C H A P T E R

1
Craniata and Vertebrata
The vertebrates or Vertebrata form an ancient group of descent. As hypotheses, they are testable and thus
with a history spanning some 545 million years. On the open to falsification when new data become available. If
one hand, they include the organisms most familiar to a hypothesis is falsified, then another one may be
us, such as fish, birds, cats and dogs, as well as humans; proposed—for example, new evidence might show that
on the other, few people are aware of the great diversity humans share a recent common ancestor with a different
in their form, structure, and habits. Indeed, they include great ape than chimpanzees, such as orangutans.
some of the largest and more complex organisms ever
evolved. But vertebrates are part of a larger grouping of
animals, and to understand their history and the devel- PHYLOGENY AND CLASSIFICATION
opment of their structure, they must be placed in phy-
logenetic context. For most of the past 250 years, the classification of organ-
In discussing vertebrates, several other groups of isms has followed the Linnean system, which uses ranks
organisms are usually considered. A monophyletic or to designate levels of organization of the organisms being
natural group (see later) of organisms is referred to as a classified. Most readers will be familiar with the main
taxon (plur., taxa). The taxa related (in terms of recent formal Linnean ranks, ordered hierarchically from most
common ancestry) to vertebrates include Echinodermata to least inclusive: Kingdom, Phylum, Class, Order,
(sand dollars, sea lilies, star fish, sea cucumbers, urchins), Family, Genus, and Species. Researchers have differed in
Hemichordata (acorn worms and pterobranchs), Uro- assigning rank to the vertebrates and their relatives. For
chordata (tunicates or sea squirts), and Cephalochordata example, some authors have recognized three phyla:
(amphioxus). These are the typical nonvertebrate (or Phylum Echinodermata, Phylum Hemichordata, and
“invertebrate”) relatives of the group in which we are Phylum Chordata. Others consider Urochordata and
mainly interested. The vertebrates themselves, or Verte- Cephalochordata as phyla on their own, separate from
brata, are included in a larger taxon termed Craniata. Chordata. Still others have viewed Urochordata as a
Within Craniata and Vertebrata are many taxa. These separate phylum, but Cephalochordata as a subphylum
taxa and the evolutionary relationships among them (see of the Phylum Chordata. If you find this confusing,
Figure 1.1) are briefly outlined here to provide an orga- you’re not alone! The different designations did—or at
nizational framework for undertaking the dissection of any rate were meant to—have some grounding in bio-
the vertebrates discussed in this manual. Before this, logical reality. They reflected a particular researcher ’s
however, it is necessary to present an explanation of perception of the magnitude of the difference in the
several important terms used in discussions of phylogeny. levels of organization (a quality that may be referred to
Phylogeny refers to the pattern of descent among taxa. It as a grade) among the taxa under consideration. Thus, if
describes, in other words, the evolutionary or genealogi- a taxon was considered a phylum, it mainly implied that
cal relationships among them. Evolution is a historical its members had a fundamentally different basic body
(and on-going) process. Therefore, the evolution of plan than if it was considered only a subphylum of a
organisms occurred in only one way—for example, larger taxon. As you have probably already realized,
humans and chimpanzees are, among living creatures, researchers’ perceptions along these lines are subjective.
either each other ’s closest relatives (they share a common In recent years, however, the formal Linnean ranking
ancestor not shared by other organisms) or they are not. system has fallen increasingly into disuse as systematists
Only one of these possibilities is correct. Evolutionary have become aware that there is no intrinsic or special
biologists try to recover the pattern of descent based on value of any particular taxon that would justify its recog-
the data they have available to them. Phylogenies are nition as a higher or lower rank, compared to other taxa.
therefore hypotheses that approximate the true pattern In other words, there is no special reason for “elevating”

The Dissection of Vertebrates, Second Edition DOI: 10.116/B978-0-12-375060-0.00001-2 1 © 2010 Elsevier Inc.
2 1. CRANIATA AND VERTEBRATA

PROTOSTOMATA DEUTEROSTOMATA

ECHINODERMATA PHARYNGOTREMATA

HEMICHORDATA CHORDATA

UROCHORDATA SOMITICHORDATA

ENTEROPNEUSTA PTEROBRANCHIA CEPHALOCHORDATA CRANIATA

DEUTEROSTOMATA PHARYNGOTREMATA CHORDATA

• first embryonic opening becomes anus; • pharyngeal skeleton • endostyle

second opening becomes mouth • pharyngeal slits • dorsal, hollow nerve cord
• basally, mesoderm forms bilaterally as • blood vascular system • notochord
out-pocketing of embryonic gut; coelom, • postanal tail
which develops within mesoderm, thus
originally has connection with gut
• basally, a ciliated looped band is present on
surface of larva

FIGURE 1.1 Cladogram showing phylogeny of Deuterostomata. Some synapomorphies of the main groups are provided in the boxes below
the cladogram.

birds or Aves to the rank of Class, equal and thereby that they share this feature because they have inherited it
excluded from, the Class Reptilia. In fact, it is improper from a common ancestor, rather than each having evolved
to do so, because the birds are properly part of the taxon the character independently, and so infer that the taxa are
named Reptilia. Here, formal ranks are not used, and descendants of the same ancestor (which we are not able
taxa are referred to simply by their name (except for the to actually recognize, and thus refer to as hypothetical).
preceding paragraph, in which ranks were used to reflect Biologists use many characters in trying to reconstruct
the historical understanding of the groups). phylogeny. The practice is complicated by the fact that
Formal names are applied to natural or monophyletic organisms can and do evolve very similar characters
groups. A monophyletic group includes an ancestor and independently of each other, an occurrence referred to as
all of its descendants (provided that the phylogeny has homoplasy. In reconstructing phylogeny, a researcher con-
been carefully reconstructed). Such groups are termed siders the totality of evidence. It is rare that only a single
clades. Clades are recognized based on common ancestry. character can be used to reconstruct phylogeny.
If two taxa are in a clade, it is because they are linked by The pattern of relationships among taxa is depicted
a common ancestor. Biologists infer such ancestral rela- visually by a cladogram, which is essentially a diagram
tionships through the presence of shared derived charac- of nodes and branches, with the nodes representing
ters or synapomorphies (see later). If two (or more) taxa ancestors and the branches that diverge from a node
share a character that is exclusive to them, then we assume representing the descendant taxa of the ancestor.1 The

1
Technically, nodes are speciation events of one ancestor into two or more descendant or daughter species. The root and internodes
(segments between the nodes) represent the common ancestors and loci of character transformations.

THE DISSECTION OF VERTEBRATES

 PHYLOGENY AND CLASSIFICATION 3
node, then, may be thought of as representing the hypo- derived trait, it is described as synapomorphic. Synapo-
thetical ancestor of the two taxa that diverge from it. The morphies do indicate phylogenetic relationship. In the
pattern of branching represents the pattern of relation- most basic sense, sharing a derived trait is a shorthand
ship. Examine the cladogram in Figure 1.1. Note the way of saying that the organisms under consideration
node from which the Hemichordata and Chordata possess a modified trait because it was inherited from an
diverge. This node represents ancestor species that split ancestor that first acquired or evolved the modification.
to produce two lineages, one that evolved into Chordata An assortment of organisms united by synapomorphies
and the other into Hemichordata. The two branches that forms a natural group or clade; that is, the clade is a real
diverge from this ancestor represent the evolutionary entity in evolutionary terms. It means that all the organ-
paths to the divergent taxa. isms included within the clade were ultimately derived
Only the branching pattern is of concern. The length from the same ancestor. All vertebrates that possess jaws
of the branches is immaterial in terms of absolute time, do so because this character was inherited from an ances-
but relative time is implied by branching sequence. tor that had evolved jaws as a modification of the man-
Clearly, the divergence of Cephalochordata and Crani- dibular arch (see later). If we wish to understand the
ata occurred after the divergence of Hemichordata and relationships among a lamprey, a fish, and a dog, the
Somitichordata. presence of jaws is a character state that indicates that
Informal names, set between quotation marks, are the dog and fish are more closely related to each other
used to designate a group of organisms that do not than either is to a lamprey. When two groups are each
descend from the same common ancestor, but that do other ’s closest relatives, they are said to be sister groups.
possess (or lack) some of the features of the taxon in A natural or monophyletic group may be recognized
which we are interested. Many of these terms were con- formally by a name. The only restriction imposed is that
sidered formal names in earlier classifications. For a monophyletic group include the ancestor and all
example, the term “protochordates” is commonly used descendants of the ancestor, even though the ancestor
to refer to the hemichordates, urochordates, and cepha- cannot be identified. A monophyletic group may also be
lochordates. Grouping them together is a shorthand way termed a clade, from which is derived the term cladistics.
of referring to them as close relatives of chordates (no An alternate name for cladistics is phylogenetic system-
quotation marks here, so this is the vernacular form of atics. Cladistics is the methodology that recognizes
the formal name Chordata), and that they lack various shared derived traits as the only valid indicators for
characters that chordates possess. We must be clear that inferring phylogenetic relationships.
informal groups, though convenient, do not reflect phy- The third type of similarity is termed homoplasic and
logeny; they are not monophyletic. results from morphologically similar solutions to par-
In discussing how biologists reconstruct phylogeny, ticular selection pressures. For example, the fusiform
the nature of the similarity among organisms must be body shape of fishes and of porpoises, which are
considered, because it is necessary to differentiate mammals, is not due to inheritance from a common
between those similarities that are useful in reconstruct- ancestor, but to selection pressure to adopt a form suit-
ing phylogeny and those that are not. One kind, termed able for moving efficiently through water. Such similar-
plesiomorphic, refers to similarity based on presence of ity does not indicate phylogenetic relationship, although
ancestral conditions or states. Consider the Vertebrata, in some cases the similarity may be so profound that it
in which the presence of vertebrae is an ancestral may lead us inaccurately to attribute its cause to phylo-
feature—in other words, it was present in the common genetic proximity (i.e., recent common ancestry). The
ancestor of all vertebrates. These structures may inform reliable method of recognizing homoplasy is to identify
us that all vertebrates share a common ancestor, but it as similarity in different monophyletic groups, follow-
their presence per se cannot be used to decipher the ing, of course, a phylogenetic analysis.
relationships among vertebrates. As a practical example, In addition to clades or monophyletic groups, we may
let us consider a turtle, a bird, and a mammal. All possess speak of grades, which are not natural groups. A grade
vertebrae, and are therefore vertebrates, but the pres- recognizes a group of organisms based on a comparable
ence of these structures does not allow us to say which level of organization or complexity. A new grade may
two of these forms are more closely related to each other be achieved through the accumulation of a number of
than either would be to the third. This similarity, there- derived characters so that a new mode of living is made
fore, is due to the retention of a trait that is ancestral for possible. In the past, some groups were formally recog-
vertebrates. When an ancestral character is shared by nized, but they were united essentially because their
various forms, it is described as symplesiomorphic. members shared a particular grade of evolution. We
A second kind of similarity is due to the inheritance of now recognize such groups as artificial rather than
a modified character state. Such modification is consid- natural. An artificial group is one that does not include
ered derived or apomorphic. When organisms share a an ancestor and all of its descendants or combines two

THE DISSECTION OF VERTEBRATES

4 1. CRANIATA AND VERTEBRATA

or more groups while excluding one or more ancestors the phylogeny outlined here follows the traditionally
(e.g., “Haemothermia” = mammals + birds). recognized scheme based primarily on morphology. Be
Probably the most familiar example is the case of aware, however, that several recent analyses based
Reptilia. Formerly, Reptilia included living and fossil mainly on mitochondrial or ribosomal gene sequences
crocodiles, turtles, snakes, lizards, as well as their extinct do not corroborate this scheme. Such discrepancies are
relatives, such as dinosaurs, pterosaurs, and plesiosaurs. noted appropriately later.
The Class Reptilia was given a rank equivalent to that To review, the main clades of deuterostomes are the
of Aves (birds) and Mammalia (mammals), even though echinoderms, hemichordates, urochordates, cephalo-
the ancestors (and early relatives) of these two groups chordates, and craniates (see Figure 1.1). It may seem
were considered reptiles. As so defined, however, Rep- surprising that the echinoderms, seemingly so different
tilia is not a natural group because it does not include from what we usually think of as vertebrates, are closely
all of its descendants, as the birds and mammals are related to vertebrates and are included with them in
excluded (and each placed in a group of equal rank). Deuterostomata. As noted earlier, however, they are
Current usage of Reptilia varies. As its traditional clearly united by strong similarities in early develop-
concept is so embedded in our thinking, some authors mental patterns.
have preferred to abandon it entirely for formal pur- One group traditionally recognized in vertebrate
poses (and prefer to use Sauropsida) but retain it in its history is Chordata, which includes Urochordata, Ceph-
colloquial sense. In this latter meaning, “reptile” repre- alochordata, and Craniata. One reason Chordata has
sents a grade that includes cold-blooded amniote tetra- been considered particularly important is that there are
pods, with scales (lacking hair or feathers); that is, the several easily recognizable characters that are clearly
features we usually associate with living reptiles such as shared by chordates. Without belaboring the point, such
turtles, crocodiles, snakes, and lizards. Other authors distinctions as “important” or “major” often imply a
redefine Reptilia as a formal group that includes the status that may not be justified. There is no real reason
typical reptiles and birds. The more basal fossil allies of why the chordates should be considered more “impor-
mammals, termed mammal-like reptiles, are excluded tant” than the next most inclusive group, for example. It
from the Reptilia and properly united with their mam- is more a matter of convenience and tradition and,
malian descendants in Synapsida. perhaps, that we have only recently begun to fully com-
The discussion given here provides the basic back- prehend that all branches in the tree of life may be con-
ground information required to interpret cladograms sidered equally important.
and how they are constructed. For more detailed discus- In any event, beginning with Chordata is convenient.
sions on cladistics and classification, consult a text in The chordates are united by the presence of the following
comparative anatomy that provides more detailed expla- synapomorphies: an endostyle; a dorsal, hollow nerve
nations of these concepts. Liem et al. (2001) provide a cord; a notochord; and a postanal tail. Another feature
particularly thorough discussion. important in chordates is the presence of pharyngeal
slits, although this feature is not exclusive to them (see
Figure 1.1). These features are present at some point
VERTEBRATE RELATIVES during the lives of all chordates, although they may be
expressed to varying degrees and restricted to part of the
All the taxa mentioned so far belong to Deuterostomata, life cycle in different vertebrate groups, or modified in
a major clade of coelomate triploblastic metazoans, mul- derived members. Humans, for example, do not possess
ticellular animals that possess three primary body layers a tail (an obvious one, at any rate), notochord and pha-
(ectoderm, mesoderm, and endoderm) and have a true ryngeal slits; but pharyngeal pouches, a notochord, and
body cavity that houses the viscera. The other major a tail are transient features that are present during embry-
clade is Protostomata, which includes annelids, arthro- onic development. The endostyle is represented by its
pods, mollusks, and many other groups. homologue, the thyroid gland.
The synapomorphies (shared derived characters) of Pharyngeal slits are bilateral apertures that connect
deuterostomes that indicate they are a clade are mainly the pharynx (essentially the “neck” of the animal), which
similarities of early embryonic development (see Figure is the anterior part of the gut, with the outside. In forms
1.1). They include type of cleavage of the fertilized egg, that are familiar to us, such as fish, the slits are part of the
pattern of mouth and anus formation, and formation of respiratory, or gas exchange, system: The gills reside on
the mesoderm and coelom (body cavity). The clades the walls of the slits and perform gas exchange as water
within Deuterostomata share these features, but several passes over them. In some fishes, like sharks, the slits
of them have become modified in some derived members. open individually onto the surface of the body; in most
Next, we must consider the pattern of relationships, other fishes, the slits open into a common chamber that
or phylogeny, among deuterostomes. For the most part, then leads out to the surface of the body by a common

THE DISSECTION OF VERTEBRATES

 VERTEBRATE RELATIVES 5
opening. Originally the slits did not function in gas Cephalochordate species commonly are referred to as
exchange. Ancestral vertebrates were suspension or filter amphioxus (which means sharp at both ends) or lancelet
feeders (as are urochordates and cephalochordates) and (little spear). Given the fact that these little creatures
the slits were the means for allowing water to exit the essentially lack a head and so are pointed at both ends,
oral cavity and pharynx. As water passed out of the amphioxus is an especially appropriate designation.
pharynx through the slits, food particles were filtered out Although amphioxus has a fish-like body (see later), it
and directed toward the rest of the digestive system. The is not an active swimmer as an adult. Instead, it burrows
endostyle, a midventral groove (on the floor of the into the substrate, usually just out from sandy beaches,
pharynx), has ciliated cells that secrete mucus, which is and assumes a position with only its mouth exposed. Its
spread around the walls of the pharynx. Food particles filter-feeding lifestyle is similar to that described earlier
suspended in the water are trapped by the mucus, and for ancestral vertebrates. Intake of water and its move-
the water then leaves the pharynx through the slits. The ment through the pharynx is accomplished by ciliary
mucus and entrapped food particles are then passed action. The pharynx has numerous slits that collectively
back into the digestive system. The slits and endostyle empty into a surrounding chamber, the atrium, before
were thus originally part of the feeding mechanism. leaving the body through a common opening. The endo-
The notochord is a relatively thin, rod-like structure style secretes mucus, which traps food particles sus-
extending dorsally along the length of the trunk and tail pended in the water.
in less derived chordates. It is an important support Taxon including Cephalochordata and Craniata is
structure, and the name Chordata is derived from noto- termed the Somitichordata (Figures 1.1 and 1.2).
chord. It is a hydrostatic structure, consisting of a fibrous Although there are several differences between these
sheath that encloses a fluid-filled central core. It is flex- sister groups, we are interested in their synapomorphies,
ible along is length, but, as it is filled with fluid, cannot for these features provide evidence of their shared ances-
easily be compressed anteroposteriorly (or telescoped). try. Among these characters are similarity in develop-
The notochord provides support for the body and allows ment of mesoderm, including the hypomere (or lateral
the side-to-side locomotory movements characteristic of plate mesoderm) and mesodermal somites, which
less derived vertebrates. In derived vertebrates, the develop into myomeres (segmented blocks of trunk
notochord is largely replaced functionally by the bone musculature, which in amphioxus extends through to
of the vertebral column. It is present embryologically; the anterior tip of the body); arrangement of the circula-
and in adult humans, notochordal tissue may persist as tory system, with dorsal and ventral aortae; and seg-
part of the intervertebral disks that lie between succes- mentally arranged spinal nerves. Some researchers also
sive vertebrae. recognize the retention of larval features—the noto-
The presence of a tubular nerve cord enclosing a chord, the nerve cord, and the postanal tail—as synapo-
fluid-filled central canal occurs only in chordates. There morphies. Others, however, consider these as retention
are additional distinctive features about the chordate of ancestral features rather than a novel development,
nerve cord. It is formed by an embryological process and that the loss of these features in Urochordata, the
called invagination, a rolling and sinking into the body sister group of the somitichordates (see later), is derived.
of ectodermal tissue. Further, it is dorsal to the digestive The urochordates are the next most related group,
tract, whereas in most nonchordates the nerve cord is sharing a common ancestor with Somitichordata. Uro-
solid and ventral. chordates include sea squirts or tunicates, which are
The postanal tail is a continuation past the anus of the sessile, sac-like organisms as adults. In the larval stage,
trunk musculature and notochord. This extension is an however, all four chordate characters, plus the pharyn-
important development that allows the locomotion par- geal slits, are present. Predictably, the three characters
ticular to vertebrates. A few chordates do not possess a lost in adults—the tail, notochord, and nerve cord—are
postanal tail as adults (e.g., frogs), but a tail is present in used in locomotion by the free-swimming larva as it
nearly all chordate larvae. searches for a suitable place to anchor itself to metamor-
Cephalochordata is usually considered the sister phose into the adult form. During this transformation,
group to the craniates, a phylogenetic arrangement the tail is absorbed, along with the nerve cord and noto-
reflecting the idea that vertebrates and cephalochordates chord, of which only small remnants remain in the adult.
share a common ancestor. All four chordate characters, The name Urochordata is derived from the fact that the
plus the presence of pharyngeal slits, are clearly present notochord is present in the tail (from the ancient Greek
during the life of a cephalochordate. The name Cepha- uron, tail). Conversely, the pharyngeal region expands
lochordata is derived from the presence of a notochord dramatically into a barrel-shaped structure with numer-
extending from the tail nearly to the tip of the head ous slits. Water and suspended food particles are drawn
(from the ancient Greek kephalos, head). The commonly into this “barrel,” which is lined with mucus from the
studied cephalochordate is Branchiostoma lanceolatum. endostyle. Food particles are trapped by the mucus, and

THE DISSECTION OF VERTEBRATES

6 1. CRANIATA AND VERTEBRATA

CHORDATA

UROCHORDATA SOMITICHORDATA

CEPHALOCHORDATA CRANIATA

MYXINOIDEA VERTEBRATA

PETROMYZONTOIDEA GNATHOSTOMATA

SOMITICHORDATA CRANIATA VERTEBRATA

• hypomere (or lateral plate mesoderm) • anterior enlargement of nervous system, forming • vertebrae or their rudimentary precursors
• mesodermal somites tripartite brain • two semicircular ducts in inner ear
• myomeres (segmented blocks of trunk • enlargement of specialized sensory organs: nose, • musculature associated with fins
musculature) in trunk and tail eyes, ears • pineal eye
• blood circulation through gills from ventral aorta • braincase protects and supports brain and sense • hypoglossal nerve
to dorsal aorta organs
• segmentally arranged spinal nerves • neural crest
• neurogenic placodes
• muscular action moves water through pharynx

FIGURE 1.2 Cladogram showing phylogeny of Chordata. Some synapomorphies of the main groups are provided in the boxes below the
cladogram.

water leaves through the slits into the atrium, the stable. Molecular evidence has been mounting over the
chamber surrounding the pharynx. last decade that points to a monophyletic relationship of
This arrangement is the traditionally accepted phylo- hemichordates with echinoderms; as well, morphologi-
genetic scheme and finds recent support in the work of cal evidence suggests monophyly. Hemichordates com-
Stach (2008). Some, however, reverse the positions of prise two clades, Enteropneusta (acorn worms) and
Urochordata and Cephalochordata, with the former con- Pterobranchia, both of which are marine animals. The
sidered the sister group to Craniata. One recent study acorn worms are reasonably diversified and well known,
removed cephalochordates from Chordata, and consid- but the pterobranchs are not as well understood. Some
ered them as a sister group to Echinodermata. Compare, but not all pterobranchs have a single pair of pharyngeal
for example, Beaster-Jones et al. (2006) with Delsuc et al. apertures, whereas all acorn worms have several
(2006). such openings. The presence of these slits and embry-
The phylogenetic position of Hemichordata is par- onic invagination of the nerve cord are about the
ticularly uncertain. They were traditionally grouped only definitive evidence of a relationship with the chor-
with the chordates; here, they are considered a sister dates. On the other hand, evidence suggests that echino-
group to the chordates, but this arrangement is far from derms originally had slits as well, although no living

THE DISSECTION OF VERTEBRATES

 CRANIATES AND VERTEBRATES 7
echinoderm possesses them. If this is true, then a mono- are more closely related to gnathostomes than to hag-
phyletic relationship between Hemichordata and Chor- fishes. Following cladistic procedure, the lampreys were
data becomes tenuous indeed. then grouped together with the gnathostomes. Because
lampreys possess rudimentary vertebrae (or, at least,
precursors of true vertebrae), termed arcualia, which are
CRANIATES AND VERTEBRATES essentially cartilaginous blocks on either side of the
nerve cord, most researchers began to restrict the Verte-
Difference of opinion exists in precisely which chordates brata to the lamprey + gnathostome assemblage, with
are to be regarded formally as Vertebrata (Figure 1.2). In the hagfishes considered the sister group to this Verte-
part this is because one of the main characters of verte- brata. An important set of features shared by both hag-
brates is, of course, the presence of vertebrae, a repeating fishes and Vertebrata (lampreys + gnathostomes) is the
series of articulating cartilaginous or bony elements development of a true head (see later), and so the name
forming the spinal column, which provides support for Craniata was applied to this clade. We note in passing
the body, muscular attachment, and protection for the that some researchers have continued to consider the
nerve or spinal cord. Vertebrae form around the noto- Vertebrata as including the hagfishes (while recognizing
chord during embryonic development and enclose the the sister group relationship between lampreys and gna-
spinal cord. thostomes), and so consider Craniata and Vertebrata as
However, not all chordates traditionally included in synonyms. Most recently, however, molecular studies
Vertebrata have complete vertebrae, as just noted; and have not corroborated the morphological evidence.
some have no trace of vertebrae at all. In large part, Instead, these studies suggest that the hagfishes and
which chordates are actually recognized as vertebrates lampreys may indeed be each other ’s closest relative, in
depends largely on the relationships of the most basal which case the “Cyclostomata” would be monophyletic.
living craniates, the hagfishes (Myxinoidea) and lam- The scheme followed here is based mainly on morpho-
preys (Petromyzontoidea), both to each other and to logical evidence and recognizes the Craniata and Verte-
unquestioned vertebrates. The hagfishes and lampreys brata as successive clades (Figure 1.2).
are clearly more derived than cephalochordates, sharing As noted earlier, a major feature of craniates is the
various characteristics with unquestioned vertebrates development of a true head. A distinct anterior enlarge-
(see later). However, they are undoubtedly less derived ment of the nervous system, forming a brain, and of
than the latter in the absence of jaws, the feature to sensory organs occurs in craniates. The brain of craniates
which they owe their designation as “agnathans” (from is tripartite, with three main primary subdivisions; the
the ancient Greek a, without; and gnathos, jaw). Their specialized sense organs—eyes, ears, and nose—are
mouths are circular, so they are also known as “cyclo- complex. These structures are protected and supported
stomes” (round mouth). The undoubted vertebrates, by a bony or cartilaginous cranium or braincase. Closely
united by the fact that they possess jaws, are grouped associated with a head is the neural crest, a unique
together as Gnathostomata (jaw-mouthed). Tradition- feature of craniates. This comprises embryonic tissue
ally, the hagfish and lamprey were considered to be each formed of cells assembled near the developing neural
other ’s closest relative, and so grouped in “Cyclosto- tube that migrate through the embryo to give rise to a
mata” as a formal taxon. As well, several groups of great variety of structures. In the head region, neural
jawless extinct forms were considered more closely crest cells initiate and largely form the vast array of
related to cyclostomes than to gnathostomes, and the cranial structures characteristic of craniates. Another
whole lot of these jawless forms were included in unique feature associated with the head are neurogenic
“Agnatha,” again, as a formal taxon. At this stage of placodes. Placodes are thickenings of the ectoderm
research, the “cyclostomes” (and other “agnathans”) occurring early in embryonic development that differen-
were usually all included in Vertebrata. tiate and help form a variety of structures of the body.
“Agnathans” diversified into many different forms Neurogenic placodes occur only on the head and are
early in craniate history, but only two forms, the hagfish involved in forming sensory receptors and neurons, and
and the lamprey, represent the jawless condition among contribute to the cranial nerves. Thus, the neural crest
living craniates. Many of the early agnathans were and neurogenic placodes, transitory though they may
excessively bony, but most of this bone was dermal and be, are distinguishing features of craniates. Pharyngeal
formed shields or plates that covered and protected the slits are still present, of course, but in craniates they are
body. These forms are informally termed “ostraco- associated with gills and are thus used for gas exchange
derms,” and are not considered in the phylogenies pre- rather than feeding. Yet another innovation of craniates
sented here. is that moving water into the pharynx and out through
About 20 years ago, morphological analyses began to the pharyngeal slits is accomplished by muscular, rather
suggest that lampreys (and some extinct “agnathans”) than ciliary, action (see Figure 1.2).

THE DISSECTION OF VERTEBRATES

8 1. CRANIATA AND VERTEBRATA

EARLY STAGES IN associated with the fins, allowing better control of the
VERTEBRATE EVOLUTION fins and thus of their locomotion through water.
Several extinct early vertebrates have extensive fossil
Before continuing with the phylogenetic story of verte- records, and were clearly the dominant forms during
brates, it is useful to examine the feeding habits of the early vertebrate history. Several of these groups are rec-
earliest vertebrates, as evolutionary innovations of the ognized as being more closely related to more derived
feeding apparatus reflect the major transitions in verte- vertebrates. One particularly interesting group is the
brate evolution. It is generally hypothesized that the conodonts, which for nearly 200 years were considered
earliest step in becoming a vertebrate occurred in crea- “invertebrates.” Recent fossil evidence clearly indicates
tures considered to represent a prevertebrate stage, that not only are they vertebrates, but according to some
although such forms may have qualified as true verte- authors, they are more derived than lampreys. Several
brates. Their precise phylogenetic position, in any event, other extinct groups possessed excessive dermal bone
is not of concern here, because we are interested in arranged as protective broad plates or shields, particu-
feeding mode. The prevertebrate was probably a sus- larly around the head, and so are termed “ostraco-
pension or filter feeder (that is, it filtered food material derms.” These, mentioned only in passing here and
that was suspended in water) and used ciliary action to excluded from Figure 1.2, include Heterostraci, Anas-
generate a current of water into its mouth and out of the pida, Osteostraci, and various others. A textbook will
pharyngeal slits; in other words, a creature very much provide further discussion of their anatomy and phylo-
like amphioxus. It did not have jaws, and its pharyngeal genetic relationships.
bars were probably collagenous. The ciliary pump The remaining vertebrates form the clade Gnathosto-
imposed limits on size, as it restricted the amount and mata (Figure 1.3; Ancient Greek, gnathos, jaw, and stoma,
type of food the animal was capable of ingesting. mouth). As their name implies, gnathostomes have jaws,
The next step involved a change from the ciliary structures that are modifications of an anterior pharyn-
pump with collagenous bars to a muscular pump with geal arch (see later). Their development was a significant
cartilaginous bars. This is the agnathan stage. The com- evolutionary advancement, perhaps the most important
bination of these characteristics meant that the intake of in vertebrate history, because jaws controlled by muscles
water, and thus food, was controlled by active expan- allow animals to grasp objects firmly. The development
sion and compression of the pharyngeal region, which of teeth confer a more certain hold and further allow the
allowed a diversification in size and type of food, and reduction of food to smaller pieces. These abilities
thus of the vertebrates themselves. The cartilaginous, allowed the exploitation of many feeding opportunities.
rather than collagenous, bars were instrumental in this. A second innovation was necessary before vertebrates
Musculature could be used to compress the pharynx, could fully exploit potential new food sources, because
including the bars, but once the muscles relaxed, the the mouth, hence body, must be guided toward an
cartilaginous bars could spring back into shape, expand- object. The control of the body in three dimensions is
ing the pharynx. allowed by the presence of paired fins with internal skel-
The third level of development is the gnathostome etal and muscular support that permitted control of the
stage, which involved the development of jaws. Jaws body in locomotion. A horizontal semicircular duct is
conferred the ability to grasp prey and close the mouth added, so gnathostomes have three semicircular ducts.
to prevent its escape; hence to seek and capture food. Other synapomorphies include the presence of five pha-
These features set the stage for the predaceous, active ryngeal slits and jointed visceral arches. In gnathostomes
lifestyle of vertebrates, in sharp contrast to the sedentary the arches are embedded deep in the body, adjacent to
lifestyles of protochordates. the pharyngeal wall, whereas in “agnathans” they are
not articulated structures and lie superficially, just
beneath the skin toward the outside of the body. The
VERTEBRATA traditional hypothesis on jaw origins considers jaws as
an anterior visceral arch (located close to the original
As noted earlier, the lampreys, or Petromyzontoidea, mouth) that was modified to form upper and lower jaws.
represent the most basal living vertebrates. Several This arch is termed the mandibular arch.
important synapomorphies mark this group. All verte- The familiar group of vertebrates that possess these
brates have at least two semicircular ducts in the features, at least initially, are the fishes, which are also
inner ear, structures concerned with improving balance the earliest gnathostomes. Most people know what a fish
and position of the organism (the single duct in hag- is, but few recognize that not all fishes are the same with
fishes possibly represents a secondary simplification of respect to their relationships to other vertebrates.
the two present in vertebrates, rather than being the Although they were once all included as “Pisces,” they
ancestral condition). Also, vertebrates have musculature do not form a natural group because some possess

THE DISSECTION OF VERTEBRATES

 VERTEBRATA 9

PETROMYZONTOIDEA GNATHOSTOMATA

PLACODERMI EUGNATHOSTOMATA

CHONDRICHTHYES TELEOSTOMI

Elasmobranchii Holocephalia Acanthodii Osteichthyes

GNATHOSTOMATA EUGNATHOSTOMATA CHONDRICHTHYES TELEOSTOMI

• jaws formed from anterior visceral arch • part of second visceral arch forms • loss of bone in internal skeleton • bony operculum covers pharyngeal slits
• paired nasal openings hyomandibular to support jaws • prismatic calcification of cartilage externally
• five pharyngeal slits • true teeth • placoid scales • gill not supported by interbranchial septum
• paired pectoral and pelvic appendages • endolymphatic duct, connects inner ear to • branchiostegal rays
• three semicircular canals in inner ear external body surface

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

features that indicate a common ancestry with tetrapods. trunk sections were linked by a movable joint. Placo-
Therefore, if “Pisces” were to be retained as a formal derms were generally small (though some were giants,
term, then the tetrapods would have to be included in reaching 6 m in length) and possessed extensive dermal
the taxon, but it would then be equivalent of Gnathos- coverings, as did the “ostracoderms,” but they share
tomata (however, see later). numerous features that unite them with all other gna-
Fish, by and large, all have a similar way of getting thostomes, including jaws and paired fins. There is,
on in the world, and it should thus be clear that our however, considerable question as to the homology of
everyday concept of fish represents a grade rather than their jaws with those of other jaw-bearing vertebrates.
a clade. That they are fish conveys the general idea that Various differences in the masticatory apparatus, such
locomotion is accomplished essentially through lateral as an internal rather than external position for the jaw
undulations of the trunk and tail with guidance muscles, may indicate that jaws were independently
supplied by paired pectoral and pelvic fins; gas exchange derived in placoderms and other gnathostomes. If so, the
occurs primarily through gills located in the pharyngeal immediate common ancestor of these two groups may
slits; the heart is a simple, tubular, single-barrelled have lacked functional jaws. Placoderms had numerous
pump; and so on. However, as some fish are more shared derived characters that indicate that they form a
closely related to other types of vertebrates, including monophyletic group, such as a unique joint in the neck
birds and mammals, our classification must reflect that allowed the head to be lifted and a distinctive upper
this. jaw articulation. Most authors consider placoderms as
The most basal fishes are the extinct Placodermi. Plac- the sister group to all remaining gnathostomes, as is
oderms (from the Ancient Greek placo, plate, and derma, done here, but some regard them as united with the
skin) had several large plates covering the head and cartilaginous fishes, Chondrichthyes (see later), in a
anterior part of the trunk. These armored head and monophyletic group.

THE DISSECTION OF VERTEBRATES

10 1. CRANIATA AND VERTEBRATA

In the remaining gnathostomes, Eugnathostomata, staggering diversity of fossil and living forms, and only
the second visceral arch is modified into a hyoid arch, a the most general of evolutionary outlines of living acti-
supporting element for the jaw (Figure 1.3). In addition, nopterygians is possible here, with additional detail pro-
eugnathostomes possess true teeth. They include the vided in Figure 1.4. Several major groupings may be
remaining fishes and the terrestrial vertebrates. Among recognized. The most basal is Polypteriformes (= Cla-
fishes, three major radiations may be recognized, the dista), a clade which includes Polypterus (bichir). Polyp-
most basal being the Chondrichthyes (Figure 1.3). This teriformes retain several of the early features of early
clade includes the sharks (Elasmobranchii) and chimae- actinopterygians, such as ganoid scales, a well-ossified
ras (Holocephali), and is united by various derived fea- skeleton, and paired ventral lungs (air sacs) connected
tures, such as placoid scales, a cartilaginous skeleton to the pharynx for aerial respiration. Many students are
with prismatic calcification, an endolymphatic duct con- surprised that lungs would be important in fishes, but
necting the inner ear with the exterior, and the presence aerial respiration is so important that bichirs drown if
of claspers in males. Despite these and other specializa- deprived of it.
tions, chondrichthyeans retain numerous plesiomorphic Actinopteri includes more derived actinopterygians,
features in their basic anatomy. The near absence of bone, with the Chondrostei—sturgeons and paddlefishes, as
however, is not ancestral, but a secondary loss. The com- well as extinct relatives—representing the basal forms of
bination of this condition and of ancestral features is a this clade. Neopterygii are the sister group to chondros-
main reason why the shark is used so extensively for dis- teans. Lepisosteidae (gars) are basal neopterygians. The
section: The ancestral features allow an understanding of sister clade to lepisosteids is composed of a relatively
the basic vertebrate systems, and the specialized absence small group, Amiidae, which includes the bowfins,
of bone facilitates the dissection of these systems. and Teleostei, which includes the most derived
Elasmobranchii includes the sharks and rays. Tradi- actinopterygians.
tionally these were considered monophyletic groups, Earlier classifications recognized three groups of
with Squalomorpha including sharks and Batoidea actinopterygians—the chondrosteans, holosteans, and
including skates and rays. However, the former may not teleosteans—as reflecting a sequence of basal, intermedi-
be monophyletic, with some being more closely related ate, and derived actinopterygians. These categories were
to batoids than to other sharks. Elasmobranchs (from the more properly evolutionary grades, with “holosteans”
Ancient Greek elasmos, thin plate, and branchia, gills) including the lepisosteids and amiids (see Figure 1.4),
have partitions between the pharyngeal slits that bear and are useful in following, in broad outline, some of the
the gills. The holocephalians (chimaeras or ratfishes) main trends in actinopterygian evolution. These include
differ in having a fleshy operculum covering the slits. changes in the feeding apparatus, fin form and position,
Also, the upper jaw is fused to the braincase, a feature and body shape.
from which the group gets its name (holocephalian: The feeding apparatus of bony fishes is structured so
from the Ancient Greek, holos, whole, and kephale, head), that the lowering jaw was ancestrally capable only of
whereas in elasmobranchs the upper jaw is separate simple lowered and closing. In this system, the upper
from the braincase. jaw was fused to the braincase. The upper and lower
Teleostomi includes the bony fishes and tetrapods jaws were long, with the articulation far back under the
(Figure 1.3). The bony fishes, as their name implies, skull, permitting a wide gape. These features are reflected
retained and improved on a bony skeleton. The acantho- by the orientation of the hyomandibular, which sloped
dians are a relatively minor group of very early, extinct posteroventrally. The feeding apparatus underwent
bony fishes, characterized by long stout spines associ- modifications, resulting in a complex kinetic system in
ated with their paired fins, of which more than two were which the jaws are protruded and allow inertial suction
often present. The other two major radiations of bony feeding. The main anatomical changes are that the jaws
fishes form a clade (including the tetrapods) termed shortened, so the hyomandibular swung forward to
Osteichthyes, and include Actinopterygii and Sarcop- assume, in derived teleosts, an anteroventral orientation.
terygii (Figures 1.3 and 1.4). A lung or air sac is consid- The maxilla, a bone of the upper jaw, was freed from the
ered an ancestral trait for this group. From it a swim jaw margin and functions as a lever in participating in
bladder evolved in some derived bony fishes. movements of the premaxilla, the most anterior element
Actinopterygii (Figure 1.4) or ray-finned fishes are the of the upper jaw. Inertial suction feeding opened up
most diverse and numerous vertebrates (about half of all numerous opportunities and is one of the main features
living vertebrates are actinopterygians) and inhabit cited in the success of actinopterygians. Associated
nearly all aquatic habitats. Their fins are supported inter- changes occurred in the position and form of the fins and
nally mainly by fibrous rays (rather than an endoskeletal of the body. Ancestrally, the tail was heterocercal and
support) and are controlled by muscles that lie mainly the paired fins were in positions similar to that in the
within the body wall. Actinopterygians include a sharks: relatively ventral, with the pectoral fins lying

THE DISSECTION OF VERTEBRATES

 VERTEBRATA 11
TELEOSTOMI

ACANTHODII OSTEICHTHYES

SARCOPTERYGII ACTINOPTERYGII

POLYPTERIFORMES ACTINOPTERI

CHONDROSTEI NEOPTERYGII

LEPISOSTEIDAE AMIIDAE TELEOSTI

OSTEICHTHYES SARCOPTERYGII ACTINOPTERYGII

• lung (or swim-bladder) formed as outpocketing of gut • muscular paired fins • fin skeletal elements and musculature mainly within
• unique pattern of dermal head bones, forming large • paired fins each with single basal skeletal element body wall
plates • scales covered with cosmine (primitively) • scales covered with ganoine (primitively)
• dermal bones forming margin of mouth, bearing rooted • enamel on teeth • single dorsal fin (primitively)
teeth
• bony fin rays (or lepidotrichia)

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

anteriorly and pelvic fins posteriorly. Also, the body is, and muscles, and so are known as the lobe-finned fish
again as in sharks, fusiform, or torpedo-shaped. These (Figure 1.5). As fish, sarcopterygians are not as diverse
features make for fast swimming. In teleosts the pectoral or successful as the actinopterygians (although this was
fins are moved dorsally and the pelvic fins anteriorly. not always the case). As a clade, however, sarcopterygi-
The tail is homocercal (superficially symmetrical) and ans are extremely successful, owing to the radiation of
the body laterally compressed. These changes allowed tetrapods. The fleshy fins of sarcopterygian fishes were
for different swimming styles, with considerably more not used for walking on terrestrial environments, but for
precision control (for example, the dorsal position of the maneuvering in shallow waters. Interestingly, a group
pectoral fins allows them to function as “brakes”). These of living sarcopterygian fishes, coelacanths (see later),
changes were also instrumental in the great radiation of swim by moving their fins the same way a terrestrial
actinopterygians. vertebrate uses its limbs to move on land.
The sister group of Actinopterygii is Sarcopterygii, Other sarcopterygian synapomorphies are provided
the second group of bony fish (including tetrapods), in Figure 1.4. The most basal clade is Actinista or coel-
which possess paired fins with internal skeletal support acanths, represented only by two living species. Its sister

THE DISSECTION OF VERTEBRATES

12 1. CRANIATA AND VERTEBRATA

ACTINOPTERYGII SARCOPTERYGII

ACTINISTA RHIPIDISTIA

DIPNOI CHOANATA

“ELPISTOSTEGIDS” STEGOCEPHALIA

RHIPIDISTIA CHOANATA STEGOCEPHALIA

• partial ventricular septum in heart • true internal nostrils (choanae); single • dactylous paired appendages (i.e., with
• heart with differentiated pulmonary and external nostril on each side of head carpals/tarsals and digits)
systemic circulation • loss of dorsal and anal fins • zygapophyseal articulations between
• infolding of tooth enamel (i.e., • head flattened vertebrae
labyrinthodont teeth) • ribs enlarged • loss of connection between skull and
pectoral girdle
• pelvic girdle attached to specialized
vertebra of vertebral column

FIGURE 1.5 Cladogram showing phylogeny of Sarcopterygii. Some synapomorphies of the main groups are provided in the boxes below
the cladogram. Dashed lines denote a paraphyletic group.

group, Rhipidistia, includes Dipnoi and Choanata forms with fully developed limbs with digits (fingers or
(Figure 1.5). Dipnoans are the lungfishes, of which only toes). The recent discovery of Tiktaalik, an “elpistostegid”
three genera survive. The choanates include several even more closely related to stegocephalians, has filled
fossil groups, which are not considered here, and Stego- in a good deal of this gap (Ahlberg and Clack, 2006;
cephali, all marked by, among other features, true inter- Daeschler et al., 2006; Shubin et al., 2006). Its pectoral fin
nal nostrils. Prestegocephalian choanates closely related is morphologically and functionally transitional between
to stegocephalians are fish such as Panderichthys and a fin and a limb, bearing expanded skeletal elements
Elpistostege, which are grouped as (the paraphyletic) with mobile joints and an array of distal segments similar
“elpistostegids” (Ahlberg et al., 2008). Among the to the distal limb pattern of basal tetrapods. The fin
notable features of “elpistostegids” are an elongated could assume a range of postures, including a position
humerus and loss of the dorsal and anal fins. Until in which the shoulder and elbow were flexed and the
recently, the gap between such fish and the earliest distal elements extended to provide a limb-like support-
stegocephalians such as Acantho-stegidae and Ichthyo- ing stance (Shubin et al., 2006). Our most recent under-
stegidae was rather pronounced—on the one hand, we standing of these groups indicates that limbs first
had forms that were clearly fish and, on the other hand, evolved in vertebrates that lived almost entirely in an

THE DISSECTION OF VERTEBRATES

 VERTEBRATA 13

“ELPISTOSTEGIDS” STEGOCEPHALIA

"NONTETRAPOD TETRAPODA
STEGOCEPHALIANS”
AMPHIBIA AMNIOTA

Synapsida Reptilia

TETRAPODA AMPHIBIA AMNIOTA

• notochord not part of braincase • manus with four digits • amniotic membrane
• occipital condyles • exoccipitals of braincase attached to skull • three ossifications in scapulocoracoid
• five or fewer digits roof • ankle with distinct astragalus
• frontal contacts orbit
• rounded occipital condyle

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

aquatic environment. It is thought that the limbs were Placodermi in a single group as the sister clade to Tele-
useful particularly in shallow areas, helping maintain ostomi, thereby eliminating Eugnathostomata as a clade.
the animal’s position so that it could wait for prey and Another study suggests that, among living gnatho-
allow it easy access to air. Perhaps these vertebrates stomes, all fishes do indeed form a monophyletic group,
could also clamber out of the water to escape predators. to the exclusion of the tetrapods, and thus that the Pisces
After all, the terrestrial environment would at that time is a natural group. The interested student is urged to
have been relatively free of predators and competition. consult the Selected References for further information
A short digression on other phylogenetic schemes is (e.g., Martin, 2001; Arnason et al., 2004; Goloboff et al.,
warranted at this point. The phylogenetic arrangement 2009).
of vertebrates just presented is the conventionally We return to our discussion of stegocephalians
accepted hypothesis, particularly among palaeontolo- (Figures 1.5 and 1.6). Omitting several fossil groups for
gists and comparative anatomists. Several recent molec- simplicity, we may recognize a major stegocephalian
ular analyses, however, are challenging this view. Some clade, Tetrapoda, defined as the clade that includes the
analyses among living forms indicate that Chondrich- last common ancestor of living amphibians and amni-
thyes do not occupy a basal position among gnatho- otes (see later). Tetrapods were and have remained
stomes. Some authors place Chondrichthyes and mainly amphibious or terrestrial, although derived

THE DISSECTION OF VERTEBRATES

14 1. CRANIATA AND VERTEBRATA

members of several lineages have reverted to a mainly term derived from the nature of their skin (lissos, smooth).
or entirely aquatic existence (e.g., the extinct ichthyo- The recent tendency, however, is to restrict Amphibia to
saurs among reptiles and the whales among mammals), the living forms (see Frost et al., 2006; although these
and others are capable of flight (e.g., birds and the extinct authors consider Amphibia and Lissamphibia as inter-
pterosaurs among reptiles, and bats among mammals). changeable), including their fossil kin and their common
They share (together with several groups omitted here) ancestor, and we follow this usage of Amphibia. The
five or fewer digits. Two tetrapod clades, Amphibia and three amphibian groups are quite distinct. They are
Amniota, may be recognized. Anura (frogs), Caudata (salamanders), and Gymnophi-
Amphibians (from the Ancient Greek amphi, both, ona (caecilians). Frogs and salamanders are reasonably
and bios, life) are so called owing to the duality of their familiar vertebrates, and are considered sister groups.
lifestyle—often a larval aquatic stage and a terrestrial Frogs are highly specialized for saltational locomotion,
adult stage are present. This term was traditionally whereas salamanders retain a more general body form
applied to living amphibians (frogs, salamanders, and and locomotion. Caecilians are specialized in being
caecilians) as well as to the many fossil groups between legless burrowers or swimmers.
fishes and amniotes (see later), and in this sense, the Amniota includes the remaining tetrapods (Figures
living amphibians were generally viewed as living rep- 1.6 and 1.7). The main innovation of amniotes is the
resentatives of the stage between fishes and amniotes. amniotic egg. Amniote embryos develop within extra-
This was due mainly to the fact that their reproductive embryonic membranes that are usually encased in a cal-
strategy is still tied to an aquatic environment (though careous or leathery egg (the term “anamniotes” refers to
this is not true of all amphibians), whereas amniotes’ vertebrates whose eggs do not have extraembryonic
reproduction is more nearly independent of water. This membranes). The membranes provide the embryo with
general impression is true in the sense that amphibians a “watery” environment that is protected against desic-
do tend to retain an ancestral reproductive strategy. cation, and thus amniotes’ reproduction has become
From this it is a small step to the view that all amphib- essentially independent of an aqueous environment in
ians, including the living forms, are therefore primitive which vertebrates ancestrally reproduced (however, a
tetrapods. However, this is both misleading and incor- relatively moist environment is still essential).
rect. On the one hand, it is wrong to think of any living The amniotes (Figures 1.6 and 1.7) include two great
organism as primitive. A creature may retain ancestral lineages, Reptilia (ignoring some fossil members) and
(or primitive, though this term is not correctly used in Synapsida, which have followed independent evolu-
this sense; unfortunately, it is well-entrenched in our tionary paths since the early history of amniotes. The
everyday mind-set) features, but that does not make the synapsids include mammal-like reptiles and mammals.
creature itself primitive. Each living organism is the The latter, Mammalia, are the living synapsids. One
product of a long evolutionary history and is a mosaic mammalian group is Monotremata, a relatively small
of both ancestral (primitive) and derived (advanced; this clade, including the echidnas and platypus, that retains
term too is inappropriate to describe organisms) fea- the ancestral reproductive strategy of laying eggs. The
tures. For example, humans retain bone, an ancestral other group, Theria, includes the marsupials (Marsupia-
vertebrate character, whereas sharks are derived lia) and the placental mammals (Eutheria). These
(advanced) in the loss of bone. The presence of this mammals have evolved reproductive modes where
ancestral feature does not make humans “more primi- embryos are retained in and nourished by the mother ’s
tive” or “less advanced” than sharks. Using the same body.
logic, frogs are not more primitive than humans just Reptilia consists of the typical living and fossil rep-
because they retain an ancestral reproductive strategy. tiles, such as turtles, lizards, snakes, and crocodiles,
The second misconception is that living amphibians along with other familiar and mainly extinct groups,
are representative of the lifestyle of the earliest stego- such as dinosaurs (including birds), pterosaurs, and ich-
cephalians. In some ways these early forms were inter- thyosaurs. Several groups may be recognized. The
mediate between fishes and more derived terrestrial turtles (Testudines) apparently compromise the sister
vertebrates, and in the past we have lumped these forms group to all other living reptiles. They are generally
together with living amphibians. But we must be careful. placed, along with several fossil groups (such as
Living amphibians, while retaining an ancestral repro- milleretids and pareiasurs), in Parareptilia (Figure 1.7;
ductive mode, are clearly very specialized. They are not see Benton, 2005, for slightly different usages of these
like the early stegocephalians, and in fact are highly terms). Several recent studies have suggested that turtles
derived vertebrates. do not comprise the sister group to all other living rep-
As noted earlier, Amphibia has been commonly used tiles (in other words, they are not basal reptiles to be
to include several fossil groups as well as the living included in Parareptilia) but are instead diapsids (see
forms, with the latter forming the clade Lissamphibia, a later) more closely related to either archosauromorphs

THE DISSECTION OF VERTEBRATES

 VERTEBRATA 15
AMPHIBIA AMNIOTA

REPTILIA SYNAPSIDA

PARAREPTILIA EUREPTILIA "NONMAMMALIAN MAMMALIA

includes SYNAPSIDS”
“NONDIAPSID DIAPSIDA
TESTUDINES
EUREPTILIANS”

Monotremata Theria

REPTILIA SYNAPSIDA

• large posttemporal (i.e., on occiput) • infratemporal fenestra

fenestra present • contact between maxilla and quadratojugal
• maxilla separated from quadratojugal by • caniniform maxillary teeth
jugal • paroccipital process contacts tabular and
• parasphenoid wings absent squamosal
• suborbital foramen in palate

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

or lepidosauromorphs. Indeed, the position of the turtles to refer to nonavian dinosaurs. Though incorrect, this
is perhaps the most disputed issue in studies of amniote reflects our shared perception of what dinosaurs are.
phylogeny, and recent works defend both basal (e.g., Such usage is fine, so long as we remember that it does
Goloboff, 2009; Werneburg and Sánchez-Villagra, 2009) not reflect formal classification, hence phylogeny.
and more derived (e.g., Li et al., 2008; Reisz and Head, The other main diapsid lineage, Lepidosauromorpha,
2008) positions. includes the extinct Sauropterygia (plesiosaurs; see later)
The remaining reptiles are usually classified as Eurep- and Lepidosauria, which consists of Rhynchocephalia
tilia, which includes fossil stem groups and Diapsida and Squamata (Figure 1.8). Rhynchocephalia is repre-
(Figure 1.7). The diapsids consist of two main lineages, sented today by only two species of Sphenodon (tuatara).
Archosauromorpha and Lepidosauromorpha (Figure Its much more speciose sister group Squamata consists of
1.8). The living archosauromorphs are the crocodylians the lizards and snakes. Within the squamates, lizards and
(Crocodylomorpha) and birds (Aves) (which belong snakes are not sister groups. This situation is rather like
respectively to the Crurotarsi and Avemetatarsalia; that of the Dinosauria mentioned earlier. The term lizard
Figure 1.8), but the group also includes their many denotes, colloquially, the group of squamates other than
extinct kin. The extinct flying reptiles, the pterosaurs snakes, but snakes are nested within this group. They are,
(Pterosauria), are a familiar example of archosauro- in other words, a group of reduced-limbed or limbless
morphs, as are the dinosaurs (Dinosauria), a clade to lizards—snakes (Serpentes, which is a monophyletic
which the birds belong; so birds are dinosaurs. Dino- group) are derived from a group of lizards (although
saurs other than birds are generally referred to as non- there remains some debate over which particular group).
avian dinosaurs but this is an informal designation, as it However, the perception attached to the colloquial mean-
is paraphyletic (because some nonavian dinosaurs are ings of lizards and snakes is a convenient shortcut, so
more closely related to birds than to other nonavian long as we remember that the term lizard does not refer
dinosaurs). More commonly, the term dinosaur is used to a monophyletic clade (unless, of course, we choose to

THE DISSECTION OF VERTEBRATES

16 1. CRANIATA AND VERTEBRATA

DIAPSIDA
ARCHOSAUROMORPHA LEPIDOSAUROMORPHA
CRUROTARSI AVEMETATARSALIA ICHTHYOSAURIA SAUROPTERYGIA LEPIDOSAURIA
includes PTEROSAURIA SQUAMATA
DINOSAURIA RHYNCHOCEPHALIA
CROCODYLOMORPHA
“NONAVIAN AVES “LIZARDS” SERPENTES
DINOSAURS”

? ?

DIAPSIDA ARCHOSAUROMORPHA LEPIDOSAUROMORPHA

• supratemporal and infratemporal fenestrae • posterodorsal process on premaxilla • supratemporal absent

• suborbital fenestra • sagittal crest on parietal • teeth absent on transverse pterygoid flanges
• ossified sternum • slender and tapering cervical ribs • dorsal intercentra absent
• complex tibio-astragalar joint • dorsal margin of ilium composed of small • thyroid fenestra in pelvic girdle
• paroccipital process reaches suspensorium anterior process and large posterior process
• medial centrale of carpus absent

FIGURE 1.8 Cladogram showing phylogeny of Reptilia. Some synapomorphies of the main groups are provided in the boxes below the
cladogram. Dashed lines denote a paraphyletic group.

define the term so as to include snakes, but then it would openings, termed temporal fenestrae (from the Latin,
be the equivalent of squamates). fenestra, window). Anapsid describes the condition
Two other reasonably familiar clades of diapsid rep- where there are no temporal fenestrae and is character-
tiles are the extinct aquatic ichthyosaurs (Ichthyosauria) istic of turtles and most basal amniotes (Figure 1.9a).
and plesiosaurs (Sauropterygia). The former had a fish- Three basic patterns of fenestration are recognized. The
like or porpoise-like body, whereas the plesiosaurs had diapsid condition has two temporal fenestrae, one above
wide bodies with paddle-like appendages to propel the other on either side of the skull (Figure 1.9b). These
them through the water. Their positions within Diapsida are the supratemporal (upper or dorsal) fenestra and the
are not entirely resolved. As shown in Figure 1.8, the infratemporal (lower or ventral) fenestra. This is the con-
plesiosaurs seem probably to fall among the lepidosau- dition present in most reptiles. A single fenestra occurs
romorphs, as noted earlier, whereas the ichthyosaurs as two variants. The euryapsid skull, characteristic of
have been considered as basal diapsids or allied to sau- two reptile groups (ichthyosaurs and plesiosaurs), bears
ropterygians within Lepidosauromorpha (see Benton, a supratemporal fenestra (Figure 1.9c), whereas the syn-
2005; Kardong, 2009). apsid skull bears an infratemporal fenestra and is char-
acteristic of synapsids (Figure 1.9d).
The pattern of fenestration is defined by the typical
AMNIOTE SKULLS AND configuration of bones that border the fenestra. The
CLASSIFICATION typical configurations of bones for the skull types are
illustrated in Figure 1.9. In the synapsid condition the
Amniotes have long been subdivided on the condition dorsal border of the fenestra is formed mainly by the
of the temporal region of the skull, that portion posterior squamosal and postorbital bones, although the parietal
to the orbit. This region can either be solid or have may occasionally participate, whereas the ventral border

THE DISSECTION OF VERTEBRATES

 AMNIOTE SKULLS AND CLASSIFICATION 17

parietal (p) postorbital (po) supratemporal

postfrontal (pof) fenestra
squamosal (sq) p
frontal (f)
prefrontal (prf) pof f
lacrimal (l) po pr
f
nasal (n)
pmx
sq l
n

jugal (j) j
maxilla (mx) qj
mx
quadratojugal (qj) infratemporal
fenestra
premaxilla (pmx)
(a) Anapsid (b) Diapsid

p p
pof f pof f

pr po pr
f f
po sq
sq l pmx l pmx
n n

j mx j
qj qj
mx

(c) Euryapsid (d) Synapsid

FIGURE 1.9 Diagrammatic illustrations of the four main amniote skull patterns.

is formed mainly by the squamosal and jugal bones, but for the former we recognize that at least the earliest
with the quadratojugal bone occasionally contributing. basal members of the clade had anapsid skulls.
The infratemporal fenestra of the diapsid skull is bor- Within Diapsida a variety of specializations evolved.
dered by the jugal, squamosal, and postorbital bones, Among those that display a fully diapsid pattern are
with the quadratojugal occasionally participating. The tuataras (Sphenodon) and crocodylians. Birds, lizards,
supratemporal fenestra is bordered by the postorbital, and snakes, however, have tended to lose one or both
squamosal, parietal, and, in many cases, the postfrontal temporal bars. This has decoupled the posterior part of
bones. Two bony bars, temporal bars (or arcades), are the skull, allowing the potential for considerable flexibil-
clearly defined in the diapsid skull, a ventral bar formed ity among the functional regions of the skull. In general,
mainly by the jugal and quadratojugal bones, and a lizards have lost the lower temporal bar and snakes both
dorsal bar, between the fenestrae, formed by the postor- the lower and upper temporal bars. At this point, we
bital and squamosal bones. The fenestra of euryapsid must elaborate on the presence of the classic diapsid
skulls is bordered usually by the parietal, postfrontal, condition in Sphenodon. We noted earlier that Sphenodon
postorbital, and squamosal bones, with the last two possesses the lower temporal bar. For many years, this
meeting ventrally below the fenestra. From these basic condition was interpreted as the retention of an ancestral
patterns, several specializations have evolved, as dis- diapsid condition, and so Sphenodon was long desig-
cussed later. nated as a living fossil. However, recent work has dem-
For much of the past century, the classification of onstrated that all lepidosaurs (rhynchocephalians and
amniotes closely reflected fenestration; and hence Anap- squamates) inherited a skull without a lower temporal
sida, Diapsida, Euryapsida, and Synapsida were used as bar; that is, it is the ancestral condition for this clade. The
formal names for amniote radiations. More recently, presence of the lower temporal bar in Sphenodon is thus
however, we have realized that while the pattern of due to secondary redevelopment of this structure, rather
fenestration does broadly reflect amniote evolution, it is than to retention of the ancestral diapsid condition (see
not tied as strictly to phylogeny as was once presumed. Mo et al., 2010). Birds have lost the upper temporal bar
At least two of these groups, Diapsida (includes archo- so the infratemporal and supratemporal fenestrae have
sauromorphs and lepidosauromorphs) and Synapsida merged into a single large opening. Further, they have
(includes mammals), are still considered monophyletic, lost the bony bar posterior to the orbit, merging the orbit

THE DISSECTION OF VERTEBRATES

18 1. CRANIATA AND VERTEBRATA

and the fenestrae. Among synapsids, in mammals the have revealed, however, that some early amniotes with
fenestra increases in size and the bony bar behind the anapsid skulls are more closely related to Diapsida than
orbit generally disappeared so that orbit and fenestra to other anapsid-skulled early amniotes. Anapsida is
merge. Although this resembles the condition in birds, still used by some authors (e.g., Benton, 2005) for the
the morphologies are convergent. clade including turtles (but see pages 14–15) and many
Euryapsida is no longer considered a valid name. It early anapsid amniotes, such as pareiasaurids, milleret-
was applied to ichthyosaurs and plesiosaurs, but we tids, and mesosaurids, although some members of this
now recognize that the euryapsid pattern evolved inde- clade do exhibit temporal fenestration (see Modesto
pendently in these groups from the diapsid condition, et al., 2009). More commonly, this clade is termed Para-
and thus that these groups (and relatives, such as plac- reptilia. As noted earlier, the phylogenetic position of
odonts) are diapsids. The euryapsid condition appar- turtles is controversial and the composition of Pararep-
ently evolved from a secondary “filling in” of the lower tilia (with or without turtles) varies accordingly. If turtles
temporal fenestra. are diapsids, it implies that the anapsid condition in
Anapsida was applied to the more basal amniotes, as turtles is a secondary development produced by “filling
the anapsid skull is the basal and nearly ubiquitous type in” of the fenestrae.
among early tetrapods. Recent phylogenetic analyses

THE DISSECTION OF VERTEBRATES