C H A P T E R

Chordates
23
• GENERAL CHARACTERISTICS,
PROTOCHORDATES, AND ORIGIN
OF THE EARLY VERTEBRATES

Chordata

Two amphioxus in feeding posture.

It’s a Long Way From Amphioxus

Along the more southern coasts of North America, half buried in It’s a long way from amphioxus
sand on the seafloor, lives a small fishlike translucent animal qui- It’s a long way to us.
etly filtering organic particles from seawater. Inconspicuous, of no It’s a long way from amphioxus
commercial value and largely unknown, this creature is nonethe- To the meanest human cuss.
less one of the famous animals of classical zoology. It is amphioxus, Well, it’s good-bye to fins and gill slits
an animal that wonderfully exhibits the five distinctive hallmarks And its welcome lungs and hair,
of the phylum Chordata—(1) dorsal, tubular nerve cord overly- It’s a long, long way from amphioxus
ing (2) a supportive notochord, (3) pharyngeal slits and (4) endo- But we all came from there.
style for filter-feeding, and (5) a postanal tail for propulsion—all
But amphioxus’ place in the sun was not to endure. For one thing,
wrapped up in one creature with textbook simplicity. Amphioxus
amphioxus lacks one of the most important of vertebrate character-
is an animal that might have been designed by a zoologist for the
istics, a distinct head with special sense organs and the equipment
classroom. During the nineteenth century, with interest in verte-
for shifting to an active predatory mode of life. Absence of a head,
brate ancestry running high, amphioxus was considered by many
together with several specialized features, suggests to zoologists today
to resemble closely the direct ancestor of vertebrates. Its exalted
that amphioxus represents an early departure from vertebrate ancestry.
position was later acknowledged by Philip Pope in a poem sung to
It seems that we are a very long way indeed from amphioxus. Never-
the tune of “Tipperary.” It ends with the refrain:
theless, while amphioxus is denied the vertebrate ancestral award, it
resembles the chordate condition immediately preceding the origin of
vertebrates more closely than any other living animal we know.

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 www.mhhe.com/hickmanipz14e CHAPTER 23 Chordates 497

THE CHORDATES
Animals most familiar to most people belong to phylum Chordata
Characteristics of Phylum Chordata
(kor-da⬘ta) (L. chorda, cord). Humans are members and share the 1. Bilateral symmetry; segmented body; three germ layers; well-
characteristic from which the phylum derives its name—the noto- developed coelom
chord (Gr. nōton, back, ⫹ L. chorda, cord) (Figure 23.1). All mem- 2. Notochord (a skeletal rod) present at some stage in the life
bers of the phylum possess this structure, either restricted to early cycle
3. Single, dorsal, tubular nerve cord; anterior end of cord
development or present throughout life. The notochord is a rodlike,
usually enlarged to form brain
semirigid body of cells enclosed by a fibrous sheath, which extends,
4. Pharyngeal pouches present at some stage in the life cycle;
in most cases, the length of the body just ventral to the central ner- in aquatic chordates these develop into pharyngeal slits
vous system. Its primary purpose is to stiffen the body, providing 5. Endostyle in floor of pharynx or a thyroid gland derived
skeletal scaffolding for the attachment of swimming muscles. from the endostyle
The structural plan of chordates shares features of many 6. Postanal tail projecting beyond the anus at some stage but
nonchordate invertebrates, such as bilateral symmetry, antero- may or may not persist
posterior axis, coelom, tube-within-a-tube arrangement, metam- 7. Complete digestive system
erism, and cephalization. However, the exact phylogenetic 8. Segmentation, if present, restricted to outer body wall,
position of chordates within the animal kingdom is unclear. head, and tail and not extending into coelom
Two possible lines of descent have been proposed. Ear-
lier speculations that focused on the arthropod-annelid-mollusc
group (Protostomia branch) of the invertebrates have fallen from origin, and a coelom primitively formed by fusion of enterocoe-
favor. It is now believed that only members of the echinoderm- lous pouches (although in most vertebrates coelom formation is
hemichordate assemblage (Deuterostomia branch) deserve seri- schizocoelus, but independently derived, as an accommodation
ous consideration as the chordate sister group. Chordates share for their large yolks). These uniquely shared characteristics indi-
with other deuterostomes several important characteristics: radial cate a natural unity among the Deuterostomia.
cleavage (p. 166), anus derived from the first embryonic opening Phylum Chordata shows a more fundamental unity of organs
(blastopore) and mouth derived from an opening of secondary and organ systems than do other phyla. Ecologically, chordates
are among the most adaptable of organic forms and are able to
occupy most kinds of habitat. They illustrate perhaps better than
Notochord any other animal group the basic evolutionary processes of origin
of new structures, adaptive strategies, and adaptive radiation.

Elastic sheath
Traditional and Cladistic Classification
A
Fibrous sheath
of the Chordates
Traditional Linnaean classification of chordates (p. 509) provides a
convenient way to indicate the taxa included in each major group.
However, in cladistic usage, some of the traditional taxa, such as
Notochord Agnatha and Reptilia, are no longer recognized. Such taxa do
not satisfy the requirement of cladistics that only monophyletic
groups are valid taxonomic entities, that is, groups that contain all
known descendants of a single common ancestor. The reptiles, for
example, are considered a paraphyletic grouping because this
B group does not contain all of the descendants of their most recent
common ancestor (p. 568). The common ancestor of reptiles as
Figure 23.1 traditionally recognized is also the ancestor of birds. As shown
A, Structure of the notochord and its surrounding sheaths. Cells of the in the cladogram (see Figure 23.3), reptiles, birds, and mammals
notochord proper are thick walled, pressed together closely, and filled compose a monophyletic group called Amniota, so named
with semifluid. Stiffness is caused mainly by turgidity of fluid-filled
because all develop from an egg having special extraembryonic
cells and surrounding connective tissue sheaths. This primitive type of
endoskeleton is characteristic of all chordates at some stage of the life membranes, one of which is the amnion. Therefore according
cycle. The notochord provides longitudinal stiffening of the main body to cladistics, reptiles can only be used as a term of convenience
axis, a base for trunk muscles, and an axis around which the vertebral to refer to amniotes that are not birds or mammals; there are no
column develops. B, In hagfishes and lampreys it persists throughout life, derived characters that unite reptiles to the exclusion of birds and
but in other vertebrates it is largely replaced by vertebrae. In mammals,
mammals. The reasons why nonmonophyletic groups are not
remnants are found in nuclei pulposi of intervertebral discs. The method
of notochord formation is different in the various groups of animals. In used in cladistic taxonomy are explained in Chapter 10 (p. 209).
amphioxus it originates from endoderm; in birds and mammals it arises The phylogenetic tree of chordates (Figure 23.2) and the
as an anterior outgrowth of the embryonic primitive streak. cladogram of chordates (Figure 23.3) provide different kinds of

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 498 PART THREE Diversity of Animal Life

Mammals
Birds

Nonavian
reptiles

Modern
amphibians

Modern
bony
fishes

Primitive
amniotes

Cartilaginous fishes
Early
tetrapods
Lampreys

er ms
cod
Pla Hagfishes

s
erm Lancelets
acod
Ostr

rdata
a locho Tunicates
Ceph

Urochordata

Free-swimming
chordate ancestor
Hemichordates

Primitive
sessile
filter feeder
Echinodermata

Hypothetical
deuterostome Echinoderms
ancestor

CENOZOIC
PRECAMBRIAN PALEOZOIC MESOZOIC
TO PRESENT

Geologic time (My ago) 570 245 66

Figure 23.2
Phylogenetic tree of the chordates, suggesting probable origin and relationships. Other schemes have been suggested and are possible. The relative
abundance in numbers of species of each group through geological time, as indicated by the fossil record, is suggested by the bulging and thinning
of that group’s line of descent.

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 Chordata (animals with notochord at some stage in life cycle)
Euchordata (chordates that retain an axial skeleton throughout life)
Craniata (euchordates with a cranium) = Vertebrata
Gnathostomata (Craniata with jaws)

hic70049_ch23_496-513.indd 499
Teleostomi (bony fishes + tetrapods)
Tetrapoda (four-limbed vertebrates)
Amniota (tetrapods with embryos having
extraembryonic membranes)

Protochordata Agnatha Osteichthyes Reptilia

(bony fishes)

Actinopterygii
(ray-finned fishes) Mammalia Lepidosauria Testudines
Cephalochordata Petromyzontida Amphibia Aves
(lancelets) (lampreys) (mammals) (lizards, snakes) (turtles) Crocodilia
Sarcopterygii (birds)
(lungfishes,
Urochordata Myxini coelacanths)
Chondrichthyes
(tunicates) (hagfishes) (sharks, rays,
chimaeras) Hair,
mammary
glands
Skull with upper and
lower temporal fenestra,
beta-keratin in epidermis
Suckerlike oral
disc, long larval Heterocercal Egg with extraembryonic membranes
stage, 7 pairs caudal fin,
of gills placoid scales, Paired limbs used for terrestrial
cartilaginous locomotion
skeleton
Unique supportive elements in skeleton or
girdles of appendages
Slime glands, Lung or swimbladder derived from gut, bony endoskeleton
accessory
hearts Jaws, 3 pairs semicircular canals, paired appendages,
gill filaments lateral to gill support
2 pairs semicircular canals, vertebrae
Distinct head and tripartite brain; paired specialized sense organs; 1 or more
pairs semicircular canals, glomerular kidneys, neural crest, ectodermal placodes

Axial skeleton retained throughout life; muscle somites present

Notochord, dorsal hollow nerve cord; pharyngeal slits;

postanal tail; endostyle

Figure 23.3
Cladogram of living members of phylum Chordata showing probable relationships of monophyletic groups composing the phylum. Each branch in the cladogram represents a monophyletic
group. Some derived character states that identify the branchings are shown at right of the branch points. Nesting brackets across the top of the cladogram identify monophyletic
groupings within the phylum. The term Craniata, although commonly equated with Vertebrata, is preferred by many authorities because it recognizes that some jawless vertebrates have a
cranium but no vertebrae. The lower set of brackets identify the traditional groupings Protochordata, Agnatha, Osteichthyes, and Reptilia. These paraphyletic groups are not recognized in
cladistic treatments, but are shown because of widespread use.

7/14/07 4:30:44 PM
 500 PART THREE Diversity of Animal Life

information. The cladogram shows a nested hierarchy of taxa FIVE CHORDATE HALLMARKS
grouped by their sharing of derived characters. These characters
may be morphological, physiological, embryological, behavioral, Five distinctive characteristics that, taken together, set chordates
chromosomal, or molecular in nature. By contrast, the branches apart from all other phyla are notochord, dorsal tubular nerve
of a phylogenetic tree are intended to represent real lineages that cord, pharyngeal pouches or slits, endostyle, and postanal
occurred in the evolutionary past. Geological information regard- tail. These characteristics are always found at some embryonic
ing ages of lineages is added to information from the cladogram stage, although they may be altered or may disappear in later
to generate a phylogenetic tree for the same taxa. stages of the life cycle. All but pharyngeal pouches or slits are
In our treatment of chordates, we have retained the unique to chordates; hemichordates also have pharyngeal slits.
traditional Linnaean classification (p. 509) because subfields of A dorsal nerve cord is present in some hemichordates, but its
zoology are organized according to this scheme and because the homology to that of chordates is uncertain.
alternative—thorough revision following cladistic principles—
would require extensive change and abandonment of familiar Notochord
rankings. However, we have tried to use monophyletic taxa as
much as possible, because such usage is necessary to reconstruct
the evolution of morphological characters in chordates.
Several traditional divisions of phylum Chordata used in
Linnaean classifications are shown in Table 23.1 . A funda-
mental separation is Protochordata from Vertebrata. Since the Notochord
former lack a well-developed head, they also are called Acra-
The notochord is a flexible, rodlike structure, extending the length
niata. All vertebrates have a well-developed skull enclosing
of the body. It is the first part of the endoskeleton to appear in
the brain and are called Craniata. We should note that some
the embryo. The notochord is an axis for muscle attachment, and
cladistic classifi cations exclude Myxini (hagfi shes) from the
because it can bend without shortening, it permits undulatory
group Vertebrata because they lack vertebrae, although retain-
movements of the body. In most protochordates and in jawless ver-
ing them in Craniata since they do have a cranium. The ver-
tebrates, the notochord persists throughout life (see Figure 23.1).
tebrates (craniates) may be variously subdivided into groups
In all vertebrates except hagfishes a series of cartilaginous or bony
based on shared characteristics. Two such subdivisions shown
vertebrae are formed from mesenchymal cells derived from blocks
in Table 23.1 are: (1) Agnatha, vertebrates lacking jaws (hag-
of mesodermal cells (somites) lateral to the notochord. In most ver-
fishes and lampreys), and Gnathostomata, vertebrates having
tebrates, the notochord is displaced by vertebrae, although remains
jaws (all other vertebrates), and (2) Amniota, vertebrates whose
of the notochord may persist between or within the vertebrae.
embryos develop within a fluid-filled sac, the amnion (reptiles,
birds, and mammals), and Anamniota, vertebrates lacking this
adaptation (fishes and amphibians). The Gnathostomata in turn Brain Dorsal nerve cord
can be subdivided into Pisces, jawed vertebrates with append-
ages, if any, in the form of fins; and Tetrapoda (Gr. tetras, four,
⫹ podos, foot), jawed vertebrates with appendages, if any, in
the form of limbs. Note that several of these groupings are
paraphyletic (Protochordata, Acraniata, Agnatha, Anamniota,
Pisces) and consequently are not accepted in cladistic classi- Dorsal Tubular Nerve Cord
fications. Accepted monophyletic taxa are shown at the top of In most invertebrate phyla that have a nerve cord, it is ventral
the cladogram in Figure 23.3 as a nested hierarchy of increas- to the alimentary canal and is solid, but in chordates the single
ingly more inclusive groupings. cord is dorsal to the alimentary canal and is a tube (although the

TABLE 23.1
Traditional Divisions of the Phylum Chordata
Urochordata Cephalo- Myxini Petromy- Chondrich- Osteichthyes Amphibia Reptilia Aves Mammalia
(tunicates) chordata (hagfishes) zontida thyes (bony fishes) (amphibians) (reptiles) (birds) (mammals)
(lancelets) (lampreys) (sharks)
Chordata
Protochordata Vertebrata
Acraniata Craniata
Agnatha Gnathostomata
Pisces Tetrapoda
Anamniota Amniota

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 www.mhhe.com/hickmanipz14e CHAPTER 23 Chordates 501

hollow center may be nearly obliterated during growth). The secrete iodinated proteins. These cells are homologous with the
anterior end becomes enlarged to form the brain in vertebrates. iodinated-hormone-secreting thyroid gland of adult lampreys and
The hollow cord is produced in the embryo by infolding of ecto- the remainder of vertebrates. In primitive chordates, endostyle
dermal cells on the dorsal side of the body above the notochord. and perforated pharynx work together to create an efficient
Among vertebrates, the nerve cord passes through the protective filter-feeding apparatus.
neural arches of the vertebrae, and the brain is surrounded by a
bony or cartilaginous cranium. Muscular, postanal tail

Pharyngeal slits

Postanal Tail
The postanal tail, together with somatic musculature and the
Pharyngeal Pouches and Slits stiffening notochord, provides the motility that larval tunicates
Pharyngeal slits are openings that lead from the pharyngeal and amphioxus need for their free-swimming existence. As a
cavity to the outside. They are formed by inpocketing of the structure added to the body behind the end of the digestive tract,
outside ectoderm (pharyngeal grooves) and evagination, or out- it clearly has evolved specifically for propulsion in water. Its effi-
pocketing, of the endodermal lining of the pharynx (pharyngeal ciency is later increased in fishes with the addition of fins. The
pouches). In aquatic chordates, the two pockets break through tail is evident in humans only as a vestige (the coccyx, a series of
the pharyngeal cavity where they meet to form the pharyngeal small vertebrae at the end of the spinal column) but most other
slit. In amniotes some pockets may not break through the pha- mammals have a waggable tail as adults.
ryngeal cavity and only grooves are formed instead of slits. In
tetrapod (four-footed) vertebrates the pharyngeal pouches give
rise to several different structures, including the Eustachian tube, ANCESTRY AND EVOLUTION
middle ear cavity, tonsils, and parathyroid glands (see p. 181). Since the mid-nineteenth century when Darwin’s theory of com-
The perforated pharynx evolved as a filter-feeding appara- mon descent became the focal point for recognizing relation-
tus and is used as such in protochordates. Water with suspended ships among groups of living organisms, zoologists have debated
food particles is drawn by ciliary action through the mouth and the question of chordate origins. It has been difficult to recon-
flows out through pharyngeal slits where food is trapped in struct the evolutionary history of the earliest chordates because
mucus. In vertebrates, ciliary action is replaced by a muscular they were probably soft-bodied creatures that had little chance
pump that drives water through the pharynx by expanding and of being preserved as fossils. Although more Cambrian chordates
contracting the pharyngeal cavity. Also modified were the aor- recently have been discovered (see pp. 507–510), the fossil record
tic arches that carry blood through the pharyngeal bars. In pro- is sparse. Consequently, such reconstructions largely come from
tochordates these are simple vessels surrounded by connective the study of living organisms, especially from an analysis of early
tissue. Early fishes added a capillary network having only thin, developmental stages, which tend to be more evolutionarily con-
gas-permeable walls, thus improving efficiency of gas transfer served than the differentiated adult forms they become.
between blood and the water outside. These adaptations led to
the evolution of internal gills, completing conversion of the
Most early efforts to identify kinship of chordates to other phyla are
pharynx from a filter-feeding apparatus in protochordates to a
now recognized as based on similarities related to analogy rather
respiratory organ in aquatic vertebrates.
than homology. Analogous structures are those that perform similar
functions but have different origins (such as wings of birds and but-
terflies). Homologous structures, on the other hand, share a com-
mon origin but may look different (at least superficially) and per-
form quite different functions. For example, all vertebrate forelimbs
Endostyle are homologous because they are derived from a pentadactyl limb
of the same ancestor, even though they may be modified as differ-
ently as a human’s arm and a bird’s wing. Homologous structures
Endostyle or Thyroid Gland share a genetic heritage; analogous structures do not. Obviously,
only homologous similarities reveal common ancestry.
Until recently, the endostyle was not recognized as a chordate
character. However, it or its derivative, the thyroid gland, is found
in all chordates, but in no other animals. The endostyle, in the Zoologists at first speculated that chordates evolved within
pharyngeal floor, secretes mucus that traps small food particles the protostome lineage (annelids and arthropods) but discarded
brought into the pharyngeal cavity. An endostyle is found in such ideas when they realized that supposed morphological
protochordates and lamprey larvae. Some cells in the endostyle similarities were not homologous. Early in the twentieth century

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 502 PART THREE Diversity of Animal Life

when further theorizing became rooted in developmental pat- of the body, and an excurrent siphon, or atrial siphon, that
terns of animals, it became apparent that the chordates must marks the dorsal side. When a sea squirt is expanded, water
have originated within the deuterostome branch of the animal enters the incurrent siphon and passes into a capacious ciliated
kingdom. As explained in Chapter 8 (p. 166 and Figure 8.10), pharynx that is minutely perforated by slits to form an elabo-
Deuterostomia, a grouping that includes the echinoderms, hemi- rate basketwork. Water passes through the slits into an atrial
chordates, and chordates, has several important embryological cavity and out through the excurrent siphon.
features, as well as shared gene sequences, that clearly separate Feeding depends on formation of a mucous net that is
it from Protostomia and establish its monophyly. Thus deutero- secreted by a glandular groove, the endostyle, located along the
stomes are almost certainly a natural grouping of interrelated midventral side of the pharynx. Cilia on bars of the pharynx pull
animals that have their common origin in ancient Precambrian the mucus into a sheet that spreads dorsally across the inner face
seas. Several lines of anatomical, developmental, and molecular of the pharynx. Food particles brought in the incurrent opening
evidence suggest that somewhat later, at the base of the Cam- are trapped on the mucous net, which is then worked into a rope
brian period some 570 million years ago, the first distinctive and carried posteriorly by cilia into the esophagus and stomach.
chordates arose from a lineage related to echinoderms and hemi- Nutrients are absorbed in the midgut and indigestible wastes are
chordates (Figure 23.2). Evidence from phylogenetic analysis of discharged from the anus, located near the excurrent siphon.
gene sequences, development, and morphology strongly suggest The circulatory system consists of a ventral heart and two
that a clade containing both echinoderms and hemichordates is large vessels, one on either side of the heart; these vessels con-
the sister group of chordates (see Figure 22.1, p. 470). Informa- nect to a diffuse system of smaller vessels and spaces serving
tion about the biology of the earliest chordates can be gleaned the pharyngeal basket (where respiratory exchange occurs), the
from examination of the two living chordate groups that are not digestive organs, gonads, and other structures. An odd feature
vertebrates, Urochordata and Cephalochordata. found in no other chordate is that the heart drives the blood first
in one direction for a few beats, then pauses, reverses its action,
and drives the blood in the opposite direction for a few beats.
SUBPHYLUM UROCHORDATA Another remarkable feature is the presence of strikingly high
amounts of rare elements in the blood, such as vanadium and
(TUNICATA) niobium. The vanadium concentration in the sea squirt Ciona
Urochordates (“tail-chordates”), more commonly called tuni- may reach 2 million times its concentration in seawater. The
cates, include about 1600 species. They are found in all seas function of these rare metals in the blood is a mystery.
from near shoreline to great depths. Most are sessile as adults, The nervous system is restricted to a nerve ganglion and
although some are free-living. The name “tunicate” is suggested plexus of nerves that lie on the dorsal side of the pharynx.
by the usually tough, nonliving tunic that surrounds the ani-
mal and contains cellulose (Figure 23.4). As adults, tunicates are Excurrent Incurrent
highly specialized chordates, for in most species only the lar- siphon siphon
val form, which resembles a microscopic tadpole, bears all the
Sensory
chordate hallmarks. During adult metamorphosis, the notochord tentacles
(which, in the larva, is restricted to the tail, hence the group Pigment
name Urochordata) and tail disappear, while the dorsal nerve spots
cord becomes reduced to a single ganglion. Nerve
Atrium ganglion
Urochordata is divided into three classes: Ascidiacea
(Gr. askiolion, little bag, ⫹ acea, suffix), Appendicularia
Pharynx
(L. appendic, hang to), and Thaliacea (Gr. thalia, luxuriance, Genital
duct
⫹ acea, suffi x). Members of Ascidiacea are by far the most Endostyle
common, diverse, and best known. They are often called “sea Anus
squirts” because some species forcefully discharge a jet of water Pharyngeal
from the excurrent siphon when irritated. All but a few ascidian slits
species are sessile animals, attached to rocks or other hard sub- Intestine
strates such as pilings or bottoms of ships. In many areas, they
Mantle
are among the most abundant of intertidal animals.
Tunic
Ascidians may be solitary, colonial, or compound. Each of the
Heart
solitary and colonial forms has its own test, but among compound
forms many individuals may share the same test (Figure 23.5). In Stomach Gonads
some compound ascidians each member has its own incurrent (ovary and
testes)
siphon, but the excurrent opening is common to the group.
Solitary ascidians (see Figure 23.4) are usually spherical or Stolons
cylindrical forms. Lining the tunic is an inner membrane, the
mantle. On the outside are two projections: an incurrent Figure 23.4
siphon, or oral siphon, which corresponds to the anterior end Structure of a common tunicate, Ciona sp.

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 www.mhhe.com/hickmanipz14e CHAPTER 23 Chordates 503

(Figure 23.6) to become a sessile adult, so

modified as to become almost unrecogniz-
able as a chordate.
Tunicates of class Thaliacea, known as
thaliaceans or salps, are barrel- or lemon-
shaped pelagic forms with transparent,
gelatinous bodies that, despite the con-
siderable size that some species reach, are
nearly invisible in sunlit surface waters.
They occur singly or in colonial chains that
may reach several meters in length (Fig-
ure 23.7). The cylindrical thaliacean body
B is typically surrounded by bands of circu-
Figure 23.5 lar muscle, with incurrent and excurrent
A, Two yellow-edged sea squirts, Rhopalaea sp., on siphons at opposite ends. Water pumped
a Philippine reef. Note the large incurrent siphon through the body by muscular contrac-
and the smaller excurrent siphon for each animal. tion (rather than by cilia as in ascidians)
B, Seven colonies of compound tunicates, Atriolum is used for locomotion by a sort of jet pro-
robustum, on a Pacific reef. Individuals in a colony
share a common tunic (yellow), but each has a
pulsion, for respiration, and as a source of
separate incurrent (oral) siphon. Each colony has a particulate food that is filtered on mucous
A single, large excurrent (atrial) siphon on top. surfaces. Many are provided with luminous
organs, which give a brilliant light at night.
Beneath the nerve ganglion is located the subneural gland, Most of the body is hollow, with the viscera forming a compact
connected by a duct to the pharynx. mass on the ventral side.
Sea squirts are hermaphroditic, with usually a single ovary The life histories of thaliaceans are often complex and are
and a single testis in the same animal. Germ cells are carried by adapted to respond to sudden increases in their food supply.
ducts into the atrial cavity, and then into the surrounding water The appearance of a phytoplankton bloom, for example, is met
where fertilization occurs. by an explosive population increase leading to extremely high
Of the five chief characteristics of chordates, adult sea squirts density of thaliaceans. Common forms include Doliolum and
have only two: pharyngeal slits and endostyle. However, the lar- Salpa, both of which reproduce by an alternation of sexual and
val form reveals the secret of their true relationship. The tadpole asexual generations.
larva (Figure 23.6) is an elongate, transparent form with all five The third tunicate class, the Appendicularia (Larvacea in some
chordate characteristics: notochord, hollow dorsal nerve cord, classifications) are curious larvalike pelagic creatures shaped like
propulsive postanal tail, and a large pharynx with endostyle and a bent tadpole. The name Larvacea refers to their resemblance to
pharyngeal slits. The larva does not feed but swims for some the larval stages of other tunicates. They feed by a method unique
hours or days before fastening itself vertically by adhesive papil- in the animal world. Each builds a delicate house, a transpar-
lae to a solid object. It then undergoes a dramatic metamorphosis ent hollow sphere of mucus interlaced with filters and passages

Notochord Tail
Nerve cord

Pharynx
Heart

Degenerating
notochord
Atrium
Free-swimming
larva Pharyngeal slit

Endostyle

Attached, early metamorphosis Late metamorphosis Adult

Figure 23.6
Metamorphosis of a solitary ascidian from a free-swimming larval stage.

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 504 PART THREE Diversity of Animal Life

SUBPHYLUM CEPHALOCHORDATA
Cephalochordates are lancelets: slender, laterally compressed,
translucent animals about 3 to 7 cm in length (Figure 23.9) that
inhabit the sandy bottoms of coastal waters around the world.
Lancelets originally bore the generic name Amphioxus (Gr. amphi,
both ends, ⫹ oxys, sharp), later surrendered by priority to Bran-
chiostoma (Gr. branchia, gills, ⫹ stoma, mouth). Amphioxus is still
used, however, as a convenient common name for all of approx-
imately 29 species in this diminutive subphylum. Five species
of amphioxus occur in North American coastal waters.
Amphioxus is especially interesting because it has the five
Figure 23.7 distinctive characteristics of chordates in simple form. Water enters
Salps. The transparent individuals of this delicate, planktonic species the mouth, driven by cilia in the buccal cavity and pharynx, then
are grouped in a chain. Visible within each individual is an opaque passes through numerous pharyngeal slits where food is trapped
gonad, an opaque gut, and a long serrated gill bar.
in mucus secreted by the endostyle, and is then moved by cilia
into the intestine. Here the smallest food particles are separated
through which water enters (Figure 23.8). Tiny phytoplankton and from the mucus and passed into the hepatic cecum where they
bacteria trapped on a feeding filter inside the house are drawn are phagocytized and digested intracellularly. Food is moved
into the animal’s mouth through a strawlike tube. When the filters through the gut by means of cilia, which are concentrated in a
become clogged with waste, which happens about every 4 hours, darkly staining area called the ileocolic ring (Figure 23.9), rather
the appendicularian abandons its house and builds a new house, than by muscular contractions as in vertebrates. As in tunicates,
a process that takes only a few minutes. Like thaliaceans, appen- filtered water passes first into an atrium, then leaves the body by
dicularians can quickly build up dense populations when food is an atriopore (equivalent to the excurrent siphon of tunicates).
abundant. At such times scuba diving among the houses, which The closed circulatory system is complex for so simple
are about the size of walnuts, is likened to swimming through a a chordate. The flow pattern is remarkably similar to that of
snowstorm! Appendicularians are paedomorphic; they are sexu- fi shes, although there is no heart. Blood is pumped forward
ally mature animals that have retained the larval body form of in the ventral aorta by peristaltic-like contractions of the ves-
their evolutionary ancestors (see the note explaining paedomor- sel wall, then passes upward through branchial arteries (aortic
phosis on p. 508). arches) in the pharyngeal bars to paired dorsal aortas which
join to become a single dorsal aorta.
Stomach Esophagus
From here blood is distributed to
body tissues by microcirculation
Pharynx
and then is collected in veins, which
Gonads Mouth
return it to the ventral aorta. Lacking
both erythrocytes and hemoglobin,
their blood is thought to transport
Spiracle nutrients but to play little role in gas
(modified House Feeding exchange. There are no gills special-
pharyngeal filters
slits) ized for respiration in the pharynx;
gas exchange occurs over the sur-
Notochord
face of the body.
The nervous system is centered
around a hollow nerve cord lying
Water above the notochord. Pairs of spinal
inflow Water nerve roots emerge at each trunk
outflow myomeric (muscle) segment. Sense
Tail organs are simple, including an ante-
rior, unpaired ocellus that functions
Figure 23.8 Incurrent as a photoreceptor. Although the
Appendicularian (larvacean) adult filters Trunk Tail anterior end of the nerve cord is not
(left) and as it appears within its enlarged into the characteristic verte-
transparent house (right), which is
about the size of a walnut. When
brate brain, it is apparently homolo-
the feeding filters become clogged gous to parts of the vertebrate brain.
with food, the tunicate abandons Sexes are separate. Gametes
its house and builds a new one. are released in the atrium, then pass

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 www.mhhe.com/hickmanipz14e CHAPTER 23 Chordates 505

Figure 23.9
Amphioxus. This interesting bottom-dwelling
cephalochordate illustrates the five distinctive chordate
characteristics (notochord, dorsal nerve cord, pharyngeal
slits, endostyle, and postanal tail). The vertebrate
ancestor is thought to have had a similar body plan.
A, Living amphioxus in typical position for filter-feeding.
Note the oral hood with tentacles surrounding the
mouth. B, Internal structure.

A
Rostrum Wheel organ Dorsal nerve cord Notochord Dorsal fin Ileocolic ring Myomere Caudal
fin

Oral hood Pharyngeal Pharyngeal Hepatic Ventral

with tentacles slits Endostyle bars Gonad cecum Atriopore Intestine fin Anus
B

through the atriopore to the outside where fertilization occurs. Adaptations That Have Guided Early
Cleavage is total (holoblastic) and a gastrula is formed by invag-
ination. Larvae hatch soon after egg deposition and gradually Vertebrate Evolution
assume the shape of adults. The earliest vertebrates were substantially larger and considerably
No other chordate shows the basic diagnostic chordate char- more active than the protochordates. Increased speed and mobil-
acteristics as clearly as amphioxus. In addition to the five chor- ity resulted from modifications of skeletal structures and muscles.
date anatomical hallmarks, amphioxus possesses several struc- The higher activity level and size of vertebrates also requires
tural features that resemble the vertebrate plan. Among these are structures specialized in the location, capture, and digestion of
a hepatic cecum, a diverticulum that resembles the vertebrate food and adaptations designed to support a high metabolic rate.
pancreas in secreting digestive enzymes and the liver in storing
glycogen, segmented trunk musculature, and the basic circu-
latory plan of more advanced chordates. As discussed on page Musculoskeletal Modifications
508, most zoologists consider amphioxus a living descendant of Most vertebrates possess both an exoskeleton and endoskeleton
an ancestor that gave rise to both cephalochordates and verte- of cartilage or bone. The endoskeleton permits almost unlimited
brates. Therefore cephalochordates are, in cladistic terms, the body size with much greater economy of building materials than
living sister group of vertebrates (see Figure 23.3). the exoskeleton of arthropods. Some vertebrates have become
the most massive organisms on earth. The endoskeleton forms
an excellent jointed scaffolding for attachment of segmented
SUBPHYLUM VERTEBRATA muscles. The segmented body muscles (myomeres) changed
from the V-shaped muscles of cephalochordates to the W-shaped
(CRANIATA) muscles of vertebrates. This increased complexity of folding
The third subphylum of chordates is the large and diverse Verte- in the myomeres provides powerful control over an extended
brata, the subject of Chapters 24 through 28. This monophyletic length of the body. Also unique to vertebrates are the presence
group shares the basic chordate characteristics with the other of fin rays of dermal origin, aiding in swimming.
two subphyla, but in addition it exhibits a number of novel char- The endoskeleton probably was composed initially of carti-
acters that the others do not share. The alternative name of the lage that later gave way to bone. Cartilage, with its fast growth
subphylum, Craniata, more accurately describes the group since and flexibility, is ideal for constructing the first skeletal frame-
all have a cranium (bony or cartilaginous braincase) but some work of all vertebrate embryos. The endoskeleton of living hag-
jawless fishes lack vertebrae. fishes, lampreys, sharks and their kin, and even in some “bony”

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 506 PART THREE Diversity of Animal Life

We should note that most vertebrates possess an extensive

exoskeleton (one that develops from the skin), although it is
Characteristics of Subphylum Vertebrata highly modified in many forms. Some of the most primitive fishes,
1. Chief diagnostic features of chordates—notochord, dorsal including ostracoderms and placoderms, were partly covered in
tubular nerve cord, pharyngeal pouches, endostyle or a bony, dermal armor. This armor is modified as scales in later
thyroid gland, and postanal tail—all present at some stage fishes. Many of the bones encasing the brain of advanced verte-
of the life cycle
brates actually develop from cells that originate from the dermis!
2. Integument of two divisions, an outer epidermis of stratified
Most vertebrates are further protected with keratinized structures
epithelium from ectoderm and an inner dermis of connective
tissue from mesoderm; many modifications of skin, such as derived from the epidermis, such as reptilian scales, hair, feathers,
glands, scales, feathers, claws, horns, and hair claws, and horns.
3. Distinctive cartilage or bone endoskeleton consisting of
vertebral column (except in hagfishes, which lack vertebrae) Centrum of vertebra
and a head skeleton (cranium and pharyngeal skeleton) Notochord Neural spine
derived largely from neural crest cells
4. Muscular pharynx; in fishes pharyngeal pouches open to
the outside as slits and bear gills; in tetrapods pharyngeal
pouches are sources of several glands
5. Complex, W-shaped muscle segments or myomeres to
provide movement
6. Complete, muscularized digestive tract with distinct liver
and pancreas
7. Circulatory system consisting of a ventral heart of multiple
chambers; closed blood vessel system of arteries, veins,
and capillaries; blood containing erythrocytes with
hemoglobin; paired aortic arches connecting ventral and
dorsal aortas and giving off branches to the gills among Physiology Upgrade
aquatic vertebrates; in terrestrial forms; aortic arches modified Vertebrates have modifications to the digestive, respiratory, cir-
into pulmonary and systemic circuits
culatory, and excretory systems that meet an increased meta-
8. Well-developed coelom divided into a pericardial cavity and
a pleuroperitoneal cavity
bolic demand. The perforated pharynx evolved in early chor-
9. Excretory system consisting of paired, glomerular kidneys dates as a filter-feeding device, which uses cilia and mucus
provided with ducts to drain waste to the cloaca to move water and to trap small suspended food particles. In
10. Highly differentiated tripartite brain; 10 or 12 pairs of vertebrates, the addition of muscles to the pharynx created a
cranial nerves; a pair of spinal nerves for each primitive powerful pump for moving water. With the origin of highly vas-
myotome; paired special sense organs derived from cularized gills, the function of the pharynx shifted to primarily
epidermal placodes gas exchange. Changes in the gut, including a shift from move-
11. Endocrine system of ductless glands scattered throughout ment of food by ciliary action to muscular action and addition
the body of accessory digestive glands, the liver and pancreas, managed
12. Nearly always separate sexes; each sex containing gonads the increased amount of food ingested. A ventral three-cham-
with ducts that discharge their products either into the cloaca
bered heart consisting of a sinus venosus, atrium, and ventricle,
or into special openings near the anus
13. Most vertebrates with two pairs of appendages supported by
and erythrocytes with hemoglobin enhanced transportation of
limb girdles and appendicular skeleton nutrients, gases, and other substances. Protochordates have no
distinct kidneys, but vertebrates possess paired, glomerular kid-
neys that remove metabolic waste products and regulate body
fluids and ions.
fishes, such as sturgeons, is mostly cartilage. Bone may have
been adaptive in early vertebrates in several ways. The presence
of bone in the skin of ostracoderms and other ancient fishes Pharyngeal slits
certainly provided protection from predators, although there are Dorsal
aorta
some more important benefits of bone. The structural strength of
bone is superior to cartilage, making it ideal for muscle attach-
Gut
ment in areas of high mechanical stress. One of the most interest- (muscularized)
ing ideas is that the function associated with the origin of bone
was for mineral regulation. Phosphorus and calcium are used
for many physiological processes and are in particularly high
demand in organisms with high metabolic rates. Storage and Chambered heart
regulation of calcium and phosphorus ions were likely important Aortic
functions of bone in the earliest vertebrates. arches Ventral aorta

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 www.mhhe.com/hickmanipz14e CHAPTER 23 Chordates 507

New Head, Brain, and Sensory Systems Figure 23.10

Notochord
When vertebrate ancestors shifted from filter-feeding to active Pikaia, an early
chordate from the
predation, new sensory, motor, and integrative controls became
Burgess Shale of British
essential for location and capture of larger prey. The anterior Columbia, Canada.
end of the nerve cord became enlarged as a tripartite brain
(forebrain, midbrain, and hindbrain) and protected by a cartilagi-
Segmented muscle
nous or bony cranium. Paired special sense organs designed for
distance reception evolved. These included eyes with lenses and
inverted retinas; pressure receptors, such as paired inner ears Dorsal
designed for equilibrium and sound reception; chemical recep- Brain Nerve Esophagus aorta Notochord Myomere
tors including taste and exquisitely sensitive olfactory organs; cord
Eye
lateral-line receptors for detecting water vibrations; and electro-
receptors for detecting electrical currents that signal prey.

Eye Otic Neural arch

vesicle
Endostyle Ventral Pharyngeal Atriopore Intestine Anus
Spinal
Brain cord aorta bar

Olfactory Figure 23.11

bulb Haikouella, a chordate with several vertebrate features from early
Cambrian shales of Haikou, China. It has been hypothesized to be the
sister group of vertebrates (craniates).

The Search for the Ancestral Vertebrate

Most of the early Paleozoic vertebrate fossils, the jawless ostra-
coderms (p. 510), share many novel features of organ system
Neural Crest, Ectodermal Placodes,
development with living vertebrates. These organ systems must
and Hox Genes have originated in an early vertebrate or invertebrate chordate
Development of the vertebrate head and special sense organs lineage. Fossil invertebrate chordates are rare and known primar-
was largely the result of two embryonic innovations present only ily from two fossil beds—the well-known middle Cambrian Bur-
in vertebrates: neural crest and ectodermal placodes. The gess Shale of Canada (p. 110) and the recently discovered early
neural crest, a population of ectodermal cells lying along the Cambrian fossil beds of Chengjiang and Haikou, China. An ascid-
length of the embryonic neural tube (see Figure 8.27 and p. 182), ian tunicate and Yunnanozoon, a probable cephalochordate,
contributes to the formation of many different structures, among are known from Chengjiang. Slightly better known is Pikaia, a
them most of the cranium, pharyngeal skeleton, tooth den- ribbon-shaped, somewhat fishlike creature about 5 cm in length
tine, some cranial nerves, ganglia, some endocrine glands, and discovered in the Burgess Shale (Figure 23.10). The presence of
Schwann cells. In addition they may regulate the development V-shaped myomeres and a notochord clearly identifies Pikaia
of adjacent tissue, such as tooth enamel and pharyngeal muscles as a chordate. The superficial resemblance of Pikaia to living
(branchiomeres). The ectodermal placodes (Gr. placo, plate) are amphioxus suggests that it may be an early cephalochordate.
platelike ectodermal thickenings that appear on either side of the A wealth of information about the origin of vertebrates is
neural tube. These give rise to the olfactory epithelium, lens of provided by Haikouella lanceolata, a small fishlike creature
the eye, inner ear epithelium, some ganglia and cranial nerves, known from over 300 fossil specimens recently discovered in
lateral-line mechanoreceptors, and electroreceptors. The placodes 530-million-year-old sediments near Haikou. It possessed sev-
also induce the formation of taste buds. Thus the vertebrate head eral characters that clearly identify it as a chordate, including
with its sensory structures located adjacent to the mouth (later notochord, pharynx, and dorsal nerve cord, but also had charac-
equipped with prey-capturing jaws), stemmed from the creation ters, including pharyngeal muscles, paired eyes, and an enlarged
of new cell types. brain, that are characteristic of vertebrates (Figure 23.11). How-
Recent studies of the distribution of homeobox genes that ever, it is not a vertebrate, because the fossils lack evidence of
control the body plan of chordate embryos (homeobox genes several diagnostic vertebrate traits, including a cranium, an ear,
are described on pp. 171–172) suggest that Hox genes were and a distinct telencephalon (anterior region of the forebrain).
duplicated at about the time of the origin of vertebrates. One Thus, it is transitional in morphology between cephalochordates
copy of Hox genes is found in amphioxus and other inverte- and vertebrates. Jon Mallatt, Jun-yuan Chen, and colleagues,
brates whereas living gnathostomes have four copies. Perhaps who have studied these fossils extensively, hypothesized Haik-
these additional copies of genes that control body plan provided ouella to be the sister taxon of vertebrates. Despite recent fos-
genetic material free to evolve a more complex kind of animal. sil discoveries of early chordates, many speculations regarding

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 508 PART THREE Diversity of Animal Life

vertebrate ancestry have focused on the living protochordates, in this case leading to the vertebrate lineage. Paedomorphosis is
part because they are much better known than the fossil forms. a well-known phenomenon in several different animal groups
(paedomorphosis in amphibians is described on pp. 550–551).
Butler and Hodos provided an explanation of how the paired eyes Although long popular, Garstang’s hypothesis has been chal-
of vertebrates evolved from the unpaired, median ocellus of an lenged recently. First, phylogenies generated from molecular
amphioxus-like ancestor. The homeotic gene Pax-6 is responsible data, along with information from fossils, suggest that the ances-
for the formation of an eye-producing region near the midbrain. tor of deuterostomes was free-swimming. Second, additional
Products of another gene, Sonic hedgehog, suppress Pax-6 phylogenies from molecular data show that the sessile ascidians
expression at the midline, thus forming paired, lateral eyes. In mice, represent a derived body form, and that free-swimming appen-
genetic manipulations that produce an absence of Sonic hedgehog dicularians are most similar in body form to ancestral chordates.
result in formation of an unpaired, median eye.
Paedomorphosis, the displacement of ancestral larval or juvenile
features into a descendant adult, can be produced by three differ-
Garstang’s Hypothesis of Chordate ent evolutionary-developmental processes: neoteny, progenesis,
Larval Evolution and postdisplacement. In neoteny, the growth rate of body form is
slowed so that the animal does not attain the ancestral adult form
The chordates have pursued two paths in their early evolution,
when it reaches maturity. Progenesis is the precocious maturation
one path leading to the sedentary urochordates, the other to active,
of gonads in a larval (or juvenile) body that then stops growing and
mobile cephalochordates and vertebrates. One hypothesis, pro-
never attains the adult body form. In postdisplacement, the onset of
posed in 1928 by Walter Garstang of England, suggested that the
a developmental process is delayed relative to reproductive matura-
chordate ancestral lineage retained into adulthood the larval form
tion, so that the ancestral adult form is not attained by the time of
of sessile tunicate-like animals. The tadpole larva of tunicates does
reproductive maturation. Neoteny, progenesis and postdisplacement
indeed bear all the right attributes to qualify as a possible vertebrate
thus describe different ways in which paedomorphosis can hap-
ancestor: notochord, hollow dorsal nerve cord, pharyngeal slits,
pen. Biologists use the inclusive term paedomorphosis to describe
endostyle, and postanal tail. At some point, Garstang suggested, the
results of these evolutionary-developmental processes.
tadpole larva failed to metamorphose into an adult tunicate, instead
developing gonads and reproducing in the larval stage. With con-
tinued evolution, a new group of free-swimming animals appeared,
the ancestors of cephalochordates and vertebrates (Figure 23.12).
Position of Amphioxus
Garstang called this process paedomorphosis (Gr. pais, Zoologists consider the cephalochordate amphioxus the clos-
child ⫹ morphē, form), a term describing the evolutionary reten- est living relative of vertebrates. Cephalochordates share several
tion of juvenile or larval traits in the adult body. Garstang sug- characters with vertebrates that are absent from tunicates, includ-
gested that evolution may occur in larval stages of animals, in ing segmented myomeres, dorsal and ventral aortas, branchial or
aortic arches, and podocytes, specialized excretory cells. How-
ever, as noted in the prologue to the chapter (p. 496), amphi-
oxus is unlike the most recent common ancestor of vertebrates
because it lacks the tripartite brain, chambered heart, special
sensory organs, muscular gut and pharynx, and neural crest tis-
sue inferred to have been present in that ancestor. In addition,
Tadpole larva the larger fins of some extinct cephalochordates suggest that
they were more free-swimming than modern amphioxus.
METAMORPHOSIS ? Despite these specializations most zoologists believe that
Adult
amphioxus has largely retained the body structure of the imme-
ascidian diate prevertebrate condition. Thus cephalochordates are proba-
bly the closest living relative of vertebrates (see Figure 23.3) (the
Paedomorphic vertebrate ancestor fossil Haikouella is probably the sister taxon of vertebrates).

The Ammocoete Larva of Lampreys

as a Model of the Primitive
Early vertebrate Vertebrate Body Plan
Lampreys (jawless fishes of the class Petromyzontida, discussed in
Figure 23.12 Chapter 24) have a freshwater larval stage called the ammocoete
Garstang’s hypothesis of larval evolution. Adult tunicates live on the
sea floor but produce a free-swimming tadpole larva. According to (Figure 23.13). In body form, appearance, life habit, and many
this hypothesis, more than 550 million years ago, some larvae began to anatomical details, the ammocoete larva resembles amphioxus.
reproduce in the swimming stage. These evolved into the first vertebrates. In fact, lamprey larvae were given the genus name Ammocoetes

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 www.mhhe.com/hickmanipz14e CHAPTER 23 Chordates 509

Traditional Linnean Classification of Living Members of Phylum Chordata

Phylum Chordata
Subphylum Urochordata (u⬘ro-kor-da⬘ta) (Gr. oura, tail, ⫹ L. chorda, cord, ⫹ ata, characterized by) (Tunicata): tunicates. Notochord
and nerve cord in free-swimming larva only; ascidian adults sessile, encased in tunic. About 1600 species.
Subphylum Cephalochordata (sef⬘a-lo-kor-da⬘ta) (Gr. kephalē, head, ⫹ L. chorda, cord): lancelets (amphioxus). Notochord, nerve
cord, and postanal tail persist throughout life; fishlike in form. 29 species.
Subphylum Vertebrata (ver⬘te-bra⬘ta) (L. vertebratus, backboned) (Craniata): vertebrates. Bony or cartilaginous cranium surrounding
tripartite brain; well-developed head with paired sense organs; usually with vertebrae; heart present, with multiple chambers, muscularized
digestive tract, paired kidneys.
Superclass Agnatha (ag⬘na-tha) (Gr. a, without, ⫹ gnathos, jaw): hagfishes, lampreys. Without true jaws or paired appendages. A
paraphyletic group.
Class Myxini (mik-sin⬘y) (Gr. myxa, slime): hagfishes. Mouth with four pairs of tentacles; buccal funnel absent; 1 to 16 pairs of
external gill openings; vertebrae absent; slime glands present. About 70 species.
Class Petromyzontida (pet⬘trō-m1̄-zon⬘ti-də) (Gr. petros, stone, ⫹ myzon, sucking): lampreys. Mouth surrounded by keratinized
teeth but no barbels, buccal funnel present; seven pairs of external gill openings; vertebrae present only as neural arches. 38 species.
Superclass Gnathostomata (na⬘tho-sto⬘ma-ta) (Gr. gnathos, jaw, ⫹ stoma, mouth): jawed fishes, tetrapods. With jaws and (usually)
paired appendages.
Class Chondrichthyes (kon-drik⬘thee-eez) (Gr. chondros, cartilage, ⫹ ichthys, fish): sharks, skates, rays, chimaeras.
Cartilaginous skeleton; intestine with spiral valve; claspers present in males; no swim bladder. About 970 species.
Class Actinopterygii (ak⬘ti-nop-te-rij⬘ee-i) Gr. aktis, ray, ⫹ pteryx, fin, wing): ray-finned fishes. Skeleton ossified; single gill
opening covered by operculum; paired fins supported primarily by dermal rays; appendage musculature within body; swim bladder
mainly a hydrostatic organ, if present; atrium and ventricle not divided. About 27,000 species.
Class Sarcopterygii (sar-cop-te-rij⬘ee-i) (Gr. sarkos, flesh, ⫹ pteryx, fin, wing): lobe-finned fishes. Skeleton ossified, single gill
opening covered by operculum; paired fins with sturdy internal skeleton and musculature within appendage; diphycercal tail;
intestine with spiral valve; usually with lunglike swim bladder; atrium and ventricle at least partly divided. 8 species. Paraphyletic
unless tetrapods are included.
Class Amphibia (am-fib⬘e-a) (Gr. amphi, both or double, ⫹ bios, life): amphibians. Ectothermic tetrapods; respiration by lungs,
gills, or skin; development through larval stage; skin moist, containing mucous glands, and lacking scales. About 5500 species.
Class Reptilia (rep-til⬘e-a) (L. repere, to creep): reptiles. Ectothermic tetrapods possessing lungs; embryo develops within shelled
egg; no larval stage; skin dry, lacking mucous glands, and covered by epidermal scales. A paraphyletic group unless birds are
included. About 8100 species.
Class Aves (ay⬘veez) (L. pl. of avis, bird): birds. Endothermic vertebrates with front limbs modified for flight; body covered with
feathers; scales on feet. About 9700 species.
Class Mammalia (ma-may⬘lee-a) (L. mamma, breast): mammals. Endothermic vertebrates possessing mammary glands; body more
or less covered with hair; brain large, with neocortex; three middle ear bones. About 4800 species.

(Gr. ammos, sand, ⫹ koitē, bed, referring to the preferred larval mistake is understandable; the exact relationship was not explained
habitat) in the nineteenth century when it was erroneously thought until metamorphosis into an adult lamprey was observed.
to be an adult cephalochordate, closely allied with amphioxus. Ammocoete larvae have a long, slender body with an oral
Ammocoete larvae are so different from adult lampreys that the hood surrounding the mouth much like amphioxus (Figure 23.13).

Ear vesicle Notochord Pronephros Stomach Dorsal Nerve Myomeres

Eye aorta cord

Brain

Median
nostril

Oral
papillae Gallbladder

Oral Pharyngeal Ventral Pronephric

hood Velum Endostyle bar aorta Heart Liver duct Coelom Intestine Cloaca

Figure 23.13
Ammocoete, freshwater larval stage of a lamprey. Although they resemble amphioxus in many ways, ammocoetes have a well-developed brain,
paired eyes, pronephric kidneys, heart, and other features lacking in amphioxus but representative of the vertebrate body plan.

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 510 PART THREE Diversity of Animal Life

Ammocoetes are filter feeders, but instead of drawing water by Myllokunmingia (Gr. myllo, sea fish, ⫹ Kunming, a city in China)
ciliary action into the pharynx as amphioxus does, ammocoetes and Haikouichthys (Haikou, a city in China, ⫹ Gr. ichthy, fish).
produce a feeding current by muscular pumping action much like These fossils push back the origin of vertebrates to at least the
modern fishes. The arrangement of body muscle into myomeres, early Cambrian. These fossils showed many typical vertebrate
the presence of a notochord serving as chief skeletal axis, and characters including a heart, paired eyes, otic (ear) capsules, and
the plan of the circulatory system all resemble these features in what has been interpreted as rudimentary vertebrae.
amphioxus. The earliest ostracoderms were armored with bone in their
Ammocoetes do have several characteristics lacking in amphi- dermis and lacked paired fins that later fishes found so impor-
oxus that are homologous to those of vertebrates. These include tant for stability (Figure 23.14). The swimming movements of one
a chambered heart, tripartite brain, paired special sense organs of the early groups, the heterostracans (Gr. heteros, different,
derived from ectodermal placodes, and pituitary gland. The kidney ⫹ ostrakon, shell) must have been imprecise, although sufficient
is pronephric (pp. 673–674) and conforms to the basic vertebrate to propel them along the ocean bottom where they searched for
plan. Instead of the numerous pharyngeal slits of amphioxus, there food. With fixed circular or slitlike mouth openings they may have
are only seven pairs of pharyngeal pouches and slits in ammocoe- filtered small food particles from the water or ocean bottom. How-
tes. From pharyngeal bars separating the pharyngeal slits project gill ever, unlike the ciliary filter-feeding protochordates, ostracoderms
filaments bearing secondary lamellae much like the more extensive sucked water into the pharynx by muscular pumping, an impor-
gills of modern fishes (see Figure 24.29, p. 533). Ammocoetes also tant innovation that suggests to some authorities that ostracoderms
have a true liver replacing the hepatic cecum of amphioxus, a gall- may have been active predators that fed on soft-bodied animals.
bladder, and pancreatic tissue (but no distinct pancreatic gland).
Ammocoetes display the most primitive condition for these
The term “ostracoderm” does not denote a natural evolutionary
characteristics of any living vertebrate. They clearly illustrate
assemblage but rather is a term of convenience for describing sev-
many shared derived characters of vertebrates that are obscured
eral groups of heavily armored extinct jawless fishes.
in the development of other vertebrates. They may approach most
closely the supposed body plan of the ancestral vertebrate.
During the Devonian period, the heterostracans underwent
a major radiation, producing numerous peculiar-looking forms.
The Earliest Vertebrates Without ever evolving paired fins or jaws, these earliest verte-
The earliest known vertebrate fossils, until recently, were armored brates flourished for 150 million years until becoming extinct
jawless fishes called ostracoderms (os-trak⬘o-derm) (Gr. ostra- near the end of the Devonian period.
kon, shell, ⫹ derma, skin) from late Cambrian and Ordovician Coexisting with heterostracans throughout much of the
deposits. During the last 10 years researchers have discovered a Devonian period were osteostracans (Gr. osteon, bone, ⫹ ostra-
number of 530-million-year-old fossils in the amazing Chengjiang kon, shell). Osteostracans had paired pectoral fins, an innovation
deposits belonging to two (possibly only one) fishlike vertebrates: that functioned to improve swimming efficiency by controlling

Anaspid
Heterostracan

Osteostracan

Figure 23.14
Three ostracoderms, jawless fishes of Silurian and Devonian times. They are shown as they might have appeared while searching for food on the
floor of a Devonian sea. All were probably filter feeders, but employed a strong pharyngeal pump to circulate water rather than the much more
limiting mode of ciliary feeding used by their protochordate ancestors (presumably resembling amphioxus for this feature).

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 www.mhhe.com/hickmanipz14e CHAPTER 23 Chordates 511

yaw, pitch, and roll. A typical osteostracan, such as Cephalaspis state shared by all jawed fishes and tetrapods. Agnathans, how-
(Gr. kephalē, head, ⫹ aspis, shield) (Figure 23.14), was a small ever, are defined principally by the absence of jaws, a character
animal, seldom exceeding 30 cm in length. It was covered with that is not unique to jawless fishes since jaws are lacking in ver-
a heavy, dermal armor of cellular bone, including a single-piece tebrate ancestors. Thus, Agnatha is paraphyletic.
head shield. Examination of internal features of the braincase The origin of jaws was one of the most important events in
reveal a sophisticated nervous system and sense organs, similar vertebrate evolution. The utility of jaws is obvious: they allow
to those of modern lampreys. predation on large and active forms of food not available to jaw-
Another group of ostracoderms, the anaspids (Figure 23.14), less vertebrates and permit manipulation of objects. Ample evi-
were more streamlined than other ostracoderms. These and other dence suggests that jaws arose through modifications of the first
ostracoderms enjoyed an impressive radiation in the Silurian and or second of the serially repeated cartilaginous gill arches. But
Devonian periods. However, all ostracoderms became extinct by how did this mandibular arch change from a function of gill sup-
the end of the Devonian period. port and ventilation to one of feeding as jaws? Expansion of this
For decades geologists have used strange, microscopic tooth- arch and evolution of new, associated muscles may have first
like fossils called conodonts (Gr. kōnos, cone, ⫹ odontos, tooth) assisted gill ventilation, perhaps to meet the increasing metabolic
to date Paleozoic marine sediments without having any idea what demands of early vertebrates. Once enlarged and equipped with
kind of creature originally possessed these elements. The discov- extra muscles, the first pharyngeal arch could have easily been
ery in the early 1980s of fossils of complete conodont animals modified to serve as jaws. Evidence for this remarkable transfor-
has changed this situation. With their phosphatized toothlike ele- mation includes, first, both gill arches and jaws form from upper
ments, myomeres, notochord, and paired eye and otic capsules, and lower bars that bend forward and are hinged in the middle
conodonts clearly belong to the vertebrate clade (Figure 23.15). (Figure 23.16). Second, both gill arches and jaws are derived
Although their exact position in this clade is unclear, they are from neural crest cells. Third, the jaw musculature is homolo-
important in understanding the evolution of early vertebrates. gous to the original gill support musculature as evidenced by
cranial nerve distribution. Nearly as remarkable as this drastic
The Swedish paleozoologist Erik Stensiö was the first to approach morphological remodeling is the subsequent evolutionary fate of
fossil anatomy with the same painstaking attention to minute detail jawbone elements—their transformation into ear ossicles of the
that morphologists have long applied to the anatomical study of liv- mammalian middle ear (see the note on p. 745).
ing fishes. He developed novel and exacting methods for gradually An additional feature characteristic of all gnathostomes is the
grinding away a fossil, a few micrometers at a time, to reveal inter- presence of paired pectoral and pelvic appendages in the form of
nal features. He was able to reconstruct not only bone anatomy, fins or limbs. These likely originated as stabilizers to check yaw,
but nerves, blood vessels, and muscles in numerous groups of pitch, and roll generated during active swimming. The fin-fold
Paleozoic and early Mesozoic fishes. His innovative methods are hypothesis has been proposed to explain the origin of paired fins.
widely used today by paleozoologists.

Gill-supporting cartilages
Early Jawed Vertebrates Hyomandibular cartilage
All jawed vertebrates, whether extinct or living, are collectively Palatoquadrate cartilage
called gnathostomes (“jaw mouth”) in contrast to the jawless Braincase
vertebrates, the agnathans (“without jaw”). Gnathostomes are a
monophyletic group since presence of jaws is a derived character

Notochord

Eye Conodont elements Myomeres Meckel's cartilage

Figure 23.16
Figure 23.15 How vertebrates got their jaws. Resemblance between jaws and
Restoration of a living conodont. Conodonts superficially resembled gill supports of primitive fishes, such as this Carboniferous shark,
amphioxus, but they possessed a much greater degree of suggests that the upper jaw (palatoquadrate) and lower jaw (Meckel’s
encephalization (paired eyes and otic [ear] capsules) and bonelike cartilage) evolved from structures that originally functioned as gill
mineralized elements—all indicating that conodonts were chordates supports. The gill supports immediately behind the jaws are hinged
and probably vertebrates. Conodont elements are considered to be like jaws and served to link the jaws to the braincase. Relics of this
part of a food-handling apparatus. transformation are seen during the development of modern sharks.

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 512 PART THREE Diversity of Animal Life

Devonian placoderm

Acanthodian

Figure 23.17
Early jawed fishes of the Devonian period, 400 million years ago. Shown are a placoderm (left) and an acanthodian (right). Jaws and gill supports
from which the jaws evolved develop from neural crest cells, a diagnostic character of vertebrates. Most placoderms were bottom dwellers that fed
on benthic animals although some were active predators. Acanthodians carried less armor than placoderms and had large, anteriorly placed eyes
and prominent spines on paired fins. Most were marine but several species lived in freshwater.

According to this hypothesis, paired fins arose from paired con- produced the modern fishes and all tetrapods, including you, the
tinuous, ventrolateral folds or fin-forming zones. The addition of reader of this book.
skeletal supports in the fins served to enhance their properties of Among the first jawed vertebrates were the heavily armored
providing stability during swimming. Evidence for this hypothesis placoderms (plak⬘o-derm) (Gr. plax, plate, ⫹ derma, skin).
is found in the paired flaps of Myllokunmingia and anaspids and These first appear in the fossil record in the early Silurian period
in the multiple paired fins of acanthodians, also described in this (Figure 23.17). Placoderms evolved a great variety of forms, some
section. However, pectoral fins appear in the fossil record before very large (one was 10 m in length!) and grotesque in appear-
pelvic fins, suggesting a more complex evolutionary scenario. In ance. They were armored fish covered with diamond-shaped
one fish lineage the muscle and skeletal supports in the paired scales or with large plates of bone. All became extinct by the end
fins became strengthened, allowing them to become adapted of the Devonian period and appear to have left no descendants.
for locomotion on land as limbs. The origin of jaws and paired However, acanthodians, a group of early jawed fishes known
appendages may be linked to a second Hox duplication, near the from the Silurian to Permian periods, and characterized by large,
origin of the gnathostomes. Both jaws and paired fins were major anteriorly set eyes and fins with large spines (Figure 23.17), are
innovations in vertebrate evolution, among the most important included in a clade that underwent a great radiation into the
reasons for the subsequent major radiations of vertebrates that bony fishes that dominate the waters of the world today.

SUMMARY
Phylum Chordata is named for the rodlike notochord that forms a Subphylum Vertebrata includes the backboned members of the
stiffening body axis at some stage in the life cycle of every chor- animal kingdom (hagfishes actually lack vertebrae but are included
date. All chordates share five distinctive hallmarks that set them with the Vertebrata by tradition because they share numerous homol-
apart from all other phyla: notochord, dorsal tubular nerve cord, ogies with vertebrates). As a group vertebrates are characterized by hav-
pharyngeal pouches, endostyle, and postanal tail. Two of the three ing a well-developed head, and by their comparatively large size,
chordate subphyla are invertebrates and lack a well-developed high degree of motility, and a distinctive body plan that embodies
head. They are Urochordata (tunicates), most of which are sessile several distinguishing features that permitted the exceptional adap-
as adults but all of which have a free-swimming larval stage, and tive radiation of the group. Most important of these are the living
Cephalochordata (lancelets), fishlike forms that include the famous endoskeleton that allows continuous growth and provides a sturdy
amphioxus. framework for efficient muscle action and attachment, a muscular
Chordates have evolutionary affinities to echinoderms and hemi- pharynx with slits and gills (lost or greatly modified in terrestrial
chordates, although their precise origins have been controversial. vertebrates) with vastly increased respiratory efficiency, a muscu-
Most zoologists now consider the chordate ancestor to have been a larized gut, chambered heart, and glomerular kidneys for meeting
small, free-swimming, filter-feeding creature. higher metabolic demands, and an advanced nervous system with

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 www.mhhe.com/hickmanipz14e CHAPTER 23 Chordates 513

a distinct brain and paired sense organs. Insight into the early evo- and ammocoetes, the larval form of living lampreys. Evolution of
lution of vertebrates is provided by examination of several fossil jaws and paired appendages likely contributed to the incredible suc-
forms, including Haikouella, conodonts, and ostracoderm fishes, cess of one group of vertebrates, the gnathostomes.

REVIEW QUESTIONS
1. What characteristics are shared by the three deuterostome phyla 7. Both sea squirts (urochordates) and lancelets
that indicate a monophyletic group of interrelated animals? (cephalochordates) are filter-feeding organisms. Describe the
2. Explain how the use of a cladistic classification for the filter-feeding apparatus of a sea squirt and explain in what
vertebrates results in important regroupings of the traditional ways its mode of feeding is similar to, and different from, that
vertebrate taxa (refer to Figure 23.3). Why are certain of amphioxus.
traditional groupings such as Osteichthyes and Agnatha not 8. Explain why it is necessary to know the life history of a
recognized in cladistic usage? tunicate to understand why tunicates are chordates.
3. Name five hallmarks shared by all chordates, and explain the 9. List three groups of adaptations that guided vertebrate
function of each. evolution, and explain how each has contributed to the
4. In debating the question of chordate origins, zoologists eventually success of vertebrates.
agreed that chordates must have evolved within the deuterostome 10. In 1928 Walter Garstang hypothesized that tunicates
assemblage rather than from a protostome group as earlier resemble the ancestral stock of the vertebrates. Explain this
argued. What embryological evidences support this view? hypothesis.
5. Offer a description of an adult tunicate that would identify it 11. What is the phylogenetic position of Haikouella, and what
as a chordate, yet distinguish it from any other chordate group. evidence supports its placement there?
6. Amphioxus long has been of interest to zoologists searching 12. Distinguish between ostracoderms and placoderms. What
for a vertebrate ancestor. Explain why amphioxus captured important evolutionary advances did each contribute to
such interest and why it no longer is considered to resemble vertebrate evolution? What are conodonts?
closely the most recent common ancestor of all vertebrates. 13. Explain how zoologists think the vertebrate jaw evolved.

SELECTED REFERENCES
Ahlberg, P. E. 2001. Major events in early vertebrate evolution. London, vertebrate origin hypotheses. Gee links much of the recent genetic,
Taylor & Francis. Evolution of vertebrates up to the split of major jawed developmental, and molecular evidence in his discussion.
fish groups, incorporating molecular, fossil, and embryological data. Gould, S. J. 1989. Wonderful life: the Burgess Shale and the nature of history.
Many important contributions, but some conclusions are controversial. New York, W.W. Norton & Company. In this book describing the
Alldredge, A. 1976. Appendicularians. Sci. Am. 235:94–102 (July). Describes marvelous Cambrian fossils of the Burgess Shale, Gould “saves the best
the biology of larvaceans, which build delicate houses for trapping for last” by inserting an epilogue on Pikaia, the first known chordate.
food. Jeffries, R. P. S. 1986. The ancestry of the vertebrates. Cambridge,
Bowler, P. J. 1996. Life’s splendid drama: evolutionary biology and the Cambridge University Press. This book is an excellent summary of
reconstruction of life’s ancestry 1860–1940. Chicago, University of the deuterostome groups and of the various competing hypotheses of
Chicago Press. Thorough and eloquent exploration of scientific debates vertebrate ancestry.
over reconstruction of history of life on earth; chapter 4 treats theories Long, J. A. 1995. The rise of fishes: 500 million years of evolution.
of chordate and vertebrate origins. Baltimore, The Johns Hopkins University Press. An authoritative,
Carroll, R. L. 1997. Patterns and processes of vertebrate evolution. New liberally illustrated evolutionary history of fishes.
York, Cambridge University Press. A comprehensive analysis of the Mallatt, J., and J.-Y. Chen. 2003. Fossil sister group of craniates: predicted
evolutionary processes that have influenced large-scale changes in and found. J. Morph. 258:1–31. Reevaluation of Haikouella fossils
vertebrate evolution. revealed several features that suggest it is the sister taxon to craniates.
Donoghue, P. C. J., P. L. Forey, and R. J. Aldridge. 2000. Conodont affinity Maisey, J. G. 1996. Discovering fossil fishes. New York, Henry Holt &
and chordate phylogeny. Biol. Rev. 75:191–251. In this summary of Company. Handsomely illustrated chronology of fish evolution with
early chordate evolution, the authors provide evidence that conodonts cladistic analysis of evolutionary relationships.
are vertebrates and that lampreys and hagfishes do not form a Shimeld, S. M., and P. W. Holland. 2000. Vertebrate innovations. Proc.
monophyletic group. Natl. Acad. Sci. 97:4449–4452. Focuses on developmental characters,
Forey, P., and P. Janvier. 1994. Evolution of the early vertebrates. Am. Sci. including neural crest, ectodermal placodes, and Hox genes.
82:554–565. Summarizes the biology and evolution of many groups of Stokes, M. D., and N. D. Holland. 1998. The lancelet. Am. Sci. 86(6):552–
ostracoderms and other primitive craniates. 560. Describes the historical role of amphioxus in early hypotheses of
Gee, H. 1996. Before the backbone: views on the origin of the vertebrates. vertebrate ancestry and summarizes recent molecular data that has
New York, Chapman & Hall. Outstanding review of the many rekindled interest in amphioxus.

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