~uulugicnl,~oburnal
ofthe Linnean Sociep (1994), 112: 389-397
The relative timing of the origin of flight and
endothermy: evidence from the comparative
biology of birds and mammals.
SARAH E. RANDOLPH
Department of<oology, Universip o f Oxford, South Parks Road, Oxford OX1 3PS.
Received Februaly 1994; accepted f o r publication July 1994.
Evidence from the comparative biology of living birds and mammals is used to address the
question ‘which came first, flight or endothermy?’. Birds and mammals have evolved different
solutions to the problems of high energy flow demanded by endothermy. The heavy apparatus
needed for processing food to allow the rapid assimilation of energy is housed in the head of
mammals, but low down in the bird’s body. The primitive inefficient tidal-flow system of ventilation
is simply enlarged in mammals, but is replaced in birds by a lighter uni-flow system through air
sacs and parabronchi. Birds avoid the weight problems associated with the mammalian systems of
viviparity and lactation by nourishing their young with large quantities of yolk within the egg and
an unprocessed diet after hatching. The apparent adaptedness for flight of the avian systems
suggests that in the animals ancestral to birds the adaptations for high energy flow were constrained
from the start by the need for aerodynamic stability, i.e. flight was initiated before endothermy.
The implications of this conclusion for the origin of flight and feathers are discussed.
ADDITIONAL KEY WORDS:-feathers
-
evolution
-
Archaeoptey
-
feeding
-
respiration
reproduction.
CONTENTS
. . . . . . . . .
Introduction
Endothermy in birds and mammals .
. . .
Feeding apparatus .
. . . . . .
Respiration
. . . . . . . .
Reproduction .
. . . . . . .
Conclusions and wider implications .
. . .
Flight was initiated before endothermy . .
Scenario for the origin of flight and endothermy
Functional origin offeathers
. . . .
Acknowledgements .
. . . . . . .
References .
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INTRODUCTION
There is still no overall consensus amongst biologists on either the original
function of feathers or the origin of flight. The earlier, more obvious, explanations
focused on the two major current functions of feathers: as aerofoils (from
Nopsca (1907) and Pycraft (1910) to Parkes (1966) and Lucas & Stettenheim
(1972)) and still favoured by Martin (1983)) Feduccia (1985) and Pennycuick
0024-4082/94/011389+09 $08.00/0
389
0 1994 The Linnean Society of London
590
S E RANDOLPH
(1986)) and as insulation (for a review of early ideas see Lucas & Stettenheim,
1972; Bock, 1969; Ostrom, 1974; Cowen & Lipps, 1982). More recently,
dissatisfaction with these ideas has led to hypotheses based on more specialized
functions, such as display and fighting (Stephan, 1974; Cowen & Lipps, 1982),
heron-like aquatic foraging (Thulborn & Hamley, 1985), water-repellance (Dyck,
1985), or based on a function appropriate to the ancestor of birds but not to
birds themselves, namely as heat shields to protect against solar radiation (Regal,
1975). Two models still compete as explanations for the origin of flight, the
gliding model (inter aliu Bock, 1965; Parkes, 1966; Martin, 1983; Pennycuick,
1986; Rayner, 1988) and the cursorial model (Ostrom, 1974, 1979; Caple,
Balde & Willis, 1983; Peters, 1985).
Many of these hypotheses involve an implicit, or even explicit, assumption
or conclusion about the relative timing of the origin of flight and endothermy
in the evolutionary line leading to modern birds. Bock (1965, 1969), Ostrom
(1974), Peters (1985), Dyck (1985) and Thulborn (1984) favour the advent of
endothermy before the origin of flight, while Parkes (1966), Regal (1975), Daly
i1980), Martin (1983), Feduccia (1985), Pennycuick (1986) and Ruben (199 1)
favour the reverse order. The object of this brief essay is to address the simple
question ‘which came first, flight or endothermy?’ in order to set a framework
within which to discuss the origin of feathers and flight. In the past the answer
to this question has been sought using evidence from the fine structure of
feathers or from the fossil record. Neither approach has proved conclusive
because (a) the structure of present-day feathers is designed for the dual function
of both flight and insulation (even in secondarily flightless birds the present
feather structure is presumably influenced by the former role in flight), and (b)
the nature of the fossil record, its incompleteness and limitation to hard
anatomy, leaves too much scope for speculation and personal interpretation
concerning the thermal physiology of Archosaurs and Archaeoptqyx.
I prefer to use a different line of evidence, the comparative biology of living
birds and mammals. In summary, I shall argue that the very different solutions
to the problems of endothermy in birds and mammals indicate that the animals
ancestral to birds were already subject to aerodynamical constraints before
endothermy evolved. Throughout, I shall use the word ‘flight’ to indicate any
sort of air-bornc locomotion, including both gliding and flapping flight unless
otherwise specified.
ENDOTHERMY IN BIRDS AND MAMMALS
Birds and mammals are the only two groups of vertebrates that show the
three interrelated characteristics of ‘warm-bloodedness’, that is a high metabolic
rate, high internal heat production (endothermy), resulting in a high constant
body temperature (homeothermy). The high energy flow demanded by this sort
of thermal physiology (often referred to simply as endothermy) has resulted in
a complex integrated suite of physical, physiological, endocrinological and
neurobiologcal systems within each group of vertebrates. A comparison of the
following three systems, fundamental to the supply of high levels of energy in
adults and juveniles, shows that birds and mammals evolved quite different
solutions to the problems of high energy flow, and in every case the avian
solution seems to facilitate aerodynamic stability.
FLIGHT, ENDOTHERMY AND BIRD ORIGIN
39 1
Feeding apparatus
A high energy flow requires the efficient acquisition and processing of food.
During the evolution of the synapsid reptiles that gave rise to mammals, the
mouth became an organ for preliminary physical and chemical reduction of
food before it reached the stomach. The reorganization of the jaw structure
and musculature and the increasing complexity of the teeth to allow both
cutting and grinding of the food can be traced with great detail from the fossil
record (Kemp, 1982). Even the new habit of keeping food in the mouth for
prolonged chewing, rather than swallowing it immediately, can be surmised
from the fossilized evidence of the possession of soft, muscular lips by the
cynodont therapsids (Kemp, 1982). At some point there also originated saliva,
with its digestive properties, thereby adding chemical reduction to mechanical
reduction while the food was still in the mouth and so speeding up the
assimilation of food energy.
The digestive system of birds is also extremely efficient (Welty & Baptista,
1988), but this relies far less on processes centred in the bird’s head and much
more on processes within the digestive tract. The theme of avian jaw evolution
is one of simplification and reduction, with a complete loss of teeth and no
need for heavy musculature to work complex grinding movements of the lower
jaw. Birds that eat hard food such as seeds, insects and shelled invertebrates,
use their beaks for preliminary crushing or extraction of the soft parts, and
large food items are torn into smaller pieces, but once in the mouth food is
swallowed rapidly. Those species that need to store large quantities of food
before digestion begins do so in the crop, situated low down above the furcula.
This is particularly common amongst grain-eaters, permitting the gathering of
large quantities of food in a short time, thus limiting the hazards of foraging;
this is comparable to grain-storage in cheek pouches by rodents. Chemical
digestion of proteins starts in the anterior glandular stomach, but mechanical
reduction of tougher foods occurs in the posterior rnuscular stomach, or gizzard,
equipped with horny plates or ridges augmented by grit swallowed for this
purpose. Thus, by comparison with mammals, all the heavy apparatus needed
for the rapid assimilation of energy from food is shifted away from the head
to a position low down in the bird’s body.
Birds’ heads are indeed much lighter than those of mammals. Skull mass as
a percentage of body mass declines from 2.2-2.1 for shrews (body mass 6-10
g) and voles (body mass I8 g) to c. 1.3 for mammals ranging in size from a
rat (body mass c. 300 g) to a fox (body mass c. 6 kg). For birds the same
measure is 1.4 for a sparrow (body mass 28 g), declining to c. 0.4 for birds
weighing 1.5-5 kg. The total head, that includes the jaw muscles, constitutes
23% of a vole’s body mass, but only 14% of a sparrow’s body mass. The
observation that flight performance is adversely affected when starlings carry
food (> 1% of their body weight) in their beaks (Cuthill & Kacelnik, 1990)
testifies to the impact of head weight on aerodynamic balance.
Respiration
Mammals use a muscular diaphragm to expand the thoracic cavity, but they
still rely on the inefficient tidal-flow system of ventilation, so their greater rate
392
S. E. RANDOLPH
of respiratory exchange depends on the very much larger gas-exchange areas
within the lung compared with ectothermic vertebrates. In lower vertebrates
the alveoli, if present, are restricted to the lung wall, but in mammals the
whole lung is a spongy mass of alveolar air sacs. Not only have the number
of alveoli increased, but the size of each alveolus has decreased, resulting in a
greatly increased total surface area (Tenny & Remmers, 1963).
The respiratory surface of birds is fundamentally different in structure,
achieving a very high respiratory rate with a small, compact lung. Instead of
the blind alveoli, birds have very much lighter lungs consisting of parabronchi,
small parallel tubes open at both ends, through which air passes in a one-way
flow. The parabronchi are connected, through a system of larger bronchi, to
air sacs that act as reservoirs, ensuring that the respiratory surfaces are flushed
with fresh air more or less continuously, especially during flight when there is
considerable coordination between respiration and wing-beats (Berger, Roy &
Hart, 1970). ‘The predominantly dorsal distribution of air sacs around the whole
body cavity (as well as within the pneumatic bones) aids stability by keeping
the bird’s centre of gravity low. Branches of the interclavicular air sac that
ramify inside the flight muscles also allow birds to cool their flight muscles
directly by providing an evaporation surface from which water vapour can
escape to the outside \ria the bronchial system (Tucker, 1968). Thus in modern
birds the way the respiratory system is adapted to yield a high rate of gas
cxchange is intimately linked with flight activity. The most obvious explanation
is that it was the prior existence of flight (low energy, gliding flight) that
selected for this particular method of achieving a high respiratory rate in birds
rather than the method that exists in mammals.
Reproduction
The problems of supplying juvenile mammals with sufficient enrrgy for their
long and complex development, at a time when their small sizc exacerbates
the demands of maintaining thermal homeostasis, have been solved by the
evolution of, first, incubation of eggs within a burrow or pouch and nutrition
of the hatchlings by maternal lactation, as seen in the monotremes, and
wbsequently viviparity. Taken together, these reproductive features allow the
boung mammal to be highly protected from the fluctuations of the external
environment and enable the mother to supply the necessary nourishment slowly
over a long period, both before and after birth, rather than all at once in the
form of yolk at the start of egg development. Lactation may have originated
through the enhancement of egg survival by the anti-microbial properties of
secretions of cutaneous glands of the mother’s incubation pouch before such
secretions played any role in nutrition of the young (Blackburn, Hayssen &
Murphy, 1989).
As a solution to the same problem of high energy demands during
development, birds also typically produce altricial young which are protected
and nourished by elaborate parental care. Birds differ, however, in providing
large quantities of yolk to nourish the embryo within the egg, which necessitates
thc srquential production of single very large eggs, each one of which is
retained internally for a very short period and then incubated externally. The
biology of extant reptiles indicates that viviparity normally evolves by increasingly
FLIGHT, ENDOTHERMY AND BIRD ORIGIN
393
prolonged internal retention of the eggs (Packard, Tracy & Roth, 1977; Shine
& Bull, 1979), but all birds show the opposite trend, which can most obviously
be related to the need for females to decrease the burden associated with egg
retention that would add to their aerodynamic loading. This trend may have
been initiated during the early stages of the evolution of flight, prior to any
increase in the size of each egg, when weight reduction may have been critical
while the flight apparatus was less than perfect. It is not that it is impossible
to be both volant and viviparous, as are bats that are primarily endothermic
mammals and have evolved flight in spite of being viviparous, but rather that
the prior existence of flight would select against the evolution of viviparity via
the route of prolonged egg retention (Blackburn & Evans, 1986). By the same
argument, the ubiquitous condition of viviparity amongst therian mammals may
account for their relatively limited success in colonizing the air.
The hatchling birds are fed a diet that is unprocessed, apart from some
softening in the parent’s crop, and similar to that of the adult, although biased
towards high protein content (e.g. insects) if the adult diet is mainly carbohydrate
(Welty & Baptista, 1988). The absence of lactation in birds may reflect the
weight advantage of only having to carry food for the young on the journey
back to the nest, while lactating mammals must carry the extra weight associated
with mammary gland enlargement at all times until the young are weaned.
Alternatively, or additionally, the absence of lactation in birds may be a
corollary of the adult feeding apparatus. Juvenile birds can deal with solid food
because their masticatory apparatus, in the gut, can continue to operate
efficiently during rapid juvenile growth, unlike mammals whose accurately
occluding teeth would operate sub-optimally in a rapidly growing jaw with
repeated tooth replacement; the liquid diet in juvenile mammals allows a delay
in tooth eruption and then only one change of teeth (Pond, 1977).
CONCLUSIONS AND WIDER IMPLICATIONS
Flight was initiated before endothemy
There are three possible explanations for the apparent adaptedness for flight
of these basic requirements for a high metabolic rate in birds. If endothermy
preceded flight then either one must envisage the happy coincidence of all
three systems as preadaptations for flight, or one can postulate different original
solutions to the problem of high energy flow, not necessarily carbon copies of
the mammalian patterns, which were later reorganized under new selection
pressures imposed by flight. This latter view is not supported by the condition
in bats, in which, despite there being many skeletal specializations for flight
similar to those in birds, the feeding, respiratory and reproductive systems have
not diverged markedly from the common mammalian plan since the adoption
of flight. More parsimonious than either of these explanations is the conclusion
that in the animals ancestral to birds the adaptations for high energy flow
were constrained from the start by the need for aerodynamic stability; i.e.
flight, in its most basic form, preceded endothermy. The argument is not that
flight was fully developed before endothermy started, but rather that flight was
initiated first.
Ostrom (1991) considers that it was the prior existence of obligate bipedality
3w
S E FUNDOI.PH
in the theropod ancestors of birds that preset the condition of complete
functional separation of avian forelimbs. This accounts for the exceptional
evolution of bipedal flight in birds while all other flying vertebratcs, past and
present, are or were quadrupedal fliers. It could, therefore, be argued that the
avian solutions to the problems of high energy flow were selected for by the
condition of bipedality rather than aerodynamic stability. Evidence from
dinosaurs, however, suggests that lowly-positioned food-processing apparatus is
correlated more with diet than with a bipedal stance; many bipedal theropods
retained relatively large heads equipped with huge teeth, while ga3troliths have
been found in the stomachs of sauropod quadrupedal herbivores (Norman,
1985). Pterosaurs, on the other hand, had skulls lightened by large foramina.
with various degrees of tooth reduction (Norman, 1985), although this cannot
neccssarily be correlated more closely with their flying habits than with their
presumed diets of fish and aquatic invertebrates. Air sacs and the associated
respiratory mechanism also seem to be correlated more with an aerial existence
than with maintaining terrestrial bipedal stability. Pterosaurs, which are generally
thought to have been primarily quadrupedal (Pennycuick, 1986, but see Padian,
19831, rcsemblcd birds in possessing structurally identical pneumatic foramina
in the long bones, while other bipedal archosaurs did not (Padian, 1983).
Finally, egg retention or viviparity would not destabilize a terrestrial biped, a5
long as the developing embryos were housed low down as in the variety of
hipedal mammals (e.g. Macropodidae among the marsupials, Heteromyidac,
Dipodidae and Pedetidae among the rodents), but the extra weight would posr
a problem for aerial stability.
Scenario for the origin ofjight and endothermy
The above conclusion, based principally on living organisms, concurs bvith
recent deductions about the life style of the salient fossilized creature, Archaeopteyx,
which, whether or not the sister-group of modern birds (inter alza Ostrom, 1985;
Thulborn, 1984) is the only example we have of a feathered ‘reptile’. Archaeopteryx
possessed features, such as asymmetric primary feathers (Feduccia & Tardoff,
1979), a robust furcula for the origin of the pectoralis muscles (Olson &
Feduccia, 1979) and a claw geometry typical of perching and trunk-climbing
birds (Feduccia, 1993), which suggest that it was air-borne. Archaeopteryx did not,
however, possess a carina on the sternum, implying that it did not use air
cavities in its pectoral muscles for heat disposal, and therefore that it may not
have generated excessive heat during flight, consistent with its being a glider
and possibly even an ectotherm (Pennycuick, 1986). In fact, all that can be
safely said is that Archaeopteryx apparently had less of a heat load problem than
modern birds; perhaps it had a lower metabolic rate or less insulation. Rayner
i 1988) concludes that Archaeopteryx was capable
of incipient flapping flight,
although only at relatively high flight speeds, which indicates a gliding rather
than cursorial origin of active flight (although the proto-flier may have run up
onto high ground from which to glide down (Rayner, 1988)). As the energetic
costs of free-falling from on high are much less than jumping up from the
ground, Rayner’s conclusion is consistent with the above argument that the
first fliers had a low energy flow. Ruben (1991), on the other hand, invokes
the particular attributes of reptilian muscle physiology to argue that, although
FLIGHT, ENDOI'HERMY AND BIRD ORIGIN
39.5
Archaeopteyx was probably ectothermic, it may have been capable of shortdistance powered, flapping flight and even ground-upwards, standstill take-off.
In either case, any increase in flapping flight would require a gradual increase
in the rate of aerobic respiration to fuel the muscles and allow prolonged airborne activity. The chief locomotory advantage of an endothermic physiology
is that it permits greater duration of high levels of activity (Bennett & Ruben,
1979). Thus the primary selection pressure for the evolution of an endothermic
physiology in birds may have been the advantage of prolonged muscular activity
associated with flapping flight rather than thermal homeostasis per se. Thereafter
the positive feedback loop between increased metabolic rates and thermal
homeostasis would come into play, as raised metabolic rates (and muscular
thermogenesis by flight muscles) result in greater heat production, and a constant
body temperature itself facilitates the maintenance of a high metabolic rate
involving complex multi-enzyme systems. A positive feedback would also operate
between the greater energy costs, and thus food requirements, imposed by
raised metabolic rates and the greater foraging capacity allowed by prolonged
flight.
This scenario is different from the one often proposed to account for the
origin of endothermy in birds. The majority, although not unanimous (e.g.
Martin, 1983; Tarsitano, 1991), view is that the ancestors of birds are to be
found among coelurosaur theropod dinosaurs (znter aha Ostrom, 1976; Gauthier,
1986). Dinosaurs are thought to have achieved inertial homeothermy by virtue
of their large size even with low rates of metabolism (McNab & Auffenberg,
1976), and are imagined to have become so adapted to the condition of
constant body temperature that when the members of the line leading to birds
decreased in size they were obliged to raise their weight specific metabolic rate
(McNab, 1983) and wrap themselves in insulating feathers to maintain this
condition. While the decrease in body size necessary to permit the origin of
flight may have been even more extreme than that suggested by the fossils of
Compsognathus and Archaeopteryx (Pennycuick, 1986), there is in fact no evidence
that this was accompanied by an increase in metabolic rate. My conclusions
based on the comparative biology of birds and mammals are that these protobirds had not achieved a high energy flow physiology before they became
airborne, and that it was flight, rather than thermal homeostasis, that selected
for raised metabolic rates.
This is also different from the commonest scenario for the origin of
endothermy in mammals, where thermal homeostasis, often linked with
nocturnality (McNab, 1978), is seen as being of central importance (McNab,
1978, 1983; Kemp, 1982). Bennett & Ruben (1979), however, argue that the
origin of endothermy in both birds and mammals was directly linked with the
development of high activity sustained by aerobic metabolism. Nevertheless, the
different means by which high energy flow systems have been achieved
emphasizes the homoplastic (Kemp, 1 988) rather than synapomorphic (Gardiner,
1982) nature of endothermy in birds and mammals.
Functional origin offeathers
Of all the suggested original functions of feathers, insulation in an endotherm
is the only one that can be discounted on the basis of the above arguments.
S. E. RANDOLPH
396
The conclusion that flight preceded endothermy does not mean that feathers
necessarily originated for fight rather than any other of the suggested functions
that do not presuppose an endothermic condition. For example, Regal’s (1975)
suggestion that feathers originated as variable thermoregulators in an ectotherm
would fit with the scenario of flight originating in a small, low metaboloc rate,
glidmg (Rayner, 1988) or flapping (Ruben, 1991) reptile. At this stage the
‘feathers’ may not have shown much structural advance over their original
scale progenitors (Regal, 1975), although any early form of flight would select
for enlargement and lightening of marginal scales, followed by the correlated
progressive evolution of flight, feathers and the systems necessary for a raised
metabolic rate.
ACKNOWLEDGEMENTS
I am grateful to Tom Kemp for his critical encouragement, to Joseph Garner
for comments on the manuscript and to the Royal Society for financial support.
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