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/ 27
sembling the Tree of Life
eviteo sy Joel Cracraft
Michael J. Donoghue
OXFORD
UNIVERSITY PRESS
2004 Timothy Rowe
Chordate Phylogeny and Development
Chordata, our own lineage (fig, 23.1), belongs to the sue-
cessively more inclusive clades Deuterostomata, Bilateria,
Metazoa, and so forth. The organization of chordates is dis-
tinctively different from that of its metazoan relatives, and
much ofthis distinction is conferred by unique mechanisms
of development (Slack 1983, Schaeffer 1987). Throughout
chordate history, modulation and elaboration of develop-
‘mental systems are persistent themes underlying diversifica-
tion, Only by understanding how ontogeny itself evolved can
we fully apprehend chordate history, diversity, and our own,
unique place in the Tree of Life. My goal here isto present a
contemporary overview of chordate history by summarizing,
current views on relationships among the major chordate
clades in light ofa blossoming understanding of molecular,
genetic, and developmental evolution, and a wave of exci
ing new discoveries from deep in the fossil record.
‘Chordates comprise a clade of approximately 56,000
named living species that includes humans and other ani-
tmals with a notochord—the embryological precursor of
the vertebral column. Chordate history can now be traced
across at least a half billion years of geological time, and
twvice that by some estimates (Wray et al, 1996, Ayala etal
1098, Bromham etal. 1998, Kumar and Hedges 1998, Hedges
2001). Chordates are exceptional among multicellular ani-
mals in diversifying across eight orders of size magnitudes
and inhabiting virtually every terrestrial and aquatic eviron-
‘ment (MeMahon and Bonner 1985), New living chordate
384
species are still being discovered both through traditional
explorations and as molecular analyses discover cryptic taxa
{in lineages whose diversities were thought to be thoroughly
‘mapped, But itis unknown whether the pace of discovery i
now keeping up with the pace of extinction, which is acel-
etating across most major chordate clades in the wake of
human population growth (Dingus and Rowe 1998)
Many chordate clades have long been recognized by char-
acteristic adult features, for instance, birds by their feathers,
‘mammals by their hair, or turtles by ther shells. But owing
in large part to such distinetiveness, few adult morpholog-
cal features have been discovered that decisively esolve the
relationships among the chordate clades, and even after 300
years of study broad segments of chordate phylogeny remain
terra incognita
Much of the hypothesized hierarchy of higher level chor-
date relationships has been deduced from paleontology and
developmental biology (Russell 1916). Thanks othe advent
of phylogenetic systematics, both fields are expressing resut=
gent interest and progress on the question of chordate phy-
Togeny. And, as they are becoming integrated with molecular
systematic analyses, a fundamental new understanding of
chordate evolution and development is emerging,
In most other metazoans, the adult fate of embryonic cells
's determined very early in ontogeny. However as chordate
ontogeny unfolds, the fates of embryonic cells are plastic fora
longer duration. Chordate cells differentiate as signals pass Ccephalochordata
Ambulacratia
1 Cretaceous
enn
= Carboniferous]
. in
Silurian
ontnin
So eae
_
Deuterostomata
=
nciroskeyai
_ @®
Wronski Ay
——
@
CChordate Phylogeny and Development 385
Figure 23.1. Chordate phylogeny, showing the relationships of extan lineages and the oldest
fossils, superimposed on a geological me column, Nodal numbers are keyed to text headings.
between adjacent cells and tissues during the integration of
developing cell lineages into functioning tissues, organs, and
organ systems, Seemingly subtle modulations in early ontog
eny by this information exchange system have occurred many
times over chordate history to yield cascades of subsequent
developmental effects that underlie chordate diversity (Hall
1992), Molecular and developmental genetic studies are now
revealing the intricate details ofthis unique, hierarchical sys-
tem of information transfer as genes are expressed in cells and
tissues in early omtogeny. These analyses, moreover, generate
datathat possess recoverable phylogenetic signal and are yield-
ing fundamental insights into the evolution of development.
An important conclusion already evident is that major
innovations in chordate design were generally derived from
preexisting genetic and developmental pathways, whose al-
{eration transformed ancestral structures into distinctive new
features with entirely different adult functions (Shubin etal.
1997). Increase in numbers of genes was a primary media-
tor of this change, and the inductive nature of chordate de-
velopment amplified that change via epigenesis, which occurs
as familiar physical forces and dynamic processes interact
‘with the cells and tissues of a developing organism. These
include gravity, adhesion, diffusion, mechanical loading, elec-
trical potentials, phase separations, differential growth among,
tissues and organs, and many others (Rowe 1996a, 19966).
Morphogenic and patterning effects are the developmental
‘outcomes of these recognized physical phenomena, because
they affect interactions among virtually all developing cells, 386 The Relationships of Animals: Deuterostomes
tissues, and organs (Newman and Comper 1990). In the
inductive environment of chordate ontogeny, epigenesis has
been especially influential, triggering its own cascades of rapid
and nonlinear developmental change. Understanding how
epigenesis mediates the genetic blueprint of ontogeny is fun-
damental to understanding how such diverse chordates 2s
sea squirts, coelacanths, and humans emerged from their
‘unique common ancestor.
Recognizing that most biologists reading this volume
study living organisms, the focus below is on extant taxa
However, extinct taxa are discussed as well, and their inclu
sion helps to emphasize the timing of origins of the major
‘extant chordate clades and to acknowledge the diversity and
antiquity of the lineages of which they are a part. Moreover,
the framework of chordate relationships presented below
came from the simultaneous consideration of all available
evidence: In resolving several parts ofthe chordate tree dis-
cussed below, evidence afforded by fossils proved more im-
portant than that derived from living species (Gauthier et al.
19882, 1989, Donoghue etal, 1989)
‘Taxonomic Names, Ancestry, and Fossils
Older views of chordate relationships make reference to
g70ups united on general similarity or common gestalt, In
contrast, the names used below designate lineages whose
members appear to be united by common ancestry (de
Queiroz and Gauthier 1992). To avoid ambiguity, the mean
ings of these names are defined in terms of particular an-
cestors of two or more living taxa (ie, node-based or crown,
clade names). follow an arbitrary but useful narativecon-
vention in specifying the crown clade names used below in
terms oftheir most recent common ancestry with humans.
For example, the name Chordata refers to the clade stem-
‘ming from the last common ancestor that humans share
with living tunicates and lancelets; the name Vertebrata des-
{gnates the clade stemming from the last common ancestor
that humans share with lampreys; and so on (fig. 23.1). Th
is arbitrary in the sense that many other possible |
ing specifiers among amniotes (vz. birds, turtles, eroco-
dilians, lizards) in place of humans would designate the
same clades
Stem-based names are used in reference toa node otter
‘minal taxon, plus all extinct taxa that are more closely re-
lated to ic than to some other node or terminal taxon. Inthe
interests of simplifying the complex taxonomy that evolved
under the Linnaean system, follow a convention now gain-
Ing popularity that employs the prefix "Pan-” to designate
stem + crown lineages (Gauthier and de Queiroz 2001), For
‘example, Pan-Mammalia refers to the clade Mammalia, plus
allextinet species closer to Mammalia than tits extant sister
taxon Reptilia. The clade Pan-Vertebrata includes Vertebrata
pls all extinct taxa closer to Vertebrata than to hagfishes,
and so forth,
Chordate Relationships
Node 1. The Chordates (Chordata)
Chordata (fig. 23.1) comprise the lineage arising from the
last common ancestor that humans share with tunicates and
Tancelets. Tunicates are widely regarded as the sister taxon
to all other chordates (Gegenbaur 1878, Schaefer 1987,
Cameron et al, 2000), and tunicate larvae are commonly,
viewed as manifesting the organization of the adult ances-
tral chordate (e., Meinertzhagen and Okamura 2001). But
some systematists contend that lancelets are the more dis-
tant outgroup (Lovirup 1977, Jeffries 1979, 1980, 1986,
Jelties and Lewis 1978). The controversy stems in part from
the fact that living adult tunicates are small and built from a
small number of cells. Even their larvae appear highly diver-
gent from other living chordate larvae. It naw seems likely
that they were secondarily simplified in having lost half or
more of the Hox genes from the single cluster that was prob-
ably present in deuterostomes ancestrally (Holland and
Garcia-Femnndez 1996), hence, too, the loss of adult struc-
tures governed by these genes. As adults, tunicates are de-
rived in losing the coelom and hindgut (Holland and Chen
2001) and are speculated to be pedomorphic in having lost,
segmentation Holland and Garcia-Ferandez 1996). One
character shared by tunicates and cranites, to the exclusion
of lancelets, is expression of the Pax 2/5/8 gene in a region
‘of the developing brain known as the isthmocerebellar-
midbrain-hindbrain boundary. The lack of Pax 25/8 expres
sion in lancelets implies ether secondary loss, or independent
‘expression in tunicates and craniates (Butler 2000), or that
tunicates share closer common ancestry with other chordates
than do lancelets. Having separated from other chordates by
at least a alf-billion years ago (Wray et al, 1996, Bromham,
etal, 1998, Kumar and Hedges 1998, Hedges 2001), and
without a useful fossil record (below), relationships among
these chordates must be viewed as tenuous (Gauthier eta.
1988a, Donoghue etal, 1989). More for narrative conve-
hience than conviction, follow current convention in trat-
ing tunicates as sister lineage to all other chordates
Chordate Characters
The notochord. The namesake feature of chordates isa
premiere example of embryonic induction and patterning
in which differentiation of the embryo along 2 dorsoventral
axis launches a cascade of subsequent developmental events
(Slack 1983, Schaeffer 1987). “Dorsalization” is controlled
by the Hedgehog gene and signaling by bone morphoge
protein, or BMP (Shimeld and Holland 2000). As in other
bilaterins, chordates develop from thee primary embryonic
layers. These are the outer ectoderm, the inner endoderm,
and the mesoderm, which arises from cells that migrate be-
tween the inner and outer layers. Chordate mesoderm de-
velops inthe upper hemisphere of the embryonic gastrula,
is identity being induced partly asitscels stream across the dorsal lip of the primordial opening (blastopore) into the
inner cavity (archenteron) of the embryo, and partly by sig-
naling from endoderm at the equator of the embryo (Hall
1992). Mesoderm cells reaching the dorsal midline condense
into a stip of cells known as chordamesoderm, which later
differentiates to become the notochord. The notochord in
tum induces overlying ectoderm to form the dorsal neural
plate, criggering another morphogenic chain of eventsas he
chordate central nervous system (CNS) differentiates and
begins to grow. In most chordates, the mesoderm immedi-
ately adjacent to the notochord takes on special properties, a5
does the ectoderm immediately adjacent to the neural plate
Elaboration ofthese dorsal structures is tied closely to evolu-
tion of the organs of information acquisition and integration,
1s well as to locomotion
The chordate centro! nervous system, Induction of a dor-
sal neural plate is directed by the underlying chordameso-
derm (above). This is the first step of neurulation, in which
the nervous system arises, becomes organized, and helps
direct the integration of other parts of the developing em-
bryo. During neurulation, longitudinal neural folds arise
along the edges of the neural plate, perhaps under the direc
tion of the adjacent mesoderm (Jacobson 2001), and meet
6on the midline to enclose a space that initially lay entirely
‘outside of the embryo. This “hollow” comprises the adult
ventricular system of the brain and central canal ofthe spi-
nal cord, Itislined with ited ependymal cellsand its lumen
fills with cerebrospinal fluid. This original “periventricular”
layer becomes the primary region from which subsequent
neural cells arise in the brain (Butler and Hodos 1996).
Molecular signaling during neurulation also produces
anteroposterior regionalization in chordate embryos. The
rostral end of the central nerve cord swells to form the brain,
which differentiates into three regions that express distinct
_gene families and witich have distinct adult fates, The rostral-
‘most (diencephalic) domain of the neural tube expresses
the Otx gene family and is connected to specialized light-
sensitive cells Behind this sa caudal hindbrain-spinal cord)
division, in which Hox genes are active and which receives
rnonvisual sensory inputs, Between the two lies an interme-
diate region marked by expression of the Pax 2/5/8 pattern-
{ng gene that is more problematically compared with a region
Jnown as the isthmocerebellar-midbrain-hindbrain bound-
ary and involves the ear (Meinertzhagen and Okamura 2001,
Butler 2000, Shimeld and Holland 2000). Pax 2/5/8 is ex-
pressed in tunicates and craniates, but not lancelets (below).
Other bilaterianshavea longitudinal nerve cord and brain
but itis ventrally positioned; hence, biologists long main-
tained that the chordate dorsal nerve cord arose indepen-
dently. However, both brains express orthologous homeobox
genes in similar spatial patterns. For instance, the fruit fly
hhasa regionalized neural tube with similarities in rostrocaudal
and mediolateral specification to chordates (Arendt and
Nabler-Jung 1999, Nielsen 1999, Butler 2000; for alterna-
tive view, see Gerhart 2000). Its rostral brain is specified by
CChordate Phylogeny and Development 387
the regulatory gene Orthodentile, a homologue to the chor:
date Otx family genes, and it receives input from paired eyes.
This suggests a common blueprint. Biologists long found it
difficult to accept the two nerve cords as homologous ow:
ing to their different positions relative to the mouth, but it
now appears that the deuterostome mouth is a new struc-
ture and not homologous to the mouth in protestomes
(Nielsen 1999).
Special sensoryorgansof the head. Aneyeanclearof unique
design were probably present in chordates ancestally. The
master control gene Pax6 is expressed during early develop-
ment in paired neural photoreceptors—eyes—in chordates
and many other bilaterians. Paired eyes and ears, however
rudimentary, were almost certainly present in chordates
ancestrally (Gehring 1998). However, Pax6 expression in
chordates is manifested in eye morphogenesis that follows a
unique hierarchy of pathways and inductive signals, and in
which considerable diversity evolved among the different
chordates lineages. Living tunicates, lancelets, and haglish
‘each appear uniquely derived, leaving equivocal exactly what
type of eye was present in chordates ancestrally. In tunicates,
the larval eye forms a small vesicle that contains a sunken,
pigmented mass. Internal to the pigment les a layer of cells,
that are directed radially toward it, and overlying the pigment
are two hemispherical refractive layers (Gegenbaur 1878)
“These same relationships occur in all other chordates. How-
ever, in tumicates an optic vesicle i present only in larvae and
is generally unpaired. Nevertheles, i is an outgrowth of the
COtx-expressing region ofthe forebrain and it expresses Pax,
as do the paired eyes of vertebrates and unlike the median
pineal eye (Meinertzhagen and Okamura 2001). In lancelets|
there is a single, median frontal eye, which also expresses
Pax6, and like the bilateral eyes of vertebrates itis inked with
cells in the primary motor center (Lacalli 1996a, 1996b,
Butler 2000). In the case of lancelets, the forward extension
of the notochord may be implicated in secondary fusion of
the single eye. Hagfsh have paired eves, but they are poorly
developed compared with most vertebrates.
‘The chordate ear or otic system eventually differentiated
into the organs of both balance and hearing in vertebrates.
Adult tunicates have sensory hair cells that support a pig-
mented otolith and are grouped into gelatinous copular
organs located inthe atrium ofthe adult, These cells express
‘members of the Pax 2/5/8 gene family, as do the otic placodes
i craniates but not ancelets) and in early development they
are topographically similar to craniate otic placodes. How-
ever, placodes themselves are not yet present. Similar gene
expression, cellular organization, and topography point to
the probable homology of the otic organ in all chordates|
(Shimeld and Holland 2000, Jeffries 2001, Meinertzhagen
and Okamura 2001),
Hormonal glands. Two hormonal glands arose in chor-
dates ancestrally o exert novel control over growth and meta-
bolism. The pituitary is compound structure that forms via
the interaction between neurectoderm, which descends from 388 The Relationships of Animals: Deuterostomes
‘the developing brain toward the roof ofthe pharynx, and oral
ectoderm that folds inward to line the inside of the mouth.
ctoderm forms Rathke’s pouch and becomes the glandular
par ofthe pituitary, whereas neural tissue from the floor of
the diencephalon becomes its infundibular portion. The in-
fundibulum is present in lancelets and craniates, but its ho-
mologue in tunicates is unclear. However, in tumicates the
homologue of the glandular portion, known as the neural
sland, les inthe same position with respect to both brain
and pharyngeal roof (Barrington 1963, 1968, Maisey 1986)
The second hormonal gland, the endos.yle, develops in
‘a groove in the floor ofthe larval pharynx in tunicates, lance-
lets, and in larval lampreys. Its cells form thyroid follicles
that secrete iodine-binding hormones. Its homologue in
gnathostomes is probably the thyroid gland, which also
develops in a median out-pocketing in the floor ofthe phar
ynx, and also forms thyroid follicles that secrete iodine-
binding hormones (Schaeffer 1987). Thyroid hormone
production is controlled in large measure by the pituitary
gland and affects growth, maintenance of general tissue
metabolism, reprocluctive phenomena, and in some taxa
metamorphosis.
Tadpole shaped orva. Unlike the ciliated egg-shaped lar-
vae of hemichordates and echinoderms, the chordate larva
{tadpole shaped, with a swollen rostral end and a muscular
tail. The rostral end houses the brain, beneath which le the
rostral end of the notochord, and the pharynx and gut tube.
Behind the pharynx is a tail equipped with muscle deriving
from caudal mesoderm (Maisey 1986, Schaeffer 1987). Al
though lacking tailsas adults, the larvae of many species have
tails of comparatively simple construction with muscle that
form bilateral bands, in contrast to the segmental muscle
blocks found in euchordates (below). A recent study of tailed
and tailless rmicate larvae (Swalla and Jeffery 1996) found.
that the Manx gene is expressed in the cells ofthe tailed form,
butitis down-regulated in the tail-less species, and that com
plete los of the tail can be attributed to disrupted expres
sion of the single gene. Whether Manx was central to the
origin of the tal in chordates is unknown, but this study
highlights the potential genetic simplicity underlying com-
plex adult structures.
Pan-Chordata
Although an extensive fossil record is known for many clades
lying within Chordata, no fossils are known at present that
Iie with any certainty on its stem,
Node 2. The Tunicates or Sea Squirts (Urochordata)
Chordate species all can be distributed between the tunicates|
and euchordates, its two principal sister clades (fig, 23.1).
The tunicates comprise a diverse marine clade that includes
roughly 1300 extant species distributed among the sessile
ascidians, and the pelagic salps and larvaceans (Jamieson
1991), Tunicate monophyly is well supported (Gegenbaur
1878, Maisey 1986). Asadults, the tunicate body isenclosed
‘within the runic, an acellular membrane made of celiulose-
like tunicin, tis derived from ectoderm, and in tunicates it
‘may contain both amorphous and crystallin calcium carbon-
ate spicules (Aizenberg et al. 2002). Echinoderms possess
crystalline calcium in ectodermal structures, raising the
‘question of whether biomineralization was present in deu-
terostomes ancestrally (see below). The tunic presents an
‘outwardly simple body, but it cloaks a much more complex
and derived organism. The pharynx is perforated by two pairs
of slits and is enormously enlarged for suspension feeding
‘The pharynx size obliterates the coelom, a cavity inside the
‘body walls that surrounds the gut in tunicat larvae and most
adult chordates, Unique incurrent and excurrent pores sup-
ply a stream of water through the huge pharynx, which in
some species serves in locomotion, All tunicates are mobile
aslarvae, but not al species have larval tails. The pelagic salps
and larvaceans are thought to be more basal and to reflect,
the primitive adult lifestyle.
Pan-Urochordata
The fosstl record of tunicates is sparse and tentative, but
potentially long, The oldest putative tunicate, Cheungkongella
aancestralis, from the Early Cambrian of China (Shu et al
2001a) is known from a single specimen. It evidently pre-
serves a two-fold division of the body into an enlarged pha-
‘ryngeal region with pharyngeal openings, a large oral siphon
surrounded by short tentacles, and a smaller excurrent si-
phon. The body appears wholly enclosed in a tuniclike outer
covering, It has shor tail-like attachment structure, a derived
feature placing Cheungkongella among crown tunicates. This
fossil if properly interpreted, marks the Early Cambrian as
‘the minimum age of divergence of tunicates from other ch
dates and implies a Precambrian origin for Chordata
‘A possible sem tunicat fossil was brought to light through
a reinterpretation of Jackelacarpus oklahomersis, a Carborit-
erous "mitrate” (Dominguez et al. 2002). High-resolution
X-ray computed tomography (e.,, Rowe etal, 1995, 1997,
1999, Digital Morphology 2003) provided new details of
internal anatomy and revealed the presence of paired tuni-
gill skeletons. Jackelocarpus and a nurnber of si
lar, tiny Paleozoic fossils have a calcite exoskeleton over their
hhead and pharynx and are generally thought to lie as stem
‘members of echinoderms or various basal chordate clades
effries 1986, Dominguez et al, 2002). The mitrates may
prove to be pataphyletic, and its members assignable to dif-
{erent deuterostome clades. The eventual placement of all of
these fossils will have bearing on our interpretation of basal
chordate relationships, and on the structure and history of
‘mineralized tissues,
Node 3. Chordates with a Brain (Euchordata)
Euchordata comprise the last common ancestor that humans
share with lancelets (but see caveats above), and all ofits descendants (fig, 23.1). Apart from the tunicatesand a single
ancient fossil of uncertain affinities (below), all other chor-
dates are members of Euchordata. Expanding on the inno-
vations that arose in chordates ancestrally, euchordates
ranifgst more complex genetic control over development.
‘This was accompanied by further elaboration of the CNS and
special sense organs, and a fundamental reorganization ofthe
‘trunk musculature and locomotor system.
Euchordate Characters
Increased genetic complexty |. Euchordates express Mot,
HNF-3, and Netrin genes, whereas only Hedgehog is expressed
in tunicates. This evident increase in homeobox expression
corresponds to elaborated dorsoventral patterning in the
CNS, Additional genes are also expressed in more elaborate
anteroposterior regionalization, including BFI and Islet genes
(Holland and Chen 2001). Tunicates express only one to five
Hox genes, whereas lancelets express 10 Hox genes in one
cluster affecting broader regions ofthe brain and nerve cord
Although poorly sampled, at least one hemichordate (Sac~
coglossus) expresses nine Hox genes in its single cluster. Tu-
nicates therefore may have lost genes that were present in
deuterostomes encestally (Holland and Garcia-Femandez
1996).
Elaboration of the brain .Lancelets were long thought
to have virtually no brain at all, but recent structural studies
reveal an elaborate brain and several unique resemblances
to the brain in craniates (Lacalli 1996a, 1996b, Butler 2000).
Reticulospinal neurons differentiate in the hindbrain, where
they are involved in undulatory swimming and movements
associated withthe startle reflex. Also present in lancelets are
homologues of trigeminal motor neurons, which are involved
in pharyngeal movement, and possibly other cranial nerves
(Fritzsch 1996, Butler 2000), Additionally, the neural tube
is differentiated into an inner ependymal cell layer (gray
ratter) and synaptic outer fibrous layer (white matter, Maisey
1986) and is innervated by intermyotomal dorsal nerve roots
that cary sensory and motor fibers (Schaeffer 1987), Sev-
cra ofthese fearues lie partly or wholly within the expres-
sion domain of Hox genes.
Flaboraton of the special senses An olfactory organ oc-
‘curs in lancelts, inthe form of the corpuscles of de Quatre
fages. These are a specialized group of anterior ectodermal
cells that send axonal projections to the CNS via the rostral
nerves. They are marked by expression of the homeobox gene
AmphiMsx, which is also expressed in craniate ectodermal
thickenings known as placodes (below), but no true placodes
have been observed in lancelets or tunicates (Shimeld and.
Holland 2000). The olfactory organ is highly developed in
neatly all other euchordates.
Segmentation. Segmentation arses when mesoderm along
either side of the notochord subsivides to form somites. These
are hollow spheres of mesoderm that mature into muscle
blocks known as rayomeres, which are separated by sheets
‘of connective tissue (myocomata). Only the mesoderm lying
Chordate Phylogeny and Development 389
clase to the notochord becomes segmented, whereas more
laterally the mesoderm produces a sheet of muscle that sur-
rounds the coelomic cavity. The segmented muscles enable
powerful locomotion, producing waves of contraction that
‘pass backward and propel the body ahead. Segmentation is
accompanied by Fringe (or its homologue) expression and,
signaling by the Notch protein, features shared with other
segmented bilaterians. These regulate the timing and syn-
chronization of cell-to-cell communication required of seg-
‘mental patterning and the formation of tissue boundaries
(Evrard et al. 1998, Jiang et al. 2000)
Other features "Also aising from mesoderm is a blood
circulatory system of stereotyped arterial design, with a dorsal
and ventral aorta linked by branchial vessels, and a comple-
mentary venous system (Maisey 1986). Other transforma-
tions traceable tothe ancestral euchordate yielded a larva that
isessentally a miniature, bilateral adult. As adults, a median
fin ridge increases thrust area while helping to stabilize move-
‘ment through the water (Schaeffer 1987).
Pan-Euchordata
‘The oldest stem euchordate fossil may be the Early Cambrian
‘Yunannozoon from the Chengjiang lagerstate of southern
‘China (Chen etal, 1995, Shuet al. 2001, Holland and Chen
2001). It is known from a single specimen that shows evi-
dence of segmental muscle blocks, an endostyle, notochord,
and a nonmineralized pharyngeal skeleton, Little more than
a flattened smear, the chordate affinities ofthis problematic
fossil are debatable
Node 4. The Lancelets (Cephalochordata)
“The lancelets, sometimes known as amphioxus, form an an-
cient lineage that today consists of only 30 species (Gans and
Bell 2001). Branchiostora consists of 23 species and Epigonich
thyes includes seven (Poss and Boschung 1996, Gans et al
1996). Lancelets are suspension feeders distributed widely in
twopical and warmn-temperate seas. The larvae are pelagic, and
cone possibly pedomorphic species remains pelagic as an adult.
Adults ofthe other species burrow into sandy substrate, pro-
‘wuding their heads into the water column to fed.
‘Adult ancelts lack an enlarged head. They are unique in
the extent of both the notochort! and cranial somite, which
extend tothe very front ofthe body. single median eye also
distinguishes them, which, based on AmphiOtx expression,
may be homologous tothe paired eyes of other chordates and
Dilaterians (Lacalli 1996a, Butler 2000). Their feeding appa-
ratus involves a unique ciliated wheel organ surrounding the
‘mouth, anda membranous antrum that surrounds the phat
ynx (Maisey 1986, Holland and Chen 2001),
Pan-Cephalochordata
A single fossil from the Early Cambrian of China, known as
Cathaymyrus (Shu et al. 1996), may be a stem cephalochor-
date and the oldest representative ofthe clade. Pikaia graclens 390 The Relationships of Animal
uterostomes
from the Middle Cambrian Burgess Shale is known from
‘humerous specimens and is popularly embraced asacephalo-
chordate (Gould 1989), but this is now questionable (Hol-
land and Chen 2001). A mitrate known as Lagynocystis
pyramidalis, from the lower Ordovician of Bohemia, may
also be a stem cephalochordate (Jeffries 1986). In all cases,
‘mote specimens and more detailed anatomical preservation
are needed to have any confidence in these assignments.
Node 5. Chordates with a Head (Craniata)
Craniata contain the last common ancestor that humans share
with hagfish, and all ts descendants (fg. 23.1). Even con-
temporary literature often confuses this clade name with the
designation Vertebrata, However, Vertebrata are properly
regarded as a clade lying within Craniata Janvier 1996).
Compared with their euchordate ancestors, ctaniates have
Increased genetic complexity, a larger brain, and more elabo-
rate paired sense organs. Larvae probably persisted as sus-
pension feeders (Mallat 1985), but adults shifted to active
predation with higher metabolic levels, more povrerful lo-
‘gesting the presence of neural crest cells. Neither specimen
shows evidence of mineralization (Shimeld and Holland
2000, Holland and Chen 2001)
Node 6. The Hagfish (Myxini)
Hagfish comprise a poorly known chordate lineage that in-
cludes 58 living species (Froese and Pauly 2001). Through-
out their life cycles, hagfish generally occupy deep marine
habitats in temperate seas, ranging from 25 to 5000 m in
depth (Moyle and Cech 2000), They scavenge lage carcasses,
burrow into soft substrate for invertebrates, and pursue small
prey through the water column. But they are difficult to
observe and little is known of their development
The monophyly of Myxint is well supported. They have
three pairs of unique tactile barbels around the nostril and
‘mouth, anda single median nostril of distinct structure. Many
other features distinguish them from other craniates, but
some may reflect secondary loss, including absence of the
epiphysis and pineal organ, reduction of the eyes, presence
of only a single adult semicircular canal, and a vestigial lt-
«eral lne system confined to the head (Hardisty 1979, Maisey
1986, 2001)
Pan-Myxini
Only three fossil species have been allied to the hagfish. The
least equivocal is Myxinikela siroka, from the Carboniferous
Mazon Creek deposits of Ilinois (Bardack 1991). A second
specimen from these same beds, Pipscus zangert (Bardack
and Richardson 1977), is more problematially a hagfish and
hhasalso been allied o lampreys (helow). Xidazoon stephanus,
known by three specimens from the Lower Cambrian of
Cina, has been compared with Pipiscius (Shu etal. 1999a,
1999b). Its mouth is defined by acirclet of about 25 plates,
and it may have a dilated pharynx and segmented tal. But
other assignments are equally warranted by the vague
anatomy it preserves, and whether it is even a chordate re-
‘mains questionable,
Node 7. Chordates with a Backbone (Vertebrata)
‘Vertebrata comprise the last common ancestor that humans
share with lampreys, and all its descendants, The relation-
ship of hagfish and lampreys to other eraniates is long de-
bated, Hagfish and lampreys were once united either as
CCyelostomata or Agnatha, jaless fishes grouped by what its
members lacked instead ofby shared unique siilartes, and
they were considered ancestral to gnathostomes (eg., Romer
1966, Carroll 1988). This grouping was largely abandoned
a diverse anatomical data showed lampreys to share more
tunique resemblances with gnathostomes than with hagfish
(Stensio 1968, Lovirup 1977, Hardisty 1979, 1982, Forey
1984b, Janvier 1996). But controversy persists, and recent
studies of the feeding apparatus have resurrected a mono-
phyletic Cyclostomata (Yalden 1985, Mallat 1997a, 1997b)
yclostome monophyly isalso supported by nbosomal DNA
(FDNA; Turbeville etal, 1994, Lipscomb etal. 1998, Mallatt
and Sullivan 1998, Mallatt etal. 2001), vasotocin comple-
‘mentary DNA (cDNA; Suzuki etal. 1995),and globin cDNA
(Lanfranchi et al. 1994), However, the results from small sub-
units of rDNA were overtumed when larger ribosomal se-
quences were used, and morphological analyses that sample
‘many different systems also refute eyclostome monophyly
(Philippe et al 1994, Donoghue etal. 2000). The question may
not be settled, but I follow current convention and treat lam
preys and haglish as successive sister taxa to gnathostomes.
Vertebrate Characters
Increased genetic complexity. Aandem duplication of,
Hox-linked Dlx genes occurred in vertebrates ancestrally,
encoding transcription factors expressed in several develop-
ing tissues and structures. They are expressed in an expanded
forebrain, cranial neural crest cells, placodes, pharyngeal
arches, and the dorsal fin fold. An additional duplication
cevidently occurred independently in lampreys and gnatho-
stomes (Amoreset al, 1998, Niedert et al. 2001, Holland and
Garcia-Fernandez 1996).
Elaboration ofthe brain and special senses i In verte
brates, exchange of products between blood and cerebrospi-
nal fluid occurs via the choroid plexus, a highly vascularized
tissue developing in the two thinnest pars ofthe ventricu-
lar roof of the brain. Vertebrate eyes are also enhanced by a
retinal macula, a small spot of most acute vision atthe cen-
ter ofthe optic axis ofthe eye, and by synaptic ribbons that
improve retinal signal processing, Extrinsic musculature
‘originating from the rigid orbital wall provides mobility to
the bilateral eyeballs, The pineal body is also photosensory,
and in some vertebrates differentiates into a well-developed
pineal eye with retina and lens, In addition, the lateral line
system extends along the sides of the trunk (Maisey 1986), Correspondingly, an extensive cartilaginous braincase that
includes embryonic trabecular cartilages arises beneath the
forebrain, and an elaborate semirigid armature supports the
brain and its special sensory organs.
Locomotor and circulatory systems. Vertebrates have dor-
sal, anal, and caudal fins that are stiffened by fn rays, inreas-
‘ng thrust and steering ability. The circulatory and muscular
systems were also bolstered. The heart comes under nervous
regulation and a stereotyped vascular architecture cartes
blood to and from the gills. Myoglobin stores oxygen in the
muscles, augmenting scope and magnitude in bursts of ac-
tivity. The kidney is also elaborated for more sensitive os-
rmoregulation and more rapid and thorough filtration of the
blood (Maisey 1986).
Pan- Vertebrata
“The oldest putative stem vertebrates are the heterostracans,
smextinct lineage extending from Late Cambrian (Anatolepis)
to the Late Devonian (Maisey 1986, 1988, Gagnier 1989,
Janvier 1996). Their skeleton consists of plates of acellular
membranous bone. Precise relationships of this clade are
controversial, bu if correct the position of heterostracans as
the sister taxon to Vertebrata may suggest that lampreys may
‘have secondaniy los a bony external skeleton. However, in
the absence of direct evidence that lampreys ever possessed
‘bone, heterostracan fossils and the characteristics of bone are
treated below (see Pan-Gnathostomata, below).
Node 8. The Lampreys (Petromyzontida)
There are approximately 35 living lamprey species, all but
three of which inhabit the norther hemisphere (Froese and
Pauly 2001). tn most, larvae hatch and live as suspension
feeders in freshwaters for several years, then migrate to the
oceans as metamorphosed adults, where they become preda-
tory and parasitic, Nonparasitic freshwater species are known
(Beamish 1985) and in some cases the metamorphosed adults
are nonpredatory and do not feed during their short adult
lives (Moyle and Gech 2000).
Lamprey monophyly is diagnosed by a unique feeding
apparatus. It consists of an annular cartilage that supports
a circular, suction-cup mouth lined with toothlike kerati-
nized denticles. A mobile, rasping tongue is supported by
a unique piston cartilage and covered by denticles whose
precise pattern diagnoses many of the different species.
Lampreys attach to a host, rasp 2 hole inits skin, and feed
on its body fluids. Lampreys also eat small invertebrates.
The structure of the branchial skeleton (Mallatt 1984,
Maisey 1986) and the single median nasohypophysial open-
ing (Janvier 1997) are unique. Lampreys have a distinctive
suite of olfactory receptor genes that serves in the detec-
tion of odorants such as bile acids (Dryer 2000). There is
also evidence that lampreys are apomorphic in having un-
dergone duplication ofa tandem pair of Dix genes, followed
by loss of several genes, independent of a comparable du-
CChordate Phylogeny and Development 393
plication and subsequent loss that occurred in gnathos-
tomes (Niedert etal. 2001)
Pan-Petromyzontida
Haitouichthyesercaicunensis (Shu etal. 1999) from the Early
‘Cambrian of China is the oldest fossil lamprey reported, but
the data for its placement are tenuous (Janvier 1999).
‘Mayomyzon pieckoenss, known by several specimens from the
Late Carboniferous Mazon Creek beds of Illinois (Bardack
and Zangerl 1968), isthe oldest unequivocal lamprey, pre-
serving unique lamprey feeding structures, including the
annular and piston cartilages. Hardstella montanensis Janvier
and Lund 1983) from the Lower Carboniferous of Montana
preserves less detail, and itis not clear whether either lies
‘within or ouside of (crown) Petromyzontida. Pipiscus zangerti
(Bardack and Richardson 1977) from the same Mazon Creek
‘beds as Mayomyzonis sometimes als tied tolampreys, as well
as hagfish, but it preserves litle relevant evidence
Node 9. Chordates with Jaws (Gnathostomata)
Gnathostomata comprise the last common ancestor that
humans share with Chondrichthyes, and all ofits descen-
ants (fig. 23.1). ts origin was marked by additional increases
in compleaity of the genome, which mediated several land-
mark innovations, including jaws, paired appendages,
eral types of bone, and the adaptive immune system
‘Although the positions of certain basal fossils are debated,
there is litle doubt regarding gnathostome monophyly
Gnathostome Characters
Increased genetic complexity 'V. Gnathostomes have at
least four Hox gene clusters, and some have as many as seven,
In addition to specifying the fate of cell lineages along the
anteroposterior axis, these gene clusters mediate limbs devel-
‘opment and other outgrowths from the body wall. tis ques-
tionable whether as many as four Hox clusters arose earlier,
either in vertebrates or craniates ancestrally (Holland and
Garcia-Fernandez 1996), but in gnathostomes their expres-
sion nevertheless manifests more complex morphology.
“There was also duplication of Hox-linked Dix genes and sev-
‘eral enhancer elements, lading to elaboration of cranial neu-
ral crestin the pharyngeal arches, placodes, and the dorsal fin
fold (Niedert et al. 2001). Immunoglobin and recombinase
activating genes also arose in gnathostomes, marking the
origin of the adaptive immune system.
‘Brain and sensory receptor enhancement IV. The gnathos-
tome forebrain is enlarged, primarily reflecting enhancement
‘of the olfactory and optic systems. The extrinsic muscles of
the eyeball are rearranged and an additional muscle (the
obliquus inferior) is added tothe suite present in vertebrates
ancestrally (Edgeworth 1935). In the ear, a third (horizon:
tal) semicircular canal arises, lying in nearly the same plane
as the synaptic ribbons of the eye, and correlates with Otxl
‘expression (Maisey 2001, Mazan et al, 2000), In addition, 394 The Relationships of Animals: Deuterostomes
the lateral line system is elaborated over much of the head
and trunk. On the trunk, itis developmentally linked to
the horizontal septum and becomes enclosed by mineral-
ized tissues that insulate and tune directional electro-
reception by the lateral line system (Northcutt and Gans
1983). The gnathostome lateral line system derives from
neural crest and lateral plate mesoderm induction, herald-
ing 2 new stage in developmental complexity. Myelination
of many nerve fibers improves impulse transmission through
much of the body (Maisey 1986, 1988).
Mineralized, bony skeleton. Many bilaterians produce
‘mineralized tissues, and both echinoderms and tunicates gen-
«rate amorphous and crystalline calcium carbonate spicules
(Aizenbergeet al. 2002), Biomineralization is thus an ancient
property, although its erratic expression outside of Craniata
allords only equivocal interpretations ofits history inthis part
of the tree. Certain other components required for bone
‘mineralization, such as calcitonin, were already present but
did not lead to bone production. However, in gnathostomes,
different types of bone form in the head and body (Maisey
1988). Bone development requires the differentiation of
specialized cell types, including fibroblasts, ameloblasts,
‘odontoblasts, and osteoblasts, which are derived from the
ectoderm and cephalic neural crest. In the formation of
membranous bone, fibroblasts first lay down a fibrous col-
lagen framework around which the other cells deposit cal-
cium phosphate as erystalline hydroxyapatite. Another type
of bone development typically involves preformation by car-
tilage, followed by deposition of hydroxyapatite crystals
around the cartilage (perichondral ossification), or within and
completely replacing it (endochondral ossification). Chon
dral ossification occurred first in the head in the oldest ex-
tinct gnathostomes (see Pan-Ganthostomata, below), and it
later spread to the axial skeleton and shoulder girdle. Ossi-
fication in the shoulder girdle is of interest because itis the
first such transformation of the embryonic lateral plate me-
soderm and because it signals the initiation of neural erest
activity in the trunk (Maisey 1988). Inthe shark lineage, the
internal skeleton consists of cartilage that is sheathed in a
layer of crystalline apatite, but fossil evidence suggests that
this isa derived condition (below).
Elaborated skull. Cartilage and/or chondral bone sur-
round the brain and cranial nerves, providing a semirigid
armature for the special sensory organs. At the back of the
head, the cephalicmost vertebral segment is “caprured” dut-
ing ontogeny by the skull to form a back wall ofthe brain-
case. Thereby, it confines several cranial nerves and vessels
to a new passage through the base of the skull, known in,
embryos as the metotic fissure. Cellular membranous bone
‘was also present, covering the top and contributing to other
parts ofthe skull (Maisey 1986, 1988).
Jows.Thenamesake characteristic of gnathostomes arses
in ontogeny from the fist pharyngeal arch, known now as,
the mandibular arch. Is upper half is the palatoquadtate
cartilage, which is atached to the braincase primitvely by
ligaments, whereas the lower half ofthe arch, Meckel's car~
tilage, forms the lower jaw and hinges to the palatoquadtate
at the back of the head. Teeth and denticles develop on in-
ner surfaces of these cartilages through an induction of ec-
toderm and endoderm, Neural crest cells populating the
‘mandibular arch derive from the mesomeres and from hind
brain thombomeres I and 2, whereas the second pharyngeal
arch, the hyoid arch, derives its neural crest from rhom-
bomere 4 (Graham and Smith 2001)
Poired appendages. Other bilaterians have multiple sets
of paired appendages that serve a broad spectrum of func
tions. It was long believed that their evolution was entirely
independent ofthe paired appendages in gnathostomes, but
this appears only partly true today. Common Hex pattern-
ing genes were likely present in the last common ancestor of
chordatesand arthropods, fot a more inclusive group. The
SonicHedgchog gene specifies patterning along anteroposte-
tior, dorsoventral, and proximodistal axes ofthe developing
limb, via BMP2 signaling proteins (Shubin etal. 1997). In
gnathostomes, independent expression of orthologous genes
‘curs in the elaboration of fins, feet, hands, and wings. As
expressed in gnathostomes, the distal limb elements are the
‘most variable elements, In basal gnathostomes they comprise
different kinds of stiffening rays, whereas in tetrapods they
are expressed as fingers and toes (Shubin etal. 1997). More-
over, somite development transformed to provide for mus-
culaization ofthe limbs, ascertain somite cells became motile
and moved into the growing limb buds (Galis 2001). Thus,
although the Hox genes have a more ancient history of ex-
pression, in gnathostomes they are expressed across. a unique
developmental cascade.
The adoptive immune system. One of the most remark-
able ghathostome innovations is the adapive immune system
(Litman et al, 1999, Laird etal. 2000). It responds adaptively
to foreign invaders or antigens such as microbes, parasites,
and genetically altered cells. Other animals have immune
‘mechanisms, but unique to gnathostomes is a system that is
specific, selective, remembered, and regulated. Its fundamen-
tal mediators are immunoglobin and recombinase activation
genes, which are present throughout gnathostomes but ab-
sent in lampreys and hagfish. The immune system is ex-
pressed ina diverse assemblage of immunoreceptor-bearing
lymphocytes that circulate throughout the body in search of
antigens. Gnathostome lymphocytes present an estimated
10 different antigen receptors, which arose seemingly in-
stantaneously as an “immunological big bang” (Schluter eal
1999) in gathostomes ancestrally
‘New endodermal derivatives. In ghathostomes, the endo
derm elaborates to form the pancreas, spleen, stomach, and
a spiral intestine (Maisey 1986),
Pan-Gnathostomata
Several extinct lineages lie along the gnathostome stem. Their
relationships remain problematic, and most have been allied
with virtually every living chordate branch (Forey 1984a, Maisey 1986, 1988, Donoghue et al. 2000). All preserve
‘mineralized and bony tissues of some kind, and the phylo-
genetic debate revolves in large degree around interpreting
the history of tissue diversification. The most ancient, if
problematic extinct pangnathostome lineage is Conodonta
Known to paleontologists for decades only from isolated,
enigmatic mineralized structures, conodonts range in the
fossil record from Late Cambrian to Late Triassic. The recent
discovery of several complete body.-fossls demonstrated that
these objects are toothlike structures aligned along the pha-
xyngeal arches and bordering the gill lefts. They re built of
dentine, calcified cartilage, and possibly more than one form
of hypermineralized enamel (Sansom et al. 1992). Microwear
features indicate that they performed as teeth, occluding
directly with no intervening soft tissues. They formed along
the same zones of endoderm-ectoderm induetion as the
pharyngeal teeth in more derived vertebrates. The mineral-
ized oropharyngeal skeleton and dentition arose at the base
of the gnathostome stem, Cambrian conodont fossils pto-
viding its oldest known expression (Donoghue et al. 2000).
Branching from or possibly below the gnathostome stem
are the heterostracans (see Pan-Vertebrata, above), whose
skeleton consists of external plates of acellular membranious
bone. In heterostracans, bones formed around the head, and
the cranial elements seemingly grew continually throughout
life. Their bone is formed of a basal lamina, a middle layer
of spongy arrays of enameloid, and an outer covering of
cnameloid and dentine. Heterostracan fossils suggest that
‘bone was acellular at frst.
‘Thenext most problematic taxon is Anaspida, which range
from Middle Silurian to Late Devonian (Forey 1984, Maisey|
1986, 1988, Donoghue etal. 2000). Anaspids are diagnosed
by the presence of branchial and postbranchial scales, pecto-
ral plates, and continuous bilateral fin folds, Perichondral
‘ossification occurred in neural and hemal arches, and the ap-
pendicular skeleton, whereas endochondral ossification oc-
‘curred infin radials and derma fin rays inthe tail. The anaspid
trunk squamation pattern suggests the presence of the hor
zontal septum, a critical feature in the trunk-powered loco-
motion that is also tied developmentally to the lateral line
system, Anaspid lateral fin folds may prove to be precursors
ofthe paired appendages of crown ghathostomes.
“Lying closer tothe gnathostome crown clade is Galeaspida,
which range through the Silurian and Devonian. Its members
are distinguished by a large median dorsal opening that com-
runicates with the oral cavity and pharyngeal chamber.
Galeaspids also have 15 or mote pharyngeal pouches. Their
chondral skeleton appears mineralized around the brain and
cranial nerves, however the bone is primitive in being acel-
lular (Maisey 1988). Lying closer to the gnathostome crown
is Osteostraci, a lineage with a similar character and tempo-
ral range as galeaspids. Ostcostracans have a dorsal head
shield with large dorsal and lateral sensory fields. They share
with crown gnathostomes cellular calcified tissues and
perichondral osification of the headshield, which encloses the
CChordate Phylogeny and Development 395,
brain and cranial nerve roots. Ossification surrounds the or-
bital wall, otic capsules, and calcified parachordal cartilages,
structures developing in extant ghathostomes via inductions
between the CNS, notochord, and the ectomesenchytne. Peri
chondral mineralization ofthe otic capsule implies interaction
between mesenchyme and the otic placode (Maisey 1988.
Also present are lobed, paired pectoral fins that are widely
viewed as homologous to the pectoral appendages in crown,
Gnathostomata (Forey 1984a, Maisey 1986, 1988, Shubin
‘etal, 1997, Donoghue eta. 2000), Supportive ofthis view is
the ontogenetic sequence in most extant gnathostomes, in
which pectoral appendages arise belore pelvic.
Node 10. Sharks and Rays (Chondrichthyes)
CChondtrichthyes ineludes sharks, skates, rays, and chimac~
13s (ig. 23.1), The chimaeras (Holocephali) include roughly
30 living species, and there are about 820 living species of
skates and rays (Batoidea) plus sharks (Moyle and Cech 2000)
“Morphology suggests that the species commonly known as
sharks do not by themselves constitute a monophyletic lin-
cage, and that some are mote closely related to the batoids
than to other “sharks” (Maisey 1986)
Earlier authors argued that these different groups evolved
independently from more primitive chordates, and that
CChondrichthyes was a grade that also included several carti-
laginous actinopterygians (below). Cartilage isan embryonic
tissue i all craniaes, and it persists throughout fe in sharks
and rays (and afew other chordates) but the perception that
“cartilaginous fishes are primitive is mistaken. In its more
restricted reference to sharks, rays, and chimeras, the name
CChondrichthyes designates a monophyletic lineage. Histo-
logical examination reveals bone at the bases ofthe teeth,
dermal demticles, and some fin spines. This suggests that
this restricted distribution of bone is a derived condition
in chondrichthyans (Maisey 1984, 1986, 1988).
(ther apomorphic characters include the presence of
micromeric prismatically calcified tssue in derral elements and
surrounding the cartilaginous endoskeleton. Chondrichthyans
also possess a specialized labial catlage adjacent to the mar
diles, the males possess pelvic claspers, and the gill struc-
ture is unique. The denticls (scales) possess distinctive neck
canals (but these may not be unique to chondrichthyans),
and the teeth have specialized nutrient foramina in their bases
with @ unique replacement pattern in which replacing teeth
attach to the inner surface of the jaws as dental arcades
(Maisey 1984, 1986). Fin structure also presents a number
of unique modifications (Maisey 1986). Relationships among,
chondrichthyans have received a great deal of attention
(Compagno 1977, Schaelferand Williams 1977, Maiscy 1984,
1986, Shirat 1996, de Carvalho 1996)
Pan-Chondrichthyes
‘The extinet relatives of chondrichthyans have a long, rich
fossil record. The oldest putative fossils are scales with neck 396 The Relationships of Animals: Deuterostomes
canals from the Late Ordovician Harding Sandstone of Colo-
rado (Sansom et al. 1996). Although present in extant sharks
and chimeroids, most well-known Paleozoic sharks lack them.
From the Silurian onward, chondrichthyan teeth are abun-
danily preserved, although in most cases their identification
rests on solely phenetic grounds, and they provide little use-
ful information on higher level phylogeny. The oldest anatori-
cally complete fossils are the Late Devonian Symmoritdae and