26 Resolving Reptile Relationships Molecular and Morphological Markers

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Michael S. Y. Lee

Tod W. Reeder

Joseph B. Slowinski

Robin Lawson

451

What, If Anything, Is a Reptile?

Although the origin of tetrapods is often synonymized with

the radiation of vertebrates into terrestrial habitats, most early

tetrapods and many extant representatives (“amphibians”)

remained partly aquatic. They possessed permeable skin and

(primitively) a breeding biology requiring free water, with

external fertilization and aquatic eggs hatching into gilled

larvae. Many tetrapod lineages (including some living amphibians)

partly circumvented this dependence on water by

acquiring internal fertilization and direct development. However,

only one lineage, Amniota, evolved additional adaptations

permitting full terrestriality, including a waterproof

epidermis and the amniotic egg (Sumida and Martin 1997).

The amniotic egg is one of the most significant vertebrate

innovations, consisting of a tough eggshell, outer and inner

protective membranes (chorion and amnion), a yolk sac for

nourishing the developing embryo, and an allantois for storage

of waste products and respiration. It allows the embryo

to develop terrestrially in its own private “pond,” bypassing

the aquatic larval stage and hatching into a fully formed neonate.

Amphibian-grade tetrapods breathe through their permeable

skin, supplemented by rather inefficient buccal

(throat-based) lung ventilation. The evolution of highly efficient

costal (rib-based) lung ventilation has been proposed

to be another critical amniote innovation, permitting them

to abandon cutaneous respiration and thus waterproof their

skin (Janis and Keller 2001).

Reptiles (Reptilia) are a subgroup of amniotes. However,

exactly which amniotes have been termed “reptiles” has been

in a state of flux. Historically (e.g., Romer 1966), Amniota

has been divided “horizontally,” by separating two advanced

clades (birds and mammals) possessing endothermy and

fluffy, insulatory body covering (feathers or hair). The leftovers,

mostly ectothermic and scaly skinned, were termed

“reptiles.” This old definition of Reptilia included living forms

such as turtles, tuataras, squamates (lizards and snakes), and

crocodiles, as well as extinct forms such as plesiosaurs, “mammal-

like reptiles” (pelycosaurs, therapsids), dinosaurs, and

pterosaurs. Thus, as defined, reptiles excluded birds (even

though these are closely related to crocodiles and dinosaurs),

but included “mammal-like reptiles” (even though these are

more closely related to mammals than to other reptiles).

Furthermore, it has recently been discovered that many extinct

groups traditionally included in reptiles, such as pterosaurs,

advanced therapsids, and theropod dinosaurs,

possessed insulatory integuments and (probably) high metabolic

rates (similar to mammals and birds), which makes their

inclusion in the traditionally defined Reptilia problematic.

Thus, the old concept of Reptilia grouped together a heterogeneous

assortment of primitive amniotes that were neither

closely related nor even very similar to each other.

With the advent of modern systematic practices advocating

classification according to phylogenetic relationships

rather than vague notions of evolutionary “advancement”

(e.g., Hennig 1966), this arrangement was increasingly seen

452 The Relationships of Animals: Deuterostomes

as unsatisfactory. Therefore, the term Reptilia has recently

been redefined by biologists to refer to a cohesive, monophyletic

group (clade) of amniotes (e.g., Gauthier et al. 1988). The

redefined Reptilia now include birds but excludes the “mammal-

like reptiles,” which have been transferred to Synapsida,

the clade consisting of mammals and their extinct relatives

(fig. 26.1). This rearrangement means that Amniota is now

divided according to ancestry into its two principal lineages,

Synapsida (mammals and their fossil relatives) and the newly

reconstituted Reptilia (turtles, tuataras, squamates, crocodilians,

birds, and their fossil relatives). The earliest amniotes

can already be assigned to either the synapsid or reptile

branch, indicating that this dichotomy occurred during the

earliest phases of amniote evolution (Reisz 1997).

This newer interpretation of Reptilia is increasingly being

adopted by the general community, partly because of

the recent evidence that birds are directly descended from

dinosaurian reptiles, and is the one used here. Thus, as presently

understood, reptiles consist of three major living lineages

(figs. 26.1, 26.2): lepidosaurs (lizards, snakes, and

tuataras), archosaurs (crocodilians and birds), and testudines

(turtles). Reptiles also have an excellent stratigraphic

record, with many important groups known exclusively

from fossils (fig. 26.1). In addition to the terrestrial adaptations

found in all amniotes (discussed above), reptiles

possess high levels of skin keratin, the ability to conserve

water by excreting uric acid, and novel eye structures

(Gauthier et al. 1988).

Figure 26.1. Relationships and temporal duration of the major groups of amniote vertebrates. The

thick lines depict the known fossil duration for each group, excluding contentious finds (e.g., the

Triassic “bird” Protoavis and the Cenozoic “therapsid” Chronoperates); black lines denote surviving

groups; gray lines denote totally extinct groups. Dashed lines indicate uncertain relationships.

Examples from each lineage are illustrated. The skull diagrams show the three major skull types

found in amniotes: synapsid (found in synapsids), diapsid (found in diapsid reptiles), and anapsid

(found in turtles, parareptiles, captorhinids and protorothyridids). Note that synapsid and diapsid

skulls each characterize discrete lineages but the anapsid skull does not.

Resolving Reptile Relationships 453

Parareptiles and Other Primitive Reptiles

Most early reptiles possessed “anapsid” skulls with a solid

temporal (or cheek) region (fig. 26.1; Williston 1917), the

primitive condition inherited from their amphibian-grade

ancestors. Many, but not all, of these anapsid-skulled reptiles

belong to a lineage termed the Parareptilia (Laurin and

Reisz 1995, Lee 2001). Examples include mesosaurs, procolophonids

and pareiasaurs (fig. 26.1). Mesosaurs have

long been enigmatic, but have recently been shown to have

parareptilian affinities (Modesto 1999). They were small,

aquatic forms with long necks, webbed feet, and narrow

snouts bearing needle-like teeth. They were weak swimmers

presumably incapable of transoceanic crossings, and the

discovery of two closely related species on opposite sides

of the present Atlantic Ocean was early evidence for continental

drift. Procolophonids were the most diverse and

longest surviving parareptiles (unless one considers turtles),

and superficially resembled stout lizards. The latest forms

possessed spiny skulls and molar-like teeth for crushing

hard invertebrates. Pareiasaurs were large (up to 3 m), slowmoving

herbivores with leaf-shaped teeth, heavy and highly

ornamented skulls, and armor plating over their back and

sides.

A few early, anapsid-skulled reptiles do not belong within

the parareptile clade (fig. 26.2). Protorothyridids were tiny,

slender, long-limbed insectivores, whereas captorhinids were

similar, but larger and more robust. Protorothyridids are

among the earliest known reptiles (being found inside petrified

tree hollows that are more than 300 million years old),

and partly on this basis were long assumed to be ancestral to

all other reptiles. However, recent cladistic analyses (Laurin

and Reisz 1995) suggest that protorothyridids are not ancestral

(basal) to all other reptiles, but like captorhinids are close

relatives of the diapsid radiation (lepidosaurs and archosaurs).

Turtles

Turtles (Testudines or Chelonians; ~300 living species) are

among the most distinct vertebrates, exhibiting striking

morphological specializations that involve not just the shell

but also associated modifications of the vertebrae, limbs, and

skull. Although the skull in all turtles is technically anapsid,

with a solid cheek region, the arrangement of bones in this

area is rather different from that of other anapsid-skulled

reptiles. This is consistent with the suggestion that the turtle

skull might be a secondarily “defenestrated” diapsid skull (see

below). Although no turtles have true cheek fenestrae, extensive

emarginations along the posterior and ventral cheek

margins have evolved repeatedly (Gaffney et al. 1991). All

teeth on the jaw margins are lost and replaced by a keratinous

beak (rhamphotheca). The orbits are positioned anteriorly,

resulting in a short facial region and long cheek region.

The turtle shell is a boxlike structure consisting of a dorsal

carapace and a ventral plastron, joined laterally by the

“bridge.” It is open anteriorly for the head and forelimbs, and

posteriorly for the tail and hind limbs. The shell is unique

among tetrapods in incorporating both dermal armor and

internal skeletal elements (e.g., ribs and clavicles), a union

that results when the lateral edges of the developing carapace

ensnare the developing ribs (Gilbert et al. 2001). The

shell is secondarily reduced in certain forms, especially

aquatic taxa such as sea turtles and soft-shelled turtles. The

dorsal vertebrae and ribs of turtles are immobile, being completely

fused to the inside of the carapace, and the body and

tail are shortened to fit within the confines of the shell. The

limb girdles of turtles lie within (rather than outside) the

ribcage, inside the protective shell, and project horizontally

through the anterior and posterior shell openings, resulting

in a low sprawling stance and broad trackway. Except in sea

turtles, the limbs can be retracted into the shell.

Most anatomical studies place turtles within a plexus

of primitive reptiles with anapsid skulls, and thus outside

of other living reptiles (which possess diapsid skulls; see

fig. 26.2A). In particular, turtles are often placed with pareiasaurs

based on features such as a consolidated braincase, a

Figure 26.2. Relationships between extant reptiles based on

anatomical traits (A; e.g., Gauthier et al. 1988) and wellsampled

genes known for tuataras (B; e.g., Hedges and Poling

1999, Raxworthy et al. 2003). Note that although molecular

data have often been suggested to require a reinterpretation of

turtle affinities, it is actually squamates that shift position

between the two trees. The relationships between turtles,

tuataras, crocodiles, and birds remain constant.

454 The Relationships of Animals: Deuterostomes

shortened vertebral column, and the presence of dermal armor

(Lee 1995, 2001; fig. 26.1). However, some other characters,

principally those of the appendicular skeleton, link

turtles with lepidosaurian diapsids (deBraga and Rieppel

1997, Rieppel and Reisz 1999). The phylogenetic relationships

of turtles remain labile because, whereas many primitive

cranial features suggesting a basal position among living

reptiles, almost as many derived appendicular traits align

them with lepidosaurs. Disconcertingly, recent analyses of

mitochondrial and nuclear genes contradict both morphological

hypotheses, instead consistently suggesting that turtles

are related to archosaurian diapsids (e.g., Kumazawa and

Nishida 1999, Hedges and Poling 1999, Janke et al. 2001,

Rest et al. 2003), an arrangement with no anatomical support

(Rieppel 2000). If so, the apparently primitive anapsid

skull of turtles would represent an evolutionary reversal.

Thus, anatomical and molecular trees cannot be reconciled,

and at least one must be wrong.

Widespread adaptive convergence has been invoked to

explain why the anatomical evidence might be misleading

(Hedges and Poling 1999, Janke et al. 2001), and indeed, the

morphological data contain much internal conflict. However,

less consideration has been given to the problems of the

molecular data sets. Most studies are plagued by poor taxon

sampling and many also encounter additional problems

(Zardoya and Meyer 2001) such as base composition bias

[e.g., 18S and 28S ribosomal RNA (rRNA)], short sequences

(e.g., nuclear amino acid residues), inappropriately fast substitution

rates (e.g., mitochondrial genes), and potential

paralogues (nuclear DNA sequences) or pseudogenes (mitochondrial

DNA sequences). The molecular data also

contain internal conflicts (C. J. Raxworthy, A. L. Clarke,

S. Hauswaldt, J. B. Pramuk, L. A. Pugener, and C. A. Sheil,

unpubl. ms.), although the trend that turtles cluster with,

or within, archosaurs is sufficiently strong to warrant consideration

as true phylogenetic signal (Hedges and Poling

1999, Kumazawa and Nishida 1999, Zardoya and Meyer

2001, Rest et al. 2003). However, there are also reasons why

multiple genes could give a (relatively) concordant, but misleading

picture. A recent combined analysis of all available

molecular data (C. J. Raxworthy, A. L. Clarke, S. Hauswaldt,

J. B. Pramuk, L. A. Pugener, and C. A. Sheil, unpubl. ms.),

and an earlier one that only included well-sampled genes

(Hedges and Poling 1999) both resulted in a tree (fig. 26.2B)

that differs from the traditional tree (fig. 26.2A) only in the

basal position of squamates. This shift pushes turtles up the

tree as the sister group of tuataras and archosaurs (or archosaurs

alone, if tuataras are not sampled). So, instead of asking

why turtles are emerging high on the molecular tree, the

question could be rephrased, Why are squamates emerging

as basal? When the question is rephrased as such, an alternative

answer emerges. Recent studies have shown that

nuclear genetic evolution occurs much faster in squamates

than in other reptiles (Hughes and Mouchiroud 2001). Mitochondrial

genetic evolution also appears to have accelerated

in certain squamates such as agamids, chameleons, and

snakes (Kumazawa and Nishida 1999, Rest et al. 2003, T.

Reeder and T. Townsend, unpubl. obs.). Although rates in

mammals have not (to our knowledge) been comprehensively

compared with those in reptiles, mammalian rates do

not appear to be any slower than those of typical reptiles (e.g.,

see Kumazawa and Nishida 1999, Janke et al. 2001), and the

long period between the mammal–reptile divergence and the

radiation of living mammals means that the synapsid clade

will always be on a long branch. The rapid divergence between

squamates and other reptiles, and the long temporal

gap at the base of the mammal clade, means that the longest

branches are those leading to squamates and to the outgroup

(mammals). Long branch attraction could thus artificially

force squamates toward the base of the reptile tree (Lee 2001).

The elevated evolutionary rates throughout the nuclear genome

of most squamates, and the mitochondrial genome of

at least some, could therefore cause multiple genetic data sets

to converge on the same but spurious tree.

The morphological–molecular conflict on turtle origins

(or, more accurately, higher level reptile phylogeny in general)

thus remains unresolved. Combined analyses (Eernisse

and Kluge 1993, Lee 2001, C. J. Raxworthy, A. L. Clarke, S.

Hauswaldt, J. B. Pramuk, L. A. Pugener, and C. A. Sheil,

unpubl. ms.) still place turtles in the traditional position

outside diapsid reptiles (fig. 26.2A). Nevertheless, if turtles

are assumed to be related to archosaurs (as suggested by some

molecular studies), it would be interesting to determine what

fossil reptiles might be the nearest relatives of turtles. This

can be ascertained by performing an analysis of all reptiles

such that living turtles are “forced” to cluster with living

archosaurs to the exclusion of other living reptiles, but all

fossil forms are allowed to “float.” Turtles then group with

extinct herbivorous archosaur relatives called rhynchosaurs,

based on shared features such as toothless, beaklike jaws and

squat bodies (Lee 2001).

Relationships among turtles have been investigated using

morphology alone (Gaffney et al. 1991) or combined with

the mitochondrial gene cyt-b and 12S mitochondrial rRNA

(Shaffer et al. 1997). The combined data set has been reanalyzed

here, and the results are summarized in figure 26.3.

The striking concordance between the morphological and

molecular data sets (Shaffer et al. 1997) is upheld. Most

clades have positive partitioned branch supports from both

morphology and molecules, indicating concordant support

(see Baker and DeSalle 1997, Gatesy et al. 1999). The most

primitive turtles are Proganochelys from the Upper Triassic

(Gaffney 1990) and the australochelids from the Upper Triassic

and Lower Jurassic (Rougier et al. 1995). They are large,

terrestrial herbivores with robust legs and extremely short

digits, superficially similar to large modern land tortoises.

Unlike living turtles, they could not retract their heads into

the shell. Instead, the vulnerable neck region was protected

by loose armor plates in Proganochelys and by an anterior

expansion of the carapace in australochelids (Rougier et al.

Resolving Reptile Relationships 455

1995). Both groups are more primitive than all other turtles

(“casichelydians”) in retaining lacrimal and supratemporal

bones in the skull, a median opening in the palate (interpterygoid

vacuity), separate rather than fused external nostrils,

and a very weakly developed anterior process on the

shoulder girdle. The remaining turtles (which include all living

forms) have the derived condition in all these features

and fall into two large clades, pleurodires and cryptodires

(each diagnosed by a different method of retracting their

head).

Pleurodires (side-necked turtles; ~75 species) retract their

heads by folding their neck laterally. They also have a unique

arrangement of jaw muscles (Gaffney 1975), where the main

jaw closing muscle (adductor mandibulae) passes over a trochlear

(pulley) formed by a bone in the roof of the mouth

(the pterygoid). Fusion of the pelvis with the shell was formerly

thought to be diagnostic of pleurodires, but this feature

might be more widespread (Rougier et al. 1995). All

living pleurodires are “terrapin-like” in morphology and fall

into two lineages, the chelids (47 species) and the pelomedusoids

(26 species). Both are now restricted to freshwater

habitats of the Southern Hemisphere.

Cryptodires (~225 species) retract their heads by folding

the neck in the vertical plane. As in pleurodires, the jaw

muscles pass over a trochlear; however, in cryptodires this is

formed by a lateral expansion of the braincase (Gaffney 1975).

Living cryptodires fall into five major groups (fig. 26.3):

trionychoids, chelydrids, chelonioids, kinosternoids, and

testudinoids. The trionychoids (26 species) are unusual in that

the last dorsal vertebra has been freed from the shell. They

include soft-shelled and pig-nosed turtles, and are all highly

aquatic, predatory freshwater forms. These are fast swimmers

and rely primarily on speed to escape predators. The shell is

reduced and highly streamlined, being very flat and covered

in smooth skin. Chelydrids (snapping turtles; two species) are

highly sedentary freshwater scavengers and ambush predators;

one species lures prey using a wormlike tongue. The chelonioids

(sea turtles and leatherbacks; seven species) are all specialized

marine forms characterized by limbs modified into

flippers. The paddlelike forelimbs are enlarged and used in

underwater flight. The buoyancy afforded by water has allowed

some sea turtles to reach gigantic proportions. Unlike typical

turtles, they partly rely on speed to escape predators and have

reduced the shell and lost the ability to retract the skull and

limbs. Kinosternoids (mud, musk, and tabasco turtles; 27

species) are unusual in having a shell with a ventral hinge that

can close firmly to protect the animal. Finally, the testudinoids

(~162 species) are a highly diverse group that includes most

remaining living turtles, including familiar forms such as

emydids (semi-aquatic to aquatic freshwater sliders) and

testudinids (terrestrial tortoises with robust domed shells and

elephantine limbs). Testudinoids are united mainly by specializations

of the shell (Gaffney and Meylan 1988).

Diapsids (Lepidosaurs and Archosaurs)

Lepidosaurs, archosaurs, and their relatives all have skulls

with two large fenestrae (holes) in each cheek, a condition

termed “diapsid” (fig. 26.1; Osborn 1903). These fenestrae

lighten the skull, and their rims provide insertion areas for

the jaw-closing muscles. In addition, these forms possess a

Figure 26.3. Relationships

between the major groups of

turtles, based on a combined

analysis of morphological and

molecular data (see text and

appendix). The two numbers to

the left of each branch show

bootstrapping frequency and

branch (Bremer) support,

respectively; the two numbers to

the right denote partitioned

branch support (morphology/

mitochondrial genes). + denotes

totally extinct taxon.

456 The Relationships of Animals: Deuterostomes

pair of suborbital fenestrae in the roof of the mouth. These

novel cranial features, and other traits, unite most diapsidskulled

reptiles as a distinct lineage (the Diapsida), to the exclusion

of anapsid-skulled reptiles (fig. 26.1; see Gauthier et al.

1988, Laurin and Reisz 1995, Lee 2001). One possible independent

evolution of the diapsid skull occurs in araeoscelids,

a group of very primitive reptiles. Some (but not all) araeoscelids

have diapsid skulls; a recent study suggests that they

are distantly related to other diapsids, implying convergent

evolution of the diapsid condition (C. J. Raxworthy, A. L.

Clarke, S. Hauswaldt, J. B. Pramuk, L. A. Pugener, and C. A.

Sheil, unpubl. ms.). There might also be at least one striking

loss of the diapsid skull condition: if turtles are truly related

to archosaurs (figs. 26.1, 26.2B), their cheeks are presumably

secondarily closed (but see above). Diapsida split quite

early in its history into two diverse lineages, one (the lepidosauromorphs)

leading to living lepidosaurs, and the other

(the archosauromorphs) leading to living archosaurs

(fig. 26.1; see Gauthier et al. 1988). Most diapsid reptiles,

except some early primitive forms, can be assigned confidently

to one of these two clades.

Lepidosaurs (Tuataras, Lizards, and Snakes)

Lepidosaurs (Lepidosauria) include living forms such as Sphenodon

(tuataras) and squamates (lizards and snakes). Their

monophyly is supported by a transversely (rather than longitudinally)

oriented cloacal slit, a separate (“sexual”) segment

in the kidney, novel features in the eye, and skin containing

a unique type of keratin and that is shed in large pieces

(Gauthier et al. 1988). There is also strong support for

lepidosaur monophyly from well-sampled mitochondrial

genes (e.g., Zardoya and Meyer 2001, Rest et al. 2003). Although

the relatively few nuclear genes so far sequenced for

both squamates and Sphenodon suggest lepidosaur paraphyly,

with squamates basal to all other living reptiles (e.g., Hedges

and Poling 1999), this arrangement might be an artifact of

elevated substitution rates in squamates coupled with inadequate

taxon sampling (see above).

Fossil relatives of living lepidosaurs include the euryapsids,

which are marine reptiles such as the armored placodonts,

long-necked plesiosaurs, and short-necked pliosaurs (fig. 26.1;

Rieppel and Reisz 1999, Mazin 2001). Euryapsids are characterized

by a diapsid skull with an extremely wide cheek

region lacking the lower strut of bone, a condition termed

“euryapsid” (Colbert 1945). The ichthyosaurs, a diverse

radiation of fishlike reptiles, might also be related to

lepidosaurs, although this is debated (Sander 2000). Among

living lepidosaurs, the tuataras (Sphenodon) are the most

primitive (or basal). They superficially resemble slow-moving,

stout iguanas and have unusually slow metabolisms and

life cycles, perhaps adaptations to their harsh cold habitat.

They are famous “living fossils” and today consist of only two

very similar species (only recently distinguished genetically;

Daugherty et al. 1990) restricted to small, rat-free islands off

New Zealand. However, in the past the tuatara clade (rhynchocephalians)

was much more diverse and included a variety

of terrestrial forms as well as elongate marine forms

(Wilkinson and Benton 1996).

Squamates (Lizards and Snakes)

Squamata are a diverse and successful radiation of more than

7000 species of lizards, amphisbaenians, and snakes (Vitt

et al. 2003). Like most ectothermic tetrapods, they are most

diverse and abundant in warmer regions. All squamates share

numerous distinctive evolutionary novelties (Estes and Pregill

1988) such as a reduced cheek region with mobility of the

quadrate bone that suspends the lower jaw (streptostyly), and

a distinct type of vertebral joint (procoely; lost in some geckos).

Male squamates have paired copulatory organs called

hemipenes. Each hemipenis is generally a forked structure

often covered in small spines for anchorage; they are usually

ensheathed within the tail and are normally only everted

during copulation. Squamates are the only reptiles to exhibit

live birth (viviparity). This trait has evolved convergently up

to 100 times within squamates, often in the context of cold

climates (Shine 1989), and, when acquired, is rarely if ever

lost (Lee and Shine 1998).

Several major clades of limbed squamates have long been

recognized (e.g., Camp 1923, Estes and Pregill 1988). However,

interrelationships between these clades, and the affinities

of three highly modified limb-reduced groups (snakes,

amphisbaenians, and dibamids), remain contentious. As a

result, a phylogenetic analysis of squamates was undertaken

combining a large anatomical and behavioral data set (399

characters, see Appendix) with sequences from four genes

(mitochondrial 12S and 16S rRNA, nuclear c-mos and c-myc;

see Appendix). The results are summarized in figure 26.4.

The combined analysis corroborates the monophyly of many

previously recognized groups, such as the lizard “families,” as

well as larger groupings such as Iguania, Iguanidae sensu lato

(= Pleurodonta), Acrodonta, Scleroglossa, Gekkota, Pygopodidae

+ Diplodactylinae, Scincoidea, Lacertoidea, Teioidea,

Anguimorpha, and Varanoidea. Snakes are placed within

anguimorphs. Although many traditional groups are supported,

the basal divergences within Scleroglossa, and the position of

dibamids and amphisbaenians, remain as enigmatic as ever.

Squamata encompasses two major basal clades: Iguania

(1000 living species) and Scleroglossa (~6000 species).

Iguanian lizards are divided into two groups that can be diagnosed

by type of tooth implantation: pleurodont iguanians

(traditionally known as iguanids; ~470 species) and the acrodont

iguanians (consisting of the agamines, leiolepidines

and chamaeleonids; ~535 species). As a group, iguanians are

difficult to diagnose, but they generally have a fleshy dewlap

in the chin region and often have other crests and ornaments

over their skulls and bodies. They also have the ability for

rapid and profound color change, a feature linked to male

Resolving Reptile Relationships 457

territoriality and visual displays, which are more highly developed

in iguanians than in other lizards. Iguanians have

lost one of the body muscles (the intercostalis ventralis); this

simplified trunk musculature might have been a constraint

preventing them from evolving a flexible snakelike morphology.

Most of the (relatively few) herbivorous lizards are

iguanians, a diet perhaps facilitated by their generally large

size. Chameleons are among the most famous and bizarre

lizards, and many of their unusual features are related to their

sit-and-wait predation strategy: the rapid and extensive color

changes (camouflage), grasping digits and prehensile tail (facilitating

a permanent tight grip on branches), independently

movable eyes on turrets, and long projectile tongue (enabling

visual sweeps and prey capture without head movement).

The remaining (non-iguanian) squamates form a group

named Scleroglossa (fig. 26.4), which is corroborated by

distinct morphological novelties (Estes and Pregill 1988),

but has not been supported by molecular data (e.g., Rest

et al. 2003). Scleroglossans mainly use their teeth for capturing

prey, rather than the tongue (as in iguanians), freeing

the tongue for chemoreception (“tasting” the air). As a

result, the tongue contains many scent-detecting cells, and

the chemosensory Jacobson’s organ in the palate is elaborated.

Scleroglossans also have a flexible hinge in the skull

roof, between the frontals and parietals. The hinge appears

to be correlated with a shift of the pineal organ and foramen

posteriorly away from the mobile frontoparietal

boundary (Schwenk 2000). It is notable that the only scleroglossans

with a pineal apparatus on this boundary are certain

mosasauroids, which have secondarily consolidated

this joint.

Gekkotan lizards (geckos and flap-footed lizards; 1050

living species) appear to be a another relatively basal group

of scleroglossans (fig. 26.4). They are usually nocturnal and

accordingly have large and distinctive eyes with slitlike vertical

pupils. In most, the eyelids are fused into a transparent

“spectacle” that is cleaned by licks from a specialized pad

on the tongue (Schwenk 2000). Unlike the vast majority

of squamates, they have a reduced clutch size (usually fixed

at two or one eggs). Most members have enlarged toe pads

that enable them to scale smooth vertical surfaces. All gekkotans

also lack many skull bones found in other squamates,

and many lack well-formed vertebral joints, all probably due

to early cessation of ossification (pedomorphosis). Vocal

communication is highly developed, with some members

having elaborate repertoires similar to those of many frogs.

Accordingly, gekkotans have well-developed larynxes

(“voiceboxes”) and highly sensitive auditory structures. One

lineage of gekkotans, the pygopodids (flap-footed lizards),

has become very snakelike. However, their phylogenetic position

within Gekkota as close relatives of diplodactylines

(Australasian geckos) is strongly supported by both morphology

(Kluge 1987) and mitochondrial and nuclear genes

(fig. 26.4; see also Donnellan et al. 1999).

Figure 26.4. Relationships between the major groups of squamates (lizards, amphisbaenians,

and snakes), based on a combined analysis of morphological and molecular data (see main text

and appendix). The numbers to the left of each branch show bootstrapping frequency and branch

(Bremer) support, respectively; the numbers to the right denote partitioned branch support

(morphology/mitochondrial genes/nuclear genes). + denotes totally extinct taxon.

458 The Relationships of Animals: Deuterostomes

Scincomorph lizards are the most diverse and “typical”

group of lizards, consisting mainly of small-bodied, generalized,

insectivorous forms such as scincids (skinks; ~1260

species), cordylids (girdled lizards and plated lizards; ~85

species), lacertids (wall lizards, sand lizards, etc.; ~275 species),

teiids (tegus, whiptails, etc.; ~117 species), gymnophthalminds

(microteiids; ~190 species), and xantusiids

(night lizards; 16 species). The evidence for scincomorph

monophyly has always been very weak, with most of the features

shared by scincomorphs also being generalized traits

widespread in other lizards. In this analysis (fig. 26.4), there

is strong evidence for three major lineages of scincomorphs,

the scincoids (skinks, cordylids), lacertoids (lacertids, teiids,

gymnophthalmids), and xantusiids. There is no evidence that

these three lineages are each other’s closest relatives, but no

alternative arrangement is strongly supported. Most scincomorphs

are agile, secretive, smallish forms that shelter beneath

leaf litter or loose rocks. This intimate association with

the substrate is most marked in skinks and gymnophthalmids

and has probably facilitated the frequent (>30 times) evolution

within these groups of burrowing habits, limb reduction,

and body elongation (e.g., Greer 1989, Pellegrino et al.

2001).

Anguimorph lizards (180 living species, not counting

snakes) are generally medium to large predators and include

anguids (e.g., galliwasps, glass lizards, slow “worms,” alligator

lizards), Heloderma (the venomous Gila monsters and

beaded lizards), xenosaurids (e.g., crocodile lizards), Varanus

(typical monitors such as the komodo dragon), and Lanthanotus

(earless monitors) All anguimorphs possess a specialized

secretory gland on the lower jaw (gland of Gabe) and

a distinctive pattern of tooth replacement. Many also have

sharp recurved teeth and a distinct zone of flexibility in each

lower jaw (the intramandibular joint; Estes and Pregill1988).

Anguimorphs also have a retractile, deeply forked tongue that

is used to pick up airborne molecules (“scents”) of prey and

other objects (independently evolved in teiid lizards) that are

then transmitted to the vomeronasal organ in the roof of the

mouth. Differences in the intensity of the scent between the

two prongs of the forked tongue allow the direction of

the source to be determined. Although most scleroglossan

lizards use this system, it is most strongly developed in

anguimorphs (Schwenk 2000). All of these traits are related

to feeding on large prey and are also found in snakes, which

are most likely part of the anguimorph radiation. In this

analysis (fig. 26.4), snakes cluster closely with extinct marine

varanoids (mosasaurs and dolichosaurs).

Amphisbaenians (160 living species) are a highly aberrant

group of long-bodied, limb-reduced squamates that

superficially resemble large fat earthworms. They are highly

specialized and efficient burrowers, with extremely solid

skulls for ramming their way through the substrate, and

scales and muscles arranged in rings around the body for

gripping the sides of burrows. They have a novel median

bone (the orbitosphenoid) surrounding the anterior braincase

and have reduced their right lung (other elongate squamates,

including snakes, have reduced the left lung). Their

eyes are among the most degenerate in vertebrates, and they

rely largely on chemical and vibrational cues to locate prey.

Their precise position within Squamata remains unclear, but

the suggestion that they might be linked to the fossil Sineoamphisbaena

is not supported in this study. Morphological

data (Lee 2001) place amphisbaenians with dibamids (another

highly modified limb-reduced group), but the possibility

of pervasive adaptive convergence means this

hypothesis of relationship requires independent corroboration.

The current molecular data neither support nor contradict

this grouping (fig. 26.4).

Snakes

Serpentes (2900 living species) are one of the many lineages

of squamates that has undergone body elongation and limb

reduction. Snakes range from tiny wormlike blindsnakes to

giant constrictors such as boas and pythons, and deadly

mambas, cobras, and sea snakes. Characteristic external features

include eyelids fused into a transparent “spectacle,”

absence of the external eardrum, retractile forked tongue, and

long, limb-reduced bodies. Each of these traits, however, has

evolved independently in certain other squamates (“lizards”),

and the key diagnostic features of snakes are internal

(Underwood 1967, Estes and Pregill 1988, Greene 1997, Lee

and Scanlon 2002). There are usually between 140 and 600

trunk vertebrae (more than in even the most elongate lizards),

and the trunk muscles are highly elaborate, permitting both

great flexibility and precise local control of body movement.

The forelimb and pectoral girdle are totally lost (vestiges remain

in even the most limb-reduced lizards). Snakes are

characterized by extremely loose skulls with highly flexible

upper and lower jaws loosely suspended from a central bony

braincase. The tooth-bearing bones of the upper jaw are all

mobile. The lateral element (the maxilla) is used to capture

prey during the initial strike; later, the palatal elements (palatines

and pterygoid) ratchet the prey into the esophagus

during the swallowing phase. In many snakes, including most

advanced forms, the left and right lower jaws are connected

anteriorly by elastic ligaments and thus can separate to engulf

of huge prey. This mechanism for increasing gape circumvents

the problem that snakes have small heads relative

to body size but swallow large prey whole (Greene 1983).

Even the earliest snakes had extensive adaptations for

predation, and this constraint appears to have prevented

snakes from evolving into omnivores or herbivores. All primitive

snakes (and indeed 80% of all snakes) are aglyphous,

lacking fangs and venom glands. Aglyphous snakes that take

larger prey kill by constriction and continuous bites. However,

several groups of advanced snakes have independently

evolved fangs (enlarged teeth with grooves or canals for injecting

venom) and venom glands (modified salivary glands).

These venomous forms often do not constrict but adopt a

Resolving Reptile Relationships 459

strike-and-release strategy to avoid injury by large struggling

prey. Opisthoglyphous snakes have fixed fangs at the back

of the jaws. This arrangement has evolved repeatedly among

colubrids (e.g., boomslangs). Proteroglyphous snakes have

fixed fangs at the front of the jaws. This arrangement characterizes

elapid snakes (e.g., cobras, sea snakes, coral snakes).

Solenoglyphous snakes have mobile fangs that are only erected

while striking. Because the fangs can be folded away when not

in use, they can be very large. Vipers (e.g., rattlesnakes and

adders) and some enigmatic colubroids (atractaspidids) have

this arrangement.

Although there is widespread agreement that snakes

evolved from lizards, the more precise details remain contentious.

Most recent morphological analyses group snakes

with either small fossorial amphisbaenians and dibamids

(e.g., Rieppel and Zaher 2000), or large predatory anguimorph

lizards (e.g., Lee 2003). The first arrangement is consistent

with the hypothesis that snakes evolved from a lineage

of burrowing lizards, which is further supported by the close

association of burrowing habits with limb reduction in living

lizards, and highly divergent eye structure suggesting that

the eyes of snakes became reduced and then re-elaborated.

The second idea links snakes to marine anguimorphs (mosasaurs

and dolichosaurs) based on features such as a unique

pattern of tooth eruption and increased flexibility of the jaw

joints, and would suggest that snakes evolved in a marine

habitat for eel-like swimming. The combined morphological

and molecular analysis of squamates favors this hypothesis

(fig. 26.4).

The phylogeny of snakes summarized in figure 26.5 is

based on a combined analysis of 263 anatomical and behavioral

traits (Lee and Scanlon 2002) and sequences from four

genes: mitochondrial 12S rRNA, 16S rRNA (Heise et al. 1995),

cyt-b, and nuclear c-mos (Slowinski and Lawson 2002). The

morphological and molecular data, separately and combined,

support some traditionally recognized clades, namely, blindsnakes,

alethinophidians, and colubroids. However, as discussed

below, there are major disagreements regarding the

position of dwarf boas and sunbeam snakes, leading to extensive

character conflict as revealed by some large negative partitioned

branch support (PBS) values.

The limbed marine snakes Pachyrhachis and Haasiophis

emerge as the most basal snakes (fig. 26.5), supporting the

view that their legs, low vertebral count, and cranial similarities

to anguimorph lizards are retained primitive features

(Lee and Scanlon 2002) rather than atavistic reversals

(Tchernov et al. 2000, Rieppel and Zaher 2000). Their marine

habits are thus relevant to the idea of a marine origin of

snakes. The most primitive terrestrial snakes are large superficially

“boalike” forms, Dinilysia and madtsoiids. These are

Figure 26.5. Relationships between the major groups of snakes, based on a combined analysis of

morphological and molecular data (see main text and appendix). The numbers to the left of each

branch show bootstrapping frequency and branch (Bremer) support, respectively; the numbers to

the right denote partitioned branch support (morphology/mitochondrial genes/nuclear genes). +

denotes totally extinct taxon.

460 The Relationships of Animals: Deuterostomes

too massive to burrow actively, an observation inconsistent

with the suggested fossorial origin of snakes. The large (“macrostomatan”)

feeding apparatus of these fossil snakes has been

interpreted as indicating affinities with higher snakes (e.g.,

Rieppel and Zaher 2000); however, the recent molecular

studies that place some macrostomatan snakes as very basal

among living snakes (see below) raise the possibility that the

macrostomatan condition was primitive for snakes as a whole.

If so, the presence of such gape adaptations in early and

apparently basal fossil snakes is no longer problematic.

Among living snakes, the most basal forms are scolecophidians

(blindsnakes): leptotyphlopids (~91 species),

typhlopids (~225 species), and anomalepidids (15 species).

However, they are not primitive by any means, but share a

suite of unique specializations indicating their monophyly,

such as bizarre consolidated skulls with spherical snouts (Lee

and Scanlon 2002). This arrangement is also supported by

molecular data (fig. 26.5). These generally small snakes are

totally fossorial and accordingly have reduced eyes, cylindrical

wormlike bodies, and glossy, dirt-resistant scales. They

gorge themselves on ants and termites using rapid oscillations

of their small, highly modified jaws (Kley and Brainerd

1999).

The remaining snakes, called alethinophidians (fig. 26.5),

are characterized by evolutionary innovations such as a pair

of bones (laterosphenoids) surrounding the anterior braincase,

a median bony wall between the olfactory lobes of the

brain, and the ability to subdue prey by constriction (lost in

some advanced venomous forms). They are usually larger,

have longer jaws, and have more developed eyes than

scolecophidians. The most primitive alethinophidians are

Anilius (red pipesnake; one species), Cylindrophis (Asian

pipesnakes; seven species), Anomochilus (dwarf pipesnakes;

two species) and uropeltids (shield-tail snakes; ~44 species).

These are partly fossorial but also frequent surface or aquatic

habitats. They lack the elaborate gape adaptations of more

advanced snakes and therefore feed mainly on elongate prey

with small cross sections, such as eels, caecilians, and earthworms

(Greene 1983).

More derived alethinophidians, termed macrostomatans,

have further evolutionary innovations to increase gape and

permit a greater range of prey. These include a chin ligament

that allows the left and right jaw rami to separate, longer jaw

elements suspended from enlarged supratemporals, and

looser palatal bones (Cundall and Greene 2000). These innovations,

and molecular data, support their monophyly

(fig. 26.5). They are active above ground for large parts or

all of their lives and possess a row of transversely enlarged

belly scales for more efficient terrestrial locomotion (lost in

some sea snakes). Macrostomatans include most “familiar”

snakes, such as boas and pythons, colubrids, and all venomous

forms.

Xenopeltis and Loxocemus, called sunbeam snakes because

of their iridescent scales, form Xenopeltidae (three species).

They share many features of the snout and scale microstructure

that indicate close relationship, an arrangement supported

by molecular data (fig. 26.5). Morphological analyses

place them as basal to all other macrostomatans (Lee and

Scanlon 2002), and accordingly, they possess relatively weak

development of macrostomatan feeding adaptations (Cundall

and Greene 2000, Slowinski and Lawson 2002). However,

molecular evidence places sunbeam snakes deep within

“true” macrostomatans, as relatives of pythons, implying

secondary reduction of their gape adaptations (e.g., Slowinski

and Lawson 2002, Wilcox et al. 2002, Vidal and Hedges

2002).

Boas (35 species) and pythons (31 species) are typically

large and include the largest living snakes. Many are arboreal,

and can swallow very large, warm-blooded prey (mammals

and birds). Accordingly, many boas and pythons have

heat-sensitive lip organs to detect prey and well-developed

powers of constriction. Erycines (sand boas; 13 species) are

a group of fossorial boas that are generally smaller than typical

boas, with most possessing highly bizarre fused tail vertebrae

that they use as an antipredator defense. Dwarf boas

(tropidophiines, ~20 species; ungaliophiines, three species)

are small, boalike snakes that feed principally on reptiles

and amphibians. Although traditionally classified as a single

group, the two groups of dwarf boas are not close relatives.

Morphological studies still place both tropidophiines and

ungaliophiines high within snakes, although not as sister

groups (Zaher 1994, Lee and Scanlon 2002), but multiple

genes suggest a much more radical position for tropidophiines

as basal alethinophidians (Slowinski and Lawson

2002, Vidal and Hedges 2002, Wilcox et al. 2002). Given that

all other basal alethinophidians are fossorial and gape-limited,

the occurrence of above-ground, macrostomatan forms

in this part of the tree would imply extensive homoplasy of

these traits in early snakes.

Bolyeriines (Round Island boas; two species) are remarkable

in that each upper jaw element (maxilla) is divided into

two moveable halves, an adaptation for gripping slippery prey

such as skinks. One species (Bolyeria) has recently become

extinct; the other (Casarea) is endangered. Morphological

and molecular data agree that these groups are all basal

macrostomatans but disagree about their precise interrelationships.

The phylogeny presented here (fig. 26.5) results

from the combined evidence. The morphological data alone

place sunbeam snakes as the most basal macrostomatans,

followed by a python-boa-erycine clade, with Round Island

and dwarf boas being aligned with advanced snakes (Lee and

Scanlon 2002). However, the molecular data alone group

sunbeam snakes with pythons, whereas sand boas, true boas,

and ungaliophiine dwarf boas form another clade (Slowinski

and Lawson 2002).

File snakes (acrochordids; three species) are highly

aquatic snakes with granular skin and sluggish, limp bodies.

They have huge jaws and can swallow extremely large

fish prey. However, they feed very infrequently and have very

slow metabolisms, perhaps reproducing only once every

Resolving Reptile Relationships 461

decade (Shine and Houston 1993). Because of their bizarre

morphology, and retention of a few apparently primitive features

of the inner ear and lower jaw, they have sometimes

been interpreted as the most basal living snakes, perhaps even

more primitive than blindsnakes. However, these traits are

reversals, because other morphological characters, such as a

unique structure of the snout joint, and loss of the coronoid

bone in the lower jaw, link acrochordids with the most advanced

snakes (colubroids). This grouping (caenophidians)

is also supported by molecular data (fig. 26.5).

Colubroidea (colubroids, ~2300 spp.) are the most rapidly

diversifying and species-rich group of snakes, and have

the dominant snakes on all continents. They are so diverse

that their internal phylogenetic relationships are uncertain,

and it is difficult to make generalizations about their morphology

and biology. They usually possess an extremely

mobile upper jaw, specialized dentitions, and elaborate palatal

mechanisms for ratcheting prey down the throat (Cundall

and Greene 2000). They also share unique elaborations of

the trunk musculature and associated rib cartilages. These

might be related to their ability for more rapid and precise

movement than more primitive snakes, which in turn is correlated

with their tendency to use more open habitats. Two

groups of highly derived, venomous colubroids have long

been recognized: vipers and elapids.

Vipers (Viperidae; ~245 species) are characterized by

solenoglyphy (mobile front fangs). They are generally stoutbodied,

sit-and-wait predators, but some arboreal forms are

more slender. The venom is usually hemotoxic, damaging the

blood circulatory system, muscles, and other tissues and

often producing hideous wounds. Typical forms include

rattlesnakes (Crotalus), adders (Vipera), and copperheads

(Agkistrodon). Elapids (Elapidae; ~250 species) are characterized

by proteroglyphy (fixed front fangs). Most are more slender

and active than vipers, but again, many exceptions exist.

The venom is usually neurotoxic, interfering with the nervous

system. Elapids include the most deadly snakes, and are the

dominant snakes in Australasia. Typical forms include cobras

(Naja), coral snakes (Micrurus), mambas (Dendroaspis), and

taipans (Oxyuranus). Living sea snakes represent two independent

marine invasions by elapids (Slowinski and Keogh 2000,

Scanlon and Lee in press): sea kraits (Laticauda) and true sea

snakes (hydrophiines). All sea snakes accordingly have fixed

front fangs that inject potent neurotoxins. They have laterally

compressed bodies and paddlelike tails to facilitate swimming,

and valves in the nostrils to exclude water. Laticauda periodically

returns to shore to deposit eggs, whereas hydrophiines

are totally marine, bearing live young underwater.

The remaining colubroids are often lumped into a wastebasket

group, the “Colubridae” (~1800 species). Typical

“colubrids” include ratsnakes (Elaphe), racers and whipsnakes

(Coluber), grass snakes (Natrix), and boomslangs (Dispholidus).

They are mainly agylphous (lacking fangs and venom systems),

although a sizable proportion are opisthoglyphous (having

fixed rear fangs). The position of the fangs in the back of the

mouth might make it more difficult for them envenomate large

victims (including humans). However, some opisthoglyphous

colubrids (e.g., boomslangs) have caused many fatalities. The

relationships of “colubrids” with each other and other colubroids

(vipers and elapids) have long been problematic because

of the species diversity of the group. However, they have recently

been partly clarified based on molecular sequences

(Kraus and Brown 1998, Slowinski and Lawson in press).

Vipers are the most basal colubroids, as has been proposed

previously based on anatomical data (Underwood 1967), with

“colubrids” and elapids forming a clade. Elapids are nested

within “colubrids,” being related to certain African forms

such as psammophiines (e.g., sandsnakes), boodontines

(e.g., housesnakes), and atractaspidids (e.g., stiletto snakes).

Such a relationship suggests an African origin for elapids. The

“Colubridae” as currently construed is thus not a true evolutionary

lineage. One solution might be to also include elapids

within Colubridae, thereby restoring colubrid monophyly.

However, given the medical importance of Elapidae, subsuming

them into the (largely harmless) Colubridae might cause

confusion, and an alternative would be to restrict Colubridae

to a apply to a small monophyletic group.

Archosaurs (Crocodiles, Pterosaurs,

Dinosaurs, and Birds)

The archosaurs (Archosauria) include some of the most spectacular

reptiles, such as crocodilians, pterosaurs, dinosaurs,

and birds (fig. 26.6; Brochu 2001b). They are characterized

by numerous anatomical traits (Gauthier et al. 1988) such

as a fully divided ventricle in the heart, special stomach chamber

(gizzard) housing swallowed stones (gastroliths) used to

pulverize food, novel pair of bones (the laterosphenoids)

forming the front of the braincase, system of air sacs within

the skull, and fenestrae in the snout and lower jaw (these

snout fenestrae are secondarily closed in living crocodilians).

Living archosaurs (crocodilians and birds) share behavioral

traits such as nest building, parental care, and vocalizations

(chirping) by nestlings. These habits are difficult to confirm

in fossil archosaurs, but smoothly worn stomach stones have

been found within complete dinosaur skeletons, and fossilized

dinosaurs have recently been found brooding nests of

eggs (Clark et al. 1999). Molecular studies reveal that the

DNA of crocodiles and birds is very similar (e.g., Zardoya and

Meyer 2001, C. J. Raxworthy, A. L. Clarke, S. Hauswaldt,

J. B. Pramuk, L. A. Pugener, and C. A. Sheil, unpubl. ms.).

The large number of advanced morphological, behavioral and

genetic features shared by birds, crocodilians and (where

known) fossil archosaurs reflect their close evolutionary relationship

and justify the current practice of classifying

birds with archosaurian reptiles, rather than the older approach

of separating birds off from all reptiles as separate

groups. The latter approach is further complicated by recent

discoveries of numerous feathered, birdlike dinosaurs

462 The Relationships of Animals: Deuterostomes

that blur the distinction between birds and nonavian reptiles

(see below).

The monophyly of living archosaurs (crocodilians and

birds), to the exclusion of other living reptiles, is strongly supported

by both morphological traits (fig. 26.2A; Gauthier et al.

1988) and molecular sequences (fig. 26.2B; Janke et al. 2001,

C. J. Raxworthy, A. L. Clarke, S. Hauswaldt, J. B. Pramuk,

L. A. Pugener, and C. A. Sheil, unpubl. ms.). Relationships

among extinct archosaurs are also well established (fig. 26.6).

Fossil forms can be assigned to two major lineages, Crurotarsi,

which leads to living crocodiles, and Ornithodira, leading to

living birds (e.g., Gauthier et al. 1988, Sereno 1999b). However,

one important fossil group, the rhynchosaurs, falls outside

both living lineages of archosaurs. Rhynchosaurs were the

dominant herbivores during the Triassic and had stout bodies,

wide, short skulls, and crushing beaks instead of toothed

jaws. If turtles are indeed related to archosaurs, as has been

proposed by some molecular workers, then they might have

affinities with rhynchosaurs (Lee 2001).

The lineage leading to living crocodilians (crurotarsans)

includes heavily armored herbivorous forms such as aetosaurs,

cursorial long-legged forms such as sphenosuchians that actively

chased terrestrial prey, giants amphibious forms such

as Sarcosuchus that were larger than the largest carnivorous

dinosaurs, as well as the ocean-going teleosaurs with flippers

and caudal fins (fig. 26.6; Gauthier et al. 1988, Brochu 2001b,

Sereno et al. 2001).

Living crocodilians (Crocodylia; 24 living species) are all

large, semi-aquatic predators. They are all morphologically

quite uniform, with long snouts, conical piercing teeth, longish

bodies, short but robust limbs, laterally compressed tails,

and leathery skin containing bony plates. There are two major

living lineages, the alligatorids (alligators and caimans) and

crocodylids (crocodiles and the “false gavial”). The relationships

of true gavials have been contentious, with anatomical

evidence suggesting that it represents an independent lineage

lying outside of both alligatorids and crocodylids (Brochu

2001a). However, mitochondrial and nuclear sequences, some

morphological characters such as narrow elongate jaws, and

the combined sequence and morphological data place true

gavials within crocodylids, next to the “false gavial” (fig. 26.6;

Gatesy et al. 2002). All living crocodilians are ambush predators

that (as adults) take sizable vertebrate prey, such as fish,

amphibians, birds, and mammals captured either near or

under water.

The lineage leading to living birds (ornithodirans) includes

pterosaurs, dinosaurs, and some other less known

groups (fig. 26.6; Gauthier 1986, Brochu 2001b). Pterosaurs

were the first vertebrates to evolve powered flight. Their

bones were extremely hollow and light (like those of birds),

and their membranous wings were suspended by a greatly

elongated fourth finger and stiff internal fibers. The shape of

their wings has long been debated, but fossils preserving soft

tissue have revealed that (at least in some taxa) the wing

membrane was wide and stretched between the forelimbs and

hind limbs, resulting in sprawling, clumsy gait. These fossils

have also revealed that pterosaurs were covered in fine, hairlike

structures (Unwin and Bakhurina 1994), and thus might

Figure 26.6. Relationships between the major groups of fossil and living archosauromorphs

(crocodiles, birds, dinosaurs, pterosaurs and their relatives). Relationships depicted are based on

Gauthier (1986), Brochu (1997), Sereno (1999b) and Gatesy et al. (2002). Taxa names with

living representatives are shown in black; totally extinct taxa are shown in boldface type. Taxa

known to possess feathers are indicated by symbol.

Resolving Reptile Relationships 463

have evolved endothermy (“warm-bloodedness”) in response

to the high metabolic demands of flapping flight.

Dinosaurs (including birds) are the most diverse and important

archosaur lineage. Unlike all other reptiles, dinosaurs

possess modifications of the hips and limbs for an upright

(rather than sprawling) gait. This permits breathing while running

and thus greater activity levels (Carrier and Farmer 2000).

Dinosaurs were primitively bipedal, but facultative or obligate

quadrapedality evolved repeatedly within the group. Very early

in their evolution, dinosaurs split into two great lineages that

each radiated extensively (fig. 26.6; Gauthier 1986, Sereno

1999b). Members of Ornithischia (bird-hipped dinosaurs)

possess a (convergently) birdlike pelvis with a backwardpointing

pubis, a new bone (predentary) at the tip of the

snout, and distinct leaf-shaped teeth. They are all herbivores

and include stegosaurs, ankylosaurs, ornithopods, ceratopsians,

and pachycephalosaurs. Saurischia (lizard-hipped dinosaurs)

are usually characterized by a reptilelike pelvis with a

forward-pointing pubis, but this has reverted to an ornithischian-

like arrangement in birds and some of their closest

theropod relatives. Saurischians also possess elongated birdlike

neck vertebrae. They consist of the herbivorous sauropods

and prosauropods, as well as the carnivorous theropods. Birds

are descended (or ascended) from theropod dinosaurs and are

thus part of Saurischia, not Ornithischia.

The theropod–bird transition has recently become one

of the most richly documented examples of macroevolution

(e.g., Ostrom 1969, Gauthier and Gall 2001, Padian and

Horner 2002). Many of the “key” features of birds, such as

the wishbone (fused clavicles), enlarged shoulder girdle, and

wrist structure permitting wing beat movements, appear in

small, lightly built theropods such as dromaeosaurs (e.g.,

Velociraptor, Deinonychus). Even birdlike egg structure and

brooding behavior have now been confirmed in theropods

(Clarke et al. 1999). Perhaps most compelling featherlike

integumentary structures have been observed in a range of

theropods from exceptional deposits in China (e.g., Xu et al.

1999, 2001, 2003, Ji et al. 2001), and increasing complexity

of such structures can be traced along the theropod lineage

leading to birds (Prum and Brush 2002). The occurrence

of proto-feathers in even quite basal theropods such as compsognathids

implies that they were widely distributed

throughout the group and arose at the base of Coelurosauria

or even earlier. This means that feathers can most parsimoniously

be inferred to have been present even in rather

unbirdlike forms such as Tyrannosaurus. The possession of

efficient insulation might have permitted theropods to thermoregulate

at smaller body size. This might explain why

theropods are the only group of dinosaurs showing a consistent

trend toward size reduction; the evolution of small

body size, in turn, might have facilitated the origin of flight.

Despite the overwhelming evidence that birds are nested

within theropods, major questions remain. First, most theropods

show no unequivocal adaptations for climbing, implying

that flight probably evolved “from the ground up” via

cursorial theropods (but see Xu et al. 2003). However, this

scenario has been argued to be biomechanically less plausible

than the alternative view that flight evolved “from the

trees down” via a gliding intermediate. The speculation that

flight evolved via theropods leaping at prey from high vantage

points might reconcile both viewpoints (Garner et al.

1999) but will be difficult to confirm. Also, the homologies

of the avian digits remain contentious. There is clear phylogenetic

evidence that the functional digits in theropod manus

are 1, 2, and 3; digits 4 and 5 gradually diminish and disappear

within the clade. However, developmental data suggest

that the digits in birds are 2, 3, and 4. This conflict can be

reconciled by assuming a homeotic frameshift occurred in

the bird manus (Wagner and Gauthier 1999), but this explanation

remains controversial (Galis et al. 2002). Finally,

the precise position of many transitional taxa (maniraptorans;

fig. 26.6) remains debated; for instance, the small, lightly

built alvarezaurids and oviraptosaurs might be very birdlike

nonavian dinosaurs, or secondarily flightless birds (Sereno

2001, Xu et al. 2002, Maryanska et al. 2002). The plethora

of intermediates connecting dinosaurs and birds has shifted

the question from whether birds are descended from dinosaurs,

to where we draw should the line between dinosaurs

and birds. There is now a strong consensus that birds are

integral part of the dinosaurian radiation and must be classified

as a subgroup of dinosaurs, in much the same way as

humans must be considered a subgroup of primate mammals.

This taxonomic arrangement correctly reveals that not all

dinosaurs became extinct at the end of the Cretaceous; rather,

one lineage (Aves) survived to diversify into more than 9000

living species.

Reptiles as a Barometer for Systematics

Phylogenetic studies of reptiles have not only furthered our

knowledge of the biodiversity and evolution of this important

and conspicuous group but also have generated some

of the most important philosophical and methodological

advances in systematics. For instance, the old concept of

Reptilia represented a classic example of a paraphyletic assemblage

(grade), and the shift toward redefining Reptilia as

a discrete monophyletic group has reflected the trend toward

delimiting taxa based on phylogenetic relationships, rather

than vague impressions of similarity or evolutionary advancement.

Many workers elaborating this approach (as “phylogenetic

taxonomy”; de Queiroz and Gauthier 1992, Cantino and

de Queiroz 2000), along with some strong opponents of this

system, are reptile systematists. These ideas were thus initially

used and debated heavily in the context of reptile studies (e.g.,

Gauthier 1986, de Queiroz and Gauthier 1992, Laurin and

Reisz 1995, Lee 1995, 1998, Dilkes 1998, Sereno 1999a,

Padian et al. 1999, Benton 2000). Thus, reptiles have been the

empirical exemplar for some of the important advances in taxonomy,

and this will continue in the years to come.

464 The Relationships of Animals: Deuterostomes

Key early papers advocating the importance of considering

as many taxa as possible in recovering phylogenetic

relationships dealt with reptiles, with these studies demonstrating

that incomplete fossil taxa can be critical. For instance,

if only living taxa are considered, birds and mammals

group together, as the “Haematothermia” (e.g., Gardiner

1993). However, most of their similarities are not present in

their putative fossil relatives (e.g., dinosaurs, therapsids). The

inclusion of fossil stem taxa reveals that the apparent derived

similarities uniting birds and mammals are convergences,

thus separating these two taxa to opposite sides of the amniote

tree (Gauthier et al. 1988). The wider implication is

that partially known taxa of any kind (e.g., those with partial

sequence data) can only be ignored at one’s peril. Similarly,

the earliest papers strongly advocating the “total evidence” or

“simultaneous analysis” approach of using as many sources

of data as possible in a single analysis to infer phylogenetic

relationships were reptile studies (e.g., Kluge 1989, Eernisse

and Kluge 1993), and as a result, combined morphological

and molecular studies are more common in reptiles than

in most other organisms (see Bromham et al. 2002). Systematists

now have a wealth of disparate sources of information

at their disposal (e.g., morphology, behavior,

allozymes, DNA and amino acid sequences, microsatellites,

genetic “language,” SINEs). The problems and insights of

integrating multiple data sets with (potentially) different

histories and evolutionary dynamics represent some of the

most promising and exciting areas of systematic biology.

Some of the most important early contributions in these

areas dealt with reptiles, and empirical studies on reptiles

will continue to be fertile ground for the growth of phylogenetic

methodology. Although this overview has perhaps

focused on areas of conflict between morphology and molecules,

it should be stressed that, by and large, they agree

more often than they disagree. For instance, most of the

major groups of reptiles (e.g., crocodiles, birds, turtles,

squamates, snakes, amphisbaenians, most lizard and snake

“families”) were recognized long ago on the basis of morphological

data and have since been corroborated by molecular

data. However, molecular data corroborating

“obvious” groupings are usually considered rather uninteresting,

and usually hardly rate a mention in the literature.

In contrast, the few areas of strong conflict (and thus novel

molecular findings) often receive wider attention, being

discussed at length in each study and furthermore encouraging

publication in a higher profile journal (e.g., Hedges

and Poling 1999, Gatesy et al. 2002). It is difficult to quantify

the extent of this “systematic” bias, which is analogous

to the greater probability of publication of experimental

results rejecting the null hypothesis. However, such a bias

is likely, and would have fostered the (erroneous) impression

that morphology and molecules are widely or even generally

in conflict, thereby encouraging the equally dubious

assumption that morphology is not very useful for inferring

phylogenetic relationships.

Appendix: Details of Analyses

The turtle data set was that of Shaffer et al. (1997), obtained

from the senior author, and reanalyzed unmodified. The

complete squamate and snake matrices are available in

TreeBASE (2003). The squamate data set consists of the

morphological characters of Lee (2000) and partial sequences

of four genes: 12S rRNA, 16S rRNA, c-mos, and cmyc

(Saint et al. 1998, T. Reeder, unpubl. obs.). The snake

data set consisted of the morphological characters of Lee and

Scanlon (2002), partial sequences of 12S rRNA and 16S rRNA

from Heise et al. (1995), and complete cyt-b and partial cmos

sequences from Slowinski and Lawson (2002). Morphological

characters were ordered as discussed in the original

studies. Protein-coding genes (cyt-b, c-mos, c-myc) were

aligned by eye using SEAL. RNA genes were aligned using

Clustal (Gibson et al. 1997), using parameters listed in the

data files; sensitivity of results to different alignment costs

will be explored in more detail elsewhere. However, the caveat

should be added that these are works in progress and

the full analyses to follow will almost certainly contain a few

alterations to the morphological data, as well as more thorough

exploration of alignments, and additional taxa for sequenced

for certain genes. Data entry and analyses were

undertaken with MacClade (Maddison and Maddison 2000)

and PAUP* (Swofford 2000). Analyses included all taxa in

the data matrices (certain taxa subsequently pruned from the

figured trees) and employed parsimony with all character

transformations assigned unit weight. Gaps were treated as

a fifth base; this approach was feasible because most parsimony-

informative gapped regions were relatively short (the

few long gaps were usually either autapomorphic or present

throughout the ingroup). Alternative tree-building methods,

character weightings, and gap treatments will be explored

elsewhere. The overall support for each clade was assessed

using branch support (Bremer 1988) and bootstrapping

(Felsenstein 1985). Partitioned branch support (Baker and

DeSalle 1997), as calculated by TreeRot (Sorenson 1999), was

used to evaluate support from each data set for each clade;

this was calculated manually from the PAUP log generated

by TreeRot. The nonzero molecular PBS values for some basal

clades of snakes are not errors but result from rearrangements

among extant taxa that occur when calculating PBS.

Acknowledgments

M.S.Y.L. thanks the symposium organizers for the invitation and

funding to attend, the Australian Research Council for ongoing

research support, Brad Shaffer for providing the turtle data set,

and Chris Raxworthy and John Gatesy for permitting citation of

manuscripts in review. T.W.R. acknowledges the National

Science Foundation for support, and William McJilton for

collection of nuclear gene data. R.L. and J.B.S. thank the

California Academy of Sciences and the National Science

foundation for support.

Resolving Reptile Relationships 465

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