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CHAPTER ONE
From Protoavis to Pigeon
Surely there is nothing very wild or illegitimate in the hypothesis
that the phylum of the Class of Aves has its foot in the Dinosaurian
Reptiles--that these, passing through a series of such
modifications as are exhibited in one of their phases by
Compsognathus, have given rise to [birds].
--Thomas H. Huxley, "On the Animals Which Are Most
Nearly Intermediate between the Birds and Reptiles," 1868
Birds in flight symbolize spirits released from the bondage of
gravity. From the day that humans first looked up at the skies,
birds have summoned a sense of wonder and mystery, enchanting
our earth-bound ancestors with their freedom and song. They fly
where they please and when they please. The power of flight has
opened up to birds a multilayered network of aerial highways and
byways, enabling them to reach any place on our planet. Birds are
the most successful terrestrial vertebrate, abundant in both
numbers of species and populations. Today they live on every
continent and occupy virtually all available ecological niches.
About 300 billion birds, over 9,000 species, now inhabit the earth,
as compared to 3,000 species of
amphibians, 6,000 species of reptiles, and 4,100 species of
mammals (Gill 1990).
The Genealogy of Birds
Although birds are one of the best-known groups of living
vertebrates, their origin, evolution, and early adaptive radiation are
poorly documented in the fossil record. The rarity of bird fossils is
generally attributed to the extreme fragility, lightness,
pneumaticity, and general smallness of their bones. Moreover, the
living habits of birds are not conducive to preservation of
specimens, as most species prefer arboreal habitat. Except for a
few solitary fossils, we have gained essentially no new knowledge
of Mesozoic birds during the past century. Archaeopteryx
lithographica from the Upper Jurassic Solnhofen Limestone of
Germany held center stage in avian evolution, being regarded by
most researchers as the oldest and most primitive of known birds.
Seventy million years after Archaeopteryx appeared, birds such
as Hesperornis and Ichthyornis, from the Late Cretaceous of
Kansas, had evolved into essentially modern forms, leaving no
clues as to their reptilian heritage. It is no surprise that the
Mesozoic has been referred to as the Dark Ages of avian history.
During the last fifteen years, the situation has changed
dramatically as more and more fossils of Mesozoic birds have
been unearthed from different sites around the globe. These
Mesozoic birds vary widely in size and possess a wide range of
body shapes and ecological adaptations. The new discoveries and
the application of cladistics have inspired novel ideas about the
antiquity of birds, their evolution, and their phylogenetic
relationships. These data have triggered a renaissance in avian
paleontology.
Birds, which took to the air during the age of the dinosaurs, are
generally classified as Aves, a class separate from the rest of the
vertebrates, such as fish, amphibians, reptiles, and mammals.
Beauty, grace, feathers, and aerial prowess conceal the true
identity and heritage of birds. What is the phylogenetic position of
birds among vertebrates? Who were their immediate evolutionary
ancestors? These questions have perplexed evolutionary biologists
since the time of Darwin. Darwin's friend and champion,
Thomas Huxley (1867, 1868a, 1868b, 1870), presented a
radical proposal that birds are merely glorified reptiles. He
classified reptiles and birds in the same group, Sauropsida. He
reasoned that, if birds had not been so outstandingly successful in
their aerial adaptation and speciation and if they had remained a
relatively small group like pterosaurs, they would now be
regarded as an order of reptiles, not a separate class of
vertebrates. Huxley was impressed with the stunning similarities
in bipedal posture, erect gait, and mesotarsal ankle joint between
Archaeopteryx and Compsognathus, a contemporary theropod
dinosaur from the Solnhofen Limestone. For several decades, the
famed Eichstatt specimen of Archaeopteryx was mistakenly
identified as a juvenile individual of Compsognathus, indicating
how alike these two genera are (Wellnhofer 1974). The fact that
theropods and birds always walked bipedally is intriguing and may
indicate a common evolutionary history, Huxley argued.
Bipedalism is a rare evolutionary event in the history of
vertebrates and requires a great deal of balancing and
coordination. In birds we see the culmination of this coordination
and proprioception. Marsh (1877, 1880) embraced Huxley's
proposal of a theropod-bird link when he described Cretaceous
toothed birds such as Hesperornis and Ichthyornis.
In 1926, however, Gerhard Heilmann (1926) swept away the
hypothesis of the theropod ancestry of birds in his influential book
The Origin of Birds. He argued that such small theropods as
coelurosaurs, however birdlike in skeletal morphology, could not
be considered the ancestors of birds because they lacked
clavicles, from which birds derive their furcula. Heilmann was
guided by Dollo's law of irreversibility: evolution does not
backtrack to recover characteristics. For birds to evolve from
theropods, the lost furcula would have to reappear. Faced with
such a paradox, Heilmann made a very reasonable suggestion. He
argued that both birds and dinosaurs had evolved from a common
ancestor. He sought the common ancestor among bipedal
"pseudosuchian thecodonts," such as Euparkeria and
Ornithosuchus, which retained the clavicle. From this ancestral
stock, two great evolutionary lineages diverged, one leading to dinosaurs
and the other to birds. For the next fifty years, Heilmann's
pseudosuchian theory enjoyed wide acceptance among
evolutionary biologists, with some new variations, such as the
crocodilian connection of birds (Walker 1972; Martin 1985).
After almost a century, John Ostrom (1969, 1973, 1976a,
1985a, 1991) revived Huxley's theropod origin of birds and
suggested that small theropods, such as dromaeosaurs, come very
close indeed to the ancestry of birds. Huxley emphasized
mesotarsal ankle structure as the key to the theropod-bird
relationship, whereas Ostrom pointed out unique wrist
morphology--the semilunate carpal--as the common link
between dromaeosaurs and birds. Dromaeosaur fossils are
known from the Cretaceous of North America and Asia. These
little theropods had slashing toe-claws and were agile and
formidable predators, which probably hunted in packs. One of the
famous dromaeosaurs from Mongolia, Velociraptor, became the
undisputed star in Steven Spielberg's movie Jurassic Park. In spite
of their mean appearances, dromaeosaurs offer important insights
into the origin of birds. Ostrom presented an impressive array of
skeletal similarities between Archaeopteryx and dromaeosaurs,
such as a long coracoid, long arms equipped with three fingers, a
swivel wrist joint, long slender hind legs, a three-toed foot, and a
stiff tail. Except for feathers, Archaeopteryx would look like a
small dromaeosaur, Ostrom argued. The striking resemblance
between Archaeopteryx and dromaeosaurs must reflect a common
descent, not evolutionary convergence. He emphasized the recent
discovery of clavicles in some coelurosaurs, which countered
Heilmann's principal objection to a theropod ancestry of birds.
Although Ostrom suggested that birds were the direct
descendants of dromaeosaurs, he used traditional classification to
separate these two groups; he placed the birds in their own class,
Aves, and dinosaurs in Class Reptilia, contrary to Huxley's
grouping. However, his former student, Robert T. Bakker (1975),
concluded that birds are actually theropod dinosaurs, not just
descended from them. Like Huxley, Bakker argued that birds
should not have their own separate class because they fly. Bats
fly, too, but they are still considered mammals. Birds are as much
dinosaurs as bats are mammals.
To understand the bird's place in the dinosaur family tree, we
must know the interrelationships of dinosaurs. Dinosaurs began
their evolutionary history as small carnivores during the Late
Triassic. They became diversified within a relatively short period
and then ruled the earth for approximately 160 million years.
During that time they adapted to a wide range of conditions and
environments and became very successful. All known dinosaurs
are divided into two major groups on the basis of pelvic structure:
Saurischia and Ornithischia. The Saurischia contains two
subgroups: the plant-eating, mostly quadrupedal sauropodomorphs
and the carnivorous, bipedal theropods. The Ornithischia includes
several subgroups of herbivorous dinosaurs--armored
thyreophorans (such as stegosaurs and ankylosaurs), and horned
plus duck-billed cerapodans (such as ceratopsians and
ornithopods) (fig. 1.1A). The theropods are the most spectacular
of all dinosaurs and are linked to the ancestry of birds.
The theropod-bird relationship is strengthened with the
application of cladistic analysis. Cladistics differs from older
methods of biological classification by using the distribution of
evolutionary novelties, called shared derived characters or
synapomorphies. A clade is a group of animals that share
uniquely evolved features and therefore a common ancestry.
Recognition of a clade or monophyletic group by synapomorphies
is the most important step in cladistic hypothesis. Willie Hennig,
the German entomologist, first formalized the cladistic method in
1966. During the past two decades, cladistics has been used
extensively to infer the phylogenetic relationships among different
groups of plants and animals. Using this technique, Jacques
Gauthier (1986) provided the first detailed hypothesis of theropod
relationships on the basis of skeletal morphology; he recognized
several monophyletic groups, or clades, in a hierarchical
pattern. These successive clades are Theropoda, Tetanurae,
Coelurosauria, Maniraptora, and Aves (fig. 1.1B). The new
phylogenetic relationship suggests that birds are a member of
theropods. In fact, birds are now considered not only glorified
theropods but also the sole surviving lineage of dinosaurs. The
flying-dinosaur image of birds is appealing to the public and also
is gaining currency among paleontologists (Weishampel, Dodson,
and Osmolska 1990; Sereno and Rao 1992; Chiappe 1995a).
If we look at Gauthier's cladograms (fig. 1.1), it becomes clear
that birds should possess all of the characteristics of dinosaurs,
saurischians, theropods, tetanurans, coelurosaurs, and
maniraptorans in a nested pattern (although some of them may
have been lost or modified), but that they are also characterized
by a suite of characters uniquely their own. In the phylogenetic
scheme, birds are the most derived group of theropods, which
acquired many evolutionary novelties in the context of their flight
adaptation. The definition and interrelationships of major clades of
birds, discussed in a later section, are shown in figure 1.1C.
The Ancestry of Birds
Dromaeosaurs were the closest relatives of birds and shared the
most recent common ancestry. The early fossil record of
dromaeosaurs is obscure. Thus far, known dromaeosaurs
appeared fairly late during the Cretaceous, when birds were
already well established. Dromaeosaurs did not continue to
become more birdlike. Instead, in their evolutionary course they
specialized in killing mechanisms and became considerably larger
than birds. The common ancestor of birds and dromaeosaurs has
yet to be found in the fossil record. However, we can speculate
from cladistic analysis that this hypothetical bird ancestor would
be very similar to dromaeosaurs in general morphology. For
simplicity, we can refer to this ancestral form as
protodromaeosaurs. Heilmann (1926) coined the neutral term
proavian for this hypothetical ancestor. How big was the
proavian? We can guess its size from the evolutionary trend in
vertebrates, defined in
Cope's law. This law states that, in the course of time, all animals
tend to evolve larger body sizes. If Cope's law holds true, the
ancestral proavian would be considerably smaller than later
dromaeosaur descendants. The proavian may match the size of
Archaeopteryx and would have given rise to two lineages, birds
and dromaeosaurs. Dromaeosaurs are currently the best
approximation of the hypothetical bird ancestor and serve as a
model when tracing avian ancestry (fig. 1.2).
The Antiquity of Birds
For years, Archaeopteryx was considered to be the oldest bird
known, but its position has recently been usurped by Protoavis
texensis from the Late Triassic Dockum Group of Texas,
predating Archaeopteryx by 75 million years (Chatterjee 1987a,
1991, 1994, 1995, in press; Kurochkin 1995; Peters 1994).
Identification of Archaeopteryx as a bird is a simple task because
Archaeopteryx possesses feathers. The recognition of Protoavis as
a primitive bird requires a thorough knowledge of comparative
anatomy of the skeleton because feather impressions were not
found with the specimens. Resembling a small nonavian theropod
in the rear, Protoavis reveals its avian identity in the front portions
of the skeleton. It is an excellent example of mosaic evolution, in
which some conservative ancestral characters of contemporary
nonavian theropods occur with the advanced characters typical of
later birds. This mingling of primitive and advanced characteristics
seems to have been a common evolutionary pattern in the
origination of higher groups of vertebrates.
The primitive characters of Protoavis include four metacarpals
in the hand, a short ascending process on the astragalus, and a
long bony tail. On the other hand, Protoavis is fully avian in some
significant ways. Its temporal configuration is modified in avian
fashion, with the development of streptostylic quadrate and upper
jaw mobility. Its braincase is highly inflated, and the orbits are
frontally placed. It has heterocoelous (saddle-shaped) centra in
the neck, as do modern birds. Protoavis has a much more efficient
and advanced wing structure than does Archaeopteryx. It has a
birdlike coracoid and furcula and a keeled sternum
for flapping flight. The hand bones show quill nodes for the
attachment of primary feathers. The pelvis shows fusion of the
ilium and ischium for strength and rigidity, whereas the hindlimbs
are reoriented to shift the functional joint from hip to knee.
Detailed cladistic analysis indicates that Archaeopteryx is a
basal taxon of Aves, whereas Protoavis had achieved a
structural organization well beyond that of Archaeopteryx and is
a member of the Ornithothoraces (fig. 1.1C). Archaeopteryx
thus seems to be a late example of the ancestral type, a "living
fossil" in the Jurassic world. The recognition of Protoavis as the
first bird marks a critical departure from earlier thinking on the
origin of birds and the evolution of flight. It provides a more
complex picture of morphological diversity early in bird evolution,
showing a bushlike adaptive radiation.
However, the discovery of a Triassic bird is not totally
surprising. More than a century ago, Yale paleontologist Othniel
Charles Marsh (1880) cogently argued that three Mesozoic taxa,
Archaeopteryx, Hesperornis, and Ichthyornis, differ so widely
from one another that the evolution of birds must have taken
place at a much earlier time, perhaps at the end of the
Triassic. He predicted that Triassic birds with a freely movable
quadrate bone would be found to fill the major morphological and
evolutionary gaps in avian history. Protoavis approaches the
predicted structure and size of the ancestral bird envisioned by
Marsh. It pushes the avian origin back to the Late Triassic, to the
very dawn of the age of the dinosaurs.
Thus, the new avian odyssey begins some 225 million years
ago, when Protoavis took to the air over tropical Texas forests.
This is the beginning of the age of birds. Throughout the Jurassic
and Cretaceous, birds diversified, perfected their flight
maneuvers, and adapted to various niches during the continental
fragmentation. The road from Protoavis to pigeon requires a long
evolutionary march, with frequent roundabouts and blind alleys. It
is paved with the temporary dominance of several different
extinct lineages until the Late Cretaceous, when Neornithes
(modern birds) emerged. Most Cretaceous birds, such as
enantiornithes, hesperornithiforms, Patagopteryx, and other less
well-known groups, disappeared about 65 million years ago, along
with nonavian dinosaurs. Rising Phoenix-like from the ashes of
this catastrophe, the neornithine lineage underwent an explosive
adaptive radiation of modern forms during the Tertiary.