Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-26T06:01:50.246Z Has data issue: false hasContentIssue false
  • English
  • Français

From baby birds to feathered dinosaurs: incipient wings and the evolution of flight

Published online by Cambridge University Press:  08 April 2016

Ashley M. Heers ,
Kenneth P. Dial  and
Bret W. Tobalske
Ashley M. Heers
Affiliation:
Division of Biological Sciences, University of Montana, Missoula, Montana 59812, U.S.A. E-mail: ashmheers@gmail.com
Kenneth P. Dial
Affiliation:
Division of Biological Sciences, University of Montana, Missoula, Montana 59812, U.S.A. E-mail: ashmheers@gmail.com
Bret W. Tobalske
Affiliation:
Division of Biological Sciences, University of Montana, Missoula, Montana 59812, U.S.A. E-mail: ashmheers@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Reconstructing the tree of life requires deciphering major evolutionary transformations and the functional capacities of fossils with “transitional” morphologies. Some of the most iconic, well-studied fossils with transitional features are theropod dinosaurs, whose skeletons and feathered forelimbs record the origin and evolution of bird flight. However, in spite of over a century of discussion, the functions of forelimb feathers during the evolution of flight remain enigmatic. Both aerodynamic and non-aerodynamic roles have been proposed, but few of the form-function relationships assumed by these scenarios have been tested. Here, we use the developing wings of a typical extant ground bird (Chukar Partridge) as possible analogues/homologues of historical wing forms to provide the first empirical evaluation of aerodynamic potential in flapping theropod “protowings.” Immature ground birds with underdeveloped, rudimentary wings generate useful aerodynamic forces for a variety of locomotor tasks. Feather development in these birds resembles feather evolution in theropod dinosaurs, and reveals a predictable relationship between wing morphology and aerodynamic performance that can be used to infer performance in extinct theropods. By spinning an ontogenetic series of spread-wing preparations on a rotating propeller apparatus across a range of flow conditions and measuring aerodynamic force, we explored how changes in wing size, feather structure, and angular velocity might have affected aerodynamic performance in dinosaurs choosing to flap their incipient wings. At slow angular velocities, wings produced aerodynamic forces similar in magnitude to those produced by immature birds during behaviors like wing-assisted incline running. At fast angular velocities, wings produced forces sufficient to support body weight during flight. These findings provide a quantitative, biologically relevant bracket for theropod performance and suggest that protowings could have provided useful aerodynamic function early in maniraptoran history, with improvements in aerodynamic performance attending the evolution of larger wings, more effective feather morphologies, and faster angular velocities.

Type
Articles
Information
Paleobiology , Volume 40 , Issue 3 , Summer 2014 , pp. 459 - 476
Copyright
Copyright © The Paleontological Society 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Aigeldinger, T., and Fish, F. 1995. Hydroplaning by ducklings: overcoming limitations to swimming at the water surface. Journal of Experimental Biology 198:1567–1574.Google Scholar
Burgers, P., and Chiappe, L. M. 1999. The wing of Archaeopteryx as a primary thrust generator. Nature 399:60–62.Google Scholar
Carney, R. M., Vinther, J., Shawkey, M. D., D'Alba, L., and Ackermann, J. 2012. New evidence on the colour and nature of the isolated Archaeopteryx feather. Nature Communications 3, art. 637. doi: 10.1038/ncomms1642.CrossRefGoogle Scholar
Chen, P., Dong, Z., and Zhen, S. 1998. An exceptionally well-preserved theropod dinosaur from the Yixian Formation of China. Nature 391:147–152.Google Scholar
Christiansen, P., and Bonde, N. 2004. Body plumage in Archaeopteryx: a review, and new evidence from the Berlin specimen. Comptes Rendus Palevol 3:99–118.Google Scholar
Clarke, J. 2013. Feathers before flight. Science 340:690–692.CrossRefGoogle ScholarPubMed
Crandell, K. E., and Tobalske, B. W. 2011. Aerodynamics of tip-reversal upstroke in a revolving pigeon wing. Journal of Experimental Biology 214:1867–1873.Google Scholar
Dial, K. P. 2003. Wing-assisted incline running and the evolution of flight. Science 299:402–404.Google Scholar
Dial, K. P. 2011. From extant to extinct: empirical studies of transitional forms and allometric correlates delimit boundaries of functional capacity. Journal of Vertebrate Paleontology 31:99.Google Scholar
Dial, K. P., and Jackson, B. E. 2011. When hatchlings outperform adults: locomotor development in Australian brush turkeys (Alectura lathami, Galliformes). Proceedings of the Royal Society of London B 278:1610–1616.Google Scholar
Dial, K. P., Randall, R. J., and Dial, T. R. 2006. What use is half a wing in the ecology and evolution of birds? BioScience 56:437–445.Google Scholar
Dial, K. P., Jackson, B. E., and Segre, P. 2008. A fundamental avian wing-stroke provides a new perspective on the evolution of flight. Nature 451:985–989.Google Scholar
Dial, K. P., Heers, A. M., and Dial, T. R.In press. Ontogenetic and evolutionary transformations: the ecological significance of rudimentary structures. InDial, K. P., Shubin, N. H., and Brainerd, E. L., eds. Great transformations in vertebrate evolution. University of Chicago Press, Chicago.Google Scholar
Dial, T. R., and Carrier, D. R. 2012. Precocial hind limbs and altricial forelimbs: partitioning ontogenetic strategies in Mallard ducks (Anas platyrhynchos). Journal of Experimental Biology 215:3703–3710.Google Scholar
Dial, T. R., Heers, A. M., and Tobalske, B. W. 2012. Ontogeny of aerodynamics in mallards: comparative performance and developmental implications. Journal of Experimental Biology 215:3693–3702.Google Scholar
Dimond, C. C., Cabin, R. J., and Brooks, J. S. 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.Google Scholar
Dyke, G., de Kat, R., Palmer, C., van der Kindere, J., Naish, D., and Ganapathisubramani, B. 2013. Aerodynamic performance of the feathered dinosaur Microraptor and the evolution of feathered flight. Nature Communications 4, art. 2489. doi: 10.1038/ncomms3489.Google Scholar
Earls, K. D. 2000. Kinematics and mechanics of ground take-off in the starling Sturnus and the quail Coturnix coturnix. Journal of Experimental Biology 203:725–739.Google Scholar
Erickson, G. M., Makovicky, P. J., Currie, P. J., Norell, M. A., Yerby, S. A., and Brochu, C. A. 2004. Gigantism and comparative life-history parameters of tyrannosaurid dinosaurs. Nature 430:772–775.Google Scholar
Erickson, G. M., Rauhut, O. W. M., Zhou, Z., Turner, A. H., Inouye, B. D., Hu, D., and Norell, M. A. 2009. Was dinosaurian physiology inherited by birds? Reconciling slow growth in Archaeopteryx. PLoS ONE 4:1–9. doi: 10.1371/journal.pone.0007390.Google Scholar
Feduccia, A., and Tordoff, H. B. 1979. Feathers of Archaeopteryx: asymmetric vanes indicate aerodynamic function. Science 203:1021–1022.Google Scholar
Fowler, D. W., Freedman, E. A., Scannella, J. B., and Kambic, R. E. 2011. The predatory ecology of Deinonychus and the origin of flapping in birds. PLoS ONE 6:e28964. doi: 10.1371/journal.pone.0028964.Google Scholar
Garner, J. P., Taylor, G. K., and Thomas, A. L. R. 1999. On the origins of birds: the sequence of character acquisition in the evolution of avian flight. Proceedings of the Royal Society of London B 266:1259–1266.Google Scholar
Gilbert, S. F., and Epel, D. 2009. Ecological developmental biology: integrating epigenetics, medicine, and evolution. Sinauer, Sunderland, Mass.Google Scholar
Godefroit, P., Demuynck, H., Dyke, G., Hu, D., Escuillie, F., and Claeys, P. 2013. Reduced plumage and flight ability of a new Jurassic paravian theropod from China. Nature Communications 4, art. 1394. doi:10.1038/ncomms2389.Google Scholar
Gould, S. 1977. Ontogeny and phylogeny. Harvard University Press, Cambridge.Google Scholar
Haeckel, E. 1866. Generelle Morphologie der Organismen. Georg Reimer, Berlin.CrossRefGoogle Scholar
Hartman, F. A. 1961. Locomotor mechanisms of birds. Smithsonian Miscellaneous Collections 143:1–91.Google Scholar
Heers, A. M., and Dial, K. P. 2012. From extant to extinct: locomotor ontogeny and the evolution of avian flight. Trends in Ecology and Evolution 27:296–305.Google Scholar
Heers, A. M., and Dial, K. P. 2013. Wings versus legs: mechanistic underpinnings of variation in locomotor strategies among birds. Integrative and Comparative Biology 53:e88.Google Scholar
Heers, A. M., Tobalske, B. W., and Dial, K. P. 2011. Ontogeny of lift and drag production in ground birds. Journal of Experimental Biology 214:717–725.Google Scholar
Holtz, T. R. 2007. Dinosaurs: the most complete, up-to-date encyclopedia for dinosaur lovers of all ages. Random House Children's Books, New York.Google Scholar
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.Google Scholar
Jackson, B. E., Segre, P., and Dial, K. P. 2009. Precocial development of locomotor performance in a ground-dwelling bird (Alectoris chukar): negotiating a three-dimensional terrestrial environment. Proceedings of the Royal Society of London B 276:3457–3466.Google Scholar
Ji, Q., Currie, P. J., Norell, M. A., and Shu-An, J. 1998. Two feathered dinosaurs from northeastern China. Nature 393:753–761.Google Scholar
Livezey, B. C., and Humphrey, P. S. 1983. Mechanics of steaming in steamer-ducks. Auk 100:485–488.CrossRefGoogle Scholar
Livezey, B. C., and Humphrey, P. S. 1986. Flightlessness in steamer-ducks (Anatidae: Tachyeres): its morphological bases and probable evolution. Evolution 40:540–558.Google Scholar
Longrich, N. R., Vinther, J., Meng, Q., Li, Q., and Russell, A. P. 2012. Primitive wing feather arrangement in Archaeopteryx lithographica and Anchiornis huxleyi. Current Biology 22:2262–2267.Google Scholar
Makovicky, P. J., and Zanno, L. E. 2011. Theropod diversity and the refinement of avian characteristics. Pp. 9–29inDyke, G. and Kaiser, G., eds. Living dinosaurs: the evolutionary history of modern birds. Wiley, Hoboken, N.J.Google Scholar
Marks, J. S. 1982. Night stalkers along the Snake. Idaho Wildlife 3:18–21.Google Scholar
Marks, J. S. 1986. Nest-site characteristics and reproductive success of long-eared owls in southwestern Idaho. Wilson Bulletin 98:547–560.Google Scholar
Marks, J. S., Cannings, R. J., and Mikkola, H. n.d. Family Strigidae. 1999. Pp. 76–151inDel Hoyo, J., Elliott, A., and Sargatal, J., eds. Handbook of the birds of the world, Vol. 5. Barn owls to hummingbirds. Lynx Edicions, Barcelona.Google Scholar
Mayr, E. 1963. Animal species and evolution, 1st ed. Belknap Press of Harvard University Press, Cambridge.Google Scholar
Muller, W., and Patone, G. 1998. Air transmissivity of feathers. Journal of Experimental Biology 201:2591–2599.Google Scholar
Norberg, R. A. 1985. Function of vane asymmetry and shaft curvature in bird flight feathers; inferences on flight ability of Archaeopteryx. Pp. 303–318inOstrom, J. H., Hecht, M. K., Viohl, G., and Wellnhofer, P., eds. The beginnings of birds. Jura Museum, Eichstatt.Google Scholar
Norell, M. A., and Xu, X. 2005. Feathered dinosaurs. Annual Review of Earth and Planetary Sciences 33:277–299.Google Scholar
Norell, M., Ji, Q., Gao, K., Yuan, C., Zhao, Y., and Wang, L. 2002. Palaeontology: “modern” feathers on a non-avian dinosaur. Nature 416:36–37.CrossRefGoogle ScholarPubMed
Nudds, R. L., and Dyke, G. J. 2010. Narrow primary feather rachises in Confuciusornis and Archaeopteryx suggest poor flight ability. Science 328:887–889.CrossRefGoogle ScholarPubMed
Ostrom, J. H. 1976. Some hypothetical anatomical stages in the evolution of avian flight. Smithsonian Contributions to Paleobiology 27:1–21.Google Scholar
Padian, K., de Ricqles, A. J., and Horner, J. R. 2001. Dinosaurian growth rates and bird origins. Nature 412:405–408.Google Scholar
Prum, R. O. 1999. Development and evolutionary origin of feathers. Journal of Experimental Zoology 285:291–306.3.0.CO;2-9>CrossRefGoogle ScholarPubMed
Prum, R. O., and Brush, A. H. 2002. The evolutionary origin and diversification of feathers. Quarterly Review of Biology 77:261–295.Google Scholar
Seebacher, F. 2001. A new method to calculate allometric length-mass relationships of dinosaurs. Journal of Vertebrate Paleontology 21:51–60.Google Scholar
Shyy, W., Aono, H., Chimakurthi, S. K., Trizila, P., Kang, C.-K., Cesnik, C. E. S., and Liu, H. 2010. Recent progress in flapping wing aerodynamics and aeroelasticity. Progress in Aerospace Sciences 46:284–327.Google Scholar
Speakman, J. R., and Thomson, S. C. 1994. Flight capabilities of Archaeopteryx. Nature 370:514.Google Scholar
Speakman, J. R., and Thomson, S. C. 1995. Feather asymmetry in Archaeopteryx. Nature 374:221–222.CrossRefGoogle Scholar
Therrien, F., and Henderson, D. M. 2007. My theropod is bigger than yours … or not: estimating body size from skull length in theropods. Journal of Vertebrate Paleontology 27:108–115.CrossRefGoogle Scholar
Tobalske, B. W., and Dial, K. P. 2007. Aerodynamics of wing-assisted incline running in birds. Journal of Experimental Biology 210:1742–1751.Google Scholar
Turner, A. H., Pol, D., Clarke, J. A., Erickson, G. M., and Norell, M. A. 2007a. A basal dromaeosaurid and size evolution preceding avian flight. Science 317:1378–1381.CrossRefGoogle ScholarPubMed
Turner, A. H., Makovicky, P. J., and Norell, M. A. 2007b. Feather quill knobs in the dinosaur Velociraptor. Science 317:1721.Google Scholar
Usherwood, J. R. 2009. The aerodynamic forces and pressure distribution of a revolving pigeon wing. Experimental Fluids 46:991–1003.Google Scholar
Usherwood, J. R., and Ellington, C. P. 2002. The aerodynamics of revolving wings. II. Propeller force coefficients from mayfly to quail. Journal of Experimental Biology 205:1565–1576.Google Scholar
Vazquez, R. J. 1992. Functional osteology of the avian wrist and the evolution of flapping flight. Journal of Morphology 211:259–268.CrossRefGoogle ScholarPubMed
Wang, X., Nudds, R. L., and Dyke, G. J. 2011. The primary feather lengths of early birds with respect to avian wing shape evolution. Journal of Evolutionary Biology 24:1226–1231.Google Scholar
Witmer, L. M. 1995. The extant phylogenetic bracket and the importance of reconstructing soft tissues in fossils. Pp. 19–33inThomason, J. J., ed. functional morphology in vertebrate paleontology. Cambridge University Press, New York.Google Scholar
Xu, X. 2006. Feathered dinosaurs from China and the evolution of major avian characters. Integrative Zoology 1:4–11.Google Scholar
Xu, X., and Zhang, F. 2005. A new maniraptoran dinosaur from China with long feathers on the metatarsus. Naturwissenschaften 92:173–177.CrossRefGoogle ScholarPubMed
Xu, X., and Guo, Y. 2009. The origin and early evolution of feathers: insights from recent paleontological and neontological data. Vertebrata PalAsiatica 47:311–329.Google Scholar
Xu, X., Zhao, Q., Norell, M., Sullivan, C., Hone, D., Erickson, G., Wang, X. L., Han, F. L., and Guo, Y. 2009. A new feathered maniraptoran dinosaur fossil that fills a morphological gap in avian origin. Chinese Science Bulletin 54:430–435.Google Scholar
Xu, X., Zheng, X., and You, H. 2010. Exceptional dinosaur fossils show ontogenetic development of early feathers. Nature 464:1338–1341.Google Scholar
Xu, X., Tang, Z., and Wang, X. 1999. A therizinosauroid dinosaur with integumentary structures from China. Nature 399:350–354.CrossRefGoogle Scholar
Xu, X., Zhou, Z., Wang, X., Kuang, X., Zhang, F., and Du, X. 2003. Four-winged dinosaurs from China. Nature 421:335–340.Google Scholar
Zheng, X., You, H., Xu, X., and Dong, Z. 2009. An Early Cretaceous heterodontosaurid dinosaur with filamentous integumentary structures. Nature 458:333–336.Google Scholar
Zheng, X., Zhou, Z., Wang, X., Zhang, F., Zhang, X., Wang, Y., Wei, G., Wang, S., and Xu, X. 2013. Hind wings in basal birds and the evolution of leg feathers. Science 339:1309–1312.Google Scholar
Zhou, Z. H., and Wang, X. L. 2000. A new species of Caudipteryx from the Yixian Formation of Liaoning, northeast China. Vertebrata Palasiatica 38:113–130.Google Scholar