An adaptive scenario for the origin of birds and of flight in birds

by Richard Cowen and Jere H. Lipps

Department of Geology, University of California, Davis, California 95616

Proceedings of the Third North American Paleontological Convention, Volume 1, 109-112. Montreal, Canada, August 5-7, 1982

ABSTRACT

If framed with care and discipline, adaptive scenarios are scientifically testable hypotheses that may illuminate and lead to the solution of complex evolutionary questions. Cladograms and phylogenetic trees do not necessarily need to precede such scenarios, because the complexity of scenarios and the extent of their anatomical, ecological, paleoenvironmental implications may make them more testable, and more robust after testing, than a simple cladogram. For our case study, we examine the origin of birds and of flight in birds, Our hypothesis is simple--that display and the related behavior of intraspecific fighting played a significant role in the evolution of avian characters, including feathers, wings, and flight. Strong contour feathers arose as display structures from preexisting thermoregulatory feathers, preferentially enlarged and strengthened, and placed on large, movable panels (the forelimbs and tail) of small archosaurs. Their adaptive value was accentuated in sexual selection through mate choice and male-to-male fighting, as in many living birds. Leaping, jumping, and flapping were selected as fighting behaviors that were also preadaptive to flight. The scenario provides a unified theme which can explain the evolution of strong feathers and flight as a result of the same sexual selective pressure, and all available evidence from Archaeopteryx is compatible with it.

SCENARIOS

Evolutionary paleontologists seek to describe and explain events in the history of life. Their hypotheses are often framed as cladograms, trees, or scenarios. Cladograms display hypotheses of relationship among organisms. Their data base is almost entirely morphological, and many cladists explicitly reject information from the stratigraphic record. Trees are hypotheses of phylogeny, and morphological and stratigraphic data are both vitally important in their formulation. Both of these styles of hypothesis seek to answer questions about what happened in evolution. They are descriptive, narrative hypotheses based on data that contain as little interpretation as possible. They are testable as hypotheses when new pieces of comparable data become available.

Scenarios are different kinds of hypotheses. They seek to answer "Why?" questions about evolutionary events. By necessity they are interpretative, and will normally include as a central theme a suggestion for a mechanism of selection, radiation, or extinction, of a clade or within a clade. The data base for a scenario will include not only morphology and stratigraphy, but also biological, ecological, and environmental reconstruction. Because the hypothesis seeks to explain rather than describe, it can rarely be tested directly, but only by testing its implications and correlates. For this reason, and because a scenario is explicitly interpretative, it has often been regarded as less rigorous than a cladogram or a tree. Critics have suggested that a scenario should not be attempted until there is general agreement on the cladogram or tree that describes an evolutionary event. A scenario is a more complex and richer hypothesis than most cladograms or trees, and framing a scenario has come in some quarters to be regarded more as writing a historical novel than preforming historical science.

We believe that evolution occurs for good reasons in a complex physical and biological worls, and that it is scientifically legitimate to ask questions and to formulate hypotheses about those reasons, in the form of scenarios. In fact, such questions and hypotheses may very well lead more effectively and more quickly to the discovery of phylogeny than would stringent morphology on its own. For example, convergent evolution is best detected when we understand the adaptive context in which morphology is molded by the functional environment. A scenario, then, might well precede a formal tree or cladogram, and might act as a constraint on phylogenetic hypotheses by eliminating implausible alternatives.

Furthermore, several current controversies show that cladograms and trees are not as objective as their proponents might hope. The distinction between primitive and derived characters is not always easy (see Houde and Olson, 1981). The relationship among early tetrapods, and the ancestry of birds, are both problem areas in which alternative trees and cladograms are currently proposed. A scenario might shed light on these controversies.

A scenarion is a hypothesis and is testable. It is tested in the same way as a cladogram or a tree, that is, by the goodness of fit of new pieces of data. A scenario formulated with care and discipline will suggest critical points for further study. Since a scenario has a wider base in data and in interpretation, it should normally be susceptible to a wider range of tests, and be more robust after surviving such tests, than either a tree or a cladogram.

Scenarios may be more simple than they appear. One selective theme may have a great number of morphological correlates, and ecological and environmental implications. All these implications would appear in the scenario, making it rich and complex, capable of extensive testing, and of great explanatory power, in spite of its underlying parsimony.

Clearly the concept of a scenario is more open to mismanagement than a cladogram. Loosely-formed scenarios are not useful. Well constructed scenarios can give a depth of interpretation that no cladogram or tree would ever attempt. Scenarios are ambitious hypotheses. It is perhaps more a matter of taste whether one attempts the difficult task of forming a powerful scenario, or tries the simpler approach of cladistic analysis.

We present here a scenario. It is a hypothesis which relates the evolution of feathers, of birds, and of flight in birds, to one selective theme of display and intraspecific threat and combat. This simple theme, we believe, is the key to understanding the dramatic evolutionary transition between vertebrate classes and between terrestrially- and aerially-dominant ways of life. We present this scenario even though there is no universal agreement on the phylogeny of the transition, in the hope that it will shed light on that phylogenetic question.

THE ORIGIN OF FEATHERS

CURRENT HYPOTHESIS FOR THE ORIGIN OF FEATHERS
Ostrom (1974) and Regal (1975) argued that feathers arose from an archosaurian scale as insulating, thermoregulatory features. Ostrom believed that feathers were an insulating coat to keep a small warm-blooded animal warm; Regal thought that feathers were originally insulating devices to keep a small animal cool in high radiation.

The only good evidence is the feathers of Archaeopteryx and the possible feather fossil Praeornis. The body covering of Archaeopteryx is faint and ambiguous, but probably consists of feathers. However, the thermoregulatory hypothesis alone cannot explain the length and strength of the large feathers that form the "wing" on the forelimb and the large vane on the tail of Archaeopteryx. Some other selective factor must have operated to give rise to feathers strong and large enough to have become pre-adaptive to flight.

THE DISPLAY HYPOTHESIS
Display is a vital function of the feathers in very many living birds. Display translates directly into reproductive success via the intraspecific communication used in sexual selection, and it is important in repelling predators. We propose, as a working hypothesis, that display was important in the evolution of feathers from scales.

Feathers are scales which have been elongated and raised as large planar structures. A sophisticated dermal musculature allows them to be raised, lowered, and waved. Birds go to great lengths to maintain plumage in good condition. All these attributes are interpreted as related to display (and some other functions). We suggest that the enlargement and the planar structure, the motility and the maintenance of plumage all arose as part of a display function during the first appearance of proto-feathers. In particular, if the archosaurian ancestor already had skin or scale display (as many living reptiles do), we expect that selection, acting on the new, improved display devices, induced the very rapid evolution of feathers (and of birds).

TESTING THE DISPLAY HYPOTHESIS
Our hypothesis and the thermoregulatory hypothesis cannot be tested directly in the fossil record, but we can search for morphological correlates.
  1. If feathers arose for display, they should be most strongly developed on areas that are prominent and easily displayed. They should be movable for maximum effect, to increase apparent size and to draw attention to agility. If display arose in a small bipedal archosaur, it would reasonably have been best developed on the arms and tail, appendages that are comparatively high on the organism, and less intimately associated with locomotion and feeding than the feet and head. Evidence from Archaeopteryx allows the display hypothesis to pass this test.

  2. If display feathers arose, some of them might be similar to display feathers in modern birds, as opposed to down or flight feathers, for example. Praeornis, from the late Jurassic of Kazakhstan (Rautian 1978), may not be a feather, but if it is it can only be a display feather.

  3. As Geist (1966) and others have documented for mammals, it is common experience with birds that the visual appearance of adults and juveniles is very different. In birds, this has nothing to do with thermoregulation or with flight, but reflects the importance of intraspecific communication accomplished by feathers. If display was important in the early evolution of feathers, Archaeopteryx might show an adult/juvenile difference. This test would provide a sharp distinction between the display hypothesis and the thermoregulatory hypothesis.

    The Eichstätt specimen of Archaeopteryx is smaller than the other four skeletons, and according to Wellnhofer (1974, 1976) it is not as strongly ossified as they are. Its feather impressions are so weak that they were not seen for 20 years after the fossil was found. Yet the specimen is not a chick: it is about 60% of adult size. The Eichstätt specimen could be a large juvenile which had not yet grown the strong plumage of an adult. It does have plumage but it does not have display feathers.

We agree that thermoregulation was an important function of proto-feathers. But we argue that display was very important, and that this scenario is testable and so far survives testing. The relative merits of the thermoregulatory and display hypotheses are less important than to recognize that they had a synergistic selective effect acting to produce well-developed feathers. Feathers have properties which promote thermoregulation and display without detriment to either function. When the demonstrated effectiveness of sexual selection in driving evolutionary change and the correlation between display and sexual selection in living birds is recognized, the apparently sudden appearance of feathers and of birds in the fossil record in not surprising.

THE EVOLUTION OF FLIGHT IN BIRDS

PREVIOUS HYPOTHESES FOR THE ORIGIN OF FLIGHT IN BIRDS
Proto-feathers must already be in existence before flight can be attempted. Thus the question of the origin of flight is independent of the question of the origin of feathers. So far, three important hypotheses for the origin of flight have been proposed: the arboreal, the cursorial, and the cursorial-predator hypotheses. We propose a new alternative: the display and threat hypothesis. It is, of course, consistent with the model we suggest for the origin of strong feathers, and requires no shift in selective mechanism.

The arboreal hypothesis, first suggested by Marsh (1880), elaborated by Heilmann (1926) and Bock (1965, 1969), is also advocated by Feduccia (1980). It proposes that a bipedal ground-runner first became adapted to an arboreal life in which it took to jumping from limb to limb, then to gliding, and finally to flying. In this scenario, contour feathers became aerodynamically important at a jumping stage, and thence evolved directly into flight feathers. Ostrom (1974, 1979) cogently argues against these ideas. He interprets the hind-limb of Archaeopteryx as adapted for ground-running, not for perching. Furthermore, no non-flying tree-dweller today is a biped, which implies that bipedality is a poor pre-adaptation for arboreal life, and thus for evolution through an arboreal stage. We accept these arguments.

The cursorial hypothesis is traced to Williston (1879) and received its modern form from Nopsca (1907, 1923). Reptilian running bipeds, through elongation of the forelimbs and development of scales on the arms, formed thrust surfaces which provided acceleration when flapped, gradually leading to long leaps and flapping flight. Criticisms of this idea include: 1. flapping tends to decrease ground traction and acceleration, thus counteracting thrust from the legs; 2. elaboration of arm surfaces would at first only increase drag; 3. only a tiny amount of thrust would have been generated by an incipient wing (Ostrom 1979).

Ostrom (1974, 1979) proposed that avian flight arose from a cursorial predator whose feathers were selected for greater length and strength through their use as a sort of "insect net". The sweeping action of the arms necessary to trap insects in the feathers would have led to more and more powerful adduction, to assaults on larger and larger prey, to higher and higher leaps in the air after flying insects, and so to flapping flight. Ostrom believed that Archaeopteryx was just at or just past the threshold of powered flight, as it lacks a sternum and strut-like coracoid as well as some minor features of the skeleton which are associated with flight in living birds. We believe that the hypothesis is inadequate because 1. no living creature operates an insect-catching device of the type suggested; 2. an insect net would have caused drag while the animal was running (Ostrom suggested that the arms were held at the sides until the last moment of the chase); 3. the wing beats required to operate the "net" differ from those required for leaping and flying, thus requiring a rapid functional shift for which we see no selective agent in the proposed model; and 4. the model requires synchronized wing action, yet we believe that a single-winged motion would have been more plausible for catching insects.

THE NEW HYPOTHESIS: DISPLAY AND THREAT
We suggest that feathers developed synergistically as display and thermoregulatory structures. We propose also that flight itself arose in birds as a direct response to selection related to sexual display and male-to-male threat and fighting. Archaeopteryx can receive full morphological interpretation in this model.

Flying birds have long forelimbs, and wing length is closely related to body size, presumably for reasons connected with flight. Such channeled selection would not have operated on bipedal proto-birds, yet considerable arm-lengthening must have occurred in the lineage leading to Archaeopteryx. We suggest that this arm lengthening provided more surface area for display, and that it was pre-adaptive to flight. Archaeopteryx had a long reptilian tail with strong feathers attached. The tail, originally held prominently as an inertial balancing organ, served as a display panel, and its feathers increased in size, strength, erectility, and possible coloration as display was accentuated. Once the strong tail display feathers had evolved, selection for fast running in small bipeds would have acted to produce aerodynamic rather than inertial stabilizers.

Display of males to females is commonly interwoven with male-to-male display and confrontation, with an ultimate resort to flighting. In living birds such fights often take place on the ground even when opponents are capable of flight. A stable bipedal stance is important, as is a position above an opponent. Selection would operate to provide wing beats for lift as well as blows with the clawed hands, leading eventually to the capability for flight.

CONCLUSIONS

The display and threat scenario has a simple theme, and it carries a large number of anatomical, behavioral, ecological, and environmental implications, all derived from an immense data base among living birds. The general correlates of display and threat are also rather widespread among other vertebrates, so that they are reasonable models to apply to the ancestors of birds. Many of the implications of our hypothesis can be tested by examination of Archaeopteryx, and the scenario survives the test. Other implications involve the environment in which flight evolved, and are likewise testable, though they are not analyzed in this paper. The display scenario suggests that birds did not evolve through a long chain of very different successive selective influences, as Bock (1965, 1969) has proposed. The scenario also explains morphology which other scenarios do not, and so it has power as well as simplicity. And if the biology of Archaeopteryx conforms to the pattern we suggest, the predecessors and descendants of this most famous fossil should be made easier to identify and to interpret biologically.

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