Evolution of Avian Flight

Abstract

The origin of birds and of bird flight has drawn scientific interest since the inception of evolutionary thinking. Though early investigations were hampered by a paucity of fossils, new discoveries have filled in many gaps and provided unprecedented detail into morphological changes that attended the evolutionary appearance of birds and bird flight. Birds are now widely regarded as the descendents of theropod dinosaurs. In contrast, form–function relationships and behaviours that might have facilitated the evolutionary acquisition of flight remain widely debated. Given the versatility of extant birds, we should not expect to find only one solution to this problem. Nevertheless, much debate seems to stem not from looking for multiple plausible functions and behaviours, but rather from traditional ‘ground up’ versus ‘trees down’ assumptions and a general lack of experimental and ecological support for inferred form–function relationships. Many researchers have therefore called for more rigorous hypothesis testing, and a plethora of new techniques and perspectives are up to the challenge.

Key Concepts:

  • Birds are the descendents of bipedal theropod dinosaurs.

  • Evolutionary assembly of the avian body plan occurred gradually, with bird‐like wings evolving before bird‐like skeletons, in conjunction with a reduction in body size and then a cranial shift in centre of mass.

  • These changes took place via a series of transitional anatomical stages that were presumably associated with transitional functions and behaviours before becoming co‐opted for flapping flight.

  • Many origin‐of‐flight hypotheses have been proposed, and it is challenging to discriminate among them. Much debate seems to stem from traditional ‘ground up’ versus ‘trees down’ assumptions and a general lack of experimental and ecological support for inferred form–function relationships.

  • A growing number of researchers have therefore suggested that hypotheses must be consistent not only with the fossil record, but also with experimental support for form–function relationships and behaviours inferred by origin‐of‐flight scenarios.

  • New techniques and perspectives are meeting this challenge and providing more rigorous insight into the origin of flight in birds.

  • For example, recent work on developing birds with dinosaur‐like anatomies clearly demonstrates that behaviours involving the cooperative use of wings and legs (e.g. wing‐assisted incline running and steaming) act as a developmental (or evolutionary) bridge between leg‐based terrestrial locomotion and wing‐based aerial locomotion, by allowing developing birds (or evolving dinosaurs) to supplement their wings with their legs until the wings can fully support body weight during flight.

Keywords: birds; theropods; evolution of flight; origin of flight; protowings; locomotion; transitional fossils; incremental adaptive stages

Figure 1.

Locomotor modularity: Extant birds are highly diverse, both morphologically and behaviourally. Much of the variation in avian locomotor strategies or styles of locomotion seems to stem from a highly modular body plan: birds have compartmentalised the single locomotor unit of their ancestors (red) into discrete wing (blue), leg (red) and tail (blue) locomotor modules, and exploited many different environments. Specialising one set of limbs for walking or running and one set for flight presumably facilitates terrestrial locomotion without compromising aerial locomotion, and vice versa. (a) Early tetrapods were presumably like extant salamanders, locomoting by moving the trunk, tail and all four limbs as a single integrated unit. (b) Early theropods were bipedal, freeing the forelimbs for other functions. (c) Extant birds are highly modular, using their wings and legs to generate different types of forces (aerodynamic, hydrodynamic and ground reaction) and move through different environments. Reproduced from Gatesy and Dial .

Figure 2.

Theropod–avian phylogeny. The evolution of flight in theropod dinosaurs was marked by many changes in skeletal morphology, feather morphology, body size and mass distribution. The pectoral girdle and forelimb were enlarged, the trunk stiffened, the pelvic girdle expanded, the femur shortened, the tail reduced and many joints modified (nodes A–I). Changes in skeletal morphology were accompanied by the appearance and evolution of feathers. Plumulaceous feathers (node A) were complemented by pennaceous feathers that first appeared as fans on the distal tail and as protowings on the distal forelimb (node D), and that became more widely distributed and more asymmetric in more derived theropods. Thus bird‐like wings (∼ nodes E–F) evolved before bird‐like skeletons (∼ node I), in conjunction with a reduction in body mass followed by a cranial shift in the centre of mass. Clades indicated by capitalised letters: (A) Theropoda, (B) Coelurosauria, (C) Maniraptora, (D) Unnamed, (E) Paraves/Eumaniraptora, (F) Avialae, (G) Pygostylia, (H) Ornithothoraces and (I) Ornithurae. Feathered theropods indicated by italicised abbreviations (all feathered theropods up through basal pygostylians included): Sa, Sciurumimus; Di, Dilong; Yu, Yutyrannus; Or, Ornithomimus; Ss, Sinosauropteryx; Sc, Sinocalliopteryx; Be, Beipiaosaurus; Su, Shuvuuia; Ca, Caudipteryx; Sm, Similicaudipteryx; Pr, Protarchaeopteryx; Yx, Yixianosaurus; Ji, Jinfengopteryx; B, BPM 1 3–13; Ra, Rahonavis; Mi, Microraptor; So, Sinornithosaurus; Ve, Velociraptor; An, Anchiornis; Xi, Xiaotingia; Pe, Pedopenna; Ar, Archaeopteryx; Je, Jeholornis; Da, Dalianraptor; En, Epidendrosaurus; Ex, Epidexipteryx; Zh, Zhongornis; Zj, Zhongjianornis; Sa, Sapeornis; Eo, Eoconfuciusornis; Co, Confuciusornis; Ch, Changchengornis. Feather morphology indicated by colours: grey, unbranched or ‘downy’ feathers (types I, II or IIIb (Prum, )); black, pennaceous feathers (types IIIa, IIIab, IV or Va). Modified from Heers and Dial . © Elsevier.

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References

AmphibiaWeb (2013) Information on Amphibian Biology and Conservation. Berkeley, California: AmphibiaWeb. Available at: http://amphibiaweb.org/ (accessed on 1 April 2013).

Alexander DE, Gong E, Martin LD, Burnham DA and Falk AR (2010) Model tests of gliding with different hindwing configurations in the four‐winged dromaeosaurid Microraptor gui. Proceedings of the National Academy of Sciences of the USA 107: 2972–2976.

Alexander RM (2002) The merits and implications of travel by swimming, flight and running for animals of different sizes. Integrative and Comparative Biology 42: 1060–1064.

Altshuler DL, Dudley R, Heredia SM and McGuire JA (2010) Allometry of hummingbird lifting performance. Journal of Experimental Biology 213: 725–734.

Beebe CW (1915) A tetrapteryx stage in the ancestry of birds. Zoologica 2: 38–52.

Biewener AA (1998) Muscle function in vivo: a comparison of muscles used for elastic energy savings versus muscles used to generate mechanical power1. American Zoologist 38: 703–717.

Bishop KL (2008) The evolution of flight in bats: narrowing the field of plausible hypotheses. Quarterly Review of Biology 83: 153–169.

Bock W (1965) The role of adaptive mechanisms in the origin of higher levels of organization. Systematic Biology 14: 272–287.

Bock W (1969) The origin and radiation of birds. Annals of the New York Academy of Sciences 167: 147–155.

Bock W (1983) On extended wings. Sciences 23: 16–20.

Bock W (1985) The arboreal theory for the origin of birds. In: Hecht MK, Ostrom JH, Viohl G and Wellnhofer P (eds) The Beginnings of Birds, p. 199–207. Eichstätt, Germany: Jura Museum.

Bock W (1986) The arboreal origin of avian flight. Memoirs of the California Academy of Sciences 8: 57–72.

Bryant HN and Russell AP (1992) The role of phylogenetic analysis in the inference of unpreserved attributes of extinct taxa. Philosophical Transactions of the Royal Society of London. Series B Biological Sciences 337: 405–418.

Bundle MW and Dial KP (2003) Mechanics of wing‐assisted incline running (WAIR). Journal of Experimental Biology 206: 4553–4564.

Burgers P and Chiappe LM (1999) The wing of Archaeopteryx as a primary thrust generator. Nature 399: 60–62.

Caple G, Balda RP and Willis WR (1983) The physics of leaping animals and the evolution of pre‐flight. American Naturalist 121: 455–476.

Carrano MT (2000) Homoplasy and the evolution of dinosaur locomotion. Paleobiology 26: 489–512.

Chatterjee S (1997) The Rise of Birds: 225 Million Years of Evolution. Baltimore: Johns Hopkins University Press.

Chen P, Dong Z and Zhen S (1998) An exceptionally well‐preserved theropod dinosaur from the Yixian Formation of China. Nature 391: 147–152.

Chiappe LM (2007) Glorified Dinosaurs: The Origin and Early Evolution of Birds. USA: Wiley‐Liss.

Chiappe LM and Dyke GJ (2002) The Mesozoic radiation of birds. Annual Review of Ecology and Systematics 33: 91–124.

Chiappe LM, Ji SA, Ji Q and Norell M (1999) Anatomy and systematics of the Confuciusornithidae (Theropoda, Aves) from the late Mesozoic of northeastern China. Bulletin of the American Museum of Natural History 242: 1–89.

Chinsamy‐Turan A (2005) The Microstructure of Dinosaur Bone: Deciphering Biology with Fine‐Scale Techniques. Baltimore: Johns Hopkins University Press.

Clack JA (2011) The fin to limb transition: new data, interpretations, and hypotheses from paleontology and developmental biology. Annual Review of Earth and Planetary Sciences 37: 163–179.

Clarke JA (2004) Morphology, phylogenetic taxonomy, and systematics of Ichthyornis and Apatornis (Avialae: Ornithurae). Bulletin of the American Museum of Natural History 286: 1–179.

Clarke JA and Norell MA (2002) The morphology and phylogenetic position of Apsaravis ukhaana from the Late Cretaceous of Mongolia. American Museum Novitates 3387: 1–46.

Clarke JA, Zhou Z and Zhang F (2006) Insight into the evolution of avian flight from a new clade of Early Cretaceous ornithurines from China and the morphology of Yixianornis grabaui. Journal of Anatomy 208: 287–308.

Cleland CE (2001) Historical science, experimental science, and the scientific method. Geology 29: 987–990.

Cowen R and Lipps JH (1982) An adaptive scenario for the origin of birds and of flight inbirds. Proceedings of the Third North American Paleontological Convention, 1982, vol. 1, pp 109–112. Montreal, Quebec, Canada.

Currie PJ and Chen P (2001) Anatomy of Sinosauropteryx prima from Liaoning, northeastern China. Canadian Journal of Earth Sciences 38: 1705–1727.

Czerkas SA, Zhang D, Li J and Li Y (2002) Flying dromaeosaurs. In: Czerkas SA (ed.) Feathered Dinosaurs and the Origin of Flight, p. 97–126. Blanding, Utah: The Dinosaur Museum.

Darwin C (1859) On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. London, UK: Murray.

De Margerie E, Sanchez S, Cubo J and Castanet J (2005) Torsional resistance as a principal component of the structural design of long bones: Comparative multivariate evidence in birds. Anatomical Record 282A: 49–66.

Del Hoyo J, Elliot A and Sargatal J (eds) (1996) Handbook of the Birds of the World. Barcelona: Lynx Edicions.

Dial KP (2003) Wing‐assisted incline running and the evolution of flight. Science 299: 402–404.

Dial KP, Green E and Irschick DJ (2008) Allometry of behavior. Trends in Ecology and Evolution 23: 394–401.

Dial KP, Heers AM and Dial TR (in press) Ontogenetic and evolutionary transformations: the ecological significance of rudimentary structures. In: Dial K, Shubin N and Brainerd B (eds) Great Transformations: Major Events in the History of Vertebrate Life. University of California Press.

Dial KP and Jackson BE (2011) When hatchlings outperform adults: locomotor development in Australian brush turkeys (Alectura lathami, Galliformes). Proceedings of the Royal Society B: Biological Sciences 278: 1610–1616.

Dial KP, Jackson BE and Segre P (2008) A fundamental avian wing‐stroke provides a new perspective on the evolution of flight. Nature 451: 985–989.

Dial KP, Randall RJ and Dial TR (2006) What use is half a wing in the ecology and evolution of birds? BioScience 56: 437–445.

Dial TR and Carrier DR (2012) Precocial hindlimbs and altricial forelimbs: partitioning ontogenetic strategies in Mallard ducks (Anas platyrhynchos). Journal of Experimental Biology 215: 3703–3710.

Dimond CC, Cabin RJ and Brooks JS (2011) Feathers, dinosaurs, and behavioral cues: defining the visual display hypothesis for the adaptive function of feathers in non‐avian theropods. BIOS 82: 58–63.

Dingus L and Rowe T (1998) The Mistaken Extinction: Dinosaur Evolution and the Origin of Birds. New York: WH Freeman.

Earls KD (2000) Kinematics and mechanics of ground take‐off in the starling Sturnis vulgaris and the quail Coturnix coturnix. Journal of Experimental Biology 203: 725–739.

Elzanowski A (2002) Archaeopterygidae (Upper Jurassic of Germany). In: Chiappe LM and Witmer LM (eds) Mesozoic Birds: Above the Heads of Dinosaurs, p. 129–159. Los Angeles: University of California Press.

Erickson GM (2005) Assessing dinosaur growth patterns: a microscopic revolution. Trends in Ecology and Evolution 20: 677–684.

Evans HE and Heiser JB (2004) What's inside: anatomy and physiology. In: Podulka S, Rohrbaugh RW and Bonney R (eds) In Cornell Lab of Ornithology. Handbook of Bird Biology, p. 4.1–4.162. Princeton, NJ: Princeton University Press.

Feduccia A (1999) The Origin and Evolution of Birds. New Haven, CT: Yale University Press.

Forster CA, Sampson SD, Chiappe LM and Krause DW (1998) The theropod ancestry of birds: new evidence from the Late Cretaceous of Madagascar. Science 279: 1915–1919.

Gao C, Chiappe LM, Meng Q et al. (2008) A new basal lineage of early Cretaceous birds from China and its implications on the evolution of the avian tail. Paleontology 51: 775–791.

Gao C and Liu J (2005) A new avian taxon from Lower Cretaceous Jiufotang formation of western Liaoning. Global Geology 24: 313–316.

Garner JP, Taylor GK and Thomas ALR (1999) On the origins of birds: the sequence of character acquisition in the evolution of avian flight. Proceedings of the Royal Society B: Biological Sciences 266: 1259–1266.

Gatesy SM (1990) Caudofemoral musculature and the evolution of theropod locomotion. Paleobiology 16: 170–186.

Gatesy SM (1991) Hind limb scaling in birds and other theropods: implications for terrestrial locomotion. Journal of Morphology 209: 83–96.

Gatesy SM (1995) Functional evolution of the hindlimb and tail from basal theropods to birds. In: Thomason JJ (ed.) Functional Morphology in Vertebrate Paleontology, p. 219–234. New York, NY: Cambridge University Press.

Gatesy SM and Baier DB (2005) The origin of the avian flight stroke: a kinematic and kinetic perspective. Paleobiology 31: 382–399.

Gatesy SM and Dial KP (1996a) Locomotor modules and the evolution of avian flight. Evolution 50: 331–340.

Gatesy SM and Dial KP (1996b) From frond to fan: Archaeopteryx and the evolution of short‐tailed birds. Evolution 50: 2037–2048.

Gauthier J (1986) Saurischian monophyly and the origin ofbirds. Memoirs of the California Academy of Sciences 8: 1–55.

Gauthier JA and Padian K (1985) Phylogenetic, functional and aerodynamic analysis of the origin of birds and their flight. In: Hecht MK, Ostrom JH, Viohl G and Wellnhofer P (eds) The Beginnings of Birds: Proceedings of the International Archaeopteryx Conference Eichstatt 1984, p. 199–207. Eichstätt, Germany: Jura Museum.

Gishlick AD (2001) The function of the manus and forelimb of Deinonychus antirrhopus and its importance for the origin of avian flight. In: Gauthier JA and Gall LF (eds) New Perspectives on the Origin and Early Evolution of Birds: Proceedings of the International Symposium in Honor of John H. Ostrom, p. 301–318. New Haven, CT: Peabody Museum of Natural History, Yale University.

Glasheen JW and McMahon TA (1996) A hydrodynamic model of locomotion in the basilisk lizard. Nature 380: 340–342.

Gould S (1977) Ontogeny and Phylogeny. Cambridge, MA: Harvard University Press.

Gould SJ (1965) Is uniformitarianism necessary? American Journal of Science 263: 223–228.

Greenewalt CH (1975) The flight of birds: the significant dimensions, their departure from the requirements for dimensional similarity, and the effect on flight aerodynamics of that departure. Transactions of the American Philosophical Society 65: 1–67.

Habib MB and Ruff CB (2008) The effects of locomotion on the structural characteristics of avian limb bones. Zoological Journal of the Linnean Society 153: 601–624.

Heers A, Baier D, Jackson B and Dial K (2011c) From baby birds to feathered dinosaurs: the ontogeny and evolution of skeletal form and function. Journal of Vertebrate Paleontology 31(suppl. 2): 124.

Heers AM, Baier DB, Jackson BE and Dial KP (2011b) Developing skeletons in motion: the ontogeny of skeletal form and function in a precocial ground bird (Alectoris chukar). Integrative and Comparative Biology 51: e55.

Heers AM and Dial KP (2012) From extant to extinct: locomotor ontogeny and the evolution of avian flight. Trends in Ecology and Evolution 27: 296–305.

Heers AM, Tobalske BW and Dial KP (2011a) Ontogeny of lift and drag production in ground birds. Journal of Experimental Biology 214: 717–725.

Heilmann G (1927) The Origin of Birds. New York: D. Appleton and Company.

Hinic‐Frlog S and Motani R (2010) Relationship between osteology and aquatic locomotion in birds: determining modes of locomotion in extinct Ornithurae. Journal of Evolutionary Biology 23: 372–385.

Holtz TR (2007) Dinosaurs: The Most Complete, Up‐To‐Date Encyclopedia for Dinosaur Lovers of all Ages. New York: Random House Children's Books.

Homberger DG and de Silva KN (2000) Functional microanatomy of the feather‐bearing integument: implications for the evolution of birds and avian flight. American Zoologist 40: 553–574.

Hopson JA (2001) Ecomorphology of avian and nonavian theropod phalangeal proportions: Implications for the arboreal versus terrestrial origin of bird flight. In: Gauthier J and Gall LF (eds) New Perspectives on the Origin and Early Evolution of Birds: Proceedings of the International Symposium in Honor of John H. Ostrom. New Haven, CT: Peabody Museum of Natural History, Yale University.

Hou L, Martin LD, Zhou Z and Feduccia A (1996) Early adaptive radiation of birds: evidence from fossils from Northeastern China. Science 274: 1164–1167.

Hou L, Zhou Z, Martin LD and Feduccia A (1995) A beaked bird from the Jurassic of China. Nature 377: 616–618.

Hu D, Hou L, Zhang L and Xu X (2009) A pre‐Archaeopteryx troodontid theropod from China with long feathers on the metatarsus. Nature 461: 640–643.

Hutchinson JR (2001) The evolution of pelvic osteology and soft tissues on the line to extant birds (Neornithes). Zoological Journal of the Linnean Society 131: 123–168.

Hutchinson JR (2002) The evolution of hindlimb tendons and muscles on the line to crown‐group birds. Comparative Biochemistry and Physiology A 133: 1051–1086.

Hutchinson JR (2011) On the inference of function from structure using biomechanical modelling and simulation of extinct organisms. Biology Letters 10.1098/rsbl.2011.0399.

Hutchinson JR and Allen V (2009) The evolutionary continuum of limb function from early theropods to birds. Naturwissenschaften 96: 423–448.

Hutchinson JR and Garcia M (2002) Tyrannosaurus was not a fast runner. Nature 415: 1018–1021.

Hutchinson JR and Gatesy SM (2006) Dinosaur locomotion: beyond the bones. Nature 440: 292–294.

Hwang S, Norell M, Ji Q and Gao K (2004) A large Compsognathid from the Early Cretaceous Yixian Formation of China. Journal of Systematic Paleontology 2: 13–30.

Hwang S, Norell MA, Qiang J and Keqin G (2002) New Specimens of Microraptor zhaoianus (Theropoda: Dromaeosauridae) from northeastern China. American Museum Novitates 3381: 1–44.

Jackson BE (2011) Ontogeny of contractile behavior in the flight muscles of birds. Society of Experimental Biology, p. 77. Glasgow. Available at: http://www.sebiology.org/meetings/Past_Meetings/Glasgow_2011/docs/Abstracts.pdf (accessed on 1 April 2013).

Jackson BE and Dial KP (2011) Scaling of mechanical power output during burst escape flight in the Corvidae. Journal of Experimental Biology 214: 452–461.

Jackson BE, Segre P and Dial KP (2009) Precocial development of locomotor performance in a ground‐dwelling bird (Alectoris chukar): negotiating a three‐dimensional terrestrial environment. Proceedings of the Royal Society B: Biological Sciences 276: 3457–3466.

Jackson BE, Tobalske BW and Dial KP (2011) Pectoralis contractile activity during WAIR and flight in pigeons. Integrative and Comparative Biology 51: e63.

Jacob F (1977) Evolution and tinkering. Science 196: 1161–1166.

Jenkins FA (1993) The evolution of the avian shoulder joint. American Journal of Science 293: 253–267.

Jetz W, Thomas GH, Joy JB, Hartmann K and Mooers AO (2012) The global diversity of birds in space and time. Nature 491: 444–448.

Ji Q, Chiappe LM and Ji S (1999) A new Late Mesozoic Confuciusornithid bird from China. Journal of Vertebrate Paleontology 19: 1–7.

Ji Q, Ji S, Lu J et al. (2005) First avialan bird from China (Jinfengopteryx elegans gen. et sp. nov.). Geological Bulletin of China 24: 197–205.

Ji Q, Ji S, You H et al. (2003) An Early Cretaceous avialan bird, Shenzhouraptor sinensis from western Liaoning, China. Acta Geologica Sinica 77: 21–27.

Ji Q, Norell MA, Gao K, Ji S and Ren D (2001) The distribution of integumentary structures in a feathered dinosaur. Nature 410: 1084–1088.

Ji S and Ji Q (2007) Jinfengopteryx compared to Archaeopteryx, with comments on the mosaic evolution of long‐tailed avialan birds. Acta Geologica Sinica 81: 8–15.

Ji S, Ji Q, Lu J and Yuan C (2007) A new giant compsognathid dinosaur with long filamentous integuments from Lower Cretaceous of northeastern China. Acta Geologica Sinica 81: 8–15.

Lauder G (1995) On the inference of structure from function. In: Thomason JJ (ed.) Functional Morphology in Vertebrate Paleontology, p. 1–18. New York, NY: Cambridge University Press.

Lauder GV (1981) Form and function: structural analysis in evolutionary morphology. Paleobiology 7: 430–442.

Lauder GV (1990) Functional morphology and systematics: studying functional patterns in an historical context. Annual Review of Ecology and Systematics 21: 317–340.

Liu H, Ellington C and Kawachi K (1998) A computational fluid dynamic study of hawkmoth hovering. Journal of Experimental Biology 201: 461–477.

Long CA (2003) Physical theory, origin of flight, and a synthesis proposed for birds. Journal of Theoretical Biology 224: 9–26.

Lyell C (1830) Principles of Geology: Being an Attempt to Explain the Former Changes of the Earth's Surface, by Reference to Causes Now in Operation . London, UK: John Murray.

Makovicky PJ and Zanno LE (2011) Theropod diversity and the refinement of avian characteristics. In: Dyke G and Kaiser G (eds) Living Dinosaurs: The Evolutionary History of Modern Birds, p. 9–29. West Sussex, UK: John Wiley.

Marsh OC (1880) Odontornithes: a monograph on the extinct toothed birds of North America. Professional Papers of the Engineer Department, U.S. Army 18: 1–201.

Marsh OC (1881) Discovery of a fossil bird in the Jurassic of Wyoming. American Journal of Science 21: 341–342.

Mayr G, Pohl B, Hartman S and Peters DS (2007) The tenth skeletal specimen of Archaeopteryx. Zoological Journal of the Linnean Society 149: 97–116.

Middleton KM and Gatesy SM (2000) Theropod forelimb design and evolution. Zoological Journal of the Linnean Society 128: 149–187.

Mivart SGJ (1871) On the Genesis of Species. New York: Appleton.

Nopsca F (1907) Ideas on the origin of flight. Proceedings of the Zoological Society of London 223–236.

Nopsca F (1923) On the origin of flight in birds. Proceedings of the Zoological Society of London 463–477.

Norberg UM (1985) Evolution of flight in birds: Aerodynamic, mechanical, and ecological aspects. In: Hecht MK, Ostrom JH, Viohl G and Wellnhofer P (eds) The Beginnings of Birds: Proceedings of the International Archaeopteryx Conference Eichstatt 1984, p. 293–302. Eichstätt, Germany: Jura Museum.

Norberg UM (1985) Evolution of vertebrate flight: an aerodynamic model for the transition from gliding to active flight. American Naturalist 126: 303–327.

Norell M, Ji Q, Gao K et al. (2002) Palaeontology: modern feathers on a non‐avian dinosaur. Nature 416: 36–37.

Norell MA and Makovicky PJ (1999) Important features of the dromaeosaurid skeleton II: information from newly collected specimens of Velociraptor mongoliensis. American Museum Novitates 3282: 1–45.

Norell MA and Makovicky PJ (1997) Important features of the dromaeosaurid skeleton: information from a new specimen. American Museum Novitates 3215: 1–28.

Norell MA and Xu X (2005) Feathered dinosaurs. Annual Review of Earth and Planetary Sciences 33: 277–299.

Novas FE and Pol D (2005) New evidence on deinonychosaurian dinosaurs from the Late Cretaceous of Patagonia. Nature 433: 858–861.

Nudds RL and Dyke GJ (2009) Forelimb posture in dinosaurs and the evolution of the avian flapping flight‐stroke. Evolution 63: 994–1002.

Ostrom JH (1974) Archaeopteryx and the origin of flight. Quarterly Review of Biology 49: 27–47.

Ostrom JH (1976) Some hypothetical anatomical stages in the evolution of avian flight. Smithsonian Contributions to Paleobiology 27: 1–21.

Ostrom JH (1979) Bird flight: how did it begin? American Scientist 67: 46–56.

Padian K (1982) Macroevolution and the origin of major adaptations: vertebrate flight as a paradigm for analysis of patterns. Proceedings of the Third North American Paleontological Convention, 1982, vol. 2, pp 387–392. Montreal, Quebec, Canada.

Padian K (1982) Running, leaping, lifting off. Sciences 22: 10–15.

Padian K (1985) The origins and aerodynamics of flight in extinct vertebrates. Paleontology 28: 413–433.

Padian K (2001) Stages in the origin of bird flight: Beyond the arboreal‐cursorial dichotomy. In: Gauthier J and Gall LF (eds) New Perspectives on the Origin and Early Evolution of Birds: Proceedings of the International Symposium in Honor of John H. Ostrom, p. 255–272. New Haven, CT: Peabody Museum of Natural History, Yale University.

Padian K (2004) Basal avialae. In: Weishampel DB, Dodson P and Osmolska H (eds) The Dinosauria, p. 210–231. Los Angeles: University of California Press.

Padian K and Chiappe LM (1998) The origin and early evolution of birds. Biological Reviews 73: 1–42.

Padian K, de Ricqles AJ and Horner JR (2001) Dinosaurian growth rates and bird origins. Nature 412: 405–408.

Paul GS (1988) Predatory Dinosaurs of the World: A Complete Illustrated Guide. New York: Simon and Schuster.

Paul GS (2002) Dinosaurs of the Air: The Evolution and Loss of Flight in Dinosaurs and Birds. Baltimore: Johns Hopkins University Press.

Pennycuick CJ (1968) Power requirements for horizontal flight in the pigeon Columba livia. Journal of Experimental Biology 49: 527–555.

Pennycuick CJ (1982) The flight of petrels and albatrosses (Procellariiformes), observed in South Georgia and its vicinity. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 300: 75–106.

Pennycuick CJ (1986) Mechanical constraints on the evolution of flight. Memoirs of the California Academy of Sciences 8: 83–98.

Peters DS (1985) Functional and constructive limitations in early evolution of birds. In: Hecht MK, Ostrom JH, Viohl G and Wellnhofer P (eds) The Beginnings of Birds: Proceedings of the International Archaeopteryx Conference Eichstatt 1984, p. 243–249. Eichstätt, Germany: Jura Museum.

Peters DS (2002) Anagenesis of early birds reconsidered. Palaeobiodiversity and Palaeoenvironments 82: 347–354.

Peters DS and Gutmann WF (1985) Constructural and functional preconditions for the transition to powered flight in vertebrates. In: Hecht MK, Ostrom JH, Viohl G and Wellnhofer P (eds) The Beginnings of Birds: Proceedings of the International Archaeopteryx Conference Eichstatt 1984, p. 239–242. Eichstätt, Germany: Jura Museum.

Poore SO, Sanchez-Haiman A and Goslow GE (1997) Wing upstroke and the evolution of flapping flight. Nature 387: 799–802.

Prum RO (1999) Development and evolutionary origin of feathers. Journal of Experimental Zoology 285: 291–306.

Prum RO and Brush AH (2002) The evolutionary origin and diversification of feathers. Quarterly Review of Biology 77: 261–295.

Pycraft WP (1906) The origin of birds. Knowledge and Science News 29: 531–532.

Qiang J, Currie PH, Norell MA and Shu-An J (1998) Two feathered dinosaurs from northeastern China. Nature 393: 753–761.

Rauhut OWM, Foth C, Tischlinger H and Norell MA (2012) Exceptionally preserved juvenile megalosauroid theropod dinosaur with filamentous integument from the Late Jurassic of Germany. Proceedings of the National Academy of Sciences of the USA 109: 11746–11751.

Rayfield EJ (2007) Finite element analysis and understanding the biomechanics and evolution of living and fossil organisms. Annual Review of Earth and Planetary Sciences 35: 541–576.

Rayner JMV (1985) Mechanical and ecological constraints of flight evolution. In: Hecht MK, Ostrom JH, Viohl G and Wellnhofer P (eds) The Beginnings of Birds: Proceedings of the International Archaeopteryx Conference Eichstatt 1984, p. 279–288. Eichstätt, Germany: Jura Museum.

Rayner JMV (1988) Form and function in avian flight. Current Ornithology 5: 1–66.

Rayner JMV (1991) Avian flight evolution and the problem of Archaeopteryx. In: Rayner JMV and Wootton RJ (eds) Biomechanics and Evolution, p. 183–212. Cambridge, UK: Cambridge University Press.

Remsen JV and Robinson SK (1990) A classification scheme for foraging behavior of birds in terrestrial habitats. Studies in Avian Biology 13: 144–160.

Richmond BG, Wright BW, Grosse I et al. (2005) Finite element analysis in functional morphology. Anatomical Record 283A: 259–274.

Russell AP (2001) Structural characteristics of the patagium of Ptychozoon kuhli (Reptilia: Gekkonidae) in relation to parachuting locomotion. Journal of Morphology 247: 252–263.

Sanz JL , Chiappe LM and Buscalioni AD (1995) The osteology of Concornis lacustris (Aves: Enantiornithes) from the lower Cretaceous of Spain and a reexamination of its phylogenetic relationships. American Museum Novitates 3133: 1–23.

Schweitzer MH, Watt JA, Avci R et al. (1999) Beta‐keratin specific immunological reactivity in feather‐like structures of the Cretaceous Alvarezsaurid, Shuvuuia deserti. Journal of Experimental Zoology 285: 146–157.

Sereno PC and Chenggang R (1992) Early evolution of avian flight and perching: new evidence from the Lower Cretaceous of China. Science 255: 845–848.

Sereno PC, Chenggang R, Jianjun L, Chiappe LM and Witmer LM (1997) The origin and evolution of dinosaurs. Annual Review of Earth and Planetary Sciences 25: 435–489.

Sereno PC, Chenggang R, Jianjun L, Chiappe M and Witmer LM (2002) Sinornis santensis (Aves: Enantiornithes) from the Early Creteceous of northeastern China. In: Chiappe LM and Witmer LM (eds) Mesozoic Birds: Above the Heads of Dinosaurs, p. 184–208. Los Angeles: University of California Press.

Sibley DA (2009) The Sibley Guide to Bird Life and Behavior. New York: Alfred A. Knopf, Inc..

Simons EL, Hieronymus TL and O'Connor PM (2011) Cross sectional geometry of the forelimb skeleton and flight mode in pelecaniform birds. Journal of Morphology 272: 958–971.

Smith KK (2006) Craniofacial development in marsupial mammals: developmental origins of evolutionary change. Developmental Dynamics 235: 1181–1193.

Tarsitano S (1985) The morphological and aerodynamic constraints on the origin of avian flight. In: Hecht MK, Ostrom JH, Viohl G and Wellnhofer P (eds) The Beginnings of Birds: Proceedings of the International Archaeopteryx Conference Eichstatt 1984, p. 319–332. Eichstätt, Germany: Jura Museum.

Tobalske BW, Altshuler DL and Powers DR (2004) Take‐off mechanics in hummingbirds (Trochilidae). Journal of Experimental Biology 207: 1345–1352.

Tobalske BW and Dial KP (2007) Aerodynamics of wing‐assisted incline running in birds. Journal of Experimental Biology 210: 1742–1751.

Turner AH, Makovicky PJ and Norell MA (2007b) Feather quill knobs in the dinosaur Velociraptor. Science 317: 1721.

Turner AH, Pol D, Clarke JA, Erickson GM and Norell MA (2007a) A basal dromaeosaurid and size evolution preceding avian flight. Science 317: 1378–1381.

Uetz P (2010) The original descriptions of reptiles. Zootaxa 2334: 59–68.

Videler JJ (2006) Avian Flight. Oxford, UK: Oxford University Press.

Wagner GP and Gauthier JA (1999) 1,2,3=2,3,4: A solution to the problem of the homology of the digits in the avian hand. Proceedings of the National Academy of Sciences of the USA 96: 5111–5116.

Webster F and Griffin D (1962) The role of the flight membranes in insect capture by bats. Animal Behaviour 10: 332–340.

Weems RE (1987) A Late Triassic footprint fauna from the Culpeper Basin Northern Virginia (USA). Transactions of the American Philosophical Society 77: 1–79.

Weishampel DB, Dodson P and Osmolska H (eds) (2004) The Dinosauria. Los Angeles: University of California Press.

Williston SW (1879) Are birds derived from dinosaurs? Kansas City Review of Science 3: 457–460.

Wilson DE and Reeder DM (eds) (2005) Mammal Species of the World: A Taxonomic and Geographic Reference, 3rd edn. Johns Hopkins University Press.

Witmer LM (1995) The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. In: Thomason JJ (ed.) Functional Morphology in Vertebrate Paleontology, p. 19–33. New York, NY: Cambridge University Press.

Witmer LM (2009) Palaeontology: feathered dinosaurs in a tangle. Nature 461: 601–602.

Xu X (2006) Feathered dinosaurs from China and the evolution of major avian characters. Integrative Zoology 1: 4–11.

Xu X and Norell MA (2007) Non‐avian dinosaur fossils from the Lower Cretaceous Jehol Group of western Liaoning, China. Geological Journal 41: 419–437.

Xu X, Norell MA, Kuang X et al. (2004) Basal tyrannosauroids from China and evidence for protofeathers in tyrannosauroids. Nature 431: 680–684.

Xu X, Tang Z and Wang X (1999b) A therizinosauroid dinosaur with integumentary structures from China. Nature 399: 350–354.

Xu X, Wang X and Wu X (1999a) A dromaeosaurid dinosaur with a filamentous integument from the Yixian Formation of China. Nature 401: 262–266.

Xu X and Wang X (2003) A new maniraptoran from the Early Cretaceous Yixian formation of western Liaoning. Vertebrata PalAsiatica 41: 195–202.

Xu X, Wang K, Zhang K et al. (2012) A gigantic feathered dinosaur from the Lower Cretaceous of China. Nature 484: 92–95.

Xu X, You H, Du K and Han F (2011) An Archaeopteryx‐like theropod from China and the origin of Avialae. Nature 475: 465–470.

Xu X and Zhang F (2005) A new maniraptoran dinosaur from China with long feathers on the metatarsus. Naturwissenschaften 92: 173–177.

Xu X, Zheng X and You H (2009) A new feather type in a nonavian theropod and the early evolution of feathers. Proceedings of the National Academy of Sciences of the USA 106: 832–834.

Xu X, Zheng X and You H (2010) Exceptional dinosaur fossils show ontogenetic development of early feathers. Nature 464: 1338–1341.

Xu X, Zhou Z and Prum RO (2001) Branched integumental structures in Sinornithosaurus and the origin of feathers. Nature 410: 200–204.

Xu X, Zhou Z and Wang X (2000) The smallest known non‐avian theropod dinosaur. Nature 408: 705–708.

Xu X, Zhou Z, Wang X et al. (2003) Four‐winged dinosaurs from China. Nature 421: 335–340.

Zelenitsky DK, Therrien F, Erickson GM et al. (2012) Feathered non‐avian dinosaurs from North America provide insight into wing origins. Science 338: 510–514.

Zhang F and Zhou Z (2000) A primitive enantiornithine bird and the origin of feathers. Science 290: 1955–1959.

Zhang F and Zhou Z (2004) Leg feathers in an Early Cretaceous bird. Nature 431: 925.

Zhang F, Zhou Z, Hou L and Gu G (2001) Early diversification of birds: evidence from a new opposite bird. Chinese Science Bulletin 46: 945–949.

Zhang F, Zhou Z, Xu X and Wang X (2002) A juvenile coelurosaurian theropod from China indicates arboreal habits. Naturwissenschaften 89: 394–398.

Zhang F, Zhou Z, Xu X, Wang X and Sullivan C (2008a) A bizarre Jurassic maniraptoran from China with elongate ribbon‐like feathers. Nature 455: 1105–1108.

Zhang F, Zhou Z and Benton M (2008b) A primitive confuciusornithid bird from China and its implications for early avian flight. Science in China 51: 625–639.

Zheng X, Zhou Z, Wang X et al. (2013) Hind wings in basal birds and the evolution of leg feathers. Science 339: 1309–1312.

Zhou Z, Clarke J and Zhang F (2008) Insight into diversity, body size and morphological evolution from the largest Early Cretaceous enantiornithine bird. Journal of Anatomy 212: 565–577.

Zhou Z and Hou L (1998) Confuciusornis and the early evolution of birds. Vertebrata PalAsiatica 36: 136–146.

Zhou Z and Zhang F (2002a) Largest bird from the Early Cretaceous and its implications for the earliest ecological diversification. Naturwissenschaften 89: 34–38.

Zhou Z and Zhang F (2002b) A long‐tailed, fig.d‐eating bird from the Early Cretaceous of China. Nature 418: 405–409.

Zhou Z and Zhang F (2003) Jeholornis compared to Archaeopteryx, with a new understanding of the earliest avian evolution. Naturwissenschaften 90: 220–225.

Zhou Z and Zhang F (2007) Mesozoic birds of China – a synoptic review. Frontiers of Biology in China 2: 1–14.

Zhou Z and Zhang F (2011) Anatomy of the primitive bird Sapeornis chaoyangensis from the Early Cretaceous of Liaoning, China. Canadian Journal of Earth Science 40: 731–747.

Zhou Z, Zhang F and Li Z (2010) A new Lower Cretaceous bird from China and tooth reduction in early avian evolution. Proceedings of the Royal Society B: Biological Sciences 277: 219–227.

Zhou ZH and Wang XL (2000) A new species of Caudipteryx from the Yixian Formation of Liaoning, northeast China. Vertebrat. Palasiatic 38: 113–130.

Zhou ZH, Wang XL, Zhang FC and Xu X (2000) Important features of Caudipteryx‐evidence from two nearly complete new specimens. Vertebrata PalAsiatica 38: 243–265.

Further Reading

Chiappe LM and Dyke GJ (2007) The beginnings of birds: recent discoveries, ongoing arguments, and new directions. In: Anderson J and Sues HD (eds) Major Evolutionary Transitions, p. 303–336. Bloomington: Indiana University Press.

Chiappe LM and Witmer LM (eds) (2002) Mesozoic Birds: Above the Heads of Dinosaurs, 576 pp. Berkeley: University of California Press.

Gatesy SM and Baier DB (2005) The origin of the avian flight stroke: a kinematic and kinetic perspective. Paleobiology 31: 382–399.

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Heers, Ashley M(Oct 2013) Evolution of Avian Flight. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0024965]