as a group are ecologically more similar to iguanians than to other autarchoglossans, and evolution of viviparity may reflect a long history of high levels of predation or predictable predation on nests of their ancestors, likely from other autarchoglossans. Complex placentas, as seen in some skinks and all xantusiids, do not occur within Iguania.

Because iguanians rely on crypsis to evade predators, filling their body cavity with eggs does not negatively affect detectability; hence, many iguanians, such as ctenosaurs and horned lizards, produce massive clutches and are extremely fecund. At the low end of relative clutch mass are those of anoles, unusual iguanians that lay a single egg at one time but produce many clutches. The single evolutionary event that resulted in the small and genetically fixed clutch size of the more than 300 Anolis species may have been related to arboreality. Alternatively, high numbers of deaths in the nest could have driven small clutch sizes, providing an advantage to individuals that distributed their eggs in time and space (bet hedging). Nevertheless, production of a single egg does not interfere with crypsis provided by the elongated, twiglike morphologic features of Anolis. For unknown reasons, probably historical, all members of the clade Gekkota have a fixed clutch size of one or two. This, too, may reflect evolution of smaller clutch size associated with mass-related maneuverability on vertical surfaces in a gekkotan ancestor. As a consequence of their more active lifestyle, autarchoglossans typically are streamlined; there are no horned lizard counterparts, although some cordylids that have reverted to ambush foraging approach a spiny tanklike body form. As a consequence, relative clutch mass is constrained and usually smaller, on average, than in non-Anolis iguanians.

Reduced clutch volume in scleroglossans and its attendant reproductive consequence (lower investment per reproductive episode) might at first glance appear to be costly. Iguanians and autarchoglossans use space in fundamentally different ways. Iguanians are territorial and live most of their lives in a relatively small area. Clutches usually are deposited within their territories or nearby; thus, nest site selection is limited by iguanian behavior. Moreover, chemical cues play a minor role in nest selection, because most iguanian species have poorly developed vomerolfaction systems. In contrast, most autarchoglossans are not constrained in their use of space by terrioriality, and they have well-developed chemosensory systems. Using their superior vomerolfactory abilities, they can seek out and choose the best possible nest sites. Many teiid nests in exposed sandy areas along streams and skink (Eumeces) nests in rotting logs are examples. Both Tupinambis and Varanus deposit clutches in termite nests, which provide heat, humidity, and protection. A survey of squamates using social-insect nests for egg-deposition sites found no iguanians; however, scleroglossans in five lizard families and three snake families use them regularly. Among iguanians, communal nesting occurs in a few iguanines, an herbivorous clade with well-developed chemosensory abilities, and a few species in which limited nest sites appear to be the foci of territories. Thus, scleroglossans could have an advantage in nest site selection that offsets any cost resulting from reduced clutch volume.

Because of dramatic differences in the use of space between iguanians (territorial) and scleroglossans, particularly autarchoglossans (nonterritorial and free ranging), social systems are drastically different. Iguanians typically have polygynous mating systems centered on defendable resources in which social signals are visual. Autarchoglossans typically have polygynous mating systems centered on sequential female defense in which a combination of visual and chemical cues predominate as social signals. A few have monogamous mating systems. Among cordylids that have reverted to ambush foraging and territoriality, the social system has also switched to resource defense polygyny.

Parthenogenesis (reproduction without fertilization) has evolved many times among lizards and in at least one snake. In such all-female unisexual "species," a female lays eggs that develop into exact genetic clones of herself. Many such parthenoforms have arisen via hybridization of sexual parental species. Because no energy is invested in making males, parthenogenetic forms have a much faster rate of increase than do sexual species. Without sexual reproduction, however, they cannot evolve. If heterozygosity itself confers fitness, asexual reproduction maintains existing heterozygosity (acquired in hybridization), whereas in sexual reproduction recombination will disrupt heterozygosity.

Conservation status

Squamate reptiles have suffered substantial habitat loss due to the extensive encroachment of humans into almost all natural biomes. Some species of lizards and snakes have been negatively affected much more severely than others. Many species that live on islands, such as those in the Caribbean, Southeast Asia, and Madagascar, are now endangered, often because humans have introduced competitors such as goats or predators that include rats, cats, dogs, and mongoose. Some species of endemic Caribbean land iguanas (genus Cyclura) are perilously close to extinction. Other species, such as those that dwell in extensive desert regions, have been more fortunate because humans have not yet been able to turn arid areas into green fields of crops. However, flat-tailed horned lizards (Phrynosoma mcalli) and fringe-toed lizards (Uma inornata) in the U.S. Southwest are threatened by habitat fragmentation and loss due to development. Biodiversity in tropical regions is high, but humans are rapidly destroying rainforests and other tropical habitats. Some species of Mexican cloud forest anguid lizards (Abronia) may well have gone extinct before they were ever collected or described.

Resources

Books

Arnold, E. N. "Cranial Kinesis in Lizards: Variations, Uses, and Origins." Vol. 30, Evolutionary Biology, edited by Max K. Hecht, Ross J. MacIntyre, and Michael T. Clegg. New York: Plenum Press, 1998.

Estes, R. "The Fossil Record and Early Distribution of Lizards." In Advances in Herpetology and Evolutionary Biology, edited by G. J. Rhodin and K. Miyata. Cambridge: Museum of Comparative Zoology, Harvard University, 1983.

Estes, R., K. de Queiroz, and J. Gauthier. "Phylogenetic Relationships Within Squamata." In Phylogenetic Relationships of the Lizard Families, edited by R. Estes and G. Pregill. Stanford, CA: Stanford University Press, 1988.

Greene, Harry W. Snakes: The Evolution of Mystery in Nature. Berkeley: University of California Press, 1997.

Pianka, E. R. Ecology and Natural History of Desert Lizards: Analyses of the Ecological Niche and Community Structure. Princeton, NJ: Princeton University Press, 1986.

Pianka, E. R., and L. J. Vitt. Lizards: Windows to the Evolution of Diversity. Berkeley: University of California Press, 2003.

Schwenk, K. "Feeding in Lepidosaurs. In Feeding: Form, Function, and Evolution in Tetrapod Vertebrates, edited by K. Schwenk. San Diego: Academic Press, 2000.

Zug, George R., Laurie J. Vitt, and Janalee P. Caldwell. Herpetology: An Introductory Biology of Amphibians and Reptiles. 2nd edition. San Diego: Academic Press, 2001.

Periodicals

Autumn, K., Y. A. Liang, S. T. Hsieh, W. Zesch, W. P. Chan, T. W. Kenny, R. Fearing, and R. J. Full. "Adhesive Force of a Single Gecko Foot-Hair." Nature 405 (2000): 681–685.

Gans, C. "The Feeding Mechanism of Snakes and Its Possible Evolution." American Zoologist 1 (1961): 217–227.

Huey, R. B. "Egg Retention in Some High Altitude Anolis Lizards." Copeia 1977 (1977): 373–375.

Huey, R. B., and E. R. Pianka. "Ecological Consequences of Foraging Mode." Ecology 62 (1981): 991–999.

Huey, R. B., and M. Slatkin. "Cost and Benefits of Lizard Thermoregulation." Quarterly Review of Biology 51 (1976): 363–384.

McDowell, S., and C. Bogert. "The Systematic Position of Lanthanotus and the Affinities of the Anguimorphan Lizards." Bulletin of the American Museum of Natural History 105, no. 1 (1954): 1–142.

Patchell, F. C., and R. Shine. "Feeding Mechanisms in Pygopodid Lizards: How Can Lialis Swallow Such Large Prey?" Journal of Herpetology 20 (1986): 59–64.

Savitsky, A. H. "Hinged Teeth in Snakes: An Adaptation for Swallowing Hard-Bodied Prey." Science 212 (1981): 346–349.

Schwenk, K. "Why Snakes Have Forked Tongues." Science 263 (1994): 1573–1577.

Smith, K. K. "Mechanical Significance of Streptostyly in Lizards." Nature 283 (1980): 778–779.

Eric R. Pianka, PhD