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Decoupling the skull and skeleton in a Cretaceous bird with unique appendicular morphologies

Nature Ecology & Evolution volume 7, pages 20–31 (2023)Cite this article

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Abstract

The Cretaceous is a critical time interval that encompasses explosive diversifications of terrestrial vertebrates, particularly the period when the earliest-branching birds, after divergence from their theropod ancestors, evolved the characteristic avian Bauplan that led eventually to their global radiation. This early phylogenetic diversity is overwhelmed by the Ornithothoraces, consisting of the Enantiornithes and Ornithuromorpha, whose members evolved key derived features of crown birds. This disparity consequently circumscribes a large morphological gap between these derived clades and the oldest bird Archaeopteryx. The non-ornithothoracine pygostylians, with an intermediate phylogenetic position, are key to deciphering those evolutionary transformations, but progress in their study has been hampered by the limited diversity of known fossils. Here we report an Early Cetaceous non-ornithothoracine pygostylian, Cratonavis zhui gen. et sp. nov., that exhibits a unique combination of a non-avialan dinosaurian akinetic skull with an avialan post-cranial skeleton, revealing the key role of evolutionary mosaicism in early bird diversification. The unusually elongated scapular and metatarsal one preserved in Cratonavis highlights a breadth of skeletal plasticity, stemming from their distinct developmental modules and selection for possibly raptorial behaviour. Mapped changes in these two elements across theropod phylogeny demonstrate clade-specific evolutionary lability.

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Fig. 1: Holotype of Cratonavis zhui, IVPP V31106.
Fig. 2: Cranial anatomy of Cratonavis.
Fig. 3: Time-calibrated Mesozoic avialan phylogeny showing the position of Cratonavis.
Fig. 4: Evolution of scapula across theropod dinosaurs.
Fig. 5: Evolution of metatarsals across theropod dinosaurs and ecological inference of Cratonavis.

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Data availability

The specimen (IVPP V31106) described in this study is archived and available on request from the Institute of Vertebrate Paleontology and Paleoanthropology (IVPP), Chinese Academy of Sciences, Beijing, China. The data matrix used in the phylogenetic analysis is provided in Supplementary Information. The CT scanning results are archived and available on Open Science Framework (https://osf.io/6jd4h/?view_only=a68708fb3f8f4a4e88494ba44f85e624) or request from the corresponding author. This published work and the nomenclatural acts it contains have been registered in ZooBank, the proposed online registration system for the International Code of Zoological Nomenclature (ICZN). The ZooBank Life Science Identifiers (LSIDs) can be resolved and the associated information viewed through any standard web browser by appending the LSID to the prefix http://zoobank.org/. The LSIDs for this publication are: urn:lsid:zoobank.org:pub:2F4C81B7-E844-470C-9D35-FFAE62F04781.

Code availability

The R code that we used in comparative analyses is archived and available on OSF (https://osf.io/6jd4h/?view_only=a68708fb3f8f4a4e88494ba44f85e624).

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Acknowledgements

We thank P. Yin for help with CT scanning, and W. Gao for photographing. This research is supported by the National Natural Science Foundation of China (42288201), the Key Research Program of Frontier Sciences, CAS (ZDBS-LY-DQC002) and the Tencent Foundation (through the XPLORER PRIZE).

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Author notes

  1. These authors contributed equally: Zhiheng Li, Min Wang.

Authors and Affiliations

  1. Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, China

    Zhiheng Li, Min Wang, Thomas A. Stidham & Zhonghe Zhou

  2. Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, Beijing, China

    Zhiheng Li, Min Wang, Thomas A. Stidham & Zhonghe Zhou

  3. University of Chinese Academy of Sciences, Beijing, China

    Thomas A. Stidham

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  1. Zhiheng Li
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Contributions

M.W. conceived the project; Z.L. and M.W. conducted the digital reconstruction; M.W. collected the data; M.W. performed the phylogenetic analysis and comparative analyses; M.W., Z.L., T.A.S. and Z.Z. wrote the manuscript.

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Correspondence to Min Wang.

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Extended data

Extended Data Fig. 1 Additional cranial anatomy of Cratonavis zhui, IVPP V31106.

a, Photograph. b, c, CT Isosurface of the whole skull in dorsal (a) and (b) ventral views. ba, basisphenoid-parasphenoid; bp, basipterygoid process; car, caudal ramus of lacrimal; de, dentary; ecp, ectopterygoid; fp, frontal process of premaxilla; fr, frontal; jmx, jugal process of maxilla; ju, jugal; jup, jugal process of postorbital; lc, lacrimal; mx, maxilla; na, nasal; pa, palatine; pi, parietal; pm, premaxilla; pmd, post-dentary mandible; po, postorbital; poq, postorbital process of jugal; pr, parasphenoid rostrum; pt, pterygoid; qju, quadratojugal process of jugal; qu, quadrate; quj, quadratojugal; rea, retroarticular process; sqq, squamosal process of quadratojugal; sr, subcellar recess; vo, vomer; l/r, left/right side. The arrowhead (a) denotes the lateral flange of the lacrimal. Scale bars, 10 mm (a–c).

Extended Data Fig. 2 CT scanning of pectoral region of C. zhui.

am, alular metacarpal; bi, bicipital tubercle; co, coracoid; dp, deltopectoral crest; dv, dorsal vertebra; fu, furcula; gl, glenoid; hu, humerus; ma, major metacarpal; m1 to m3, major digit phalanx 1 to 3; mi, minor metacarpal; mi1, minor digit phalanx 1; ol, olecranon; ra, radius; rd, radiale; sp, scapula; uc, uncinate; un, ulna; l/r, left/right side. The arrowheads denote the lateral fossae of the dorsal centra. Scale bar, 10 mm.

Extended Data Fig. 3 Additional pelvis and hindlimb anatomy of C. zhui.

a, Photograph. b, CT Scanning. fe, femur; fi, fibula; il, ilium; isp, ischiatic peduncle; mt I–V, metatarsal I to V; pop, postacetabular process; prp, preacetabular process; pt, posterior trochanter; pu, pubis; pup, pubic peduncle; py, pygostyle; ti, tibiotarsus; 1–8, sacral vertebrae one to eight; l/r, left/right side. Scale bar, 10 mm.

Extended Data Fig. 4 Time-calibrated phylogeny of theropod dinosaurs.

The phylogeny is a super tree encompassing major theropod groups that preserve complete appendicular elements used as the backbone for comparative analysis (see Methods).

Extended Data Fig. 5 Evolution of scapula across theropod dinosaurs.

Scapula length changes among major theropod groups (line drawing of scapulocoracoid/scapula scaled with humerus in selected taxa). The phylogenetical signals were quantified using the Blomberg’s K and Pagel’s lambd with P-value of the likelihood radio test. Node name: a: Allosauroidea, b: Tyrannosauroidae, c: Compsognathidae, d: Therizinosauria, e: Alvarezsauria, f: Ornithomimosauria, g: Oviraptorosauria, h: Scansoriorpterygidae, i: Troodontidae, j: Dromaeosauridae.

Extended Data Fig. 6 Scaling relationship between scapula and humerus/femur length across theropod dinosaurs using phylogenetic generalized least squares (pgls).

a, Scapula against humerus. b, Scapula against femur. Statistically significant relationship is denoted by p-value (*<0.01).

Extended Data Fig. 7 Evolution of metatarsals across theropod dinosaurs.

Changes of metatarsal I length along the line to early avialans (metatarsal I and hallux colored in red and green, respectively). The phylogenetical signals were quantified using the Blomberg’s K and Pagel’s lambd with P-value of the likelihood radio test. Node name: a: Allosauroidea, b: Tyrannosauroidae, c: Compsognathidae, d: Therizinosauria, e: Alvarezsauria, f: Ornithomimosauria, g: Oviraptorosauria, h: Scansoriorpterygidae, i: Troodontidae, j: Dromaeosauridae.

Extended Data Fig. 8 Changes of metatarsal I length across theropod dinosaurs.

a, Metatarsals I/III length ratio mapped onto time-calibrated theropod phylogeny. b, Size and phylogenetically corrected metatarsal I length mapped onto time-calibrated paravian phylogeny. The phylogenetical signals were quantified using the Blomberg’s K and Pagel’s lambd with P-value of the likelihood radio test.

Extended Data Fig. 9 Scaling relationship between metatarsals I and III length across theropod dinosaurs.

Results using the phylogenetic generalized least squares regression (pgls). Statistically significant relationship is denoted by p-value (*<0.01).

Extended Data Fig. 10 Results of canonical variate analysis to predicate the ecologies of modern bird samples.

The modern samples can be 87.5% correctly assigned to their original ecological classifications using selected morphological traits.

Supplementary information

Supplementary Information

Supplementary Note 1, Supplementary Tables 1–5, supplementary information about the morphological characters and dataset used in the phylogenetic analyses, and references.

Reporting Summary

Supplementary Tables 2 and 3

Supplementary Table 2. Appendicular element length dataset of theropods used in phylogenetic comparative analyses. Supplementary Table 3. Dataset used in morphometric analysis.

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Li, Z., Wang, M., Stidham, T.A. et al. Decoupling the skull and skeleton in a Cretaceous bird with unique appendicular morphologies. Nat Ecol Evol 7, 20–31 (2023). https://doi.org/10.1038/s41559-022-01921-w

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