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GAIA N'15, LlSBOAlLISBON, DEZEMBRO/DECEMBER 1998, pp. 399-403 (ISSN: 0871-5424)
THE EVOLUTION OF FEATHERS FROM
DINOSAUR HAIR
Peter J. GRIFFITHS
University of Wolverhampton, School of Health Sciences. Uchfield Street. Wolverhampton WV1 10J. UNITED KINGDOM
ABSTRACT: The significance of finding feathered theropod dinosaurs is discussed in terms _
ofthe theories of the evolution offeathers, birds and endothermy. The plumulous proximal
portion of the isolated Archaeopteryx feather suggests that endothermy had already
evolved in the dinosaur· bird lineage by the Late Jurassic. It is suggested that adipose tissue would have played a major role in providing insulation in endothermic ancestral theropod dinosaurs. Small endothermic dinosaurs may have found an additional form of
insulation an advantage. This may initially have evolved as"hair" in the dinosaurs, rather
than the more morphologically complex branched feather. As avian epidermal appendages
are composed ofthe unique <I> keratin family, it is unlikely that feathers were derived directly
from archosaurian scales, but must have involved intermediate structures. It is suggested
that feathers could consequently have been derived from dinosaur "hair".
RESUME: La decouverte significative de dinosaures theropodes a plumes a entraine une discussion en fonction des theories sur I'evolution des plumes, des oiseaux et de I'endothermie. La partie proximale duveteuse de la plume isolee de I' Archaeopteryx suggere une
evolution de I'endothermie dans la lignee dinosaure-oiseau a la fin du Jurassique. On pense
que Ie tissu adipeux auraitjoue un role majeur en fournissant de la chaleur chez les dinosaures theropodes endothermes. Ainsi, les petits auraient pu en trouver un avantage supplementaire. Chez les dinosaures, il y aurait d'abord pu avoir une evolution vers des "poils"
plutot que des plumes ramifiees, morphologiquement tres compliquees. Etant donne que
les tissus epidermaux des animaux a plumes sont composes de I'unique famille keratine <1>, iI
est improbable que les plumes aient directement derive des ecailles archosauriennes, mais
ont dO faire intervenir des structures intermediaires. Par consequent, les plumes auraient
pu provenir des "poi Is" de dinosaures.
INTRODUCTION
The recent discovery of several species of
feathered theropod dinosaur from the Liaoning
Province of China, locality of the early birds Sinornis
(SERENO & RAo, 1992) and Confuciusornis (HOU et
al. 1995), has fuelled the debate regarding the origin
and initial function offeathers , and also speculation
concerning the possibility that dinosaurs were
endothermic. Sinosauropteryx prima (J I & J I, 1996),
a small compsognathid dinosaur is described as
having epidermal appendages resembling the
plumules of modern birds (CHEN, DONG & ZHEN,
1998). Protoarchaeopteryx robusta (JI & JI, 1997)
and Caudipteryx zoui (JI et al., 1998) are both
described as having pennaceous feathers attached
to the fore limbs and tail, while Caudipteryx is
reported as also having plumulaceous feathers
around the body (JI et al., 1998). The discovery of
feathered non-avian theropod dinosaurs provides
supporting evidence forthe hypothesis thatfeathers
evolved initially for the purpose of insulation or
display, becoming secondarily adapted for flight. In
addition, the discovery of feathered non-avian
dinosaurs gives support to the hypothesis that birds
evolved from the theropods, and that dinosaurs
ancestral to birds were endothermic.
THE THEROPOD ANCESTRY OF BIRDS
It is generally accepted by most palaeontologists
that birds evolved from the theropod dinosaurs
(OSTROM, 1973), and cladistic analyses suggests
that among the theropod dinosaurs, the dromaeosaurs share the most characters with the earliest known bird Archaeopteryx, and also with modern
birds (GAUTH IER, 1986; HOLTZ, 1994).
The hypothesis that birds evolved from the theropod dinosaurs has recently received further support
399
artigos/papers
P. J. GRIFFITHS
morphologically very similar to those of modern
birds.
with the discovery of a new species of fossil bird
from the Upper Cretaceous of Madagascar, Rahona
ostromi (FORSTER et a/., 1998). Rahona has bony
protrusions on the forearms which in modern birds
serve as the attachment points for flight feathers,
suggesting not only that it was feathered but also
that it was capable of flight. Most interestingly, Rahona has a large, retractable sickle-shaped claw on
the second toe ofthe hind foot, similar to the slashing
claws of Velociraptor(OSBORN , 1924) and Deinonychus (OSTROM, 1969).
The earliest known fossil feather is that of Archl;leopteryx lithographica (MEYER, 1861). A recent
analysis shows the feather to be morphologically
identical to the tenth secondary flight feather of the
magpie which has a wing shape (and presumably
aerodynamic characteristics) similar to that of Archaeopteryx (GRIFFITHS, 1996). This is the only described individual fossil feather attnbutable to
Archaeopteryx, and so it is not known if the species
possessed feathers specialised specifically for inSUlation .
It has been suggested that the second toe of
Archaeopteryx may have been hyperextensible
(PAUL, 1988; SERENO, 1997). In addition, although
the pedal claws are considerably smaller than those
of the wing (GRIFFITHS, 1994), the claw of the
second toe is significantly larger than those of the
other toes, and has a different morphology. For
example, in the Eichstatt specimen WELLNHOFFER
(1974) reports that the claw of the second toe has a
curvature with a greater angle from the vertical
chord across the articular facet to claw tip (160°)
compared to the other toes (132°_146°) , which
supports the suggestion that the second toe of
Archaeopteryx may have been hyperextenslble.
While a slashing claw is found in Rahona , such a
claw is not present in Iberomesornis (SANZ et a/.,
1988)or Concornis(SANZ& BUSCALIONI, 1992)from
the Lower Cretaceous of Spain, or Confuc/Usorms
(HOU et a/., 1995) and Sinornis (SERENO & RAO,
1992) from China. This would suggest that the
slashing claw of Rahona may be a retained
plesiomorphic character.
However, an examination of the morphology of
the isolated Archaeopteryx feather reveals some interesting features. On distal portions of the feather,
individual barbs and even barbules can clearly be
observed forming the usual pennaceous structure
which allows the barbs to zip together creating the
typical flight-feather vane capable of generating
aerodynamic lift. In comparison , the morphology of
the feather is quite different proximally where individual barbs cannot be distinguished. In this region,
the feather has a tufted appearance suggesting that
the hooklets attached to the barbules are fewer in
number or are absent, and that the barbs are much
thinner than in the distal parts of the feather. Consequently the isolated Archaeopteryx feather appears
to have a plumulaceous region at the base which
would efficiently trap air against the skin. This feature is identical to that found in the flight feathers of
modern birds which have few if any down feathers
on the wing. The plumulaceous base of the Archaeopteryx feather indicates that it was capable of providing insulation and so supports the hypothesIs that
Archaeopteryxwas endothermic (GRIFFITHS, 1996).
EVOLUTION OF ENDOTHERMY AND DOWN
FEATHERS
The discovery of apparently flightless, feathered
non-avian theropod dinosaurs provides strong
supporting evidence for the hypothesis that feathers
evolved initially for the purpose of display or Insulation, becoming secondarily adapted for flight during
the subsequent evolution of birds (REGAL, 1975). An
alternative hypothesis for the origin of feathers (FEDUCCIA 1974) is that they evolved initially for flight,
and subsequently become adapted for insulation
when the birds became endothermic, although this
now seems less likely in view of the recent finds.
As the Archaeopteryx feather is already morphologically specialised and exhibits characteristics
enabling the dual functions both of flight and Insulation, Archaeopteryx can give no indication of the initial role of feathers , but does make clear that
feathers capable of providing insulation as well as
flight were already present during the Late Jurassic.
It is logical to assume that endothermy and feathers
evolved in taxa ancestral to Archaeopteryx.
Modern birds are unquestionably endothermic
and have down feathers which are specialised for insulation as well as flight feathers. At some point
along the dinosaur - bird lineage, both endothermy
and feathers for insulation evolved , although not
necessarily at the same time . The first discovered
fossil down feather has been classified as lIerdopteryx viai (LACASA, 1985) from the Lower Cretaceous of EI Montsec, Spain. This location has
yielded a variety of specialised feathers which are
THE ROLE OF ADIPOSE TISSUE FOR
INSULATION
In contrast to birds, mammals use two different
mechanisms for insulation, hair and also a layer of
adipose tissue under the dermis. Hair plays a similar
role in insulation as down feathers , trapping a layer
of air against the skin thus reducing heat loss by convection and radiation. In adipose tissue , lipid droplets are stored in large specialised cells which are
embedded in connective tissue, particularly in the
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THE EVOLUTION OF FEATHERS FROM DINOSAUR HAIR
dermis. The dermal layer of adipose ti ssue prevents
the loss of heat from deep within the body, helping to
maintain core temperature.
The potential role of adipose tissue for insulation
must be taken into account when considering the
evolution of endothermy in birds, particularly with regard to the ancestral dinosaurs and the debate as to
whether they were endothermic. Once there is a necessity for regulation of the internal temperature to
within small tolerances, then insu lation becomes an
immediate advantage due to the high energetic expense of the metabolic generation of heat. This
wou ld be particularly important for smaller species
with a high surface area to volume ratio where heat
loss would be more sign ificant. There wou ld therefore be a very high selection pressure, particularly
for small species of dinosaur living in a colder climate, to evolve some form of insulation. This could
most simply be achieved with a layer of adipose tissue under the skin. Adipose tissue is widely distributed among modern sauropsids, and in modern
birds is used not only for energy storage but also insulation, particularly in species which come into frequent con tact with water.
A thick layer of ad ipose tissue , wh ile it may provide excellent in su lation, is however relatively
heavy. In terms of insulation efficiency to weight, the
ratio is low (GRIFFITHS, 1996). Th is is not normally a
problem, but becomes a serious disadvantage
where weight is of consideration such as when attempting to fly.
Conversely, down feathers and hair have a high
insulation efficiency to weight ratio and therefore
have the advantage over adipose tissue where
weight is of consideration. The early mammals are
thought to have been small shrew-like creatu res
with a large surface area to volume ratio, thus heat
loss from the surface would have been a major problem. Hair would have been a big advantage in providing extra insulation and reducing heat loss ,
particularly if the early mammals were mainly nocturnal and active when ambient temperatures were
lower. Mammals seem to have increased in size
later in their evolutionary history, and large mammals frequently have reduced hair cover, particularly those living in warmer climates, as seen in
modern elephants, although large mammals such
as mammoths retained a thick hair covering when
faced with adverse climatic conditions.
The situation appears to be the reverse for birds
which probably originated from larger theropod ancestors and initially became progressively smaller
as flight evolved. Archaeopteryx is smaller than
most known theropods, with the exception of Compsognathus (WAGNER, 1861) wh ich was an unusually
small theropod. Similarly, the thrush sized Lower
Cretaceous birds Iberomesomis, Concornis and
also Sinornis were much smaller than Archaeopteryx. Bird evolution therefore appears to have involved an initial reduction in size, probably because
it is easier for small birds to generate aerodynamic
lift (SANZ & BONAPARTE , 1992), although Confuciusomis appears to be an exception as the y were of a
similar size to Archaeopteryx.
THE EVOLUTION OF FEATHERS
MADERSON (1972) has suggested that protofeathers may have evolved from the tips of archosaurian scales with the scale eventually regress,i ng
to leave the feather, on the basis that both fe athers
and the epidermis of scales in birds were thought to
contain f3 keratin, while the interfollicular skin adjacent to feathers and the inner surface of scales contained a keratin. This hypothesis received support
from the work of DHOUAILLY, HARDY & SEN GEL
(1980), who showed that it was possible to convert
the prospective scales on the feet of ch ick embryos
to feathers with the use of Retinioc Acid, known to
play an important role in positional signalling and
pattern formation during cell differentiation in developing embryos.
However, BRUSH (1993) has shown that the
avian keratins in feathers, down, scutes and beaks
are quite different from the keratin of reptiles, and is
composed of a family of <I> keratins. These are more
closely related to a keratins than f3 keratins. There is
little evidence that <I> keratin and a keratin diverged
from a common ancestral gene, or that <I> keratin was
derived from existing a keratin genes, although <I>
keratin cou ld perhaps be derived from a cytokeratin
protein. <I> keratin forms f3-pleated sheets which
spontaneously assemble into filaments by self association, rather than the a helixes which a keratin can
form. The <I> keratins exist as two main groups: a
larger molecule of 13,500 Da found in scales, claws
and beaks, and a smaller molecule of 10,500 Da
found in feathers and down. The amino acid sequences of the <I> keratin of feathers and down is
more similar to the sequence of amino acids in
scutes than in reticulate scales, and closer still to
beak and then claw keratins (BRUSH, 1980).
As Archaeopteryx has feathers which are essentially modern in structure, it could be assumed that
they were also composed of <I> keratin . In addition to
feathers, the keratin sheaths of the claws have been
preserved in Archaeopteryx. There is no sign of a
beak in any of the specimens although it is unlikely
that Archaeopteryx possessed a beak as teeth were
still present. Also, there are no indications of scutes
or reticulate scales in any of the specimens.
401
P. J. GRIFFITHS
This introduces additional complexity into any
hypothesis concerning the origin of feathers as it is
necessary to postulate the evolution of a new family
of genes coding for these new proteins, which must
have been present in epidermal appendages priorto
the evolution of feathers. The molecular structure of
the <I> keratins would suggest that it is unlikely that
feathers evolved directly from archosaurian scales.
As feather keratins are closer to beak and claw
keratins than scute or scale keratins, it again suggests that a number of intermediate stages were involved in feather evolution (BRUSH, 1996).
DINOSAUR HAIR
Avian feathers can be morphologically
distinguished from mammalian hairon the basis that
they have a complex branching structure, while
mammalian hair consists of single filaments. From a
developmental perspective, hair is more simple to
form than the structurally complex branching
feather, and consequently mammalian hair follicles
are morphologically simpler than avian feather
follicles. If the evolution of epidermal appendages
were driven by the necessity of providing insulation
rather than providing an aerodynamically functional
vane, it is parsimonious to consider the initial
evolution of an unbranched structure to be more
probable than a complex branching one.
Unbranched single filaments (hair) are therefore
more likely than branched feathers to have initially
evolved as a structure required for the purposes of
insulation.
If the dinosaurs were to be considered endothermic, hairwould have the advantage of conferri ng additional insulation to that provided by a layer of
adipose tissue. This may have been important to
smaller species of dinosaur with a high surface area
to volume ratio which were challenged with the problem of heat loss that larger dinosaur species wou ld
not experience.
An analysis of the epidermal appendages of Sinosauropteryx (CHEN, DONG & ZHEN , 1998), describes the structures as being possibly hollow,
rather course structures that may resemble the plumules of modern birds, with short quills and long filamentous barbs, but with no signs of barbules or
hooklets. However, as it has not yet been possible to
isolate a single structure for analysis, it is not clear if
these structures really are branched rather than being composed of single filaments, or if they even
have any real relationship with modern feathers.
Preserved impressions of possible integumentary structures have also been described associated
with the non-avian theropod Pelecanimimus polyoden (PEREZ-MORENO et al., 1994) from the Lower
Cretaceous location of Las Hoyas, Spain. These
structures are described as consisting of a primary
system of subparallel fibres arranged perpendicular
to the bone surface , with a less conspicuous secondary system orientated in parallel. Again, it is not
clear if these are branched structures rather than
single filaments.
Branching filamentous structures which can only
be described as symmetrical feathers have been
found associated with the two new species from the
Liaoning province of China, Protoarchaeopteryx
and Caudipteryx (JI et al., 1998) . While the
phylogenetic analysis places Caudipteryx as a
sistergrouptothe Avialae, the systematic position of
Protoarchaeopteryx is less clear and appears to be
unresolved from the Velociraptorinae (GAUTHIER,
1986; HOLTZ, 1994) root, and may also be a sister
group to the Avialae (JI et al., 1998). Although
Protoarchaeopteryx has relati vely long arms
compared to non-avia n coelurosaurs they are
shorter than Archaeopteryx. The arms of
Caudipteryx are shorter than non-avian
coelurosaurs. In either species it appears to be
unlikely that they were able to fly. However, there is a
distinct possibility that they were the flightless
descendants of birds, and inherited feathers from
flying ancestors. This hypothesis is supported by the
observation that the some of the feathers of
Protoarchaeopteryx and perhaps Caudipteryx were
pennaceous. PAUL (1988) has even suggested that
all the dromaeosaurs are descended from flying
protobirds. This is not impossible as they appear to
have evolved after Archaeopteryx, and even
Protoarchaeopteryx, Caudipteryx and
Sinosauropteryx are found in deposits that probably
date from the early Cretaceous (SMITH, EVENSEN &
YORK, 1996).
FEATHERS FROM DINOSAUR HAIR
Feathers could conceivably have evolved from
dinosaur"hair", perhaps similar in morphologytothe
structures reported associated with Pelicanimimus.
Such appendages may wel l have been composed of
filaments of <I> keratin, rather than IX keratin as in
mammalian hair. Subsequently, the epidermal appendages became split to form the branching structure of barbs. Such a branching structure could
possibly be represented by the appendages reported associated with Sinosauropteryx, with short
quills and long filamentous barbs. The branching
then become more complex to form barbules. Hooks
subsequently evolved allowing the barbules to zip
together to form the pennaceous structure of modern feathers, as exhibited by Archaeopteryx and
modern birds. This hypothesis therefore proposes a
series of progressively more complex structures,
each of which is functionally advantageous in terms
of initially providing insulation, and then finally lead-
402
THE EVOLUTION OF FEA THERS FROM DINOSAUR HAIR
ing to a feather capable of generating aerodynamic
lift. A change in the morphology of the epidermal appendage from ha ir to feather would involve an increase in complexity of the morphology of the
appendage follicle, and so would be caused by epigenetic factors.
PAUL, G .S (1988) - Predatory Dinosaurs of the World. Simon &
Schuster, New York, 403 pp.
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