On the Ancestry of Feathers in Mesozoic Dinosaurs

Campione, Nicolás E.; Barrett, Paul M.; Evans, David C.

doi:10.1007/978-3-030-27223-4_12

Nicolás E. Campione^3,4,5,
Paul M. Barrett⁶ &
David C. Evans⁷

Part of the book series: Fascinating Life Sciences ((FLS))

1517 Accesses
8 Citations
13 Altmetric

Abstract

Over the last two decades, the dinosaur fossil record has revealed much about the nature of their epidermal structures. These data challenged long-standing hypotheses of widespread reptile-like scalation in dinosaurs and provided additional evidence that supported the deeply nested position of birds within the clade. Moreover, in recent years, the discovery of filamentous structures in numerous species across the dinosaurian evolutionary tree suggests a model of deep feather homology within dinosaurs, with the appearance of feathers hypothesised to coincide with the dinosaur origin. Thanks to phylogenetic comparative methods, these homologies can now be tested empirically and form the basis of this study. Based on a dataset of 77 dinosaur species that preserve integumentary structures, we undertake a series of model-fitting and ancestral state reconstruction analyses to interpret the evolutionary history and ancestral integumentary condition in dinosaurs. Our results provide the first empirical support for the evolution of feathers in an ordered fashion, but reveal that these evolutionary trends were not always towards ‘more complex’ conditions. Ancestral state reconstructions demonstrate that irrespective of the preferred phylogenetic framework, the ancestral pterosaur condition or whether any one major dinosaur lineage had a Late Triassic-feathered representative, support values for a filamentous/feathered dinosaur ancestor are low. More examples of feathered taxa from across the dinosaur tree, and in particular the discovery of as yet unknown feathered Triassic taxa, will be needed in order to overturn current support for a scaly dinosaurian ancestor.

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References

Anderson BG, Lucas SG, Barrick RE, Heckert AB, Basabilvaso GT (1998) Dinosaur skin impressions and associated skeletal remains from the upper Campanian of southwestern New Mexico: new data on the integument morphology of hadrosaurs. J Vertebr Paleontol 18(4):739–745. https://doi.org/10.1080/02724634.1998.10011102
Article Google Scholar
Andrews CW (1913) A descriptive catalogue of the marine reptiles of the Oxford Clay: based on the Leeds Collection in the British Museum (Natural History), London. Part 2. British Museum (Natural History), London
Google Scholar
Arbour VM, Burns ME, Bell PR, Currie PJ (2014) Epidermal and dermal integumentary structures of ankylosaurian dinosaurs. J Morphol 275:39–50. https://doi.org/10.1002/jmor.20194
Article PubMed Google Scholar
Avanzini M (2000) Synaptichnium tracks with skin impressions from the Anisian (middle Triassic) of the Southern Alps (Val di Non – Italy). Ichnos 7:243–251. https://doi.org/10.1080/10420940009380164
Article Google Scholar
Bakker RT, Galton PM (1974) Dinosaur monophyly and a new class of vertebrates. Nature 248:168–172. https://doi.org/10.1038/248168a0
Article Google Scholar
Baron MG, Norman DB, Barrett PM (2017) A new hypothesis of dinosaur relationships and early dinosaur evolution. Nature 543:501–506. https://doi.org/10.1038/nature21700
Article CAS PubMed Google Scholar
Barrett PM, Butler RJ, Edwards NP, Milner AR (2008) Pterosaur distribution in time and space: an atlas. Zitteliana B 28:61–107
Google Scholar
Barrett PM, Evans DC, Campione NE (2015) Evolution of dinosaur epidermal structures. Biol Lett 11:20150229. https://doi.org/10.1098/rsbl.2015.0229
Article CAS PubMed PubMed Central Google Scholar
Bell PR (2012) Standardized terminology and potential taxonomic utility for hadrosaurid skin impressions: a case study for Saurolophus from Canada and Mongolia. PLoS One 7:e31295. https://doi.org/10.1371/journal.pone.0031295
Article CAS PubMed PubMed Central Google Scholar
Bell PR (2014) A review of hadrosaurid skin impressions. In: Eberth DA, Evans DC (eds) Hadrosaurs. Indiana University Press, Bloomington, pp 572–590
Google Scholar
Bell PR, Fanti F, Currie PJ, Arbour VM (2014) A mummified duck-billed dinosaur with a soft-tissue cock’s comb. Curr Biol 24:70–75. https://doi.org/10.1016/j.cub.2013.11.008
Article CAS PubMed Google Scholar
Bell PR, Campione NE, Persons WS IV, Currie PJ, Larson PL, Tanke DH, Bakker RT (2017) Tyrannosauroid integument reveals conflicting patterns of gigantism and feather evolution. Biol Lett 13:20170092. https://doi.org/10.1098/rsbl.2017.0092
Article PubMed PubMed Central Google Scholar
Bennett SC (2015) New interpretation of the wings of the pterosaur Rhamphorhynchus muensteri based on the Zittel and Marsh specimens. J Paleontol 89:845–869. https://doi.org/10.1017/jpa.2015.68
Article Google Scholar
Bernardi M, Petti FM, Avanzini M (2010) A webbed archosaur footprint from the Upper Jurassic (Carnian) of the Italian Southern Alps. In: Milàn J, Lucas SG, Lockley MG, Spielmann JA (eds) Crocodile Tracks and Traces, vol 21. New Mexico Museum of Natural History and Science, Bulletin, pp 65–68
Google Scholar
Bonaparte JF, Novas FE, Coria RA (1990) Carnotaurus sastrei Bonaparte, the horned, lightly built carnosaur from the middle Cretaceous of Patagonia. Los Angeles County Nat His Mus Contrib Sci 416:1–42
Google Scholar
Brown B (1917) A complete skeleton of the horned dinosaur Monoclonius, and description of a second skeleton showing skin impressions. Bull Am Mus Nat Hist 37:281–306
Google Scholar
Brusatte SL (2012) Dinosaur paleobiology. Wiley, Chichester
Book Google Scholar
Brush AH (2000) Evolving a protofeather and feather diversity. Am Zool 40:631–639. https://doi.org/10.1093/icb/40.4.631
Article Google Scholar
Buchwitz M, Voigt S (2012) The dorsal appendages of the Triassic reptile Longisquama insignis: reconsideration of a controversial integument type. Paläontol Z 86:313–331. https://doi.org/10.1007/s12542-012-0135-3
Article Google Scholar
Butler RJ, Upchurch P, Norman DB (2008) The phylogeny of the ornithischian dinosaurs. J Syst Palaeontol 6:1–40. https://doi.org/10.1017/S1477201907002271
Article Google Scholar
Chang C, Wu P, Baker RE, Maini PK, Alibardi L, Chuong C-M (2009) Reptile scale paradigm: Evo-Devo, pattern formation and regeneration. Int J Dev Biol 53:813–826. https://doi.org/10.1387/ijdb.072556cc
Article PubMed PubMed Central Google Scholar
Charig AJ (1979) A new look at the dinosaurs. British Museum (Natural History), London
Google Scholar
Chen PJ, Dong ZM, Zhen SN (1998) An exceptionally well-preserved theropod dinosaur from the Yixian Formation of China. Nature 391:147–152. https://doi.org/10.1038/34356
Article CAS Google Scholar
Chen CF, Foley J, Tang PC, Li A, Jiang TX, Wu P, Widelitz RB, Chuong CM (2015) Development, regeneration, and evolution of feathers. Annu Rev Anim Biosci 3:169–195. https://doi.org/10.1146/annurev-animal-022513-114127
Article PubMed Google Scholar
Cheng X, Wang X, Jiang S, Kellner AWA (2015) Short note on a non-pterodactyloid pterosaur from Upper Jurassic deposits of Inner Mongolia, China. Hist Biol 27:749–754. https://doi.org/10.1080/08912963.2014.974038
Article Google Scholar
Chiappe LM, Göhlich UB (2010) Anatomy of Juravenator starki (Theropoda: Coelurosauria) from the Late Jurassic of Germany. Neues Jahrb Geol Palaontol Abh 258:257–296. https://doi.org/10.1127/0077-7749/2010/0125
Article Google Scholar
Christiansen NA, Tschopp E (2010) Exceptional stegosaur integument impressions from the Upper Jurassic Morrison Formation of Wyoming. Swiss J Geosci 103:163–171. https://doi.org/10.1007/s00015-010-0026-0
Article Google Scholar
Coria RA, Chiappe LM (2007) Embryonic skin from the Late Cretaceous sauropods (Dinosauria) of Auca Mahuevo, Patagonia, Argentina. J Paleontol 81:1528–1532. https://doi.org/10.1666/05-150.1
Article Google Scholar
Cruickshank ARI (1972) The proterosuchian thecodonts. In: Joysey KA, Kemp TS (eds) Studies in vertebrate evolution. Oliver & Boyd, Edinburgh, pp 89–119
Google Scholar
Cunningham CW, Omland KE, Oakley TH (1998) Reconstructing ancestral character states: a critical reappraisal. Trends Ecol Evol 13:361–366. https://doi.org/10.1016/S0169-5347(98)01382-2
Article CAS PubMed Google Scholar
Czerkas SA (1992) Discovery of dermal spines reveals a new look for sauropod dinosaurs. Geology 20:1068–1070
Article Google Scholar
Czerkas SA (1994) The history and interpretation of sauropod skin impressions. Gaia 10:173–182
Google Scholar
Czerkas SA, Czerkas SJ (1997) The integument and life restoration of Carnotaurus. In: Wolberg DL, Stump E, Rosenberg G (eds) Dinofest International: Proceedings of a Symposium held at Arizona State University. Academy of Natural Sciences, Philadelphia, pp 155–158
Google Scholar
Czerkas SA, Ji Q (2002) A new rhamphorhynchoid with a headcrest and complex integumentary structures. In: Czerkas SA (ed) Feathered dinosaurs and the origin of flight. The Dinosaur Museum, Blanding, pp 15–41
Google Scholar
Dalla Vecchia FM (2009) Anatomy and systematics of the pterosaur Carniadactylus gen. n. Rosenfeldi (Dalla Vecchia, 1995). Riv Ital Paleontol Stratigr 115:159–188. https://doi.org/10.13130/2039-4942/6377
Article Google Scholar
Davis M (2014) Census of dinosaur skin reveals lithology may not be the most important factor in increased preservation of hadrosaurid skin. Acta Palaeontol Pol 59:601–605. https://doi.org/10.4202/app.2012.0077
Article Google Scholar
DePalma RA, Burnham DA, Martin LD, Larson PL, Bakker RT (2015) The first giant raptor (Theropoda: Dromaeosauridae) from the Hell Creek Formation. Paleontological Contributions 14. https://doi.org/10.17161/paleo.1808.18764
Dhouailly D (2009) A new scenario for the evolutionary origin of hair, feather, and avian scales. J Anat 214:587–606. https://doi.org/10.1111/j.1469-7580.2008.01041.x
Article PubMed PubMed Central Google Scholar
Di-Poï N, Milinkovitch MC (2016) The anatomical placode in reptile scale morphogenesis indicates shared ancestry among skin appendages in amniotes. Sci Adv 2:e1600708. https://doi.org/10.1126/sciadv.1600708
Article CAS PubMed PubMed Central Google Scholar
Dodson P, Forster CA, Sampson SD (2004) Ceratopsidae. In: Weishampel DB, Dodson P, Osmólska H (eds) The Dinosauria, 2nd edn. University of California Press, Berkeley, pp 494–513
Chapter Google Scholar
Ellenberger P (1974) Contribution à la classification des pistes de vertébrés du Trias. Les types du Stormberg d’Afrique du Sud. II. Le Stormberg Superieur. Palaeovertebrata, Memoire Extraordinaire, Montpellier
Google Scholar
Evans DC, Reisz RR (2007) Anatomy and relationships of Lambeosaurus magnicristatus, a crested hadrosaurid dinosaur (Ornithischia) from the Dinosaur Park Formation, Alberta. J Vertebr Paleontol 27(2):373–393. https://doi.org/10.1671/0272-4634(2007)27[373
Article Google Scholar
Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15. https://doi.org/10.1086/284325
Article Google Scholar
Foster J, Hamblin A, Lockley M (2003) Apatopus trackway and other footprints from the Chinle Group of southern Utah: an update. Ichnos 10:165–167. https://doi.org/10.1080/10420940390258003
Article Google Scholar
Foth C (2012a) On the identification of feather structures in stem-line representatives of birds: evidence from fossils and actuopalaeontology. Paläontol Z 86:91–102. https://doi.org/10.1007/s12542-011-0111-3
Article Google Scholar
Foth C (2012b) The influence of taphonomy on fossil body plumages and the identification of feather structures in stem-lineage representatives of birds. In: Royo-Torres R, Gascó F, Alcalá L (eds) 10th Annual Meeting of the European Association of Vertebrate Paleontologists. ¡Fundamental! 20:77–79
Google Scholar
Foth C, Tischlinger H, Rauhut OWM (2014) New specimen of Archaeopteryx provides insights into the evolution of pennaceous feathers. Nature 511:79–82. https://doi.org/10.1038/nature13467
Article CAS PubMed Google Scholar
Foth C, Haug C, Haug JT, Tischlinger H, Rauhut OWM (2020) Two of a feather: a comparison of the preserved integument in the juvenile theropod dinosaurs Sciurumimus and Juravenator from the Kimmeridgian torleite formation of southern Germany. In: Foth C, Rauhut OWM (eds) The evolution of feathers – a palaeontological perspective. Springer, Heidelberg
Google Scholar
Frey E, Martill DM (1998) Soft tissue preservation in a specimen of Pterodactylus kochi (Wagner) from the Upper Jurassic of Germany. Neues Jahrb Geol Palaontol Abh 210:421–441
Article Google Scholar
Frey E, Tischlinger H, Buchy MC, Martill DM (2003) New specimens of Pterosauria (Reptilia) with soft parts with implications for pterosaurian anatomy and locomotion. In: Bufferaut E, Mazin J-M (eds) Evolution and palaeobiology of pterosaurs. Geological Society of London, Special Publications 217:233–266. https://doi.org/10.1144/GSL.SP.2003.217.01.14
Funston GF, Currie PJ (2016) A new caenagnathid (Dinosauria: Oviraptorosauria) from the Horseshoe Canyon Formation of Alberta, Canada, and a reevaluation of the relationships of Caenagnathidae. J Vertebr Paleontol 36:e1160910. https://doi.org/10.1080/02724634.2016.1160910
Article Google Scholar
Gauthier J (1986) Saurischian monophyly and the origin of birds. In: Padian K (ed) The origin of birds and the evolution of flight. Memoirs of the California Academy of Science 8:1–55
Google Scholar
Godefroit P, Cau A, Hu DY, Escuillie F, Wu WH, Dyke G (2013) A Jurassic avialan dinosaur from China resolves the early phylogenetic history of birds. Nature 498:359–362. https://doi.org/10.1038/nature12168
Article CAS PubMed Google Scholar
Godefroit P, Sinitsa SM, Dhouailly D, Bolotsky YL, Sizov AV, McNamara ME, Benton MJ, Spagna P (2014a) A Jurassic ornithischian dinosaur from Siberia with both feathers and scales. Science 345:451–455. https://doi.org/10.1126/science.1253351
Article CAS PubMed Google Scholar
Godefroit P, Sinitsa SM, Dhouailly D, Bolotsky YL, Sizov AV, McNamara ME, Benton MJ, Spagna P (2014b) Response to Comment on “A Jurassic ornithischian dinosaur from Siberia with both feathers and scales”. Science 346:434c. https://doi.org/10.1126/science.1260146
Article CAS Google Scholar
Horner JR (1984) A “segmented” epidermal tail frill in a species of hadrosaurian dinosaur. J Paleontol 58:270–271
Google Scholar
Hu DY, Hou LH, Zhang LJ, Xu X (2009) A pre-Archaeopteryx troodontid theropod from China with long feathers on the metatarsus. Nature 461:640–643. https://doi.org/10.1038/nature08322
Article CAS PubMed Google Scholar
Hu DY, Clark JA, Eliason CM, Qiu R, Li QG, Shawkey MD, Zhao C, D’Alba L, Jiang JK, Xu X (2018) A bony-crested Jurassic dinosaur with evidence of iridescent plumage highlights complexity in early paravian evolution. Nat Commun 9:217. https://doi.org/10.1038/s41467-017-02515-y
Article CAS PubMed PubMed Central Google Scholar
Ji Q, Yuan CX (2002) Discovery of two kinds of protofeathered pterosaurs in the Mesozoic Daohugou Biota in the Ningcheng region and its stratigraphic and biologic significances. Geological Review 48:221–224
Google Scholar
Ji Q, Currie PJ, Norell MA, Ji SA (1998) Two feathered dinosaurs from northeastern China. Nature 393:753–761. https://doi.org/10.1038/31635
Article CAS Google Scholar
Ji Q, Ji SA, Lü JC, You HL (2005) First avialian bird from China (Jinfengopteryx elegans gen. et sp. nov.). Geol Bull China 24(3):197–210
Google Scholar
Jiang SX, Wang XL (2011) Important features of Gegepterus change (Pterosauria: Archaeopterodactyloidea, Ctenochasmatidae) from a new specimen. Vertebrata PalAsiatica 49(2):172–184
Google Scholar
Kellner AWA (1996) Reinterpretation of a remarkably well preserved pterosaur soft tissue from the Early Cretaceous of Brazil. J Vertebr Paleontol 16:718–722. https://doi.org/10.1080/02724634.1996.10011360
Article Google Scholar
Kellner AWA, Wang XL, Tischlinger H, de Almeida Campos D, Hone DWE, Meng X (2010) The soft tissue of Jeholopterus (Pterosauria, Anurognathidae, Batrachognathinae) and the structure of the pterosaur wing membrane. Proc R Soc B 277:321–329. https://doi.org/10.1098/rspb.2009.0846
Article PubMed Google Scholar
King MJ, Sarjeant WAS, Thompson DB, Tresise G (2005) A revised systematic ichnotaxonomy and review of the vertebrate ichnofamily Chirotheriidae from the British Triassic. Ichnos 12(4):241–299. https://doi.org/10.1080/10420940591009312
Article Google Scholar
Klein H, Voigt S, Saber H, Schneider JW, Hminna A, Fischer J, Lagnaoui A, Brosig A (2011) First occurrence of a Middle Triassic tetrapod ichnofauna from the Argana Basin (western High Atlas, Morocco). Palaeogeogr Palaeoclimatol Palaeoecol 307(1–4):218–231. https://doi.org/10.1016/j.palaeo.2011.05.021
Article Google Scholar
Kundrát M (2004) When did theropods become feathered? Evidence for pre-Archaeopteryx feathery appendages. J Exp Zool B Mol Dev Evol 302:355–364. https://doi.org/10.1002/jez.b.20014
Article PubMed Google Scholar
Lefèvre U, Cau A, Cincotta A, Hu DY, Chinsamy A, Escuillié F, Goderfroit P (2017) A new Jurassic theropod from China documents a transitional step in the macrostructure of feathers. Sci Nat 104:74. https://doi.org/10.1007/s00114-017-1496-y
Article CAS Google Scholar
Lefèvre U, Cau A, Hu D, Godefroit P (2020) Feather evolution in non-avialan paravians. In: Foth C, Rauhut OWM (eds) The evolution of feathers – a palaeontological perspective. Springer, Heidelberg
Google Scholar
Lingham-Soliar T (2014) Comment on “A Jurassic ornithischian dinosaur from Siberia with both feathers and scales”. Science 346:434b. https://doi.org/10.1126/science.1259983
Article CAS Google Scholar
Lü JC (2002) Soft tissue in an Early Cretaceous pterosaur from Liaoning Province, China. Memoir of the Fukui Prefectural Dinosaur Museum 1:19–28
Google Scholar
Lü JC (2009) A baby pterodactyloid pterosaur from the Yixian Formation of Ningcheng, Inner Mongolia, China. Acta Geologica Sinica (English Edition) 83:1–8. https://doi.org/10.1111/j.1755-6724.2009.00001.x
Article Google Scholar
Lü JC, Brusatte SL (2015) A large, short-armed, winged dromaeosaurid (Dinosauria: Theropoda) from the Early Cretaceous of China and its implications for feather evolution. Sci Rep 5:11775. https://doi.org/10.1038/srep11775
Article CAS PubMed PubMed Central Google Scholar
Lü JC, Ji Q, Wei XF, Liu YQ (2012) A new ctenochasmatoid pterosaur from the Early Cretaceous Yixian Formation of western Liaoning, China. Cretac Res 34:26–30. https://doi.org/10.1016/j.cretres.2011.09.010
Article Google Scholar
Maddison WP (1991) Squared-change parsimony reconstructions of ancestral states for continuous-valued characters on a phylogenetic tree. Syst Zool 40:304–314
Article Google Scholar
Maderson PFA, Alibardi L (2000) The development of the sauropsid integument: a contribution to the problem of the origin and evolution of feathers. Am Zool 40:513–529. https://doi.org/10.1093/icb/40.4.513
Article Google Scholar
Maidment SCR (2010) Stegosauria: a historical review of the body fossil record and phylogenetic relationships. Swiss J Geosci 103:199–210. https://doi.org/10.1007/s00015-010-0023-3
Article Google Scholar
Mantell GA (1852) On the structure of the Iguanodon, and on the fauna and flora of the Wealden Formation. Notices of the Meetings of the Royal Institution 1:141–146
Google Scholar
Martill DM, Unwin DM (1989) Exceptionally well preserved pterosaur wing membrane from the Cretaceous of Brazil. Nature 340:138–140
Article Google Scholar
Mayr G, Peters SD, Plodowski G, Vogel O (2002) Bristle-like integumentary structures at the tail of the horned dinosaur Psittacosaurus. Naturwissenschaften 89:361–365. https://doi.org/10.1007/s00114-002-0339-6
Article CAS PubMed Google Scholar
Mayr G, Pittman M, Saitta E, Kaye TG, Vinther J (2016) Structure and homology of Psittacosaurus tail bristles. Palaeontology 59:793–802. https://doi.org/10.1111/pala.12257
Article Google Scholar
Mazin J-M, Hantzpergue P, Lafaurie G, Vignaud P (1995) Pterosaur trackways from the Tithonian-of-Crayssac (Quercy, France). Comptes Rendus de l’Académie des Sciences, Série IIA, Sciences de la Terre et des Planètes 321:417–424
Google Scholar
McKellar RC, Chatterton BDE, Wolfe AP, Currie PJ (2011) A diverse assemblage of Late Cretaceous dinosaur and bird feathers from Canadian amber. Science 333:1619–1622. https://doi.org/10.1126/science.1203344
Article CAS PubMed Google Scholar
Morris WJ (1976) Hypsilophodont dinosaurs: a new species and comments on their systematics. In: Churcher CS (ed) Athlon: essays on palaeontology in honour of Loris Shano Russell. Toronto University Press, Toronto, pp 93–113
Google Scholar
Musser JM, Wagner GP, Prum RO (2015) Nuclear β-catenin localization supports homology of feathers, avian scutate scales, and alligator scales in early development. Evol Dev 17:185–194. https://doi.org/10.1111/ede.12123
Article CAS PubMed Google Scholar
Norell MA, Xu X (2005) Feathered dinosaurs. Annu Rev Earth Planet Sci 33:277–299. https://doi.org/10.1146/annurev.earth.33.092203.122511
Article CAS Google Scholar
Norman DB (1985) The illustrated encyclopedia of dinosaurs. Salamander Books, London
Google Scholar
O’Connor J (2020) The plumage of basal birds. In: Foth C, Rauhut OWM (eds) The evolution of feathers – a palaeontological perspective. Springer, Heidelberg
Google Scholar
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) Vegan: Community Ecology Package, version 2.4, 2nd edn. CRAN
Google Scholar
Ortega F, Escaso F, Sanz JL (2010) A bizarre, humped Carcharodontosauria (Theropoda) from the Lower Cretaceous of Spain. Nature 467:203–206. https://doi.org/10.1038/nature09181
Article CAS PubMed Google Scholar
Ostrom JH (1976) Archaeopteryx and the origin of birds. Biol J Linn Soc 8:91–182. https://doi.org/10.1111/j.1095-8312.1976.tb00244.x
Article Google Scholar
Ouyang H, Ye Y (2002) The first mamenchisaurian skeleton with complete skull: Mamenchisaurus youngi. Sichuan Science and Technology Press, Chengu
Google Scholar
Padian K (2008) The Early Jurassic pterosaur Dorygnathus banthensis (Theodori, 1830). Spec Pap Palaeontol 80:1–107
Google Scholar
Padian K, Rayner JMV (1993) Structural fibres of the pterosaur wing: anatomy and aerodynamics. Naturwissenschaften 80:361–364
Article Google Scholar
Padian K, Li C, Pchelnikova J (2010) The trackmaker of Apatopus (Late Triassic, North America): implications for the evolution of archosaur stance and gait. Palaeontology 53:175–189. https://doi.org/10.1111/j.1475-4983.2009.00924.x
Article Google Scholar
Paradis E (2012) Analysis of phylogenetics and evolution with R, 2nd edn. Springer, New York
Book Google Scholar
Paul GS (1988) Physiological, migratorial, climatological, geophysical, survival, and evolutionary implications of Cretaceous polar dinosaurs. J Paleontol 62:640–652
Google Scholar
Pinegar RT, Loewen MA, Cloward KC, Hunter RJ, Weege CJ (2003) A juvenile allosaur with preserved integument from the basal Morrison Formation of central Wyoming. J Vertebr Paleontol 23(3 Suppl):87A–88A
Google Scholar
Prieto-Márquez A (2010) Global phylogeny of Hadrosauridae (Dinosauria: Ornithopoda) using parsimony and Bayesian methods. Zool J Linnean Soc 159:435–502
Article Google Scholar
Prieto-Márquez A, Chiappe LM, Joshi SH (2012) The lambeosaurine dinosaur Magnapaulia laticaudus from the Late Cretaceous of Baja California, Northwestern Mexico. PLoS One 7:e38207. https://doi.org/10.1371/journal.pone.0038207
Article CAS PubMed PubMed Central Google Scholar
Prum RO (1999) Development and evolutionary origin of feathers. J Exp Zool (Mol Dev Evol) 285:291–306
Article CAS Google Scholar
Prum RO, Brush AH (2002) The evolutionary origin and diversification of feathers. Q Rev Biol 77:261–295. https://doi.org/10.1086/341993
Article PubMed Google Scholar
Rauhut OWM, Foth C, Tischlinger H, Norell MA (2012) Exceptionally preserved juvenile megalosauroid theropod dinosaur with filamentous integument from the Late Jurassic of Germany. Proc Natl Acad Sci U S A 109:11746–11751. https://doi.org/10.1073/pnas.1203238109
Article PubMed PubMed Central Google Scholar
Reisz RR, Sues HD (2000) The ‘feathers’ of Longisquama. Nature 408:428. https://doi.org/10.1038/35044204
Article CAS PubMed Google Scholar
Saitta ET, Rogers C, Brooker RA, Abbott GD, Kumar S, O’Reilly SS, Donohoe P, Dutta S, Summons RE, Vinther J (2017) Low fossilization potential of keratin protein revealed by experimental taphonomy. Palaeontology 60(4):547–556. https://doi.org/10.1111/pala.12299
Article Google Scholar
Saveliev SV, Alifanov VR (2014) A new type of skin derivatives in ornithischian dinosaurs from the Late Jurassic of Transbaikalia (Russia). Dokl Biol Sci 456:182–184. https://doi.org/10.1134/s0012496614030053
Article CAS PubMed Google Scholar
Sawyer RH, Knapp LW (2003) Avian skin development and the evolutionary origin of feathers. J Exp Zool B Mol Dev Evol 298B:57–72. https://doi.org/10.1002/jez.b.26
Article Google Scholar
Sawyer RH, Glenn T, French JO, Mays B, Shames RB, Barnes GL Jr, Rhodes W, Ishikawa Y (2000) The expression of beta (β) keratins in the epidermal appendages of reptiles and birds. Am Zool 40:530–539. https://doi.org/10.1668/0003-1569(2000)040[0530:TEOBKI]2.0.CO;2
Article CAS Google Scholar
Sawyer RH, Salvatore BA, Potylicki TTF, French JO, Glenn TC, Knapp LW (2003a) Origin of feathers: Feather beta (β) keratins are expressed in discrete epidermal cell populations of embryonic scutate scales. J Exp Zool B Mol Dev Evol 295B:12–24. https://doi.org/10.1002/jez.b.5
Article CAS Google Scholar
Sawyer RH, Washington LD, Salvatore BA, Glenn TC, Knapp LW (2003b) Origin of archosaurian integumentary appendages: the bristles of the wild turkey beard express feather-type β keratins. J Exp Zool B Mol Dev Evol 297B:27–34. https://doi.org/10.1002/jez.b.17
Article CAS Google Scholar
Schluter D, Price T, Mooers AØ, Ludwig D (1997) Likelihood of ancestor states in adaptive radiation. Evolution 51:1699–1711. https://doi.org/10.1111/j.1558-5646.1997.tb05095.x
Article PubMed Google Scholar
Schweitzer MH, Watt JA, Avci R, Knapp L, Chiappe L, Norell M, Marshall M (1999) Beta-keratin specific immunological reactivity in feather-like structures of the Cretaceous alvarezsaurid, Shuvuuia deserti. J Exp Zool (Mol Dev Evol) 285:146–157. https://doi.org/10.1002/(SICI)1097-010X(19990815)285:2<146::AID-JEZ7>3.0.CO;2-A
Article CAS Google Scholar
Sereno PC (2012) Taxonomy, morphology, masticatory function and phylogeny of heterodontosaurid dinosaurs. ZooKeys 226:1–225. https://doi.org/10.3897/zookeys.226.2840
Article Google Scholar
Sharov AG (1970) An unusual reptile from the Lower Triassic of Fergana. Paleontol Zh 4:112–116
Google Scholar
Sharov AG (1971) New flying reptiles from the Mesozoic of Kazakhstan and Kirgizstan. Trudy Palaontologicheskogo Instituta Akademia Nauk SSSR 130:103–113
Google Scholar
Starrfelt J, Liow LH (2016) How many dinosaur species were there? Fossil bias and true richness estimated using a Poisson sampling model. Philos Trans R Soc B Biol Sci 371:20150219. https://doi.org/10.1098/rstb.2015.0219
Article CAS Google Scholar
Sullivan C, Wang Y, Hone DWE, Wang YQ, Xu X, Zhang FC (2014) The vertebrates of the Jurassic Daohugou Biota of northeastern China. J Vertebr Paleontol 34:243–280. https://doi.org/10.1080/02724634.2013.787316
Article Google Scholar
Sullivan C, Xu X, O’Connor JK (2017) Complexities and novelties in the early evolution of avian flight, as seen in the Mesozoic Yanliao and Jehol Biotas of Northeast China. Palaeoworld 26:212–229. https://doi.org/10.1016/j.palwor.2016.12.001
Article Google Scholar
Swofford DL, Maddison WP (1987) Reconstructing ancestral character states under Wagner parsimony. Math Biosci 87:199–229. https://doi.org/10.1016/0025-5564(87)90074-5
Article Google Scholar
Thompson RS, Parish JC, Maidment SCR, Barrett PM (2012) Phylogeny of the ankylosaurian dinosaurs (Ornithischia: Thyreophora). J Syst Palaeontol 10:301–312. https://doi.org/10.1080/14772019.2011.569091
Article Google Scholar
Thornley AL (1970) Epidermal remnants of Proterosuchus vanhoepeni (HTN). Palaeontol Afr 132:57–60
Google Scholar
Unwin DM (2006) The Pterosaurs: from deep time. Pi, New York
Google Scholar
Upchurch P, Barrett PM, Dodson P (2004) Sauropoda. In: Weishampel DB, Dodson P, Osmólska H (eds) The Dinosauria, 2nd edn. University of California Press, Berkeley, pp 259–322
Chapter Google Scholar
Van der Reest AJ, Wolfe AP, Currie PJ (2016) A densely feathered ornithomimid (Dinosauria: Theropoda) from the Upper Cretaceous Dinosaur Park Formation, Alberta, Canada. Cretac Res 58:108–117. https://doi.org/10.1016/j.cretres.2015.10.004
Article Google Scholar
Wang XL, Zhou ZH, Zhang FC, Xu X (2002) A nearly completely articulated rhamphorhynchoid pterosaur with exceptionally well-preserved wing membranes and “hairs” from Inner Mongolia, northeast China. Chin Sci Bull 47:226–230. https://doi.org/10.1360/02tb9054
Article Google Scholar
Wang XL, Kellner AWA, Zhou ZH, de ACD (2007) A new pterosaur (Ctenochasmatidae, Archaeopterodactyloidea) from the Lower Cretaceous Yixian Formation of China. Cretac Res 28:245–260. https://doi.org/10.1016/j.cretres.2006.08.004
Article Google Scholar
Wild R (1993) A juvenile specimen of Eudimorphodon ranzii Zambelli (Reptilia, Pterosauria) from the upper Triassic (Norian) of Bergamo. Rivista del Museo Civico di Scienze Naturali 16:95–120
Google Scholar
Witmer LM (2009) Dinosaurs: fuzzy origins for feathers. Nature 458:293–295. https://doi.org/10.1038/458293a
Article CAS PubMed Google Scholar
Witton MP (2016) Recreating an age of reptiles. Rhedphare, UK
Google Scholar
Xing LD, McKellar RC, Wang M, Bai M, O’Connor JK, Benton MJ, Zhang JP, Wang Y, Tseng KW, Lockley MG, Li G, Zhang WW, Xu X (2016) Mummified precocial bird wings in mid-Cretaceous Burmese amber. Nat Commun 7:12089. https://doi.org/10.1038/ncomms12089
Article CAS PubMed PubMed Central Google Scholar
Xu X (2006) Feathered dinosaurs from China and the evolution of major avian characters. Integr Zool 1:4–11. https://doi.org/10.1111/j.1749-4877.2006.00004.x
Article PubMed Google Scholar
Xu X (2020) Filamentous integuments in non-avialan theropods and their kin: advances and future perspectives for understanding the evolution of feathers. In: Foth C, Rauhut OWM (eds) The evolution of feathers – a palaeontological perspective. Springer, Heidelberg
Google Scholar
Xu X, 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, Wang XL, Wu XC (1999a) A dromaeosaurid dinosaur with a filamentous integument from the Yixian Formation of China. Nature 401:262–266. https://doi.org/10.1038/45769
Article CAS Google Scholar
Xu X, Tang ZL, Wang XL (1999b) A therizinosauroid dinosaur with integumentary structures from China. Nature 399:350–354. https://doi.org/10.1038/20670
Article CAS Google Scholar
Xu X, Zhou ZH, Wang XL (2000) The smallest known non-avian theropod dinosaur. Nature 408:705–708. https://doi.org/10.1038/35047056
Article CAS PubMed Google Scholar
Xu X, Zhou ZH, Wang XL, Kuang XW, Zhang FC, Du XK (2003) Four-winged dinosaurs from China. Nature 421:335–340. https://doi.org/10.1038/nature01342
Article CAS PubMed Google Scholar
Xu X, Norell MA, Kuang XW, Wang XL, Zhao Q, Jia CK (2004) Basal tyrannosauroids from China and evidence for protofeathers in tyrannosauroids. Nature 431:680–684. https://doi.org/10.1038/nature02855
Article CAS PubMed Google Scholar
Xu X, Zheng XT, You HL (2009) A new feather type in a nonavian theropod and the early evolution of feathers. Proc Natl Acad Sci U S A 106:832–834. https://doi.org/10.1073/pnas.0810055106
Article PubMed PubMed Central Google Scholar
Xu X, Wang KB, Ma QY, Xing LD, Sullivan C, Hu DY, Cheng SQ, Wang S (2012) A gigantic feathered dinosaur from the Lower Cretaceous of China. Nature 484:92–95. https://doi.org/10.1038/nature10906
Article CAS PubMed Google Scholar
Xu X, Zhou ZH, Dudley R, Mackem S, Chuong CM, Erickson GM, Varricchio DJ (2014) An integrative approach to understanding bird origins. Science 346:1253293. https://doi.org/10.1126/science.1253293
Article CAS PubMed Google Scholar
Xu X, Zheng XT, Sullivan C, Wang XL, Xing LD, Wang Y, Zhang XM, O’Connor JK, Zhang FC, Pan YH (2015) A bizarre Jurassic maniraptoran theropod with preserved evidence of membranous wings. Nature 521:70–73. https://doi.org/10.1038/nature14423
Article CAS PubMed Google Scholar
Xu X, Currie P, Pittman M, Xing LD, Meng QJ, Lü JC, Hu DY, CY Y (2017) Mosaic evolution in an asymmetrically feathered troodontid dinosaur with transitional features. Nat Commun 8:14972. https://doi.org/10.1038/ncomms14972
Article PubMed PubMed Central Google Scholar
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 338:510–514. https://doi.org/10.1126/science.1225376
Article CAS PubMed Google Scholar
Zhang FC, Zhou ZH, Xu X, Wang XL, Sullivan C (2008) A bizarre Jurassic maniraptoran from China with elongate ribbon-like feathers. Nature 455:1105–1108. https://doi.org/10.1038/nature07447
Article CAS PubMed Google Scholar
Zheng XT, You HL, Xu X, Dong ZM (2009) An Early Cretaceous heterodontosaurid dinosaur with filamentous integumentary structures. Nature 458:333–336. https://doi.org/10.1038/nature07856
Article CAS PubMed Google Scholar

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Acknowledgements

We thank the editors (C. Foth and O. Rauhut) for inviting us to contribute to this volume, for their insightful comments, and for their patience. We thank P. Bell, R. Benson, R. Butler, M. Davis and M. Young for discussions related to feather evolution and dinosaur skin.

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Authors and Affiliations

Palaeoscience Research Centre, School of Environmental and Rural Science, University of New England, Armidale, NSW, Australia
Nicolás E. Campione
Palaeobiology Programme, Department of Earth Sciences, Uppsala University, Uppsala, Sweden
Nicolás E. Campione
Subdepartment of Evolution and Development, Department of Organismal Biology, Uppsala University, Uppsala, Sweden
Nicolás E. Campione
Department of Earth Sciences, Natural History Museum, London, UK
Paul M. Barrett
Department of Natural History, Royal Ontario Museum, Toronto, ON, Canada
David C. Evans

Authors

Nicolás E. Campione
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Paul M. Barrett
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David C. Evans
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Correspondence to Nicolás E. Campione .

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Department of Geosciences, University of Fribourg, Fribourg, Switzerland
Christian Foth
Department for Earth and Environmental Sciences, Ludwig-Maximilians-Universität, Palaeontology and Geobiology, GeoBioCenter, München, Germany
Oliver W. M. Rauhut

12.1 Electronic Supplementary Material

Supplementary Appendix 12.1

(4 kb)

Appendix

Character coding data set used in the analyses

Taxon	Char1a	Char2a	Char1b	Char2b	Char1c	Char2c	Max	Min
Crurotarsi	0	0	0	0	0	0	247.2	0
Pterosauria	0	0	1	1	3	2	212	66
Allosaurus_fragilis	0	0	0	0	0	0	157.3	152.1
Albertosaurus_sarcophagus	0	0	0	0	0	0	72.1	66
Anchiornis_huxleyi	2	1	2	1	2	1	163.5	157.3
Archaeopteryx_lithographica	2	1	2	1	2	1	152.1	145
Auca_Maheuvo_titanosaur	0	0	0	0	0	0	83.6	72.1
Aurornis_xui	2	1	2	1	2	1	163.5	157.3
Barosaurus_lentus	0	0	0	0	0	0	157.3	152.1
Beipiaosaurus_inexpectus	1	1	1	1	1	1	129.4	125
Brachylophosaurus_canadensis	0	0	0	0	0	0	83.6	72.1
Camarasaurus_sp.	0	0	0	0	0	0	157.3	152.1
Carnotaurus_sastrei	0	0	0	0	0	0	83.6	72.1
Caudipteryx_dongi	2	1	2	1	2	1	129.4	125
Caudipteryx_zhoui	2	1	2	1	2	1	129.4	125
Centrosaurus_apertus	0	0	0	0	0	0	83.6	72.1
cf._Stegosaurus_sp.	0	0	0	0	0	0	157.3	152.1
Chasmosaurus_belli	0	0	0	0	0	0	83.6	72.1
Compsognathus_longipes	0	0	0	0	0	0	152.1	145
Concavenator_corcovatus	0	0	0	0	0	0	129.4	125
Confuciusornis_sanctus	2	1	2	1	2	1	129.4	125
Corythosaurus_casuarius	0	0	0	0	0	0	83.6	72.1
Corythosaurus_intermedius	0	0	0	0	0	0	83.6	72.1
Daspletosaurus_torosus	0	0	0	0	0	0	83.6	72.1
Dilong_paradoxus	2	1	2	1	2	1	129.4	125
Diplodocus_sp.	0	0	0	0	0	0	157.3	152.1
Dyoplosaurus_acutosquameus	0	0	0	0	0	0	83.6	72.1
Edmontosaurus_annectens	0	0	0	0	0	0	72.1	66
Edmontosaurus_regalis	0	0	0	0	0	0	83.6	72.1
Eosinopteryx_brevipenna	2	1	2	1	2	1	163.5	157.3
Epidexipteryx_hui	2	1	2	1	2	1	163.5	157.3
Euoplocephalus_tutus	0	0	0	0	0	0	83.6	72.1
Gigantspinosaurus_szechuanensis	0	0	0	0	0	0	163.5	157.3
Gorgosaurus_libratus	0	0	0	0	0	0	83.6	72.1
Gryposaurus_monumentensis	0	0	0	0	0	0	83.6	72.1
Gryposaurus_notabilis	0	0	0	0	0	0	83.6	72.1
Hesperosaurus_mjosi	0	0	0	0	0	0	157.3	152.1
Hypacrosaurus_altispinus	0	0	0	0	0	0	72.1	66
Jinfengopteryx_elegans	2	1	2	1	2	1	129.4	125
Juravenator_starkii	1	1	1	1	1	1	152.1	145
Kulindadromeus_zabaikalicus	2	1	2	1	2	1	169	144
Lambeosaurus_clavinitialis	0	0	0	0	0	0	83.6	72.1
Lambeosaurus_magnicristatus	0	0	0	0	0	0	83.6	72.1
Liaoningosaurus_paradoxus	0	0	0	0	0	0	129.4	125
Magnipaulia_laticaudus	0	0	0	0	0	0	83.6	72.1
Maiasaura_peeblesorum	0	0	0	0	0	0	83.6	72.1
Mamenchisaurus_youngi	0	0	0	0	0	0	163.5	152.1
Mantellisaurus_atherfieldensis	0	0	0	0	0	0	129.4	125
Microraptor_gui	2	1	2	1	2	1	125	113
Microraptor_zhaoianus	2	1	2	1	2	1	125	113
Ornithomimus_edmontonicus	2	1	2	1	2	1	83.6	66
Parasaurolophus_walkeri	0	0	0	0	0	0	83.6	72.1
Pedopenna_daohugouensis	2	1	2	1	2	1	163.5	157.3
Pelorosaurus_becklesii	0	0	0	0	0	0	139.8	132.9
Prosaurolophus_maximus	0	0	0	0	0	0	83.6	72.1
Protarchaeopteryx_robusta	2	1	2	1	2	1	129.4	125
Psittacosaurus_sp.	1	1	1	1	1	1	129.4	125
Rahonavis_ostromi	2	1	2	1	2	1	72.1	66
Saurolophus_angustirostris	0	0	0	0	0	0	72.1	66
Saurolophus_osborni	0	0	0	0	0	0	72.1	66
Scansoriopteryx_heilmanni	2	1	2	1	2	1	163.5	157.3
Scelidosaurus_harrisonii	0	0	0	0	0	0	199.3	190.8
Sciurumimus_albersodoefri	1	1	1	1	1	1	157.3	152.1
Scolosaurus_cutleri	0	0	0	0	0	0	83.6	72.1
Shuvuuia_deserti	1	1	1	1	1	1	83.6	72.1
Similicaudipteryx_yixianensis	2	1	2	1	2	1	129.4	125
Sinocalliopteryx_gigas	1	1	1	1	1	1	129.4	125
Sinornithosaurus_millenii	2	1	2	1	2	1	129.4	125
Sinosauropteryx_prima	1	1	1	1	1	1	129.4	125
Tarbosaurus_bataar	0	0	0	0	0	0	72.1	66
Tarchia_kielanae	0	0	0	0	0	0	72.1	66
Tehuelchesaurus_benitezii	0	0	0	0	0	0	157.3	152.1
Tenontosaurus_sp.	0	0	0	0	0	0	125	113
Tianyulong_confuciusi	1	1	1	1	1	1	163.5	157.3
Triceratops_horridus	0	0	0	0	0	0	72.1	66
Tyrannosaurus_rex	0	0	0	0	0	0	72.1	66
Velociraptor_mongoliensis	2	1	2	1	2	1	83.6	72.1
Xiaotingia_zhengi	1	1	1	1	1	1	163.5	157.3
Yutyrannus_huali	1	1	1	1	1	1	129.4	125

Codings are explained in the text. Char1 refers to a multistate treatment of the filamentous/feathered condition; Char2 lumps all non-scaly conditions into a single state (i.e. binary); a, b, and c represent different assumptions made for ancestral condition in pterosaurs. Maximal and minimal ages are in millions of years

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Campione, N.E., Barrett, P.M., Evans, D.C. (2020). On the Ancestry of Feathers in Mesozoic Dinosaurs. In: Foth, C., Rauhut, O. (eds) The Evolution of Feathers. Fascinating Life Sciences. Springer, Cham. https://doi.org/10.1007/978-3-030-27223-4_12

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DOI: https://doi.org/10.1007/978-3-030-27223-4_12
Published: 12 March 2020
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Online ISBN: 978-3-030-27223-4
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12.1 Electronic Supplementary Material

Supplementary Appendix 12.1

Appendix

Appendix

Character coding data set used in the analyses

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