Vertebrata

As noted above, the lampreys, or Petromyzontoidea, represent the most basal living vertebrates. Several important synapomorphies mark this group. All verte­brates have at least two semicircular ducts in the inner ear, structures concerned with improving balance and position of the organism (the single duct in hagfishes possibly represents a secondary simplification of the two present in vertebrates, rather than being the primitive condition).

Several extinct early vertebrates have extensive fossils records, and were clearly the dominant forms during early vertebrate history. Several of these groups are rec­ognized as being more closely related to more derived vertebrates. One particularly interesting group are the conodonts, which for nearly 200 years were considered as “invertebrates.” Recent fossil evidence clearly indi­cates that not only are they vertebrates, but according to some authors, they are more derived than lampreys. Several other extinct groups possessed excessive dermal bone arranged as protective broad plates or shields, par­ticularly around the head, and so are termed “ostraco- derms.” These, mentioned only in passing here and excluded from Figure 1.2, include Heterostraci, Ana- spida, Osteostraci, and various others. A textbook will provide further discussion of their anatomy and phylo­genetic relationships.

The remaining vertebrates form the clade Gnathosto- mata (Figure 1.3; ancient Greek, gnathos, jaw, and stoma, mouth). As their name implies, gnathostomes have jaws, structures that are modifications of an ante­rior or mandibular pharyngeal arch (see below). Their development was a significant evolutionary advance­ment, perhaps the most important in vertebrate history, because jaws controlled by muscles allow animals to grasp objects firmly.

The familiar group of vertebrates that possess these fea­tures, at least initially, are the fishes, which are also the earliest and in many ways among the most primitive gnathostomes. Most people know what a fish is, but few recognize that not all fishes are the same with respect to their relationships to other vertebrates. Although they were once all included as “Pisces,” they do not form a natural group because some possess features that indi­cate a common ancestry with tetrapods. Therefore, if “Pisces” were to be retained as a formal term, then the tetrapods would have to be included in the taxon, but it would then be equivalent to Gnathostomata (however, see below).

Fish, by and large, all have a similar way of getting on in the world, and it should thus be clear that our every­day concept of fish represents a grade rather than a clade.

The most primitive fishes are the extinct Placodermi. Placoderms (from the ancient Greek placo, plate, and derma, skin) had several large plates covering the head and anterior part of the trunk. These armored head and trunk sections were linked by a movable joint. Placo- derms were generally small (though some were giants, reaching 6 m in length) and possessed extensive dermal coverings, as did the “ostracoderms,” but they share numerous features that unite them with all other gnathostomes, including jaws and paired fins. There is, however, considerable question as to the homology of their jaws with those of other jaw-bearing vertebrates. Various differences in the masticatory apparatus, such as an internal rather than external position for the jaw muscles, may indicate that jaws were independently derived in placoderms and other gnathostomes. If so, the immediate common ancestor of these two groups may have lacked functional jaws. Placoderms had numerous shared derived characters that indicate that they form a monophyletic group, such as a unique joint in the neck that allowed the head to be lifted and a dis­tinctive upper jaw articulation. Most authors consider placoderms as the sister group to all remaining gnathos- tomes, as is done here, but some regard them as united with the cartilaginous fishes, the Chondrichthyes (see below), in a monophyletic group.

In the remaining gnathostomes, the Eugnathostomata, the second visceral arch is modified into a hyomandibula, a supporting element for the jaw (Figure 1.3).

FIGURE 1.3 Cladogram showing phylogeny of the Vertebrata. Some Synapomorphies of the main groups are provided in the boxes below the cladogram.

features in their basic anatomy. The near absence of bone, however, is not primitive, but a secondary loss. The combination of this condition and of ancestral features is a main reason why the shark is used so extensively for dissection: The primitive features allow an under­standing of the basic vertebrate systems, and the special­ized absence of bone facilitates the dissection of these systems.

The Elasmobranchii includes the sharks and rays. Tra­ditionally these were considered monophyletic groups, with the Squalomorpha including sharks and Batoidea including skates and rays. However, the former may not be monophyletic, with some being more closely related to batoids than to other sharks. Elasmobranchs (from the ancient Greek elasmos, thin plate, and branchia, gills) have partitions between the pharyngeal slits that bear the gills. The holocephalians (chimaeras or rat­fishes) differ in having a fleshy operculum covering the slits. Also, the upper jaw is fused to the braincase, a feature from which the group gets its name (holo- cephalian: from the ancient Greek, holos, whole, and kephale, head), whereas the upper jaw is separate from the braincase.

The Teleostomi includes the bony fishes and tetrapods (Figure 1.3). The bony fishes, as their name implies, retained and improved on a bony skeleton. The acan- thodians are a relatively minor group of very early, extinct bony fishes, characterized by long stout spines associated with their paired fins, of which more than two were often present. The other two major radiations of bony fishes form a clade (including the tetrapods) termed the Osteichthyes, and include the Actinopterygii and Sarcopterygii (Figures 1.3, 1.4). A lung or air sac is considered a primitive trait for this group. From it a swim bladder evolved in some derived bony fishes.

The Actinopterygii (Figure 1.4) or ray-finned fishes are the most diverse and numerous vertebrates (about half of all living vertebrates are actinopterygians) and inhabit nearly all aquatic habitats. Their fins are supported internally by lepidotrichia or rays and are controlled by muscles that lie within the body wall. Actinopterygians include a staggering diversity of fossil and living forms, and only the most general of evolu­tionary outlines of living actinopterygians is possible here, with additional detail provided in Figure 1.3. Several major groupings may be recognized. The most basal is the Polypteriformes (= Cladista), which include Polypterus (bichir). They retain several of the early fea­tures of early actinopterygians, such as ganoid scales, well-ossified skeleton, and paired ventral lungs (air sacs) connected to the pharynx for aerial respiration. Many students are surprised that lungs would be important in fishes, but aerial respiration is so important that bichirs drown if deprived of it.

The Actinopteri includes more derived actinopterygians, with the Chondrostei—sturgeons and paddlefishes, as well as extinct relatives—representing the basal forms of this clade. The Neopterygii are the sister group to chondrosteans. The Lepisosteidae (gars) are basal neopterygians. The sister clade to lepisosteids is com­posed of a relatively small group, Amiidae, which includes the bowfins, and the Teleostei, which includes the most advanced actinopterygians.

Earlier classifications recognized three groups of actinopterygians, the chondrosteans, “holosteans,” and teleosteans, as reflecting a sequence of primitive, intermediate, and advanced actinopterygians. These cat­egories were more properly evolutionary grades, with “holosteans” including the lepisosteids and amiids (see Figure 1.4), and are useful in following, in broad outline, some of the main trends in actinopterygian evo­lution. These include changes in the feeding apparatus, fin form and position, and body shape.

The feeding apparatus of bony fishes is structured so that the lower jaw was primitively capable only of simple lowering and closing. In this system, the upper jaw was fused to the braincase. The upper and lower jaws were long, with the articulation far back under the skull, permitting a wide gape. These features are reflected by the orientation of the hyomandibula, which sloped posteroventrally. The feeding apparatus under­went modifications, resulting in a complex kinetic system in which the jaws are protruded and allow iner­tial suction feeding. The main anatomical changes are that the jaws shortened, so the hyomandibula swung forward to assume, in advanced teleosts, an anteroven- tral orientation. The maxilla, a bone of the upper jaw, was freed from the jaw margin and functions as a lever in participating in movements of the premaxilla, the most anterior element of the upper jaw. Inertial suction feeding opened up numerous opportunities and is one of the main features cited in the success of actinopterygians. Associated changes occurred in the position and form of the fins and of the body. Primi­tively, the tail was heterocercal and the paired fins were in positions similar to that in the sharks: relatively vental, with the pectoral fins lying anteriorly and pelvic fins posteriorly. Also, the body is, again as in sharks, fusiform, or torpedo-shaped. These features make for fast swimming. In teleosts, the pectoral fins are moved dorsally and the pelvic fins anteriorly. The tail is homo­cercal (superficially symmetrical) and the body laterally compressed. These changes allowed for different swim­ming styles, with considerably more precision control (for example, the dorsal position of the pectoral fins allows them to function as “brakes”). These changes were also instrumental in the great radiation of actinopterygians.

The sister group of the Actinopterygii is the Sar- copterygii, the second group of bony fish (but including tetrapods), which possess paired fins with internal skele­tal support and muscles, and so are known as the lobe- finned fish (Figure 1.5). As fish, sarcopterygians were never as diverse or successful as the actinopterygians. As a clade, however, sarcopterygians are extremely suc­cessful, owing to the radiation of tetrapods. The fleshy fins of sarcopterygian fishes were not used for walking on terrestrial environments, but for maneuvering in shallow waters. Interestingly, a group of living sar- copterygian fishes, ceolocanths (see below), swim by moving their fins the same way a terrestrial vertebrate uses its limbs to move on land.

Other sarcopterygian synapomorphies are provided in Figure 1.4. The most basal clade is the Actinista or coelocanths, represented only by two living species. Its sister group, the Rhipidistia, includes the Dipnoi and Choanata (Figure 1.5). Dipnoans are the lungfishes, of which only three genera survive. The choanates include several fossil groups, which are not considered here, and the Stegocephali, all marked by, among other features, true internal nostrils. Prestegocephalian choanates include several fish groups. The sister group to stego- cephalians are the Elpistostegidae, which are notable for an elongated humerus and loss of the dorsal and anal fins. Among the earliest stegocephalians are the Acan- thostegidae and Ichthyostegidae, which possessed fully developed limbs with more than five digits (fingers or toes). Our most recent understanding of these groups indicated that limbs first evolved in vertebrates that lived almost entirely in an aquatic environment. It is thought that the limbs were useful particularly in shallow areas, helping maintain the animal’s position so it could wait for prey and allowing it easy access to air. Perhaps these vertebrates could also clamber out of the water to escape predators. After all, the terrestrial envi­ronment would at that time have been relatively free of predators and competition.

A short digression on other phylogenetic schemes is warranted at this point. The phylogenetic arrangement of vertebrates just presented is the conventionally accepted hypothesis. Several recent molecular analyses, however, are challenging this view. One analysis indi­cates that the Chondrichthyes do not occupy a basal position among gnathostomes. Some authors place Chondrichthyes and Placodermi in a single group as the sister clade to Teleostomi, thereby eliminating the Eug- nathostomata as a clade. Another study suggests that, among living gnathostomes, all fishes do indeed form a monophyletic group, to the exclusion of the tetrapods, and thus that the Pisces is a natural group. The inter­ested student is urged to consult the Selected References for further information (e.g., Arnason et al., 2004; Martin, 2001).

We may return to our discussion of stegocephalians (Figures 1.5, 1.6). Omitting several fossil groups for simplicity, we recognize a major stegocephalian clade, the Tetrapoda, defined as the clade that includes the last common ancestor of living amphibians and amniotes (see below). Tetrapods were and have remained mainly amphibious or terrestrial, although advanced members of several lineages have reverted to a mainly or entirely aquatic existence (e.g., the extinct ichthyosaurs among reptiles and the whales among mammals), and others are capable of flight (e.g., birds and the extinct pterosaurs among reptiles and bats among mammals). They share (together with several groups omitted here) five or fewer digits. Two tetrapod clades, the Amphibia and the Amniota, may be recognized.

Amphibians (from the ancient Greek amphi, both, and bios, life) are so called owing to the duality of their lifestyle—often a larval aquatic stage and a terrestrial adult stage are present. Amphibians are often viewed as intermediate between fishes and amniotes, mainly because their reproductive strategy is still tied to an aquatic environment (though this is not true of all amphibians), whereas amniotes’ reproduction is more nearly independent of water. This general impression is true in the sense that amphibians do tend to retain an ancestral reproductive strategy. From this it is a small step to the view that all amphibians, including the living forms, are therefore primitive tetrapods. However, this is both misleading and incorrect. On the one hand, it is wrong to think of any living organism as primitive. A creature may retain ancestral or primitive features, but that does not make the creature itself primitive. Each living organism is the product of long evolutionary history and is a mosaic of both ancestral (primitive) and advanced (derived) features. For example, humans retain bone, an ancestral vertebrate character, whereas sharks are derived (advanced) in the loss of bone. The presence of this ancestral feature does not make humans “more primitive” or “less advanced” than sharks. Using the same logic, frogs are not more primitive than humans just because they retain an ancestral reproduc­tive strategy.

The second misconception is that living amphibians are representative of the lifestyle of the earliest stego- cephalians. In some ways these early forms were inter­mediate between fishes and more derived terrestrial vertebrates, and in the past we have lumped these forms together with living amphibians. But we must be careful. Living amphibians, while retaining an ancestral repro­ductive mode, are clearly very specialized. They are not like the early stegocephalians, and in fact are highly derived vertebrates.

The Amphibia includes several fossil groups as well as the living forms. The latter form the clade Lissamphibia,

FIGURE 1.4 Cladogram showing phylogeny of the Teleostomi. Some Synapomorphies of the main groups are provided in the boxes below the cladogram.

FIGURE 1.5 Cladogram showing phylogeny of the Sarcopterygii. Some Synapomorphies of the main groups are provided in the boxes below the cladogram.

FIGURE 1.6 Cladogram showing phylogeny of the Choanata. Some synapomorphies of the main groups are pro­vided in the boxes below the cladogram. Dashed gray lines denote a paraphyletic group.

a term referring to their nature of their skin (lissos, smooth). The three lissamphibian groups are quite dis­tinct. They are the Salienta (frogs), Urodela (salaman­ders), and Gymnophiona (caecilians). Frogs and salamanders are reasonably familiar vertebrates, and are considered sister groups. Frogs are highly special­ized for saltational locomotion, whereas salamanders retain a more general body form and locomotion. Caecilians are specialized in being legless burrowers or swimmers.

The Amniota includes the remaining tetrapods (Figures 1.6, 1.7). The main innovation of amniotes is the amni­otic egg. Amniote embryos develop within extraembry- onic membranes that are usually encased in a calcareous or leathery egg (the term “anamniotes” refers to verte­brates whose eggs do not have extraembryonic mem­branes). The membranes provide the embryo with a “watery” environment that is protected against desic­cation, and thus amniotes’ reproduction has become essentially independent of an aqueous environment in which vertebrates ancestrally reproduced (however, a relatively moist environment is still essential).

The amniotes (Figure 1.7) include two great lineages, the Reptilia (ignoring some fossil members) and Synap- sida, which have followed independent evolutionary paths since the early history of amniotes. The synapsids include mammal-like reptiles and mammals. The latter, the Mammalia, are the living synapsids. One mam­malian group is the Monotremata, a relatively small clade, including the echidnas and platypus, that retains the ancestral reproductive strategy of laying eggs. The other group, the Theria, includes the marsupials

FIGURE 1.7 Cladogram showing phylogeny of the Tetrapoda. Some Synapomorphies of the main groups are provided in the boxes below the cladogram. Dashed gray lines denote a paraphyletic group.

(Marsupialia) and the placental mammals (Eutheria). These mammals have evolved reproductive modes where embryos are retained in and nourished by the mother’s body.

The Reptilia includes the typical living and fossil rep­tiles, such as turtles, lizards, snakes, and crocodiles, along with other familiar and mainly extinct groups, such as dinosaurs (which includes the birds), pterosaurs, and ichthyosaurs. Several groups may be recognized. The turtles (Testudines) apparently are the sister group to all other reptiles (though recent molecular evidence contradicts this, suggesting turtles may be more closely related to dinosaurs and crocodiles than was previously thought). The remaining living reptiles are usually placed in the Sauria, which includes Archosauromorpha (crocodiles and birds) and Lepidosauromorpha (lizards and snakes).