Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

The developing bird pelvis passes through ancestral dinosaurian conditions

Nature volume 608, pages 346–352 (2022)Cite this article

Subjects

An Author Correction to this article was published on 14 November 2023

This article has been updated

Abstract

Living birds (Aves) have bodies substantially modified from the ancestral reptilian condition. The avian pelvis in particular experienced major changes during the transition from early archosaurs to living birds1,2. This stepwise transformation is well documented by an excellent fossil record2,3,4; however, the ontogenetic alterations that underly it are less well understood. We used embryological imaging techniques to examine the morphogenesis of avian pelvic tissues in three dimensions, allowing direct comparison with the fossil record. Many ancestral dinosaurian features2 (for example, a forward-facing pubis, short ilium and pubic ‘boot’) are transiently present in the early morphogenesis of birds and arrive at their typical ‘avian’ form after transitioning through a prenatal developmental sequence that mirrors the phylogenetic sequence of character acquisition. We demonstrate quantitatively that avian pelvic ontogeny parallels the non-avian dinosaur-to-bird transition and provide evidence for phenotypic covariance within the pelvis that is conserved across Archosauria. The presence of ancestral states in avian embryos may stem from this conserved covariant relationship. In sum, our data provide evidence that the avian pelvis, whose early development has been little studied5,6,7, evolved through terminal addition—a mechanism8,9,10 whereby new apomorphic states are added to the end of a developmental sequence, resulting in expression8,11 of ancestral character states earlier in that sequence. The phenotypic integration we detected suggests a previously unrecognized mechanism for terminal addition and hints that retention of ancestral states in development is common during evolutionary transitions.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Archosaurian phylogeny and pelvic evolution on the line to birds.
Fig. 2: Embryological series of A. mississippiensis pelves showing that Alligator retains the same states throughout prehatching ontogeny.
Fig. 3: Embryological series of C. coturnix japonica (Japanese quail) showing the transition from ancestral to derived pelvic states across avian prehatching ontogeny.
Fig. 4: Avian morphogenesis extends across 3D geometric morphometric PC space from ancestral to derived conditions.

Similar content being viewed by others

Data availability

All data files used for analyses are hosted on Dryad (https://doi.org/10.5061/dryad.xd2547dj2). All fossils are reposited in recognized natural history institutions.

Code availability

All code is hosted on Dryad (https://doi.org/10.5061/dryad.xd2547dj2).

Change history

References

  1. Gatesy, S. M. in Functional Morphology in Vertebrate Paleontology (ed. Thomason, J. J.) 219–234 (Cambridge University Press, 1995).

  2. Hutchinson, J. R. The evolution of pelvic osteology and soft tissues on the line to extant birds (Neornithes). Zool. J. Linnean Soc. 131, 123–168 (2001).

    Article  Google Scholar 

  3. Turner, A. H., Makovicky, P. J. & Norell, M. A. A review of dromaeosaurid systematics and paravian phylogeny. Bull. Am. Museum Nat. Hist. 371, 1–206 (2012).

    Article  Google Scholar 

  4. Ostrom, J. H. On a new specimen of the Lower Cretaceous theropod dinosaur Deinonychus antirrhopus. Breviora 439, 1–21 (1976).

    Google Scholar 

  5. Bunge, A. Untersuchungen zur Entwickelungsgeschichte des Beckengürtels der Amphibien, Reptilien, und Vögel. PhD thesis, Universität Dorpat (1880).

  6. Johnson, A. On the development of the pelvic girdle and skeleton of the hind limb of the chick. Q. J. Microsc. Sci. 23, 399–411 (1883).

    Google Scholar 

  7. Mehnert, E. Untersuchungen über die entwisklung des os pelvis der vögel. Morphologisches Jahrbuch 13, 259–295 (1887).

    Google Scholar 

  8. Gould, S. J. Ontogeny and Phylogeny (Harvard University Press, 1977).

  9. Mayr, E. Recapitulation reinterpreted: the somatic program. Q. Rev. Biol. 69, 223–232 (1994).

    Article  Google Scholar 

  10. Abzhanov, A. von Baer’s law for the ages: lost and found principles of developmental evolution. Trends Genet. 29, 712–722 (2013).

    Article  CAS  PubMed  Google Scholar 

  11. Diogo, R., Smith, C. M. & Ziermann, J. M. Evolutionary developmental pathology and anthropology: a new field linking development, comparative anatomy, human evolution, morphological variations and defects, and medicine. Dev. Dyn. 244, 1357–1374 (2015).

    Article  PubMed  Google Scholar 

  12. Ksepka, D. T. Feathered dinosaurs. Curr. Biol. 30, R1347–R1353 (2020).

    Article  CAS  PubMed  Google Scholar 

  13. Lowe, C. B., Clarke, J. A., Baker, A. J., Haussler, D. & Edwards, S. V. Feather development genes and associated regulatory innovation predate the origin of Dinosauria. Mol. Biol. Evol. 32, 23–28 (2015).

  14. Bhullar, B.-A. S. et al. How to make a bird skull: major transitions in the evolution of the avian cranium, paedomorphosis, and the beak as a surrogate hand. Integr. Comp. Biol. 56, 389–403 (2016).

    Article  PubMed  Google Scholar 

  15. Fabbri, M. et al. The skull roof tracks the brain during the evolution and development of reptiles including birds. Nat. Ecol. Evol. 1, 1543–1550 (2017).

    Article  PubMed  Google Scholar 

  16. Bhullar, B.-A. S. et al. A molecular mechanism for the origin of a key evolutionary innovation, the bird beak and palate, revealed by an integrative approach to major transitions in vertebrate history. Evolution 69, 1665–1677 (2015).

    Article  PubMed  Google Scholar 

  17. Louchart, A. & Viriot, L. From snout to beak: the loss of teeth in birds. Trends Ecol. Evol. 26, 663–673 (2011).

    Article  PubMed  Google Scholar 

  18. O'Connor, P. M. Evolution of archosaurian body plans: skeletal adaptations of an air-sac-based breathing apparatus in birds and other archosaurs. J. Exp. Zool. A 311A, 629–646 (2009).

    Article  Google Scholar 

  19. Heers, A. M. & Dial, K. P. From extant to extinct: locomotor ontogeny and the evolution of avian flight. Trends Ecol. Evol. 27, 296–305 (2012).

    Article  PubMed  Google Scholar 

  20. Mayr, G. Evolution of avian breeding strategies and its relation to the habitat preferences of Mesozoic birds. Evol. Ecol. 31, 131–141 (2017).

    Article  Google Scholar 

  21. Gatesy, S. M. Caudofemoral musculature and the evolution of theropod locomotion. Paleobiology 16, 170–186 (1990).

    Article  Google Scholar 

  22. Gatesy, S. M. & Dial, K. P. Locomotor modules and the evolution of avian flight. Evolution 50, 331–340 (1996).

    Article  PubMed  Google Scholar 

  23. Hutchinson, J. R. The evolution of locomotion in archosaurs. C. R. Palevol. 5, 519–530 (2006).

    Article  Google Scholar 

  24. Hutchinson, J. R. & Gatesy, S. M. Adductors, abductors, and the evolution of archosaur locomotion. Paleobiology 26, 734–751 (2000).

    Article  Google Scholar 

  25. Organ, C. L., Shedlock, A. M., Meade, A., Pagel, M. & Edwards, S. V. Origin of avian genome size and structure in non-avian dinosaurs. Nature 446, 180–184 (2007).

  26. Gegenbaur, C. Gundriss der Vergleichenden Anatomie (Engelmann, 1878).

  27. Huxley, T. H. Further evidence of the affinity between the dinosaurian reptiles and birds. Q. J. Geol. Soc. Lond. 26, 12–31 (1870).

    Article  Google Scholar 

  28. Carroll, S. B. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134, 25–36 (2008).

    Article  CAS  PubMed  Google Scholar 

  29. Romer, A. S. The development of the thigh musculature of the chick. J. Morphol. Physiol. 43, 347–385 (1927).

    Article  Google Scholar 

  30. Schroeter, S. & Tosney, K. W. Spatial and temporal patterns of muscle cleavage in the chick thigh and their value as criteria for homology. Am. J. Anat. 191, 325–350 (1991).

    Article  CAS  PubMed  Google Scholar 

  31. Kardong, K. V. Vertebrates: Comparative Anatomy, Function, Evolution 8th edn (McGraw-Hill Education, 2019).

  32. Chung, K. et al. Structural and molecular interrogation of intact biological systems. Nature 497, 332–337 (2013).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  33. Egawa, S., Saito, D., Abe, G. & Tamura, K. Morphogenetic mechanism of the acquisition of the dinosaur-type acetabulum. R. Soc. Open Sci. 5, 180604 (2018).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  34. Hutchinson, J. R. The evolution of hindlimb tendons and muscles on the line to crown-group birds. Comp. Biochem. Physiol. A 133, 1051–1086 (2002).

    Article  Google Scholar 

  35. Giffin, E. B. Postcranial paleoneurology of the Diapsida. J. Zool. 235, 389–410 (1995).

    Article  Google Scholar 

  36. Carpenter, E. M. Hox genes and spinal cord development. Dev. Neurosci. 24, 24–34 (2002).

    Article  CAS  PubMed  Google Scholar 

  37. Gaunt, S. J. Evolutionary shifts of vertebrate structures and Hox expression up and down the axial series of segments: a consideration of possible mechanisms. Int. J. Dev. Biol. 44, 109–117 (2000).

    CAS  PubMed  Google Scholar 

  38. Diogo, R., Ziermann, J., Molnar, J., Siomava, N. & Abdala, V. Muscles of Chordates: Development, Homologies and Evolution (Taylor & Francis, 2018).

  39. Felice, R. N., Randau, M. & Goswami, A. A fly in a tube: macroevolutionary expectations for integrated phenotypes. Evolution 72, 2580–2594 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  40. Olson, E. C. & Miller, R. L. Morphological Integration (University of Chicago Press, 1958).

  41. Schlosser, G. in Modularity in Development and Evolution (eds Schlosser, G. & Wagner, G. P.) 519–582 (University of Chicago Press, 2004).

  42. Lee, H. W., Esteve-Altava, B. & Abzhanov, A. Evolutionary and ontogenetic changes of the anatomical organization and modularity in the skull of archosaurs. Sci. Rep. 10, 16138 (2020).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  43. Felice, R. N. et al. Evolutionary integration and modularity in the archosaur cranium. Integr. Comp. Biol. 59, 371–382 (2019).

    Article  PubMed  Google Scholar 

  44. Goswami, A., Smaers, J. B., Soligo, C. & Polly, P. D. The macroevolutionary consequences of phenotypic integration: from development to deep time. Philos. Trans. R. Soc. B 369, 20130254 (2014).

    Article  CAS  Google Scholar 

  45. Iijima, M. & Kobayashi, Y. Convergences and trends in the evolution of the archosaur pelvis. Paleobiology 40, 608–624 (2014).

    Article  Google Scholar 

  46. Adams, D. C. Evaluating modularity in morphometric data: challenges with the RV coefficient and a new test measure. Methods Ecol. Evol. 7, 565–572 (2016).

    Article  Google Scholar 

  47. Bjarnason, A. & Benson, R. A 3D geometric morphometric dataset quantifying skeletal variation in birds. MorphoMuseuM 7, e125 (2021).

    Article  Google Scholar 

  48. Giffin, E. B. Endosacral enlrgements in dinosaurs. Mod. Geol. 16, 101–112 (1991).

    Google Scholar 

  49. Giffin, E. B. Paleoneurology: reconstructing the nervous systems of dinosaurs. Paleontol. Soc. Special Pub. 7, 229–242 (1994).

    Article  Google Scholar 

  50. Ferguson, M. W. J. in Biology of the Reptilia Vol. 14 (eds Gans, C. et al.) 329–492 (John Wiley and Sons, 1985).

  51. Hamburger, V. & Hamilton, H. L. A series of normal stages in the development of the chick embryo. J. Morphol. 88, 49–92 (1951).

    Article  CAS  PubMed  Google Scholar 

  52. Ainsworth, S. J., Stanley, R. L. & Evans, D. J. R. Developmental stages of the Japanese quail. J. Anat. 216, 3–15 (2010).

    Article  PubMed  Google Scholar 

  53. Dingerkus, G. & Uhler, D. Enzyme clearing of Alcian blue stained whole small vertebrates for demonstration of cartilage. Stain Technol. 52, 229–232 (1977).

    Article  CAS  PubMed  Google Scholar 

  54. Ovchinnikov, D. Alcian blue/Alizarin red staining of cartilage and bone in mouse. Cold Spring Harbor Protoc. 2009, pdb.prot5170 (2009).

    Article  Google Scholar 

  55. Rigueur, D. & Lyons, K. M. Whole-mount skeletal staining. Methods Mol. Biol. 1130, 113–121 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Schultze, O. Ueber herstellung und conservirung durchsichtiger embryonen zum stadium der skeletbildung. Anatomischer Anzeiger 13, 3–5 (1897).

    Google Scholar 

  57. Horobin, R. W. in Educational Guide Special Stains and H&E 2nd edn (eds Kumar, G. L. & Kiernan, J. A.) 159–166 (Carpinteria, 2010).

  58. Carril, J., Tambussi, C. P. & Rasskin-Gutman, D. The network ontogeny of the parrot: altriciality, dynamic skeletal assemblages, and the avian body plan. Evol. Biol. 48, 41–53 (2021).

    Article  Google Scholar 

  59. Maxwell, E. E. Comparative embryonic development of the skeleton of the domestic turkey (Meleagris gallopavo) and other galliform birds. Zoology 111, 1095–1113 (2008).

    Article  Google Scholar 

  60. Maxwell, E. E. Ossification sequence of the avian order Anseriformes, with comparison to other precocial birds. J. Morphol. 269, 1095–1113 (2008).

    Article  PubMed  Google Scholar 

  61. Maxwell, E. E. & Harrison, L. B. Ossification sequence of the common tern (Sterna hirundo) and its implications for the interrelationships of the Lari (Aves, Charadriiformes). J. Morphol. 269, 1056–1072 (2008).

    Article  PubMed  Google Scholar 

  62. Maxwell, E. E. & Larsson, H. C. E. Comparative ossification sequence and skeletal development of the postcranium of palaeognathous birds (Aves: Palaeognathae). Zool. J. Linnean Soc. 157, 169–196 (2009).

    Article  Google Scholar 

  63. Ikeda, T. et al. Distinct roles of Sox5, Sox6, and Sox9 in different stages of chondrogenic differentiation. J. Bone Mineral Metab. 23, 337–340 (2005).

    Article  Google Scholar 

  64. Lefebvre, V., Behringer, R. R. & de Crombrugghe, B. L-Sox5, Sox6 and Sox9 control essential steps of the chondrocyte differentiation pathway. Osteoarthritis Cartilage 9, S69–S75 (2001).

    Article  PubMed  Google Scholar 

  65. Smits, P. et al. The transcription factors L-Sox5 and Sox6 are essential for cartilage formation. Dev. Cell 1, 277–290 (2001).

    Article  CAS  PubMed  Google Scholar 

  66. Cancedda, R., Castagnola, P., Cancedda, F. D., Dozin, B. & Quarto, R. Developmental control of chondrogenesis and osteogenesis. Int. J. Dev. Biol. 44, 707–714 (2000).

    CAS  PubMed  Google Scholar 

  67. Eames, B. F., De La Fuente, L. & Helms, J. A. Molecular ontogeny of the skeleton. Birth Defects Res. C 69, 93–101 (2003).

    Article  CAS  Google Scholar 

  68. Miller, E. J. & Matukas, V. J. Chick cartilage collagen: a new type of α1 chain not present in bone or skin of the species. Proc. Natl Acad. Sci. USA 64, 1264–1268 (1969).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  69. Zhang, G., Eames, B. F. & Cohn, M. J. Evolution of vertebrate cartilage development. Curr. Topics Dev. Biol. 86, 15–42 (2009).

    Article  CAS  Google Scholar 

  70. Ninomiya, Y., Showalter, A. & Olsen, B. in The Role of Extracellular Matrix in Development (ed. Trelstad, R. L.) 255–275 (Alan R. Liss, 1984).

  71. Botelho, J. F., Smith-Paredes, D., Nuñez-Leon, D., Soto-Acuña, S. & Vargas, A. O. The developmental origin of zygodactyl feet and its possible loss in the evolution of Passeriformes. Proc. R. Soc. B 281, 20140765 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  72. Botelho, J. F. et al. Skeletal plasticity in response to embryonic muscular activity underlies the development and evolution of the perching digit of birds. Sci. Rep. 5, 09840 (2015).

    Article  Google Scholar 

  73. Huh, J. W., Laurer, H. L., Raghupathi, R., Helfaer, M. A. & Saatman, K. E. Rapid loss and partial recovery of neurofilament immunostaining following focal brain injury in mice. Exp. Neurol. 175, 198–208 (2002).

    Article  CAS  PubMed  Google Scholar 

  74. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).

    Article  CAS  PubMed  Google Scholar 

  75. Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Bookstein, F. L. Morphometric Tools for Landmark Data: Geometry and Biology (Cambridge University Press, 1997).

  77. R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).

  78. Geomorph: software for geometric morphometric analyses (R package version 3.2.1) (2020).

  79. Rohlf, F. J. The TPS series of software. Hystrix 26, 9–12 (2015).

    Google Scholar 

  80. Charrad, M., Ghazzali, N., Boiteau, V. & Niknafs, A. NbClust: an R package for determining the relevant number of clusters in a data set. J. Stat. Softw. 61, 1–36 (2014).

    Article  Google Scholar 

  81. Buser, T. J., Sidlauskas, B. L. & Summers, A. P. 2D or not 2D? Testing the utility of 2D vs. 3D landmark data in geometric morphometrics of the sculpin subfamily Oligocottinae (Pisces; Cottoidea). Anat. Rec. 301, 806–818 (2018).

    Article  Google Scholar 

  82. Oksanen, J. et al. vegan: community ecology package (R package version 2.5-7). https://CRAN.R-project.org/package=vegan (2020).

  83. Adams, D. C., Rohlf, F. J. & Slice, D. E. A field comes of age: geometric morphometrics in the 21st century. Hystrix 24, 7–14 (2013).

    Google Scholar 

  84. Theska, T., Sieriebriennikov, B., Wighard, S. S., Werner, M. S. & Sommer, R. J. Geometric morphometrics of microscopic animals as exemplified by model nematodes. Nat. Protoc. 15, 2611–2644 (2020).

    Article  CAS  PubMed  Google Scholar 

  85. Goodall, C. Procrustes methods in the statistical analysis of shape. J. R. Stat. Soc. B 53, 285–339 (1991).

    MathSciNet  MATH  Google Scholar 

  86. Drake, A. G. & Klingenberg, C. P. The pace of morphological change: historical transformation of skull shape in St Bernard dogs. Proc. Biol. Sci. 275, 71–76 (2008).

    PubMed  Google Scholar 

  87. Friendly, M. HE plots for repeated measures designs. J. Stat. Softw. 37, 1–40 (2010).

    Article  Google Scholar 

  88. Agnolin, F. L., Motta, M. J., Brissón Egli, F., Lo Coco, G. & Novas, F. E. Paravian phylogeny and the dinosaur–bird transition: an overview. Front. Earth Sci. 6, 252 (2019).

    Article  ADS  Google Scholar 

  89. Erickson, G. M. et al. Insights into the ecology and evolutionary success of crocodilians revealed through bite-force and tooth-pressure experimentation. PLoS ONE 7, e31781 (2012).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  90. Ezcurra, M. D. The phylogenetic relationships of basal archosauromorphs, with an emphasis on the systematics of proterosuchian archosauriforms. PeerJ 4, e1778 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  91. Nesbitt, S. J. The early evolution of archosaurs: relationships and the origin of major clades. Bull. Am. Museum Nat. Hist. 352, 1–292 (2011).

    Article  Google Scholar 

  92. Nesbitt, S. J. et al. A mid-Cretaceous tyrannosauroid and the origin of North American end-Cretaceous dinosaur assemblages. Nat. Ecol. Evol. 3, 892–899 (2019).

    Article  PubMed  Google Scholar 

  93. Pritchard, A. C. & Sues, H.-D. Postcranial remains of Teraterpeton hrynewichorum (Reptilia: Archosauromorpha) and the mosaic evolution of the saurian postcranial skeleton. J. Syst. Paleontol. 17, 1745–1765 (2019).

    Article  Google Scholar 

  94. Rauhut, O. W. M., Hübner, T. R. & Lanser, K.-P. A new megalosaurid theropod dinosaur from the late Middle Jurassic (Callovian) of north-western Germany: implications for theropod evolution and faunal turnover in the Jurassic. Palaeontologia Electronica 19, 29A (2016).

    Google Scholar 

  95. Cau, A. The assembly of the avian body plan: a 160-million-year long process. Boll. Soc. Paleontol. Ital. 57, 1–25 (2018).

    Google Scholar 

  96. Cau, A., Brougham, T. & Naish, D. The phylogenetic affinities of the bizarre Late Cretaceous Romanian theropod Balaur bondoc (Dinosauria, Maniraptora): dromaeosaurid or flightless bird? PeerJ 3, e1032 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  97. Perrin, A. Recherches sur les affinités zoologiques de l’Hatteria punctata. Ann. Sci. Nat. 20, 33–102 (1895).

    Google Scholar 

  98. Osawa, G. Beitrage zur Anatomie der Hatteria punctata. Arch. Mikrosk. Anat. 51, 48–691 (1898).

    Google Scholar 

  99. Gregory, W. K. & Camp, C. L. Studies in comparative myology and osteology III. Bull. Am. Museum Nat. Hist. 38, 447–563 (1918).

    Google Scholar 

  100. Byerly, T. The myology of Sphenodon puncatum. Univ. Iowa Stud. Nat. Hist. 11, 3–51 (1925).

    Google Scholar 

  101. Walker, A. D. in Problems in Vertebrate Evolution (eds Andrews, S. M. et al.) 319–358 (Linnean Society, 1977).

  102. Rowe, T. B. Homology and evolution of the deep dorsal thigh musculature in birds and other reptilia. J. Morphol. 189, 327–346 (1986).

    Article  PubMed  Google Scholar 

  103. Dilkes, D. W. Appendicular myology of the hadrosaurian dinosaur Maiasaura peeblesorum from the Late Cretaceous (Campanian) of Montana. Trans. R. Soc. Edin. 90, 87–125 (1999).

    Article  Google Scholar 

  104. Carrano, M. T. & Hutchinson, J. R. Pelvic and hindlimb musculature of Tyrannosaurus rex (Dinosauria: Theropoda). J. Morphol. 253, 207–228 (2002).

    Article  PubMed  Google Scholar 

  105. Allen, V. et al. Comparative architectural properties of limb muscles in Crocodylidae and Alligatoridae and their relevance to divergent use of asymmetrical gaits in extant Crocodylia. J. Anat. 225, 569–582 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  106. Klinkhamer, A. J., Wilhite, D. R., White, M. A. & Wroe, S. Digital dissection and three-dimensional interactive models of limb musculature in the Australian estuarine crocodile (Crocodylus porosus). PLoS ONE 12, e0175079 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  107. George, J. C. & Berger, A. J. Avian Myology (Academic Press, 1966).

  108. Vanden Berge, J. C. & Zweers, G. A. in Handbook of Avian Anatomy: Nomina Anatomica Avium (eds Baumel, J. J. et al.) 189–250 (Publications of the Nuttall Ornithological Club 23, 1993).

  109. Wellnhofer, P. Archaeopteryx: The Icon of Evolution (Verlag Dr. Friedrich Pfeil, 2009).

  110. Padian, K. & Chiappe, L. M. The origin of birds and their flight. Sci. Am. 278, 38–47 (1998).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  112. Demuth, O. E., Rayfield, E. J. & Hutchinson, J. R. 3D hindlimb joint mobility of the stem-archosaur Euparkeria capensis with implications for postural evolution within Archosauria. Sci. Rep. 10, 15357 (2020).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  113. Gilmore, C. W. Osteology of the carnivorous Dinosauria in the United States National Museum, with special reference to the genera Antrodemus (Allosaurus) and Ceratosaurus. Bull. US Natl Museum 110, 1–159 (1920).

    Google Scholar 

  114. Barsbold, R., Osmólska, H., Watabe, M., Currie, P. J. & Tsogtbaatar, K. A new oviraptorosaur (Dinosauria, Theropoda) from Mongolia: the first dinosaur with a pygostyle. Acta Palaeontol. Polonica 45, 97–106 (2000).

    Google Scholar 

  115. Sullivan, R. M., Jasinski, S. E. & Van Tomme, M. P. A. A new caenagnathid Ojoraptorsaurus boerei, n. gen., n. sp. (Dinosauria, Oviraptorosauria), from the Upper Ojo Alamo Formation (Naashoibito Member), San Juan Basin, New Mexico. New Mexico Museum Nat. Hist. Sci. Bull. 53, 418–428 (2011).

    Google Scholar 

  116. Kardon, G. Muscle and tendon morphogenesis in the avian hind limb. Development 125, 4019–4032 (1998).

    Article  CAS  PubMed  Google Scholar 

  117. Alberch, P., Gould, S. J., Oster, G. F. & Wake, D. B. Size and shape in ontogeny and phylogeny. Paleobiology 5, 296–317 (1979).

    Article  Google Scholar 

  118. Romer, A. S. The development of tetrapod limb musculature—the thigh of Lacerta. J. Morphol. 71, 251–298 (1942).

Download references

Acknowledgements

We thank the Rockefeller Wildlife Refuge for Alligator eggs. Discussions with B. Wynd on ordination methods and variance–covariance matrices benefitted the final manuscript. We thank B. Pohl and the Wyoming Dinosaur Center for access to the Thermopolis specimen of Archaeopteryx, E. Updike and the Lawrence Livermore National Laboratory for laminography, J. Molnar for segmentation, D. Schwarz for access to the Berlin specimen, and A. Kirk and A. Baines for providing macrophotogrammetry. J.A. Gauthier provided useful comments and feedback throughout. M. Fox provided support for mounting and CT scanning at Yale. The Virginia Tech Paleobiology Research Group and H. Ueda provided discussion, and M. Stocker and S. Xiao gave feedback on earlier versions of the manuscript. C. Gordon provided feedback on the modularity discussion. M. Faunes and M. Cereghino provided assistance and feedback on the CLARITY protocol and segmentation. J. Nikolaus provided assistance with confocal microscopy. R. Diogo provided valuable feedback on earlier versions of this study. C.T.G. and R.M.C. were supported by National Science Foundation Graduate Research Fellowships. C.T.G. was supported by a National Science Foundation Postdoctoral Research Fellowship in Biology. J.F.B. was supported by ANID Fondecyt de Iniciacion 11180122. R.M.C. was supported by National Science Foundation grant EAR-0917538 and software donations from FEI and Capturing Reality.

Author information

Authors and Affiliations

  1. Department of Earth and Planetary Sciences, Yale University, New Haven, CT, USA

    Christopher T. Griffin, João F. Botelho, Michael Hanson, Matteo Fabbri, Daniel Smith-Paredes & Bhart-Anjan S. Bhullar

  2. Yale Peabody Museum of Natural History, Yale University, New Haven, CT, USA

    Christopher T. Griffin, João F. Botelho, Michael Hanson, Matteo Fabbri, Daniel Smith-Paredes & Bhart-Anjan S. Bhullar

  3. Department of Geosciences, Virginia Tech, Blacksburg, VA, USA

    Christopher T. Griffin & Sterling J. Nesbitt

  4. Departamento Biología Celular y Molecular, Pontificia Universidad Católica de Chile, Santiago, Chile

    João F. Botelho

  5. Nagaunee Integrative Research Center, Field Museum of Natural History, Chicago, IL, USA

    Matteo Fabbri

  6. Department of Integrative Biology, University of South Florida, Tampa, FL, USA

    Ryan M. Carney

  7. Division of Vertebrate Paleontology, American Museum of Natural History, New York, NY, USA

    Mark A. Norell

  8. RIKEN Center for Biosystems Dynamics Research, Kobe, Japan

    Shiro Egawa

  9. Department of Ecology and Evolutionary Biology, Brown University, Providence, RI, USA

    Stephen M. Gatesy

  10. Jackson School of Geosciences, The University of Texas at Austin, Austin, TX, USA

    Timothy B. Rowe

  11. Rockefeller Wildlife Refuge, Louisiana Department of Wildlife and Fisheries, Grand Chenier, LA, USA

    Ruth M. Elsey

Authors
  1. Christopher T. Griffin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. João F. Botelho
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael Hanson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Matteo Fabbri
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Daniel Smith-Paredes
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ryan M. Carney
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mark A. Norell
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Shiro Egawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Stephen M. Gatesy
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Timothy B. Rowe
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Ruth M. Elsey
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Sterling J. Nesbitt
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Bhart-Anjan S. Bhullar
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

C.T.G., J.F.B. and B.-A.S.B. designed the project. C.T.G., J.F.B. and B.-A.S.B. conceived and designed the experiments. C.T.G., J.F.B., M.H. and M.F. conducted experiments, and C.T.G. conducted analyses. S.M.G. assisted in planning of analyses and interpretation of data. C.T.G., J.F.B., M.H., M.F., R.M.C., M.A.N., S.E., D.-S.P., R.M.E., T.B.R., S.J.N. and B.-A.S.B. contributed material and/or material information. C.T.G. and B.-A.S.B. planned and wrote the manuscript with input from all authors.

Corresponding author

Correspondence to Bhart-Anjan S. Bhullar.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature thanks Rui Diogo and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data figures and tables

Extended Data Fig. 1 Growth series of Alligator mississippiensis embryonic pelvis, hindlimb and tail stained for cartilage and connective tissue.

A. Cartilage precursor and early cartilage (SOX-9, green) and cartilage (collagen II, blue). Approximate embryonic stages, top to bottom: F13 (15 days), F14 (16–17 days), F15 (18–20 days), F17 (22–23 days), F18 (25–26 days), F19 (27–28 days). B. Cartilage (collagen II, blue) and connective tissue (collagen I, purple). Approximate embryonic stages, top to bottom: F13 (15 days), F14 (16–17 days), F15 (18–20 days), F16 (21 days), F17 (22–23 days), F19 (27–28 days). [2 columns].

Extended Data Fig. 2 Growth series of Alligator mississippiensis embryonic pelvis, hindlimb and tail stained for skeletal muscles, cartilage and nervous tissues.

A. Cartilage (collagen II, blue) and skeletal muscle (MF-20, red). Approximate embryonic stages, top to bottom: F13 (15 days), F16 (21 days), F17 (22–23 days), F19 (27–28 days). B. Skeletal muscle (MF-20, red) and nervous tissue (NF-M, blue). Approximate embryonic stages, top to bottom: F13 (15 days), F15 (18–20 days), F16 (21 days), F17 (22–23 days). [2 columns].

Extended Data Fig. 3 Growth series of Coturnix coturnix japonica embryonic pelvis, hindlimb and tail stained for cartilage and connective tissue.

A. Cartilage precursor and early cartilage (SOX-9, green). Approximate embryonic stages, top to bottom: HH24 (4 days of development), HH28 (5.5 days), HH29–30 (5.5–6.5 days), HH30 (6–6.5 days), HH34 (7.5 days). B. Cartilage precursor and early cartilage (SOX-9) and cartilage (collagen II, blue; collagen IX, purple). Approximate embryonic stages, top to bottom: HH27 (5 days), HH29 (5.5–6 days), HH30 (6–6.5 days), HH31 (6.5 days), HH34 (7.5 days). C. Connective tissue (tenascin, blue; collagen I, purple). Approximate embryonic stages, top to bottom: HH24 (4 days), HH27 (5 days), HH29 (5.5–6 days), HH30 (6–6.5 days), HH32 (7 days). [2 columns].

Extended Data Fig. 4 Growth series of Coturnix coturnix japonica embryonic pelvis, hindlimb and tail stained for skeletal muscle, cartilage, connective tissue, and nervous tissue.

A. Skeletal muscle (MF-20; red) and cartilage precursor and early cartilage (SOX-9, green). Approximate embryonic stages, top to bottom: HH24 (4 days), HH28–29 (5.5–6 days), HH29 (5.5–6 days), HH30 (6–6.5 days) HH34 (7.5 days). B. Skeletal muscle (MF-20, red) and connective tissue (tenascin, blue; collagen I, purple). Approximate embryonic stages, top to bottom: HH24 (4 days), HH27 (5 days), HH29 (5.5–6 days), HH30 (6–6.5 days), HH32 (7 days). C. Nervous tissue (NF-M, blue) and cartilage precursor and early cartilage (SOX-9, green). Approximate embryonic stages, top to bottom: HH24 (4 days), HH28–29 (5.5–6 days), HH29 (5.5–6 days), HH30 (6–6.5 days) HH34 (7.5 days). [2 columns].

Extended Data Fig. 5 The distal ends of the pubis in Alligator mississippiensis remain unfused during early organogenesis of the pelvis.

A. Stage F14 (16–17 days of development) pelvis in right ventrolateral view (reversed). B. Stage F14 pelvis in right oblique ventrolateral view. C. Stage 16 (21 days) pelvis in right oblique anterolateral view. D. Stage 18 (24–26 days) pelvis ventral view. E. Stage 19 (27–28 days) pelvis in right anterolateral view. Blue stains are collagen II. [2 columns].

Extended Data Fig. 6 Embryological series of other avian taxa stained for cartilage precursor and early cartilage (SOX-9), skeletal muscle (MF-20), and nervous tissue (NF-M).

Note that the ancestral states described in Coturnix development (e.g., anteriorly short ilium, non-retroverted pubis, pubic ‘boot’) appear in early organogenetic stages of these taxa as well. A. Growth series of the Domestic Chicken (Gallus gallus domesticus), a galloanseriform. Approximate embryonic stage, top to bottom: HH29, HH29, HH34. B. Growth series of the Chilean Tinamou (Nothoprocta perdicaria), a paleognath. Approximate embryonic stage, top to bottom: HH30, HH34. B. Growth series of the Budgerigar (Melopsittacus undulatus), a neoavian. Approximate embryonic stage, top to bottom: HH31 (early), HH31 (late), HH35. [2 columns].

Extended Data Fig. 7 Geometric morphometrics with results of cluster analyses.

A. 2D geometric morphometrics with results of cluster analysis. Note that the PC1 axis is inverted for ease of comparison. B. 3D geometric morphometrics with results of cluster analysis. C. 3D geometric morphometrics with intermediate quail embryonic stages excluded from geometric morphometric analysis, with results of cluster analysis. [2 columns].

Extended Data Fig. 8 Results of 3D geometric morphometrics performed on partitions of landmarks.

A. Ilium landmarks (landmarks 1–5). B. Pubis landmarks (landmarks 6–9). C. Ischium landmarks (landmarks 10–13). D. Ilium and pubis landmarks (landmarks 1–9) E. Pubis and ischium landmarks (landmarks 6–13). F. Ilium and ischium landmarks (landmarks 1–5, 10–13). G. extremes of ilium and extremes of pubis landmarks (landmarks 1, 3, 7, 8). [2 columns].

Extended Data Fig. 9 Quantified ontogenetic allometric trajectories of Coturnix and Alligator pelvic development suggests that Coturnix ontogeny is characterized by heterochronic acceleration.

Both trajectories start at similar shapes, but Alligator shape change during ontogeny is minimal, whereas Coturnix pelvic shape changes greatly with a steep slope. This suggests that acceleration is present in avian pelvic ontogeny, as is expected for terminal addition117. The differing ontogenetic trajectories of Coturnix and Alligator suggests that the avian pelvis did not evolve via peramorphosis. This is supported by the observation that the Alligator pubis slightly proverts and the ilium becomes proportionally taller during ontogeny (Figs. 2, 4), as well as descriptions of Lacerta ontogeny indicating a similar conservatism in developmental trajectory118. [1 column].

Extended Data Fig. 10 Variance-covariance plots for paravians, other archosaurs, and ornithischians.

Note that paravians and other archosaurs are nearly identical, especially in direction, and ornithischians are often divergent. The pelvis does not depict a specific taxon, but illustrates how proportions and angles were measured. [2 columns].

Supplementary information

Supplementary Information

This file contains Supplementary Text 1–5, Supplementary Figs. 1–7 and Supplementary Tables 1–3.

Reporting Summary

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Griffin, C.T., Botelho, J.F., Hanson, M. et al. The developing bird pelvis passes through ancestral dinosaurian conditions. Nature 608, 346–352 (2022). https://doi.org/10.1038/s41586-022-04982-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41586-022-04982-w

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing