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Fibular reduction and the evolution of theropod locomotion

Nature (2024)Cite this article

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Abstract

Since Hampé’s classic developmental experiments in the mid-twentieth century1,2, the reduced avian fibula has sparked sustained curiosity3,4,5,6. The fibula transformed throughout dinosaur evolution from a columnar structure into its splint-like avian form, a change long thought to be of little biomechanical consequence3,6. Here we integrated comparative three-dimensional kinematic analyses with transitional morphologies from the fossil record to refute this assumption and show that the reduced fibula serves a crucial function in enabling extreme knee long-axis rotation (LAR). Extreme LAR is fundamental to avian locomotion and is regularly exploited by living birds to execute complex terrestrial manoeuvres7. We infer that the evolution of this capacity was preceded by restriction of the knee to hinge-like motion in early theropod dinosaurs, driven by the origin of a mid-shank articulation8 that precluded ancestral patterns of tibiofibular motion. Freeing of the fibula from the ankle joint later enabled mobilization of this initially static articulation and, in doing so, established a novel pattern of tibiofibular kinematics essential to the extreme levels of LAR retained by modern birds. Fibular reduction thus ushered in a transition to LAR-dominated three-dimensional limb control, profoundly altering the course of theropod locomotor evolution.

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Fig. 1: Crural architecture of extant reptiles.
Fig. 2: Intracrural motion in living reptiles.
Fig. 3: Articular raycasting analysis of archosaurian knee LAR.
Fig. 4: The evolutionary origin of extreme knee LAR in birds.

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Data availability

Helmeted guineafowl and American alligator calibration images, X-ray videos and CT files for both in vivo and cadaveric studies have been deposited in the XMAPortal at http://xmaportal.org/webportal in collections titled ‘Fibular Reduction’ under study identifiers BROWN20, BROWN58 and BROWN71. Green iguana X-ray data have been deposited in the Jena Collection of X-ray Movies at https://szeb.thulb.uni-jena.de and are available on request as described by ref. 54. Meshes for Marasuchus are available on request from J. Hutchinson, and meshes for Dinornis are available on request from the Collections Manager of the Natural History Collections of the Canterbury Museum; both have been published18. Meshes and/or CT files for all other fossil specimens are available on Morphosource at https://www.morphosource.org/ (Rahonavis (project ID 00000C784); Allosaurus, Deinonychus and Ichthyornis (project ID 000638782; open download)). Extant avian meshes are available for download from Morphosource (Poecile (media ID 000093666; https://www.morphosource.org/concern/media/000093666?locale=en)) or the Idaho Museum of Natural History Virtualization Laboratory (all other taxa) at https://virtual.imnh.iri.isu.edu/. Source data are provided with this paper.

Code availability

The custom oRelFast.mel Maya embedded language script used to calculate joint kinematics in this study is available at https://bitbucket.org/xromm/xromm_other_mel_scripts/src/main/misc_utilities/. XMALab is pre-existing software previously described52 and is available at https://bitbucket.org/xromm/xmaportal/src/master/, and the XROMM Maya Tools are pre-existing scripts available at https://bitbucket.org/xromm/xromm_mayatools/src/master/.

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Acknowledgements

We thank D. Baier for developing and maintaining the XROMM Maya Tools; J. Hermanson, S. Nesbitt, T. Owerkowicz, K. Roorda, M. Stocker and R. Wilhite for providing cadaveric archosaur specimens; J. Hutchinson for providing Marasuchus meshes; M. Fox and V. Rhue for assistance with micro-CT scanning of and access to YPM specimens; V. Allen, P. Falkingham, R. Kambic, J. Lomax, T. Roberts, H. Tsai and M. Turner for assistance with X-ray data collection; and C. Gordon, C. Griffin, K. Jenkins, M. Margulis-Ohnuma, D. Meyer, K. Middleton, Z. Morris, J. Napoli, A. Ruebenstahl, M. J. Schwaner and A. Schulz for helpful discussion. A.R.M. and S.M.G. were supported by the Bushnell Research and Education Fund. A.R.M. was supported by a US NSF GRFP and PRFB (DBI-2209144), a Sigma Xi Grant-in-Aid of Research, a Society of Vertebrate Paleontology Cohen Award for Student Research, an Association of Women Geoscientists/Paleontological Society Winifred Goldring Award, a Brown University Presidential Fellowship, and a Yale Institute for Biospheric Studies Gaylord Donnelley Postdoctoral Environmental Fellowship. S.M.G. (grants IOS-0925077, DBI-0552051, IOS-0840950, DBI-1262156 and EAR-1452119) and B.-A.S.B. (CAREER (DEB-2046868)) were also supported by the US NSF. J.A.N. was supported by the Volkswagen Foundation (AZ 90222), the Daimler and Benz Foundation (32-08/12) and the German Research Council (DFG EXC 1027).

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Authors and Affiliations

  1. Yale Institute for Biospheric Studies, Yale University, New Haven, CT, USA

    Armita R. Manafzadeh

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

    Armita R. Manafzadeh & Bhart-Anjan S. Bhullar

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

    Armita R. Manafzadeh & Bhart-Anjan S. Bhullar

  4. Department of Ecology, Evolution, and Organismal Biology, Brown University, Providence, RI, USA

    Stephen M. Gatesy

  5. Institut für Biologie, Humboldt Universität zu Berlin, Berlin, Germany

    John A. Nyakatura

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Contributions

A.R.M. and S.M.G. conceived the study and designed the experiments. A.R.M., S.M.G. and J.A.N. collected the X-ray data. A.R.M., S.M.G., J.A.N. and B.-A.S.B. collected the CT data. A.R.M. conducted the analyses and wrote the manuscript. All authors edited and approved the final manuscript.

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Correspondence to Armita R. Manafzadeh.

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Extended data figures and tables

Extended Data Fig. 1 In vivo intracrural kinematics in reptiles.

XROMM-derived kinematics measured from Iguana (a), Alligator (b), and Numida (c) for the sequences displayed in Supplementary Videos 1–3. Representative crural poses reproduced from Fig. 2 are marked on each graph; note that Alligator configuration ii precedes configuration i, temporally. All scale bars for crura are 1 cm. Data were originally collected from left limbs in Iguana and Numida but have been mirrored to match right-handed sign conventions following ref. 18. Following ref. 18, at the knee, Z rotation corresponds to flexion-extension, extension is positive; Y rotation corresponds to abduction-adduction, adduction is positive; and X rotation corresponds to long-axis rotation, external rotation is positive. Within the crus, Z rotation corresponds to pitch, distal fibula rotating anteriorly is positive; Y rotation corresponds to yaw, distal fibula rotating medially is positive; X rotation corresponds to long-axis rotation or roll, external rotation is positive; Z translation is mediolateral, lateral motion of the fibula is positive; Y translation is anteroposterior, anterior motion of the fibula is positive; and X translation is proximodistal, distal motion of the fibula is positive. Note the flipped vertical axis in graphs displaying Knee LAR versus intracrural LAR. Video frames figured are n = 1200 for Iguana, n = 266 for Alligator, and n = 226 for Numida.

Source Data

Extended Data Fig. 2 X-ray Reconstruction of Moving Morphology evidence for avian intracrural motion.

Scientific rotoscoping14 requires alignment of mesh models to the shadows of bones in X-ray videos. During the guineafowl sequence displayed in Fig. 2, the proximal fibula is visible in X-ray videos as a faint shadow lateral to the larger elements of the knee. When the left fibular mesh is properly aligned to its shadow in two video frames (i and ii; a), the fibular head nestles within the femoral fibular trochlea (b; posterior view; proper articulation indicated with arrows). However, if the intracrural configurations from these two frames are swapped, the fibular head either interpenetrates with the lateral femoral condyle or disarticulates from the femur (c; posterior view; articular errors indicated with circles). Time points i and ii match those in Fig. 2 (i = t1 and ii = t3) and Extended Data Fig. 1.

Extended Data Fig. 3 Morphology of the avian intracrural articulation.

Eight microcomputed tomography slices taken at five-millimetre intervals along a portion of a right helmeted guineafowl crus, demonstrating morphology of the articulation between the tibiotarsus (to the left in each slice) and the fibula (to the right in each slice). Slice positions are indicated on a 3-D model of the crus in posterior view, with the fibula coloured cyan as in Figs. 1, 2 and 4. The bright spot within the fibula in slice iv results from the presence of an implanted radiopaque marker for ex vivo XROMM analysis (see Methods).

Extended Data Fig. 4 Ex vivo intracrural kinematics in archosaurs.

XROMM-derived kinematics measured from manipulations of Alligator (a), compared against in vivo data reproduced from Extended Data Fig. 1 (b), and from manipulations of Numida (c), compared against in vivo data reproduced from Extended Data Fig. 1 (d), display differences in intracrural mobility between species. In the lefthand column, points falling parallel to the horizontal axis (bolded) reflect the fibula axially rotating perfectly in concert with the tibiotarsus/tibia, with no measured intracrural LAR, whereas points paralleling the 1:1 line (bolded) reflect no axial rotation between the fibula and the femur. Note that in the bird, a much larger range of intracrural motion allows the fibula to stay tightly nestled within the femoral fibular trochlea (as indicated by proximity to the 1:1 line throughout), although this capacity weakens somewhat with internal rotation at the knee (left-hand portion of the graph). Note that in the alligator, a negative slope in the X-Y intracrural translation graph (compared to the negligible slope in the same graph for the bird) captures the skewing motion of the fibula visible in Fig. 2 and Supplementary Video 2. Representative knee poses corresponding to those in Fig. 3 are marked on each graph in a and c. Sign conventions match those in Extended Data Fig. 1. Video frames figured are n = 19,789 for Alligator and n = 10,723 for Numida.

Source Data

Extended Data Fig. 5 Additional views of articular raycasts for archosaurian knee long-axis rotation.

a, Articular raycasts in the alligator (left) and bird (right) right knee joints. Posterior view. b, Target points of the rays shown on isolated femora. Caudal view. c, Full rays shown on isolated femora. Caudal view. d, Full rays shown on isolated crura. Proximal view. e, Origin points of the rays shown on isolated crura. Proximal view. Rays coloured by length as in Fig. 3, throughout.

Extended Data Fig. 6 Comparison of non-maniraptoran tetanuran and avian proximal tibias/tibiotarsi across body sizes.

a, Homologous medial and lateral proximal surfaces coloured on non-maniraptoran tetanuran tibias demonstrate consistently roughly linear medial articular surfaces (yellow). Redrawn after literature figures; sources listed in Supplementary Information. b, Homologous medial and lateral proximal surfaces colored on avian tibiotarsi demonstrate consistently curved medial articular surfaces (yellow). All scale bars are 1 cm, except for Poecile, which is 1 mm. Differences in proximal medial surface curvature in these two groups yield a stark difference in the inferred capacity of the medial femoral condyle to travel along an arc-like path between rows, summarized by potential trajectories marked on each surface, following Figs. 3 and 4.

Supplementary information

Supplementary Information

Supplementary Text and Supplementary Fig. 1.

Reporting Summary

Supplementary Video 1

An XROMM-derived sequence of in vivo iguana hindlimb skeletal motion, with focus on the right knee in lateral view. Fibula colored cyan as in Figs. 1, 2 and 4.

Supplementary Video 2

An XROMM-derived sequence of in vivo alligator hindlimb skeletal motion, with focus on the right knee in lateral view. Fibula colored cyan as in Figs. 1, 2 and 4.

Supplementary Video 3

An XROMM-derived sequence of in vivo bird hindlimb skeletal motion, with focus on the knee joints in posterior view. Fibulas colored cyan as in Figs.1, 2 and 4.

Supplementary Video 4

A sample of 500 frames from an XROMM-derived sequence of cadaveric alligator knee motion, including articular raycasting. Articular cartilage semi-transparent. Fibula colored cyan as in Figs. 1, 2 and 4. Rays colored by length as in Fig. 3.

Supplementary Video 5

A sample of 500 frames from an XROMM-derived sequence of cadaveric bird knee motion, including articular raycasting. Fibula colored cyan as in Figs. 1, 2 and 4. Rays colored by length as in Fig. 3.

Source data

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Manafzadeh, A.R., Gatesy, S.M., Nyakatura, J.A. et al. Fibular reduction and the evolution of theropod locomotion. Nature (2024). https://doi.org/10.1038/s41586-024-08251-w

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