Feather Evolution in Pennaraptora

  • Ulysse Lefèvre
  • Andrea Cau
  • Dongyu Hu
  • Pascal GodefroitEmail author
Part of the Fascinating Life Sciences book series (FLS)


Two decades of paleontological discoveries of basal birds and non-avian theropods with preserved integumentary structures, especially in Late Jurassic to Early Cretaceous deposits from northeastern China, have greatly improved our understanding of the origin and early evolution of birds and their plumage. Here, we present a concise review of the plumage evolution within pennaraptora, the most inclusive clade containing Oviraptorosauria and Paraves. Feather or feather-like morphotypes were particularly diversified in non-avialan paravians, suggesting that they probably already fulfilled a wide array of biological roles, including thermoregulation and visual display. The feather-like structures in non-eumaniraptoran paravians were obviously not adapted for flight. However, Microraptor and maybe some of its relatives preserve large pennaceous feathers along the limbs and tail, similar in morphology and organization to those in modern birds, so that they could have functioned in active flight or passive gliding. Several aerodynamic innovations and flight-related morphological adaptations were (likely independently) experimented within the paravian clade close to the origin of birds. The origin and early evolution of complex feathers and flight abilities in paravian theropods were not linear processes, but more complex than previously thought.


  1. Agnolin FL, Novas FE (2013) Avian ancestors: a review of the phylogenetic relationships of the theropods Unenlagiidae, Microraptoria, Anchiornis and Scansoriopterygidae. Springer, DordrechtCrossRefGoogle Scholar
  2. Alexander DE, Gong E-P, Martin LD, Burnham DA, Falk AR (2010) Model tests of gliding with different hindwing configurations in the four-winged dromaeosaurid Microraptor gui. Proc Natl Acad Sci USA 107:2972–2976CrossRefGoogle Scholar
  3. Balmford A, Jones IL, Thomas ALR (1993) On avian asymmetry: evidence of natural selection for symmetrical tails and wings in birds. Proc R Soc B 252:245–251CrossRefGoogle Scholar
  4. Benett SC (2007) Articulation and function of the pteroid bone of pterosaur. J Vertebr Paleontol 27:881–891CrossRefGoogle Scholar
  5. Chatterjee S, Templin JR (2007) Biplane wing planform and flight performance of the feathered dinosaur {Microraptor} gui. Proc Natl Acad Sci USA 104:1576–1580CrossRefPubMedPubMedCentralGoogle Scholar
  6. Chen P-J, Dong Z-M, Zhen S-N (1998) An exceptionally well-preserved theropod dinosaur from the Yixian Formation of China. Nature 391:147–152CrossRefGoogle Scholar
  7. Chen P, Wang Q, Zhang H, Cao M, Li W, Wu S, Shen Y (2005) Jianshangou Bed of the Yixian Formation in West Liaoning, China. Sci China Ser D Earth Sci 48:298–312CrossRefGoogle Scholar
  8. Currie PJ, Chen P (2001) Anatomy of Sinosauropteryx prima from Liaoning, northeastern China. Can J Earth Sci 38:1705–1727CrossRefGoogle Scholar
  9. Feo TJ, Field DJ, Prum RO (2015) Barb geometry of asymmetrical feathers reveals a transitional morphology in the evolution of avian flight. Proc R Soc Lond B 282Google Scholar
  10. Fitzpatrick S (1998) Birds’ tails as signaling devices: markings, shape, length, and feather quality. Am Nat 151:157–173CrossRefPubMedPubMedCentralGoogle Scholar
  11. Foth C (2011) The morphology of neoptile feathers: ancestral state reconstruction and its phylogenetic implications. J Morphol 272:387–403CrossRefPubMedPubMedCentralGoogle Scholar
  12. Foth C, Rauhut WM (2017) Re-evaluation of the Haarlem Archaeopteryx and the radiation of maniraptoran theropod dinosaurs. BMC Evol Biol 17:236CrossRefPubMedPubMedCentralGoogle Scholar
  13. Foth C, Tischlinger H, Rauhut OWM (2014) New specimen of Archaeopteryx provides insights into the evolution of pennaceous feathers. Nature 511:79–82CrossRefPubMedPubMedCentralGoogle Scholar
  14. Gatesy SM, Dial KP (1996) From frond to fan: Archaeopteryx and the evolution of short-tailed birds. Evolution 50:2037–2048CrossRefPubMedPubMedCentralGoogle Scholar
  15. Godefroit P, Demuynck H, Dyke GJ, Hu D, Escuillié F, Claeys P (2013a) Reduced plumage and flight ability of a new Jurassic paravian theropod from China. Nat Commun 4:1394CrossRefGoogle Scholar
  16. Godefroit P, Cau A, Hu D, Escuillié F, Wenhao W, Dyke GJ (2013b) A Jurassic avialan dinosaur from China resolves the early phylogenetic history if birds. Nature 498:359–362CrossRefGoogle Scholar
  17. Godefroit P, Sinitsa SM, Dhouailly D, Bolotsky YL, Sizov AV, McNamara ME, Benton MJ, Spagna P (2014) A Jurassic ornithischian dinosaur from Siberia with both feathers and scales. Science 345:451–455CrossRefGoogle Scholar
  18. Han G, Chiappe LM, Ji S-A, Habib M, Turner AH, Chinsamy AT, Liu X, Han L (2014) A new raptorial dinosaur with exceptionally long feathering provides insights into dromaeosaurid flight performance. Nat Commun 5:4382CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hone DWE (2012) Variation in the tail length of non-avian dinosaurs. J Vertebr Paleontol 32:1082–1089CrossRefGoogle Scholar
  20. Hopson JA (2001) New perspectives on the origin and early evolution of birds. Peabody Museum of Natural History, New Haven, CTGoogle Scholar
  21. Hu D, Hou L, Zhang L, Xu X (2009) A pre-{Archaeopteryx} troodontid theropod from China with long feathers on the metatarsus. Nature 461:640–643CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hu D, Clarke JA, Eliason CM, Qiu R, Li Q, Shawkey MD, Zhao C, D’Alba L, Jiang J, Xu X (2018) A bony-crested Jurassic dinosaur with evidence of iridescent plumage highlights complexity in early paravian evolution. Nat Commun 9:217CrossRefPubMedPubMedCentralGoogle Scholar
  23. Ji Q, Ji SA (1996) On discovery of the earliest bird fossil in China and the origin of birds. Chin Geol 233:30–33Google Scholar
  24. Ji S, Ji Q (2007) {Jinfengopteryx} compared to {Archaeopteryx}, with comments on the mosaic evolution of long-tailed avialan birds. Acta Geol Sin 81:337–343CrossRefGoogle Scholar
  25. Ji Q, Currie PJ, Norell MA, Ji S-A (1998) Two feathered dinosaurs from the northeastern China. Nature 393:753–761CrossRefGoogle Scholar
  26. Ji Q, Norell MA, Gao K, Ji S (2001) The distribution of integumentary structures in a feathered dinosaur. Nature 410:1084–1088CrossRefGoogle Scholar
  27. Ji Q, Ji S, Lu J, You H, Chen W, Liu Y, Liu Y (2005) First avialan bird from China (Jinfengopteryx elegans gen. et sp. nov.). Geol Bull China 24:197–205Google Scholar
  28. Lee MSY, Cau A, Naish D, Dyke GJ (2014) Sustained miniaturization and anatomical innovation in the dinosaurian ancestors of birds. Science 345:562–566CrossRefPubMedPubMedCentralGoogle Scholar
  29. Lee S-I, Kim J, Park H, Jablonski PG, Choi H (2015) The function of the alula in avian flight. Sci Rep 5:9914CrossRefPubMedPubMedCentralGoogle Scholar
  30. Lefèvre U, Cau A, Cincotta A, Hu D, Chinsamy A, Escuillié F, Godefroit P (2017) A new Jurassic theropod from China documents a transitional step in the macrostructure of feathers. Sci Nat 104:1–13CrossRefGoogle Scholar
  31. Li Q, Gao K-Q, Meng Q, Clarke JA, Shawkey MD, D’Alba L, Pei R, Ellison M, Norell MA, Vinther J (2012) Reconstruction of Microraptor and the evolution of iridescent plumage. Science 335:1215–1219CrossRefGoogle Scholar
  32. Lindgren J, Sjövall P, Carney RM, Cincotta A, Uvdal P, Hutcheson SW, Gustafsson O, Lefèvre U, Escuillié F, Heimdal J, Engdahl A, Gren JA, Kear BP, Wakamatsu K, Yans J, Godefroit P (2015) Molecular composition and ultrastructure of Jurassic paravian feathers. Sci Rep 5(1):13520CrossRefPubMedPubMedCentralGoogle Scholar
  33. Lingham-Soliar T (2012) The evolution of the feather: Sinosauropteryx, life, death and preservation of an alleged feathered dinosaur. J Ornithol 153:699–711CrossRefGoogle Scholar
  34. Longrich N (2006) Structure and function of hindlimb feathers in Archaeopteryx lithographica. Paleobiology 32:417–431CrossRefGoogle Scholar
  35. Longrich NR, Vinther J, Meng Q, Li Q, Russell AP (2012) Primitive wing feather arrangement in Archaeopteryx lithographica and Anchiornis huxleyi. Curr Biol 22:2262–2267CrossRefPubMedPubMedCentralGoogle Scholar
  36. Lü J, Brusatte S (2015) A large, short-armed, winged dromaeosaurid (Dinosauria: Theropoda) from the Early Cretaceous of China and its implication for feather evolution. Sci Rep 5:11775CrossRefPubMedPubMedCentralGoogle Scholar
  37. Lucas AM, Stettenheim PR (1972) Avian anatomy: integument, parts I. U.S. Agricultural Research Service, Washington, DCGoogle Scholar
  38. O’Connor JK, Chang H (2015) Hindlimb feathers in paravians: primarily “wings” or ornaments? Biol Bull 42:616–621CrossRefGoogle Scholar
  39. Osmólska H, Currie PJ, Barsbold R (2004) Oviraptorosauria. In: Weishampel DB, Dodson P, Osmólska H (eds) The Dinosauria. University of California Press, Berkeley, CAGoogle Scholar
  40. Pei R, Li Q, Meng Q, Norell MA, Gao K-Q (2017) New specimens of Anchiornis huxleyi (Theropoda: Paraves) from the Late Jurassic of northeastern of China. Bull Am Mus Nat Hist 411:1–66CrossRefGoogle Scholar
  41. Pérez-Moreno BP, Sanz JL, Buscalioni AD, Moratalla JJ, Ortega F, Rasskin-Gutman D (1994) A unique multitoothed ornithomimosaur dinosaur from the Lower Cretaceous of Spain. Nature 370:363–367CrossRefGoogle Scholar
  42. Persons SW, Currie PJ, Norell MA (2014) Oviraptorosaur tail forms and functions. Acta Palaeontol Pol 59:553–567Google Scholar
  43. Saitta ET, Gelernter R, Vinther J (2017) Additional information on the primitive contour and wing feathering of paravian dinosaurs. Palaeontology 61:273–288CrossRefGoogle Scholar
  44. Sanz JL, Chiappe LM, Perez-Moreno BP, Buscalioni AD, Moratalla JJ, Ortega F, Poyato-Ariza FJ (1996) An Early Cretaceous bird from Spain and its implications for the evolution of avian flight. Nature 382:442–445CrossRefGoogle Scholar
  45. Senter P (2006) Scapular orientation in theropods and basal birds, and the origin of flapping flight. Acta Palaeontol Pol 51:305–313Google Scholar
  46. Thomas ALR (1993) On the aerodynamics of birds’ tail. Philos Trans R Soc B 340:361–380CrossRefGoogle Scholar
  47. Turner AH, Makovicky PJ, Norell MA (2007) Feather quill knobs in the dinosaur Velociraptor. Science 317:1721CrossRefPubMedPubMedCentralGoogle Scholar
  48. Turner AH, Makovicky PJ, Norell MA (2012) A review of dromaeosaurid systematics and paravian phylogeny. Bull Am Mus Nat Hist 371:1–206CrossRefGoogle Scholar
  49. Wang M, O’Connor JK, Xu X, Zhou Z (2019) A new Jurassic scansoriopterygid and the loss of membranous wings in theropod dinosaurs. Nature 569:256–259CrossRefGoogle Scholar
  50. Weidensaul S (ed) (1995) Raptors: the birds of prey. Michigan University Press, New York, NYGoogle Scholar
  51. Witmer LM (2009) Fuzzy origins for feathers. Nature 458:293–295CrossRefGoogle Scholar
  52. Xing L, McKellar RC, Wang M, Bai M, O’onnor JK, Benton MJ, Zhang J, Wang Y, Tseng K, Lockley MG, Li G, Zhang W, Xu X (2016) Mummified precocial bird wings in mid-Cretaceous Burmese amber. Nat Commun 7:12089CrossRefPubMedPubMedCentralGoogle Scholar
  53. Xu X (2006) Scales, feathers and dinosaurs. Nature 440:287–288CrossRefPubMedPubMedCentralGoogle Scholar
  54. Xu X, Guo Y (2009) The origin and early evolution of feathers: insights from recent paleontological and neontological data. Vertebrata PalAsiatica 47:311–329Google Scholar
  55. Xu X, Zhang F (2005) A new maniraptoran dinosaur from China with long feathers on the metatarsus. Naturwissenschaften 92(4):173–177CrossRefPubMedPubMedCentralGoogle Scholar
  56. Xu X, Tang Z, Wang X (1999a) A therizinosaurid dinosaur with integumentary structures from China. Nature 399Google Scholar
  57. Xu X, Wang X, Wu X-C (1999b) A dromaeosaurid dinosaur with a filamentous integument from the Yixian Formation of China. Nature 401:262–266CrossRefGoogle Scholar
  58. Xu X, Zhou Z, Wang X (2000) The smallest known non-avian theropod dinosaur. Nature 408:705–708CrossRefGoogle Scholar
  59. Xu X, Zhou Z-H, Prum RO (2001) Branched integumental structures in Sinornithosaurus and the origin of feathers. Nature 410:200–204CrossRefGoogle Scholar
  60. Xu X, Zhou Z, Wang X, Kuang X, Zhang F, Du X (2003) Four winged dinosaurs from China. Nature 421:335–340CrossRefGoogle Scholar
  61. Xu X, Norell MA, Kuang X, Wang X, Zhao Q, Jia C (2004) Basal tyrannosauroids from China and evidence for protofeathers in tyrannosauroids. Nature 431:680–684CrossRefGoogle Scholar
  62. Xu X, Zheng X, You H (2010) Exceptional dinosaur fossils show ontogenetic development of early feathers. Nature 464:1338–1341CrossRefPubMedPubMedCentralGoogle Scholar
  63. Xu X, You H, Du K, Han F (2011) An Archaeopteryx-like theropod from China and the origin of Avialae. Nature 475:465–470CrossRefPubMedPubMedCentralGoogle Scholar
  64. Xu X, Wang K, Zhang K, Ma Q, Xing L, Sullivan C, Hu D, Cheng S, Wang S (2012) A gigantic feathered dinosaur from the Lower Cretaceous of China. Nature 484:92–95CrossRefGoogle Scholar
  65. Xu X, Zheng X, Sullivan C, Wang X, Xing L, Wang Y, Zhang X, O’Connor JK, Zhang F, Pan Y (2015) A bizarre Jurassic maniraptoran theropod with preserved evidence of membranous wings. Nature 521:70–73CrossRefPubMedPubMedCentralGoogle Scholar
  66. Xu X, Currie P, Pittman M, Xing L, Meng Q, Lü J, Hu D, Yu C (2017) Mosaic evolution in an asymmetrically feathered troodontid dinosaur with transitional features. Nat Commun 8:14972CrossRefPubMedPubMedCentralGoogle Scholar
  67. Zelenitsky DK, Therrien F, Erickson GM, DeBuhr CL, Kobayashi Y, Eberth DA, Hadfield F (2012) Feathered non-avian dinosaurs from North America provide insight into wing origins. Science 338:510–514CrossRefPubMedPubMedCentralGoogle Scholar
  68. Zhang F, Zhou Z (2000) A primitive enantiornithine bird and the origin of feathers. Science 290:1955–1959CrossRefPubMedPubMedCentralGoogle Scholar
  69. Zhang F, Zhou Z, Xu X, Wang X (2002) A juvenile coelurosaurian theropod from China indicates arboreal habits. Naturwissenschaften 89:394–398CrossRefPubMedPubMedCentralGoogle Scholar
  70. Zhang F, Zhou Z, Xu X, Wang X, Sullivan C (2008a) A bizarre Jurassic maniraptoran from China with elongated ribbon-like feathers. Nature 455:1105–1108CrossRefPubMedPubMedCentralGoogle Scholar
  71. Zhang F, Zhou Z, Benton MJ (2008b) A primitive confuciusornithid bird from China and its implications for early avian flight. Sci China Ser Earth Sci 51:625–639CrossRefGoogle Scholar
  72. Zheng X, Zhou Z, Wang X, Zhang F, Wang Y, Wei G, Wang S, Xu X (2013) Hind wings in basal birds and the evolution of leg feathers. Science 339:1309–1312CrossRefGoogle Scholar
  73. Zhou Z, Zhang F-C (2006) Origin and early evolution of feathers: evidence from the early cretaceous of China. Acta Zool Sin 52:125–128Google Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Ulysse Lefèvre
    • 1
    • 2
  • Andrea Cau
    • 3
    • 4
  • Dongyu Hu
    • 5
    • 6
  • Pascal Godefroit
    • 2
    Email author
  1. 1.Department of GeologyUniversity of LiègeLiègeBelgium
  2. 2.Earth and Life History O.D.Royal Belgian Institute of Natural SciencesBruxellesBelgium
  3. 3.Earth, Life and Environmental Sciences DepartmentAlma Mater Studiorum, Bologna UniversityBolognaItaly
  4. 4.Geological and Palaeontological Museum “G. Capellini”BolognaItaly
  5. 5.Paleontological Institute, Shenyang Normal UniversityShenyangChina
  6. 6.Key Laboratory for Evolution of Past Life in Northeast AsiaMinistry of Land and Resources (Shenyang Normal University)ShenyangChina

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