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.
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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.
All code is hosted on Dryad (https://doi.org/10.5061/dryad.xd2547dj2).
Gatesy, S. M. in Functional Morphology in Vertebrate Paleontology (ed. Thomason, J. J.) 219–234 (Cambridge University Press, 1995).
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).
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).
Ostrom, J. H. On a new specimen of the Lower Cretaceous theropod dinosaur Deinonychus antirrhopus. Breviora 439, 1–21 (1976).
Bunge, A. Untersuchungen zur Entwickelungsgeschichte des Beckengürtels der Amphibien, Reptilien, und Vögel. PhD thesis, Universität Dorpat (1880).
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).
Mehnert, E. Untersuchungen über die entwisklung des os pelvis der vögel. Morphologisches Jahrbuch 13, 259–295 (1887).
Gould, S. J. Ontogeny and Phylogeny (Harvard University Press, 1977).
Mayr, E. Recapitulation reinterpreted: the somatic program. Q. Rev. Biol. 69, 223–232 (1994).
Abzhanov, A. von Baer’s law for the ages: lost and found principles of developmental evolution. Trends Genet. 29, 712–722 (2013).
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).
Ksepka, D. T. Feathered dinosaurs. Curr. Biol. 30, R1347–R1353 (2020).
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).
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).
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).
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).
Louchart, A. & Viriot, L. From snout to beak: the loss of teeth in birds. Trends Ecol. Evol. 26, 663–673 (2011).
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).
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).
Mayr, G. Evolution of avian breeding strategies and its relation to the habitat preferences of Mesozoic birds. Evol. Ecol. 31, 131–141 (2017).
Gatesy, S. M. Caudofemoral musculature and the evolution of theropod locomotion. Paleobiology 16, 170–186 (1990).
Gatesy, S. M. & Dial, K. P. Locomotor modules and the evolution of avian flight. Evolution 50, 331–340 (1996).
Hutchinson, J. R. The evolution of locomotion in archosaurs. C. R. Palevol. 5, 519–530 (2006).
Hutchinson, J. R. & Gatesy, S. M. Adductors, abductors, and the evolution of archosaur locomotion. Paleobiology 26, 734–751 (2000).
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).
Gegenbaur, C. Gundriss der Vergleichenden Anatomie (Engelmann, 1878).
Huxley, T. H. Further evidence of the affinity between the dinosaurian reptiles and birds. Q. J. Geol. Soc. Lond. 26, 12–31 (1870).
Carroll, S. B. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134, 25–36 (2008).
Romer, A. S. The development of the thigh musculature of the chick. J. Morphol. Physiol. 43, 347–385 (1927).
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).
Kardong, K. V. Vertebrates: Comparative Anatomy, Function, Evolution 8th edn (McGraw-Hill Education, 2019).
Chung, K. et al. Structural and molecular interrogation of intact biological systems. Nature 497, 332–337 (2013).
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).
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).
Giffin, E. B. Postcranial paleoneurology of the Diapsida. J. Zool. 235, 389–410 (1995).
Carpenter, E. M. Hox genes and spinal cord development. Dev. Neurosci. 24, 24–34 (2002).
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).
Diogo, R., Ziermann, J., Molnar, J., Siomava, N. & Abdala, V. Muscles of Chordates: Development, Homologies and Evolution (Taylor & Francis, 2018).
Felice, R. N., Randau, M. & Goswami, A. A fly in a tube: macroevolutionary expectations for integrated phenotypes. Evolution 72, 2580–2594 (2018).
Olson, E. C. & Miller, R. L. Morphological Integration (University of Chicago Press, 1958).
Schlosser, G. in Modularity in Development and Evolution (eds Schlosser, G. & Wagner, G. P.) 519–582 (University of Chicago Press, 2004).
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).
Felice, R. N. et al. Evolutionary integration and modularity in the archosaur cranium. Integr. Comp. Biol. 59, 371–382 (2019).
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).
Iijima, M. & Kobayashi, Y. Convergences and trends in the evolution of the archosaur pelvis. Paleobiology 40, 608–624 (2014).
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).
Bjarnason, A. & Benson, R. A 3D geometric morphometric dataset quantifying skeletal variation in birds. MorphoMuseuM 7, e125 (2021).
Giffin, E. B. Endosacral enlrgements in dinosaurs. Mod. Geol. 16, 101–112 (1991).
Giffin, E. B. Paleoneurology: reconstructing the nervous systems of dinosaurs. Paleontol. Soc. Special Pub. 7, 229–242 (1994).
Ferguson, M. W. J. in Biology of the Reptilia Vol. 14 (eds Gans, C. et al.) 329–492 (John Wiley and Sons, 1985).
Hamburger, V. & Hamilton, H. L. A series of normal stages in the development of the chick embryo. J. Morphol. 88, 49–92 (1951).
Ainsworth, S. J., Stanley, R. L. & Evans, D. J. R. Developmental stages of the Japanese quail. J. Anat. 216, 3–15 (2010).
Dingerkus, G. & Uhler, D. Enzyme clearing of Alcian blue stained whole small vertebrates for demonstration of cartilage. Stain Technol. 52, 229–232 (1977).
Ovchinnikov, D. Alcian blue/Alizarin red staining of cartilage and bone in mouse. Cold Spring Harbor Protoc. 2009, pdb.prot5170 (2009).
Rigueur, D. & Lyons, K. M. Whole-mount skeletal staining. Methods Mol. Biol. 1130, 113–121 (2014).
Schultze, O. Ueber herstellung und conservirung durchsichtiger embryonen zum stadium der skeletbildung. Anatomischer Anzeiger 13, 3–5 (1897).
Horobin, R. W. in Educational Guide Special Stains and H&E 2nd edn (eds Kumar, G. L. & Kiernan, J. A.) 159–166 (Carpinteria, 2010).
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).
Maxwell, E. E. Comparative embryonic development of the skeleton of the domestic turkey (Meleagris gallopavo) and other galliform birds. Zoology 111, 1095–1113 (2008).
Maxwell, E. E. Ossification sequence of the avian order Anseriformes, with comparison to other precocial birds. J. Morphol. 269, 1095–1113 (2008).
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).
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).
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).
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).
Smits, P. et al. The transcription factors L-Sox5 and Sox6 are essential for cartilage formation. Dev. Cell 1, 277–290 (2001).
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).
Eames, B. F., De La Fuente, L. & Helms, J. A. Molecular ontogeny of the skeleton. Birth Defects Res. C 69, 93–101 (2003).
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).
Zhang, G., Eames, B. F. & Cohn, M. J. Evolution of vertebrate cartilage development. Curr. Topics Dev. Biol. 86, 15–42 (2009).
Ninomiya, Y., Showalter, A. & Olsen, B. in The Role of Extracellular Matrix in Development (ed. Trelstad, R. L.) 255–275 (Alan R. Liss, 1984).
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).
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).
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).
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).
Bookstein, F. L. Morphometric Tools for Landmark Data: Geometry and Biology (Cambridge University Press, 1997).
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).
Geomorph: software for geometric morphometric analyses (R package version 3.2.1) (2020).
Rohlf, F. J. The TPS series of software. Hystrix 26, 9–12 (2015).
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).
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).
Oksanen, J. et al. vegan: community ecology package (R package version 2.5-7). https://CRAN.R-project.org/package=vegan (2020).
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).
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).
Goodall, C. Procrustes methods in the statistical analysis of shape. J. R. Stat. Soc. B 53, 285–339 (1991).
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).
Friendly, M. HE plots for repeated measures designs. J. Stat. Softw. 37, 1–40 (2010).
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).
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).
Ezcurra, M. D. The phylogenetic relationships of basal archosauromorphs, with an emphasis on the systematics of proterosuchian archosauriforms. PeerJ 4, e1778 (2016).
Nesbitt, S. J. The early evolution of archosaurs: relationships and the origin of major clades. Bull. Am. Museum Nat. Hist. 352, 1–292 (2011).
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).
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).
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).
Cau, A. The assembly of the avian body plan: a 160-million-year long process. Boll. Soc. Paleontol. Ital. 57, 1–25 (2018).
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).
Perrin, A. Recherches sur les affinités zoologiques de l’Hatteria punctata. Ann. Sci. Nat. 20, 33–102 (1895).
Osawa, G. Beitrage zur Anatomie der Hatteria punctata. Arch. Mikrosk. Anat. 51, 48–691 (1898).
Gregory, W. K. & Camp, C. L. Studies in comparative myology and osteology III. Bull. Am. Museum Nat. Hist. 38, 447–563 (1918).
Byerly, T. The myology of Sphenodon puncatum. Univ. Iowa Stud. Nat. Hist. 11, 3–51 (1925).
Walker, A. D. in Problems in Vertebrate Evolution (eds Andrews, S. M. et al.) 319–358 (Linnean Society, 1977).
Rowe, T. B. Homology and evolution of the deep dorsal thigh musculature in birds and other reptilia. J. Morphol. 189, 327–346 (1986).
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).
Carrano, M. T. & Hutchinson, J. R. Pelvic and hindlimb musculature of Tyrannosaurus rex (Dinosauria: Theropoda). J. Morphol. 253, 207–228 (2002).
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).
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).
George, J. C. & Berger, A. J. Avian Myology (Academic Press, 1966).
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).
Wellnhofer, P. Archaeopteryx: The Icon of Evolution (Verlag Dr. Friedrich Pfeil, 2009).
Padian, K. & Chiappe, L. M. The origin of birds and their flight. Sci. Am. 278, 38–47 (1998).
Xu, X., You, H., Du, K. & Han, F. An Archaeopteryx-like theropod from China and the origin of Avialae. Nature 475, 465–470 (2011).
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).
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).
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).
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).
Kardon, G. Muscle and tendon morphogenesis in the avian hind limb. Development 125, 4019–4032 (1998).
Alberch, P., Gould, S. J., Oster, G. F. & Wake, D. B. Size and shape in ontogeny and phylogeny. Paleobiology 5, 296–317 (1979).
Romer, A. S. The development of tetrapod limb musculature—the thigh of Lacerta. J. Morphol. 71, 251–298 (1942).
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. R.M.C. was supported by National Science Foundation grant EAR-0917538 and software donations from FEI and Capturing Reality.
The authors declare no competing interests.
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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].
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].
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].
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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