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The developing bird pelvis passes through ancestral dinosaurian conditions

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.

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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.

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).

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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. R.M.C. was supported by National Science Foundation grant EAR-0917538 and software donations from FEI and Capturing Reality.

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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.

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Correspondence to Bhart-Anjan S. Bhullar.

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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].

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].

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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

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