The developing bird pelvis passes through ancestral dinosaurian conditions – Nature.com


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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).
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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.
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
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
Department of Geosciences, Virginia Tech, Blacksburg, VA, USA
Christopher T. Griffin & Sterling J. Nesbitt
Departamento Biología Celular y Molecular, Pontificia Universidad Católica de Chile, Santiago, Chile
João F. Botelho
Nagaunee Integrative Research Center, Field Museum of Natural History, Chicago, IL, USA
Matteo Fabbri
Department of Integrative Biology, University of South Florida, Tampa, FL, USA
Ryan M. Carney
Division of Vertebrate Paleontology, American Museum of Natural History, New York, NY, USA
Mark A. Norell
RIKEN Center for Biosystems Dynamics Research, Kobe, Japan
Shiro Egawa
Department of Ecology and Evolutionary Biology, Brown University, Providence, RI, USA
Stephen M. Gatesy
Jackson School of Geosciences, The University of Texas at Austin, Austin, TX, USA
Timothy B. Rowe
Rockefeller Wildlife Refuge, Louisiana Department of Wildlife and Fisheries, Grand Chenier, LA, USA
Ruth M. Elsey
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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.
Correspondence to Bhart-Anjan S. Bhullar.
The authors declare no competing interests.
Nature thanks Rui Diogo and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
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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].
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].
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].
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].
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].
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].
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].
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].
This file contains Supplementary Text 1–5, Supplementary Figs. 1–7 and Supplementary Tables 1–3.
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Griffin, C.T., Botelho, J.F., Hanson, M. et al. The developing bird pelvis passes through ancestral dinosaurian conditions. Nature (2022). https://doi.org/10.1038/s41586-022-04982-w
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DOI: https://doi.org/10.1038/s41586-022-04982-w
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