VERTEBRATES, OVERVIEW

Carl Gans* and Christopher J. Bell† *Department of Integrative Biology, University of Texas at Austin and †Department of Geological Sciences, University of Texas at Austin

I. Introduction neurectoderm An embryonic tissue that gives rise to II. General Vertebrate Characteristics the central tube of the nervous system. III. Early Chordate and Vertebrate History notochord A stiff, flexible, longitudinal rod running IV. Vertebrate Classification along the middorsal portion of the chordate body. V. Definitions and Diagnoses of Major Chordate It is situated dorsal to the coelom and ventral to the Groups central tube of the nervous system. pharynx The anterior portion of the alimentary canal, characterized by lateral buds that provide skeletal GLOSSARY support for the gill region. tuberculum interglenoideum An anterior projection of chordate A member of the group Chordata. The the first (cervical) vertebra in salamanders. The tu- Chordata includes the most recent common ancestor berculum interglenoideum bears articular facets that of tunicates and cephalochordates and all of that insert into the foramen magnum of the skull and ancestor’s descendants. Tunicates, lancelets, hag- provide additional articulation points between the fishes, and vertebrates are all chordates. skull and the vertebral column. ectoderm An embryonic tissue that provides the future outside layer of the animal. ectothermy A method of body temperature control in which the animal utilizes external sources for gaining VERTEBRATES INCLUDE ALL the fishes, amphibians, and giving up heat, thus achieving temperature con- reptiles, birds, and mammals. These animals are united trol without affecting metabolic rate. in a more inclusive group, the Chordata, that includes endothermy A method of body temperature control in the closest living relatives of vertebrates, the hagfishes, which the animal modifies its metabolic rate to lancelets, and tunicates. There are approximately achieve the desired body temperature. 54,450 known species of chordates, over 51,000 of neural crest An embryonic tissue intermediate be- which are classified as members of Vertebrata. Nearly tween neurectoderm and ectoderm, with cells mi- half (approximately 24,000) of the known species of grating widely to their final destination. This tissue vertebrates are members of a single group of ray-finned gives rise to anterior skeletal elements, many por- fishes, the actinopterygians. The vertebrates are found tions of the future head and pharynx, and all pigment on all major land masses and in all major oceans and cells. Sometimes also referred to as mesectoderm. seas on Earth.

Encyclopedia of Biodiversity, Volume 5 Copyright  2001 by Academic Press. All rights of reproduction in any form reserved. 755 756 VERTEBRATES, OVERVIEW

I. INTRODUCTION basal chordates or echinoderms), or historical stages in the development of groups of vertebrates (i.e., fishes, The vertebrates include most of the major groups of reptiles, and mammals). animals that humans encounter and interact with on Although a few arthropods and mollusks achieve Earth, and in common parlance, the term ‘‘vertebrate’’ large, indeed giant, sizes, most of the largest species, is often equivalent to ‘‘animal.’’ Vertebrates include all whether terrestrial, aquatic, or aerial, are vertebrates, the fishes, amphibians, reptiles, birds, and mammals; and this latter group includes the largest animals they are found on every major landmass and in all of known. However, some vertebrates are small, almost the world’s oceans and major seas. The fossil record of tiny, and this poses interesting questions of how they the group is excellent and extends back to the late perform the basic functions of reproduction, locomo- Cambrian period of the early Paleozoic, more than 500 tion, respiration, food processing, and waste discharge. million years ago. The vertebrates are members of a Vertebrate size reduction involves two strategies: (1) nested series of more inclusive groups, extending all maintenance of the adult pattern at a reduced body size the way down the tree of life to a common ancestor and (2) the acquisition of metamorphosis, meaning that they share with bacteria, the most primitive life forms the life processes, and the structures that facilitate them, known. In order to properly understand the vertebrates, change markedly at one or more stages and sizes of de- it is necessary not only to briefly discuss the characteris- velopment. tic features unique to the group but also to evaluate Vertebrates may be visualized as elongate, tubular the features they share with their closest living relatives, creatures possessed of a central tubule, this being a gut the hagfishes, lancelets, and tunicates. These organisms or alimentary canal. The anterior end of the gut forms plus vertebrates constitute the group Chordata. In the a mouth and buccal structures, whereas the posterior pages that follow, we summarize some generalized char- end is modified for the storage and ultimate elimination acteristics of chordates and vertebrates, examine the of waste. The central tubule is placed in a lined cavity, early history of these groups as it is revealed from the the coelom, that also houses various diverticulae of the study of the fossil record, and provide explicit defini- gut that support aspects of such visceral functions as tions and diagnoses for all of the major chordate groups. gas exchange (i.e., gills and lungs, heart, and vessels), digestion (pancreas and liver), fluid balance (kidneys), and reproduction (gonads). The entire animal is coated by a multilayered epidermis that protects the internal II. GENERAL VERTEBRATE tissues from mechanical stresses and can serve as a CHARACTERISTICS physiological barrier. The space between coelom and epidermal layer is occupied by the somatic musculo- The diversity among vertebrate groups makes it possible skeletal system that facilitates locomotion and supports to utilize functional analyses and paleontological data and maintains the shape of the coelom and hence of to reconstruct a phylogenetic sequence of vertebrates the entire animal. and to place the currently surviving (extant) vertebrate The musculoskeletal system involves the cartilages groups into a historical sequence. This sequence per- and bones of the internal skeleton and the striated so- mits the development of explanatory schemes for some matic musculature. Externally, the system underlies the conditions observed in humans. Consequently, the epidermis, this portion forming a dermis having skele- study of the comparative morphology and physiology togenic properties. Two additional median and tubular of vertebrates has proved important for the understand- structures complete this architectural scheme. The first ing of the human condition. These studies in turn led tube, the notochord, lies just dorsal to the gut and is to the development of curricular variants for students filled with vacuolated cells, their turgor pressure turn- training themselves for careers in human medicine. Ex- ing the notochord into a stiffened skeletal rod. The amples are approaches to applied physiology and mor- second, still more dorsal, tube consists of neuronal cells phology of the precursors’ conditions. Such instruc- that involve sensory function and transmission of sig- tional variants may be presented as the sequential nals to the musculature. development of the history of a topic such as gas ex- The entire animal may have various appendages such change, digestion, or embryology. Alternatively, the as fins or limbs, each having characteristic internal skel- study may involve a series of steps, each explaining the etal supports and motile capacity developed by the con- condition in one of the subgroups of animals represent- traction of the attaching striated musculature, which is ing putative precursors for the vertebrate condition (i.e., subdivided into myotomes, paired blocks that parallel VERTEBRATES, OVERVIEW 757 the notochord. The notochord provides a capacity for and major physiological systems, for instance the multi- resisting longitudinal stresses, while the appendages ple senses, the head skeleton, the vertebral column, and involve support of the animal above the substrate and the digestive system. This clear diversity of vertebrate the transmission of laterally directed force patterns. specializations has long raised questions about the Whereas this general pattern seems to characterize adaptive reasons to explain why these comparable char- vertebrate structure, the group shows major curiosities. acteristics are modified in vertebrates and why and how The various groups of nonvertebrate creatures can gen- a multiplicity of such characteristics might be associated erally be diagnosed by a relatively few characteristics. In and consequently subject to possibly simultaneous se- contrast, there are no fewer than 25 new characteristics lection. Actually, the answer to this conundrum has shared by vertebrates (Table I). These involve multiple been available for some 30 years. Rather than looking at the functions of the many ‘‘vertebrate characteristics,’’ namely, aspects seen in the adult condition, it is more informative to base comparisons on the stages of verte- TABLE I brate embryology or development. The traditional rules Derived Characters of Vertebrata and Their Embryonic Origina that posited firm conditions, such as that the ectoderm formed all the epidermis and the mesoderm all of the Vertebrate characters Embryonic origin striated musculature, soon broke down. In particular, Nervous system the neural crest, an embryonic tissue intermediate be- Sensory nerves with ganglia, cranial NC, P tween the ectoderm and the neurectoderm, proved to Sensory nerves with ganglia, trunk NC be the source of many diverse tissues. Similarly, the Peripheral motor ganglia NC neurogenic epidermal placodes formed a set of embry- Second- and higher-order motor neurons NC onic tissues that provided a source for many shared Forebrain NC? vertebrate characteristics (Table I). The most interest- Chromatophores NC ing aspect was the discovery that many otherwise indis- Paired special sense organs tinguishable adult tissues could be derived from differ- Nose P ent embryonic sources, depending on their position Eyes (accessory organs) NC?, (P) in the embryo. Thus cephalic striated muscle has a Ears P histological pattern equivalent to that of the striated Lateral-line mechanoreceptors P muscle of the trunk but is of neural crest rather than Lateral-line electroreceptors P mesodermal origin. Similarly, the bones of the skull are Gustatory organs NC?, P derived from neural crest and the more posterior and Pharyngeal and alimentary modifications serially equivalent vertebral bones are of (sclerodermal) Cartilaginous bars NC mesodermal origin. Branchiomeric muscle ME Consequently, the vertebrate characteristics either Smooth muscle of gut MH are derived from neural crest of neurogenic epidermal Calcitonin cells NC placodes or are induced by these tissues. In contrast to Chromaffin cells, adrenal cortex NC searching for 25 functional issues, the developmental Circulatory system approach makes it possible to recognize two or three Gill capillaries, endothelium ME associated aspects and note that these provided the Major vessels, trunk M cause of the vertebrate condition. Wall of aortic arches NC Muscular heart MH Skeletal system Anterior neurocranium and sensory NC III. EARLY CHORDATE AND capsules VERTEBRATE HISTORY Cephalic armor and derivatives NC Armor of trunk NC??, ME? Vertebrates are members of a more inclusive group of animals, the chordates. The history of both chordates a M, mesoderm; ME, mesoderm, epimere; MH, mesoderm, hypo- and vertebrates extends back into the Cambrian period mere; NC, neural crest; NC?, intermediate between neurectoderm and neural crest; P, placodes; (P), placodes provide lens and peripheral in the early Paleozoic. Although the fossil record of component, but not sensory tissues. Origin of the various trunk early chordates is generally quite poor, several fossil armors is uncertain. Table modified from Gans (1993). localities have produced fossils that are likely to repre- 758 VERTEBRATES, OVERVIEW sent the remains of early chordate animals. Controversy ments, and the tetrapods, which mainly occupied over the interpretation of anatomical features of these terrestrial habitats. At present, there are two major clas- animals is in part due to the fact that the important sification systems in use. The Linnaean classification characteristics by which we recognize chordates are system was first published by Linnaeus about 1758 soft anatomical features that are not easily fossilized. and organizes major divisions of life into kingdoms Exquisite preservation of soft-bodied organisms in the (Plantae, Animalia, Fungi, etc.), with major body plans Burgess Shale in Canada (middle Cambrian, approxi- organized into phyla (singular: phylum). The basic mately 530 million years ago) resulted in the discovery ranks descend from phylum to class, order, family, ge- of several specimens of a chordate-like animal named nus, and species. This classification system is familiar to Pikaia gracilans. These important fossils appear to dis- most teachers and students and remains the dominant play major chordate structural features, including myo- classification taught to elementary and high school stu- tomes (segmented muscle blocks) and a stiff, longitudi- dents in the United States (Fig. 1). In the past several nal rod running along the middorsal portion of the decades, a nonranked classification system was de- body, the notochord. Some controversy regarding the scribed by Hennig, a European entomologist. This clas- precise phylogenetic position of Pikaia persists due to sification system, termed ‘‘phylogenetic systematics’’ or a lack of adequate description of these fossils in the ‘‘cladistics,’’ organizes taxa into nested sets of monophy- primary literature. Recent discoveries in early Cambrian letic groups based on common ancestry (a monophy- deposits in China stimulated renewed interest in the letic group contains an ancestor and all of that ancestor’s origin and diversification of chordates. Yunnanozoon descendants). A classification system based on natural lividum was described as an early representative of the groupings of taxa (based on ancestor–descendant rela- cephalochordates (Chen et al., 1995; Chen and Li, tionships) is thus achieved. Phylogenetic systematics is 1997), and Haikouela lanceolata was recently identified rapidly becoming an important alternative classification as a potential craniate from the early Cambrian (Chen et al., 1999) but these interpretations are controversial (Shu et al., 1996). The earliest fossils attributed to the Vertebrata are enigmatic bits of bone from the late Cam- brian described under the name Anatolepis heintzi. The vertebrate affinity of these fossils was challenged on various grounds, but recent analyses showed they con- tain dentine, a form of the calcium phosphate mineral apatite (the major mineral component of bone) that is found only in vertebrate skeletal tissues (Smith et al., 1996). Homoiosteles and stylophorans, Paleozoic animals with a highly asymmetrical body form and a calcite skeleton resembling that of echinoderms, are another problematic extinct group. Fossils range in age from middle Cambrian to middle Devonian. The body can be divided into two distinct regions: a compact, asym- metrical region and a long segmented appendage. Inter- pretation of these fossils as ‘‘calcichordates,’’ a distinct assemblage of stem-group chordates (see Jefferies, 1986, 1997) is controversial. Most authors treat them as aberrant echinoderms, and the controversy over their affinity is based in part on interpretations of orientation and locomotion (see Parsley, 1997).

IV. VERTEBRATE CLASSIFICATION

The classification of chordates has a long and compli- FIGURE 1 A traditional, Linnean classification of the major chordate cated history. Traditionally, the vertebrates were di- groups. The major vertebrate groups are ranked into eight categories, vided into fishes, which occupied aquatic environ- all given the equivalent rank of class. VERTEBRATES, OVERVIEW 759

FIGURE 2 A graphic representation of a cladisitic classification of chordates. The major groups are arranged in a nested hierarchy, and taxon names are defined based on shared ancestry. The groups nested within Tetrapoda are depicted in Fig. 3. See text for definitions and diagnoses.

system and is increasingly being utilized in biological Taxa are diagnosed by a list of characteristics hypothe- sciences (including paleontology). Although we pro- sized to have first appeared in the common ancestor of vide ancestry-based definitions for all the major the members of the group; this assemblage of characters chordate groups discussed below, we include three fig- can be used to identify a taxon (see Rowe, 1987, for ures to illustrate the differences in classification systems further discussion). now in use. Figure 1 illustrates a version of a Linnaean classification system, in which taxa are placed in equiva- lent ranks. Figures 2 and 3 are graphic representations A. Chordata of cladistic classifications, showing the hierarchical ar- Chordata is defined as the most recent common ances- rangement of nested taxa (Fig. 2 shows the relationships tor of tunicates and cephalochordates, and all of that of the major chordate groups, and Fig. 3 shows the ancestor’s descendants. Chordates share a common, relationships of the major groups nested within the generalized body plan and can be diagnosed by four taxon Tetrapoda). features shared by members of all the major groups: a notochord, pharyngeal slits, a hollow dorsal nerve tube, and a postanal tail (an extension of the body posterior to V. DEFINITIONS AND DIAGNOSES OF the anus). The notochord is a stiff, flexible rod running MAJOR CHORDATE GROUPS dorsal to the coelom along the length of the body be- neath the central nervous system. In many vertebrates, The major chordate groups discussed below are defined the notochord is almost completely replaced by blocks in terms of their ancestry; in other words, membership of bone forming vertebrae. Pharyngeal slits are lateral in a given taxon is dependent upon shared ancestry. openings from the pharynx (an organ situated behind 760 VERTEBRATES, OVERVIEW

FIGURE 3 A graphic representation of a cladisitic classification of tetrapods. The major groups are arranged in a nested hierarchy, and taxon names are defined based on shared ancestry. See text for definitions and diagnoses. the mouth that constitutes part of the digestive tract). tor’s descendants. Cephalochordates are diagnosed by These features are found in all chordates at some point the presence of segmented muscle blocks. The lancelets during their lifetime, but they are not retained as fully are marine organisms that live in shallow, tropical and functional units throughout life in all chordates. temperate seas surrounding all the continental land The tunicates (urochordates) are a group of basal masses except Antarctica. Two major groups are recog- chordates represented by approximately 3000 species. nized and are classified under the names Branchiostoma They are entirely marine. Some tunicates spend their (23 species) and Epigonichthyes (7 species; Poss and entire life as pelagic organisms, floating in the water Boschung, 1996). Lancelets lack a well-differentiated column. One group of tunicates, the sea squirts, un- head region. A rudimentary brain is present, but sig- dergo a dramatic metamorphosis from a planktonic lar- nificant regions of the brain found in vertebrates appear val form to a sessile adult (attached to a substrate); a to be absent. A recent volume addressing many aspects notochord is present in the tail of the larval stage but of lancelet biology (Gans et al., 1996) provides an im- is resorbed in the adult during metamorphosis. The portant foundation for future research on this group. pharynx enlarges in the adult and expands to form a barrel-shaped branchial basket through which a con- C. Craniata stant flow of water passes as the animal filter-feeds. Craniata is defined as the most recent common ancestor of hagfishes and Vertebrata, and all of that ancestor’s B. Cephalochordata descendants. Craniates are diagnosed by the presence Cephalochordata is defined as the most recent common of a differentiated head, with well-developed paired ancestor of lancelets and Craniata, and all of that ances- sense organs designed to act as distance receptors. There VERTEBRATES, OVERVIEW 761 are 43 described species of hagfishes; all are marine correlation and relative chronology of Paleozoic and organisms, and the group has a worldwide distribution. early Mesozoic rocks. The systematic position of cono- Hagfishes are scavengers, feeding on dead and mori- donts was debated for decades, and various authorities bund fishes, worms, mollusks, and crustaceans. They suggested affinities with many different animal groups. lack recognizable vertebral structures but have weakly In 1983, a conodont fossil with soft-body preservation developed, irregularly shaped plates that are positioned was reported for the first time (Briggs et al., 1983). almost randomly along the nerve chord in the tail re- Subsequent finds that preserve greater anatomical detail gion. Their eyesight is poor, but they have well-devel- revealed several features that can be interpreted as a oped senses of smell and touch. Reproductive biology notochord, a dorsal nerve cord, myotomes, and a dis- is poorly understood; only a few embryos are known. tinct head region with very large eyes. These features Hagfishes were not known as fossils until 1991. The suggest that conodonts may well have been chordates, first reported fossil was found in Pennsylvanian age or possibly vertebrates, but the relationships of cono- rocks in Illinois (Bardack, 1991). It differs from living donts and other jawless fishes are still quite controver- forms in at least a few features (better developed eyes, sial (for reviews, see Benton, 1997; Zimmer, 2000). different position of the gills, and some aspects of the feeding apparatus). E. Gnathostomata Gnathostomata is defined as the most recent common D. Vertebrata ancestor of Chondrichthyes and Osteichthyes, and all Vertebrata is defined as the most recent common ances- of that ancestor’s descendants. Gnathostomata is diag- tor of lampreys and Gnathostomata, and all of that nosed by the presence of jaws, an enlarged forebrain, ancestor’s descendants. As noted above, Vertebrata is and a skeleton in the paired pectoral and pelvic append- diagnosed by a suite of characters (see Table I). In ages. The evolution of jaws provided new opportunities all vertebrates there is at least some development of for vertebrates by opening the door to truly predatory vertebral elements. The basal members of Vertebrata, habits, with new food-handling capabilities and a the lampreys, have only rudimentary development of broader diversity in potential diet. Among living verte- these structures. Lamprey vertebral elements consist of brates the chondrichthyans constitute the basal mem- tiny distinct cartilages, situated above the dorsal nerve bers of Gnathostomata. There are approximately 850 cord. The homologies of these elements with vertebral species of living chondrichthyans, including the sharks, units in other vertebrates are not known. Many adult skates, rays, and chimaeras. The majority are marine, lampreys are parasites on other fish, and sometimes act but a few species inhabit freshwater environments. as scavengers. They have a circular mouth with a rasp- There is no bony skeleton; the skeleton is predomi- ing tongue; the mouth is used like a suction cup to nantly cartilaginous, with only minor calcification oc- attach the lamprey to a fish, and the tongue is used to curring throughout. Males have special structures called open a hole in the body cavity of the fish, providing claspers that help facilitate internal fertilization. The access to the body fluids on which the lampreys feed. sharks first appear in the fossil record in the late Dev- Some lampreys spend significant portions of their adult onian, chimaeras appear in the Carboniferous, and rays lives in marine habitats, but all lampreys return to fresh- appear in the Jurassic. The whale shark (Rhincodon ty- water to breed. There are approximately 32 living spe- pus) is the largest living fish, achieving lengths of up cies of lampreys. to 15 meters. Many earlier classifications placed lampreys, hag- fishes, and a diverse suite of extinct jawless fishes into the class Agnatha (‘‘without jaws’’). A great diversity of F. Osteichthyes jawless marine vertebrate groups populated Ordovician, Osteichthyes is defined as the most recent common Silurian, and Devonian seas. One enigmatic group, the ancestor of Actinopterygii and Sarcopterygii, and all of conodonts, were first discovered in 1856 and subse- that ancestor’s descendants. Osteichthyes is diagnosed quently were found to be remarkably abundant in ma- by the presence of lungs (see below) and by most of rine rocks dating from the late Cambrian through the the bony skeleton being formed from cartilaginous pre- Triassic. For over a century, conodonts were known cursors. Many bony fishes have an elongated sac, the only from abundant, tiny, phosphatic, toothlike fossils gas bladder, situated dorsal to the digestive tract. Gas that showed a remarkable diversity in form. These fos- bladders can serve either a buoyancy control function sils were, and remain, important tools for establishing (swim bladder) or a gas exchange function (respiratory 762 VERTEBRATES, OVERVIEW gas bladder). In the latter condition, they are highly the southern continents of Africa, Australia, and South vascularized and serve as a supplementary reserve for America. The Australian lungfish is the least derived of oxygen to be used in respiration. Although gas bladders the three; it cannot live out of water but can survive and lungs differ in their position relative to the digestive in stagnant pools by coming to the surface to gulp air. tract (lungs are ventral to the digestive tract) and lungs The South American and African lungfishes can survive tend to be paired while gas bladders are single, their out of water for relatively long periods of time. developmental origins and gross anatomical features are quite similar. These similarities provide some evidence that the two structures are homologous. Actinopterygii I. Tetrapoda includes a remarkably diverse assemblage of fishes, in- Tetrapoda is defined as the most recent common ances- cluding more than half of the living species of known tor of Amphibia and Amniota, and all of that ancestor’s vertebrates; over 24,000 valid species are known (see descendants. Tetrapoda is diagnosed by the presence Eschmeyer, 1998). The skeleton of actinopterygians is of differentiated fingers and toes and by a bony joint extensively ossified and the internal pectoral skeleton formed between the occipital condyles of the skull and has broad bony plates that facilitate support of fin rays. the anterior vertebral elements. Extant amphibians share three morphological char- acteristics: (1) loss of several skull bones found in ex- G. Sarcopterygii tinct amphibian groups; (2) short or absent ribs; (3) Sarcopterygii is defined as the most recent common pedicellate dentition (an upper tooth crown resting on ancestor of Actinistia and Choanata, and all of that a lower pedicel). The relationships among the three ancestor’s descendants. Sarcopterygii is diagnosed by major extant amphibian groups are not well supported, the presence of fleshy, lobed appendages, with differen- but combined analyses of morphological and molecular tiated proximal limb bones in the pectoral and pelvic data favor a sister taxon relationship between Anura fins, and by the presence of a ring of four or more (frogs and toads) and Caudata (salamanders). Batrachia bony plates in the eye (the sclerotic, or scleral, ring). is defined as the most recent common ancestor of Anura Actinistia includes at least one, and possibly two, spe- and Caudata, and all of its descendants. In this arrange- cies of living coelacanths. These fishes fist appear in ment, Batrachia and Gymnophiona (the caecilians) are the fossil record in the Devonian and make their last sister taxa (Fig. 1; see also Cannatella and Hillis, 1993). appearance in the fossil record near the end of the There are approximately 165 species of living caeci- Cretaceous, approximately 70 million years ago. The lians. All extant caecilians are limbless, and their distri- discovery of a extant species of coelacanth off the coast bution encompasses tropical and subtropical regions of of South Africa in 1938 was therefore quite surprising. Central and South America, Africa, India, and Southeast Waters near the Comoro Islands (situated between the Asia. Most caecilians are fossorial, spending the major- northern tip of Madagascar and the African mainland) ity of their life underground. One South American yielded a second specimen in 1952, and subsequently group (Typhlonectes) is secondarily aquatic. The otic approximately 200 additional specimens were recov- capsules, exoccipital, basioccipital, and parasphenoid ered. An additional population of coelacanths was re- ossifications of the braincase are fused into a solid unit cently discovered in Indonesia (Erdmann et al., 1998; (the os basale). Caecilians possess a pair of sensory Forey, 1998). Analysis of the DNA of the Indonesian organs called tentacles that are unique among verte- coelacanth suggests that it might belong to a new spe- brates. The tentacles are protrusible organs, usually cies, but this interpretation is controversial (Holden, situated between the external naris and the orbit, and 1999). probably function in chemoreception. Although the or- bits of caecilians are often covered with skin (and some- times bone), the eyes are photoreceptive in most species H. Choanata that have been examined. In some caecilians, the eye Choanata is defined as the most recent common ances- is closely associated with the tentacle and in at least tor of Dipnoi and Tetrapoda, and all of that ancestor’s one species, they eye is protruded from the skull during descendants. Choanata is diagnosed by the presence of protrusion of the tentacle (Nussbaum, 1992). The de- folded tooth enamel and choanae (internal nostrils that rived groups of caecilians fuse many elements of the open directly into the palatal portion of the roof of the skull and lack a tail. The fossil record of caecilians is mouth). The lungfishes (Dipnoi) first appear in the notably poor but extends back at least as far as the fossil record in the Devonian and are represented by six Cretaceous. The Jurassic Eocaecilia shares many charac- living species. Their modern distribution is restricted to teristics with extant caecilians (including the reported VERTEBRATES, OVERVIEW 763 presence of a tentacular foramen) but retains limbs a tadpole. The tadpole has a more or less oval-shaped and other anatomical features not seen in extant forms body with a tail; there is no distinct head region, but (Jenkins and Walsh, 1993). the mouth includes a beak and a number of rows of There are approximately 415 described species of chitinous toothlike structures. During metamorphosis extant salamanders, the majority of which are found in many morphological and physiological changes take the Northern Hemisphere. A significant radiation of place that completely transform the animal’s appearance tropical South American salamanders extends as far and the way it interacts with its environment (e.g., the south as southern Brazil and Bolivia. Caudates share tail is resorbed, limbs grow, the axial and appendicular a number of morphological features of the skeleton, skeleton is dramatically transformed, the digestive tract including the loss of the quadratojugal ossification and shortens, gills disappear, and respiration function is the presence of intravertebral spinal foramina in the transferred to lungs). Many frogs show variants of di- atlas vertebra. Most salamanders also have a reduced rect development. number of bones in the pectoral girdle relative to extinct amphibian groups and frogs (caecilians lack a pectoral girdle), and they have an anteriorly projecting process J. Amniota on the atlas (the first vertebra), the tuberculum inter- Amniota is defined as the most recent common ancestor glenoideum, which forms accessory articulations be- of Reptilia and Mammalia, and all of that ancestor’s tween the skull and the vertebral column. Members of descendants. Amniota is diagnosed by a suite of charac- one large assemblage of caudates (the Plethodontidae) ters, including presence of an amniote egg (see below), lack lungs, and this condition is also found in one caniniform teeth, two or more vertebrae in contact with gymnophionan. The early history of salamanders is the pelvic girdle, internal fertilization, and keratin (a poorly known, but fossils belonging to Caudata (as protein that acts as the building block for scales, nails, defined above) are known from the Mesozoic. Stem- hooves, hair, and feathers). The amniote egg includes group salamanders (outside of Caudata as defined a series of extraembryonic membranes that surround above, but on the evolutionary stem leading to modern the developing embryo and provide all the nutritional, salamanders) are reported from the Jurassic. A recent waste disposal, and gas exchange requirements during review of Mesozoic taxa was provided by Evans and development. In reptiles (including birds) and the Mo- Milner (1996). notremata (basal mammals), the embryo and extraem- There are more than 4100 described species of extant bryonic membranes are encapsulated in an egg with anurans, distributed on all the major continental land- either a leathery exterior or a hard shell. Because this masses except Antarctica. Skeletal features shared by is a self-contained fluid-filled system, eggs can be laid frogs include the fusion of forearm bones (radius and away from water. Although fishes, amphibians, and ulna), fusion of the lower leg bones (tibia and fibula), most reptiles are often referred to as ‘‘cold-blooded,’’ elongation of the ankle bones, reduced number of trunk many species in these groups manage to maintain ele- vertebrae (10 or fewer among extant frogs), and pres- vated body temperature at a constant level. This is ence of a urostyle (a rodlike, posterior bony extension achieved by shuttling between heat sources and heat of the vertebral column). Many of these skeletal features sinks (ectothermy). However, birds and mammals gen- are associated with jumping ability and evolved as early erally maintain a constant temperature by changing the as the early Jurassic (Shubin and Jenkins, 1995). The basal metabolic rate (endothermy). There is substantial fossil record of the group is extensive (see recent review evidence suggesting that some of the fossil reptiles did by Sanchiz, 1998) and at least two stem-group frogs are maintain body temperatures above the level of the envi- now know from the early Triassic (Evans and Borsuk- ronment. There has been much argument about the Bialynicka, 1998). question of whether the mechanism by which this was Many amphibians have a larval stage followed by achieved was ectothermy or endothermy. The earliest metamorphosis into the adult form. Metamorphosis was known members of the Amniota appear in the fossil defined by Duellman and Trueb (1986, p. 173) as ‘‘a record during the Pennsylvanian period. series of abrupt postembryonic changes involving struc- tural, physiological, biochemical, and behavioral trans- formations.’’ The transformations that take place in K. Reptilia frogs are the most dramatic of any within the Tetrapoda. Reptilia is defined as the most recent common ancestor The majority of frog species have a larval stage in the of Chelonia and Sauria, and all of that ancestor’s descen- life cycle (following hatching from an egg and preceding dants. Reptilia is diagnosed by several features of the development of the mature adult body form) known as skull, including the presence of suborbital fenestrae 764 VERTEBRATES, OVERVIEW

(paired openings in the skull that are situated ventral and tongue. All squamates have paired, evertible hemi- to the orbital region). penes. Many squamate species lack, or have reduced, There are approximately 260 species of extant Chelo- limbs and girdles. nia (turtles). They are found on all continental land- There are approximately 4150 species of extant liz- masses except Antarctica and also occupy all of the ards, widely distributed on all the continents except world’s tropical and temperate oceans and seas. All Antarctica. A number of extinct groups were fully ma- turtles lack marginal teeth, but the earliest known stem- rine, but today only one species utilizes a marine habitat group turtles (Proganochelys) from the Triassic have a (the marine iguana of the Galapagos Islands feeds on few small teeth on the palatal portion of the skull; all marine algae). Many groups of lizards have lost or re- extant chelonians lack palatal teeth. The palate is firmly duced limbs. The two North American species of Helod- attached to the braincase. The presence of a hard, bony erma are venomous. Lizards first appear in the fossil shell is one of the most distinguishing features of turtles. record in the Jurassic. The upper portion of the shell (the carapace) is formed Both morphological and molecular data indicate that in part from the vertebral column and ribs. During snakes evolved from within lizards, but their precise development these elements fuse with dermal ossifica- phylogenetic position among other squamates is unre- tions to form a generally continuous, hard bony shell. solved. There are approximately 2700 species of extant The generally flat, ventral plate (the plastron) of the snakes, with a distribution encompassing tropical shell is formed anteriorly by dermal bones and skeletal oceans and seas and all continents except Antarctica. elements that are probably homologous with elements Several species spend most or all of their lives in open of the pectoral girdle in other vertebrates. The bony ocean habitats. Most snakes are limbless, but some basal shell of most turtles is covered by a series of keratinous members retain vestigial pelvic girdle and limb ele- scutes; in some forms, these scutes are lacking and a ments. A few poorly known Mesozoic snakes had well- leathery skin covers the carapace and plastron. Turtles developed limbs. All snakes are carnivorous, and several are unique among vertebrates in having the pectoral lineages of advanced snakes evolved potent venom that girdle enclosed by the rib cage. Turtles first appear in lets them subdue prey. Most snake species have an the fossil record during the Triassic. extremely modified and flexible skull structure that permits them to eat animals much more bulky than themselves and to ingest prey that is of a greater diame- L. Sauria ter than their own head. Snakes first appear in the fossil Sauria is the most recent common ancestor of Lepido- record during the Cretaceous, but their fossil record as sauria and Archosauria, and all of that ancestor’s de- a whole is relatively poor and consists predominantly scendants. Sauria is diagnosed by the presence of a of isolated vertebrae. specialized ankle joint, long and generally slender hind Amphisbaenia is a small group of squamates with limbs, and relatively larger leg muscles. approximately 160 extant species. They are found in Lepidosauria can be defined as the most recent com- Africa, the Iberian Peninsula, the Middle East, Mexico, mon ancestor of Squamata and the extant rhynchoce- from Panama to Argentina in South America, and Geor- phalian (Sphenodon; see below), and all of that ances- gia and Florida in the southeastern United States. As a tor’s descendants. Lepidosauria is diagnosed by various result of their subterranean habits and the fact that features of the skull and the presence of a transverse almost one-third of the described species are known cloacal slit, a distally notched tongue, and a modified from only one specimen, many aspects of their biology middorsal scale row. Rhynchocephalians were a very and systematics are not well understood. Three species diverse and widespread group of lepidosaurs during the of Bipes retain anterior limbs, but all other species are Mesozoic era, but by approximately 60 million years limbless. The compact and well-ossified skull is the ago, they were extinct everywhere except in New primary burrowing tool and is covered with relatively Zealand. The last surviving rhynchocephalians are re- large scales. The scales of the skin are usually rectangu- stricted to a few islands in New Zealand. These relict lar and are arranged in rings that encircle the body populations are classified in the genus Sphenodon, and and allow rectilinear locomotion. Amphisbaenians first two species are currently recognized. appear in the fossil record in the late Paleocene of Squamata includes all the lizards and snakes as well North America. as the fossorial amphisbaenians. A number of anatomi- Archosauria is defined as the most recent common cal features are shared by these three groups, including ancestor of Crocodylia and Aves, and all of that ances- aspects of the skull, postcranial skeleton, musculature, tor’s descendants. Archosaurs are diagnosed by a num- VERTEBRATES, OVERVIEW 765 ber of anatomical features and also by behavioral charac- the dentary bone (the only bone in the lower jaw of teristics such as nest building and parental care of mammals) and the squamosal bone of the skull. Bones young. The two extant groups of archosaurs represent homologous with the quadrate and articular are still only a tiny fraction of the past diversity of this group, present in mammals, but their positional relationship which includes the Mesozoic flying reptiles (ptero- and function has been transformed. The incus and mal- saurs), all the dinosaurs, and many extinct crocodylians. leus in the middle ear of mammals are homologous There are 22 extant species of Crocodylia (alligators, with the quadrate and articular (respectively) in other crocodiles, and caimans), most of which are found in vertebrates. The 4810 species of extant mammals can the Tropics. Two species of alligators extend into tem- be found on all continents and major bodies of water perate regions in North America and China. The earliest on Earth. known crocodylians were terrestrial, but all living spe- Monotremata is represented by three living species cies are found in aquatic habitats. Some extant species (duck-billed platypus and two species of echidna) that are found in nearshore marine habitats, but none are are found only in Australia and New Guinea, but the fully marine. Crocodylians have a complete secondary fossil record of this group extends back to the Creta- palate that forms the roof of the mouth (similar to the ceous and reveals that monotremes were once found in configuration seen in mammals). Stem-group crocodyl- South America. The monotremes are the only mammals ians are known from the late Triassic, but the earliest that lay eggs. The marsupials are found today only in true crocodylians are found in early Jurassic rocks. Australia and surrounding islands, North America, and Aves is defined as the most recent common ancestor South America. Their earliest appearance in the fossil of all extant birds, and all of that ancestor’s descendants. record is in the Cretaceous of North and South America, There are approximately 9700 species of extant birds. and fossils are known from all continental landmasses. In traditional classifications, Aves was considered to be Marsupials differ from other mammals in a number of a separate class of vertebrates, equivalent in rank to the physiological and anatomical features, especially those Amphibia, Mammalia, and Reptilia. Cladistic classifica- related to reproduction. The gestation period in marsu- tions recognize birds as a distinctive group of verte- pials is very short compared with that of other mammals brates, but one that is nested within Reptilia, specifically and the young are born in a nearly embryonic state. within the Dinosauria. Although not accepted by all After birth, development takes place in a pouch (or ornithologists, there is strong morphological support sometimes under a fold of skin) on the mother’s abdo- for this hypothesis. Birds and dinosaurs share such mor- men. The Placentalia includes a diverse assemblage of phological features as an in-turned femoral head, oppos- mammals that include many of the most familiar mam- able thumb, and a perforate acetabulum. An additional mals and the only mammals to adopt a completely or suite of characters indicate that birds are nested within predominantly marine lifestyle (whales, dolphins, por- theropod dinosaurs. Aves (as defined above) is diag- poises, seals, sea lions, walruses) and to achieve pow- nosed by the loss of teeth, the presence of a pneumatic ered flight (bats). Human beings are members of a pla- foramen in the humerus (upper arm bone), and fusion cental mammal group, the Primates. of uncinate processes with the ribs. Most extant bird lineages appear in the fossil record at least by the early Cenozoic, and several are reported from the Cretaceous. See Also the Following Articles AMPHIBIANS, BIODIVERSITY OF • BIRDS, BIODIVERSITY OF • M. Mammalia ENDANGERED BIRDS • ENDANGERED MAMMALS • ENDANGERED REPTILES AND AMPHIBIANS • FISH Mammalia is defined as the most recent common ances- BIODIVERSITY OF • MAMMALS, BIODIVERSITY OF • REPTILES, tor of Monotremata and Theria (marsupials plus placen- BIODIVERSITY OF tals), and all of that ancestor’s descendants. Mammalia is diagnosed by a large number of anatomical and physi- ological features, including the presence of mammary Bibliography glands and a unique jaw joint. Mammary glands in Bardack, D. (1991). First fossil hagfish (Myxinoidea): A record from females produce milk to nourish the rapidly growing the Pennsylvanian of Illinois. Science 254, 701–703. young during postnatal development. In most verte- Benton, M. J. (1997). Vertebrate Paleontology, 2nd ed. Chapman & Hall, London. brates the jaw joint is formed between the quadrate Briggs, D. E. G., Clarkson, E. N. K., and Aldridge, R. J. (1983). The bone of the skull and the articular bone of the lower conodont animal. Lethaia 16, 1–14. jaw, but in mammals, the jaw joint is formed between Cannatella, D. C., and Hillis, D. M. (1993). Amphibian relationships: 766 VERTEBRATES, OVERVIEW

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