Feathers have long been seen as a key attribute of birds, and indeed there have been many hypotheses
about their origin. Perhaps the new recognition of details of feather ultrastructure in the earliest
fossil birds, including melanosomes, will help resolve major questions about bird origins.
Origin of birds from dinosaurs
When the first specimen of Archaeopteryx was reported from the Solnhofen limestones of
southern Germany in 1861, just two years after
publication of Charles Darwin's 'On the origin of species', Thomas Huxley was quick to note that
the new feathered fossil was a dinosaur in bird's clothing. The legs, arms, and head of the new
fossil were very like those of small theropod dinosaurs such as Compsognathus, discovered
at the same time in the Solnhofen rocks. In fact, Huxley was absolutely right, and yet a century
or more of obfuscation followed his brilliant insight.
Inexplicably, most palaeontologists veered away from the seemingly obvious, and argued that birds,
of which Archaeopteryx was accepted as the oldest, originated from among basal archosaurs
in the Triassic. Through the twentieth century, many workers pointed to Euparkeria from
the Middle Triassic of South Africa, as a likely ancestor. Euparkeria is a basal
archosaur, and so this hypothesis of avian origins might be called the Basal archosaur model.
Euparkeria (left) and Archaeopteryx (right).
Reasons for rejecting a theropod origin for birds were probably as much to do with the time scale as anything else: surely something as complex as a bird must have taken a long time to evolve, and so one should seek ancestors in rocks more than 50 million years older than the 150-Myr old Archaeopteryx - in other
words, soemthing from the Triassic.
The Basal archosaur model was blown out of the water by the thorough and inspired work by John Ostrom, published in the 1970s (e.g. Ostrom 1976). He catalogued the hundreds of detailed homologies in the anatomy of the bird Archaeopteryx and the dromaeosaurid dinosaur
Deinonychus, which he had named in 1969. Ostrom did not present his observations in a cladistic context, but when this was done (e.g. Gauthier 1986; Chiappe & Witmer 2002; Turner et al. 2007), the Dinosaur model, presented first by Huxley, was multiply confirmed.
Since 1986, supporters of the Basal archosaur model have sought likely bird ancestors in the Triassic, pointing at enigmatic small diapsid reptiles such as Longisquama (right) or Megalancosaurus. Often their argument has focused on debating and rejecting the evidence presented by supporters of the Dinosaur model, and those criticisms have sharpened and focused the presentation of the evidence. As things stand, the Dinosaur model is a clear phylogenetic hypothesis supported by hundreds of bits of information (all the apomorphies on the dinosaur cladogram that link birds with various inclusively hierarchical clades). The Basal archosaur model does not rest on a phylogenetic hypothesis or apomorphies, and so is currently incomparably weaker than the Dinosaur model.
New work suggests that the characters of birds arose piecemeal over a span of 100 Myr. Birds
today are exquisitely adapted organisms, showing an apparently integrated set of morphological
and functional attributes for flight, such as wings, feathers, high metabolic rate, lightweight
skeleton, and highly developed sight and orientation senses. Until recently, the majority of
these characters were thought to have arisen relatively rapidly and perhaps as an integrated
set, in forms such as Archaeopteryx from the latest Jurassic (150 Myr ago), the basal member
of Avialae/ Aves, the 'bird clade'. Now, most supposed avian characters pertain to wider clades:
- the furcula may characterise Theropoda
- feathers of some kind are found in Coelurosauria (and may occur more widely still)
- pennaceous feathers characterise Maniraptora/ Metornithes
- flight-type feathers and wings characterise Paraves (Dromaeosauridae, Troodontidae, Avialae)
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(Left) Cladogram illustrating the relationship of birds with major groups of non-avian
coelurosaurian theropods. The numbers in circles at each branching node indicate the first
appearance of feathers and other key morphological characters. 1, unbranched feathers; 2,
uncinate processes on ribs; 3, true branched feathers; 4, retroverted pubis; 5, reversed hallux;
6, asymmetrical flight feathers; 7, pygostyle; 8, horny beak; 9, alula (bastard wing); 10, large,
keeled sternum. Taxa indicated with an asterisk are known to have possessed either protofeathers
or true feathers (From Zhou et al. 2003).
The consequence of the new work is that the key characteristics that distinguish
birds from reptiles and mammals apparently arose step-by-step, not necessarily for the function
to which they were subsequently deployed, and over the span of at least most of the Jurassic
and Early Cretaceous, some 100 Myr in all. This revolution in understanding requires a
closer exploration of each avian innovation in order to determine how it was pieced together and
which were integrated with each other.
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Origin of feathers
The spectacular discoveries in the Jehol biotas from China (e.g. Zhang & Zhou 2000; Zhou et al. 2003; Benton et al. 2008) have indicated that most theropod dinosaurs had feathers, or feather-like structures; basic filamentous structures are also found in ornithischians (Zheng et al. 2009).
The basic types of feathers, from simple thread-like filaments, through down feathers, to
pennaceous contour and flight feathers have long been established. Importantly, these also mark
key stages in the developmental-evolutionary model for feather origins (Prum & Brush 2002;
Chuong et al. 2003). A key part of the model is that pennaceous feathers pass through these
simpler phases during development, and the order of appearance of these feather types in the
fossil record appears concordant. Feathers are defined as integumentary appendages characterized
by the unique tubular organization of the feather follicle and germ (Prum 1999), and by their
capacity for bipinnate structure (Prum 1999).
The order of occurrence of feather types in the fosils (see cladogram above) appears to
replicate certain aspects of these pathways. Most notable is that the most basal feathered
theropods, such as Sinosauropteryx, show only simple filamentous appendages, similar
to Stage I, and true pennaceous feathers (e.g. Stages IIIa, IV, V) appear only in more derived
theropods. Detailed study of the feathers of a diversity of Jehol theropods and birds, and
especially their ultrastructures, should help test these hypotheses further.
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The evolutionary transition series of feather morphologies predicted by the developmental
theory of feather evolution (Prum 1999). The model hypothesizes the origin and diversification
of feathers proceeded through a series derived evolutionary novelties in developmental mechanisms
within the tubular feather germ and follicle. Stage I - The origin of an undifferentiated tubular
collar and feather germ yielded the first feather, a hollow cylinder. Stage II - The origin of
differentiated barb ridges resulted in a mature feather with a tuft of unbranched barbs and a
basal calamus emerging from a superficial sheath. Stage IIIa - The origin of helical displacement
of barb ridges and the new barb locus resulted in a pinnate feather with an indeterminate number
of unbranched barbs fused to a central rachis. Stage IIIb - The origin of peripheral barbule plates
within barb ridges yielded a feather with numerous branched barbs attached to a basal calamus.
There is insufficient information to establish a sequence for Stage IIIa and Stage IIIb, but
both those stages are required in the next stage. Stages IIIa+IIIb - The origin of a feather
with both a rachis and barbs with barbules created a bipinnate, open pennaceous structure.
Stage IV - The origin of differentiated proximal and distal barbules created the first closed,
pennaceous vane. Distal barbules grew terminally hooked pennulae to attach to the simpler,
grooved proximal barbules of the adjacent barb. Stage Va - Lateral displacement of the new barb
locus by differential new barb ridge addition to each side of the follicle led to the growth of
a closed pennaceous feather with an asymmetrical vane resembling modern rectrices and remiges.
Stage Vb - Division and lateral displacement of the new barb loci yielded opposing, anteriorly
and posteriorly oriented patterns of helical displacement producing a main feather and an
afterfeather with a single calamus. The afterfeather could have evolved at any time following
Stage IIIb, but likely occurred after Stage IV based on modern afterfeather morphology.
See Prum (1999) for details of additional stages in the evolution of feather diversity
(Stages Vc-f). |
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Origin of bird characters: future work
In our recent work (Zhang et al. 2010), we demonstrated the existence of melanosomes in feathers from the Jehol Group, observed phaeomelanosomes in fossil feathers for the first time, and demonstrated the presence of both eumelanosomes and phaeomelanosomes in all bird and dinosaur feathers examined. These finding are confirmed independently by Li et al. (2010) in their study of the Jurassic dinosaur Anchiornis.
The new discoveries about the nature and timing of acquisition of characters test functional scenarios for the origin of feathers. Ornithologists discuss reasons for the origin of feathers, whether primarily for display (Mayr 1960), flight (Pennycuick 1986), insulation (Bock 1985), sunscreens (Regal 1975), insect catching (Ostrom 1976), or assisting running and jumping (Caple et al. 1983). The observation that pennaceous feathers originated after simpler feather types indicates that feathers did not originate for flight (Prum 1999). The
observation that the most basal dinosaur with feathers, Sinosauropteryx (Zhang et al. 2010), and the oldest dinosaur with feathers, Anchiornis (Li et al. 2010) displayed a range of colours and particularly showed colour patterning, especially stripes and spots, suggests that display was an early function of feathers.
Glynn Willett of Learn Without Limits has added a further suggestion to the mix, that feathers might have been of value in defence, especially for smaller dinosaurs. So, combining the obvious observation that feathers provide a measure of insulation to the body, however sparsely distributed they were in the first feathered dinosaurs, and that strikingly patterned feather coverings provide signals (whether to others of the same species or to potential predators), perhaps these points might be worth considering as contributing factors in the early evolution of feathers:
- Feathers keep the body warmer than scales
- Feathers change the body outline to make it look bigger or hide the body
- Feathers are detachable which means a predator often only ends up with a
mouthful or paws full of feathers
- Bright, contrasting patterns of stripes and spots in black/ white/ grey/ ginger might act as 'startle' patterns that would cause a larger predator to stop long enough for the smaller prey to escape
- Such bright patterns, and the fluffing effects of feathers, might have assisted males to look larger/ more impressive and so secure mating success
However, key questions remain unanswered: (1) How do the ultrastructures of modern feathers compare with those of their ancestors, and how many dermal appendages of birds do not conform to the requirement of feathers to exhibit tubularity? (2) What was the phylogenetic timing and sequence of acquisition of feather types among Dinosauria in deep time, and how does this relate to recent discoveries about cascades of genomic control of feather morphogenesis? (3) How many aspects of the pigments and feather ultrastructure that determine colour in
modern feathers can be identified in ancient bird and dinosaur feathers? (4) How do colours and colour patterns map across the body in ancient organisms, and what do these patterns tell us about behaviour? (5) What contribution is there from taphonomic processes, and, in particular, morphological degradation, on the spectrum of feather morphologies preserved in fossils?
Literature cited
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