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Origins of Avian Flight – a New Perspective

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Origins of Avian Flight – a New Perspective Origins of avian flight – a new perspective Larry D. Martin Department of Ecology and Evolutionary Biology; Museum of Natural History and Biodiversity Research Center, University of Kansas, Lawrence, KS 66045, USA e-mail: [email protected] ABSTRACT - The discovery of a primitive bird-like dromaeosaur (Microraptor) with four functional wings vindicates Beebe’s suggestion that birds went through a tetrapteryx stage in the origin of flight. Flight originated from an arboreal glid- ing ancestor and Longisquama may be more central to understanding how this came about than previously supposed. Keywords: Dromaeosaur, Microraptor, Longisquama, birds, flight, Upper Triassic, Lower Cretaceous Les origines du vol avien – Perspectives nouvelles - La découverte d’un dromaeosaure semblable à un oiseau primitif (Microraptor) avec quatre ailes fonctionnelles justifie la suggestion de Beebe selon laquelle les oiseaux sont passés par un stade tetrapteryx dans l’origine du vol. Le vol est apparu chez un ancêtre arboricole planeur, et Longisquama est peut être plus important qu’on l’a supposé pour comprendre les modalités de cette transition. INTRODUCTION the stratigraphically older Deinonychus studied by Ostrom (1969). In this sense the fossil record did not provide an Much of the argument over flight origins revolves orderly progression from terrestrial “maniraptorians” to fly- around Archaeopteryx, the first bird to be recognized from ing birds. In fact, Archaeopteryx, a very typical bird in most the Mesozoic and still the oldest known bird. Archaeop- respects, is significantly older than any credible evidence for teryx displays a remarkable combination of avian and reptil- dromaeosaurs, the dinosaurs thought to be closest to birds. ian characters and has become the archetype of a “missing Functionally there are additional problems. All of link.” It was discovered in 1861, only two years after Dar- the then known dromaeosaurs were fast running terrestrial win’s Origin of Species, but did not immediately become a predators with shortened arms and the scapula arranged di- major player in speculation about avian origins. In 1864, agonally across the chest. Modern birds develop these traits Huxley became the chief proponent of the idea that the then when becoming flightless, but it was hard to see how they newly discovered bipedal dinosaurs were good ancestors for could easily be modified in the other direction to form a bipedal birds and this was the dominant theory until the be- flight capable wing, and indeed no flightless bird showing ginning of the 20th century (Witmer, 1991). The discovery these modifications is known to have ever regained flight. of older and more primitive bipedal archosaurs provided an Dromaeosaurs are usually slender and deep bod- alternative ancestry lacking specializations that seemed to ied—decidedly unbirdlike proportions. Some had an en- bar dinosaurs from direct avian ancestry. Heilmann’s (1926) larged claw on the second digit of the foot presumably as book The Origin of Birds solidified the resultant position that a weapon for predation, and shared with ramphorhynchoid birds are only related to dinosaurs in sharing a basal archo- pterosaurs a system of anteriorly projecting rods extending saurian ancestor (Martin, 2004). The dinosaur argument lay from the prezygopophyses and chevrons of the tail. In these dormant for over sixty years until revived by Ostrom (1973) respects, they are specialized as compared to Archaeopteryx along with the terrestrial origin of avian flight. Ostrom did and other birds. We can easily understand how they might not think that all dinosaurs stood equally close to birds, and be derived from primitive flying birds, as similar changes to demonstrated that some advanced “theropods” were clearly the shoulder girdle and forelimbs also occurred in flightless more birdlike than are other dinosaurs. His observations are birds (Gastornis; Struthio) derived from flying ancestors. It supported by many subsequent studies extending compari- is harder to see how dromaeosaurs could resemble an avian sons to late Cretaceous “maniraptorians”, like Bambiraptor ancestor. In particular, their highly derived body propor- (Burnham, 2004), which are significantly more birdlike than tions would have prevented them from being very successful ORYCTOS vol. 7, 2008 45 Figure 1 - Reconstruction of Microraptor based on Xu et al., 2003 and examination of several additional specimens: a) wings out as re- stored in Xu et al., 2003; b) hind wing posterior against the tail so that they combine to make an enlarged airfoil as in the Archaeopteryx tail (fig. 2c); c) front and hind wings oriented posteriorly to form a broad gliding surface. climbers. birds is usually framed to avoid this problem. Bipedality The best evidence for transitional forms between predates flight and birds were derived from small, fast run- “maniraptorians” and more typical birds comes from the Je- ning predatory dinosaurs with sophisticated powers of hand hol fauna of Liaoning, China (120,000,000 years old or a lit- manipulation (Padian, 1985; Gishlick, 2001). The move- tle older). These deposits show a diversity of animals living ments involved with prey capture were modified to provide on or near the shorelines of Early Cretaceous lakes (Zhou et a power supplement to the legs in running and, with further al., 2003). Judging from the fossil plants and insects, the sur- modification, led to flight from the “ground-up.” Because the rounding countryside was forested. The deposits preserve a airfoil surface in birds is composed of feathers, this scenario combination of small terrestrial, arboreal, flying and aquatic presupposes that feathers had already evolved. organisms. Most supporters of a cursorial origin of flight as- sume that feathers originated for a nonflight function (insula- ORIGIN OF FLIGHT tion, prey capture) and were later recruited for aerial propul- sion. The earliest examples might lack any traces of features The origin of avian flight is one of the most inter- giving airfoil capability. Fibrous structures lacking diag- esting problems in biology. Pterosaurs and bats incorporate nostic feather features have been described from the Early the arms and legs into a continuous fold of skin (patagium) Cretaceous Chinese deposits as feather progenitors and were and can be compared directly with living examples of glid- found in a variety of dinosaurs and other archosaurs (pte- ing mammals (Bock, 1985). In birds, the legs and the wings rosaurs) (Ji et al., 1998; Czerkas and Ji, 2002; Mayr et al., are decoupled with little evidence showing that a full pata- 2002; Xu et al., 2001; Wang et al. 2002). This broad phy- gium was ever present, although there are distinct patagial logenetic distribution implies that feathers evolved early in surfaces on the wings and some birds have limited powers archosaur evolution and were replaced later with scales in of flight with very little feather development (megapode a variety of lineages including all the dinosaurs known to chicks). Modern birds are accomplished bipeds, and differ be covered with scales (carnosaurs, compsognathids, sauro- in this respect from bats and pterosaurs although some bats pods, hadrosaurs, ceratopsians, ornithomimosaurs (Martin show brief bursts of bipedal locomotion on the ground and and Czerkas, 2000)). we would expect pterosaurs to do the same if only to free These putative fiber-like feathers are arranged in the wings for take off. If all other examples of flight in ter- a variety of patterns, but few resemble the distribution of restrial vertebrates are rooted in arboreal quadrupedal forms, feathers in modern birds or Archaeopteryx, and they often should bipedality be an expected precursor to avian flight? It seem to form the outline of crests or flaps. Individually wouldn’t seem likely, if flight originated in an arboreal glider they appear to be solid, and without a continuous branching as is nearly certain with bats and pterosaurs. Such animals pattern. They often lie closely parallel to each other (Xu et place aerodynamic lift above the body mass and distribute al., 2001). Feathers are hollow, widely spaced from each it down the length of the body to ensure stability. It is hard other and usually arranged in distinct “tracts”, but not long to see how the legs could avoid being involved in the early “crests”. They are normally composed of multiple branches gliding phases. The hypothesis of a dinosaurian origin of (barbs) converging towards a central rachis. None of these ORYCTOS vol. 7, 2008 46 features are clearly demonstrated in the so-called protofeath- than do other dromaeosaurs. Its status as a dromaeosaur is ers and their anatomical arrangement and distribution is of- strongly supported by an enlarged second digit claw on the ten identical with muscles and ligaments (Lingham-Soliar, foot and forward projecting elongations of the prezygopo- 1999; 2003a, b). An interpretation of some of these struc- hyses and chevrons on the caudal vertebrae. Cladistically it tures as collagen and/or muscle fibers is consistent with their occupies the same plesiomorphic sister-group relationship to anatomical distribution and better fits their tendency to di- the other dromaeosaurs that Caudipteryx has to the ovirap- vide into progressively smaller bundles of fibers. It is also tosaurs (Hwang et al., 2002). The posterior wing is similar likely that scales and taphonomic accidents have in some ad- in size and morphology to the anterior one with the longest ditional cases, been misinterpreted as protofeathers or even feathers coming off the foot. feathers. It would seem, that even on an unquestioned fossil Xu et al. (2003) assigned their material to Micro- bird, anatomical characters should be visible before we ac- raptor Xu, Zhou, and Wang, 2000a. The combination of cept an identification of feathers for a fibrous haze surround- tiny toes, flight feathers on the tarsometatarsus and nature ing the skeleton. of the femur and pelvis make it almost impossible for Mi- Unquestioned feathers eventually made the cover croraptor to have walked efficiently, let alone run. It must of Nature (Xu et al., 2003) on a supposed dinosaur, Caudip- have been completely arboreal.
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