Late Cretaceous bird from Madagascar reveals unique development of beaks

Abstract

Mesozoic birds display considerable diversity in size, flight adaptations and feather organization1,2,3,4, but exhibit relatively conserved patterns of beak shape and development5,6,7. Although Neornithine (that is, crown group) birds also exhibit constraint on facial development8,9, they have comparatively diverse beak morphologies associated with a range of feeding and behavioural ecologies, in contrast to Mesozoic birds. Here we describe a crow-sized stem bird, Falcatakely forsterae gen. et sp. nov., from the Late Cretaceous epoch of Madagascar that possesses a long and deep rostrum, an expression of beak morphology that was previously unknown among Mesozoic birds and is superficially similar to that of a variety of crown-group birds (for example, toucans). The rostrum of Falcatakely is composed of an expansive edentulous maxilla and a small tooth-bearing premaxilla. Morphometric analyses of individual bony elements and three-dimensional rostrum shape reveal the development of a neornithine-like facial anatomy despite the retention of a maxilla–premaxilla organization that is similar to that of nonavialan theropods. The patterning and increased height of the rostrum in Falcatakely reveals a degree of developmental lability and increased morphological disparity that was previously unknown in early branching avialans. Expression of this phenotype (and presumed ecology) in a stem bird underscores that consolidation to the neornithine-like, premaxilla-dominated rostrum was not an evolutionary prerequisite for beak enlargement.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Fig. 1: Cranium of the Cretaceous enantiornithine bird Falcatakely forsterae (UA 10015, holotype).
Fig. 2: Mosaic evolution of the avialan facial skeleton as depicted among select early branching forms.
Fig. 3: Geometric morphometric analyses of the facial shape of Falcatakely among paravians.

Data availability

UA 10015 is catalogued into the collections at the Université d’Antananarivo. Details regarding the development of the digital files and the derivatives of these files (such as DICOM or PLY) used as part of the study are included in the Supplementary Information and archived on the MorphoSource website (https://www.morphosource.org/Detail/ProjectDetail/Show/project_id/7894). Phylogenetic character information and parameters used in the analyses are provided in the Supplementary Information. Executable files for phylogenetic analyses, character–taxon matrices, an interactive three-dimensional morphospace plot and interactive three-dimensional PDFs are hosted on DRYAD (https://doi.org/10.5061/dryad.mkkwh70wg). This published study, including the novel genus (urn:lsid:zoobank.org:act:5BA26059-B428-4896-BFEA-2475419C61FC) and species (urn:lsid:zoobank.org:act:69314771-F0D8-4C15-946C-524164385FB7) along with the associated nomenclatural acts, have been registered in ZooBank: urn:lsid:zoobank.org:pub:4595D69E-FE12-4DAD-B155-89F084254F73.

References

  1. 1.

    Xu, X. et al. An integrative approach to understanding bird origins. Science 346, 1253293 (2014).

    PubMed  Google Scholar 

  2. 2.

    Zhou, Z., Clarke, J. & Zhang, F. Insight into diversity, body size and morphological evolution from the largest Early Cretaceous enantiornithine bird. J. Anat. 212, 565–577 (2008).

    PubMed  PubMed Central  Google Scholar 

  3. 3.

    Brusatte, S. L., O’Connor, J. K. & Jarvis, E. D. The origin and diversification of birds. Curr. Biol. 25, R888–R898 (2015).

    CAS  PubMed  Google Scholar 

  4. 4.

    O’Connor, J. K. in The Evolution of Feathers (eds Foth, C. & Rauhut, O. W. M.) 147–172 (Springer, 2020).

  5. 5.

    O’Connor, J. K. & Chiappe, L. M. A revision of enantiornithine (Aves: Ornithothoraces) skull morphology. J. Syst. Palaeontol. 9, 135–157 (2011).

    Google Scholar 

  6. 6.

    Huang, J. et al. A new ornithurine from the Early Cretaceous of China sheds light on the evolution of early ecological and cranial diversity in birds. PeerJ 4, e1765 (2016).

    PubMed  PubMed Central  Google Scholar 

  7. 7.

    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).

    PubMed  Google Scholar 

  8. 8.

    Young, N. M. et al. Embryonic bauplans and the developmental origins of facial diversity and constraint. Development 141, 1059–1063 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Mayr, G. Comparative morphology of the avian maxillary bone (os maxillare) based on an examination of macerated juvenile skeletons. Acta Zool. 101, 24–38 (2020).

    Google Scholar 

  10. 10.

    Hu, H., O’Connor, J. K. & Zhou, Z. A new species of Pengornithidae (Aves: Enantiornithes) from the Lower Cretaceous of China suggests a specialized scansorial habitat previously unknown in early birds. PLoS ONE 10, e0126791 (2015).

    PubMed  PubMed Central  Google Scholar 

  11. 11.

    Bailleul, A. M. et al. An Early Cretaceous enantiornithine (Aves) preserving an unlaid egg and probable medullary bone. Nat. Commun. 10, 1275 (2019).

    PubMed  PubMed Central  ADS  Google Scholar 

  12. 12.

    Hou, L., Chiappe, L. M., Zhang, F. & Chuong, C.-M. New Early Cretaceous fossil from China documents a novel trophic specialization for Mesozoic birds. Naturwissenschaften 91, 22–25 (2004).

    CAS  PubMed  ADS  Google Scholar 

  13. 13.

    O’Connor, J. K. et al. Phylogenetic support for a specialized clade of Cretaceous enantiornithine birds with information from a new species. J. Vertebr. Paleontol. 29, 188–204 (2009).

    Google Scholar 

  14. 14.

    O’Connor, J. K., Chiappe, L. M., Gao, C. & Zhao, B. Anatomy of the Early Cretaceous enantiornithine bird Rapaxavis pani. Acta Palaeontol. Pol. 56, 463–475 (2011).

    Google Scholar 

  15. 15.

    O’Connor, J. K., Wang, M. & Hu, H. A new ornithuromorph (Aves) with an elongate rostrum from the Jehol Biota, and the early evolution of rostralization in birds. J. Syst. Palaeontol. 14, 939–948 (2016).

    Google Scholar 

  16. 16.

    Field, D. J. et al. Complete Ichthyornis skull illuminates mosaic assembly of the avian head. Nature 557, 96–100 (2018).

    CAS  PubMed  ADS  Google Scholar 

  17. 17.

    Field, D. J., Benito, J., Chen, A., Jagt, J. W. M. & Ksepka, D. T. Late Cretaceous neornithine from Europe illuminates the origins of crown birds. Nature 579, 397–401 (2020).

    CAS  PubMed  ADS  Google Scholar 

  18. 18.

    Chiappe, L. M. & Witmer, L. M. Mesozoic Birds: Above the Heads of Dinosaurs (Univ. California Press, 2004).

  19. 19.

    Li, Z., Zhou, Z., Wang, M. & Clarke, J. A. A new specimen of large-bodied basal enantiornithine Bohaiornis from the Early Cretaceous of China and the inference of feeding ecology in Mesozoic birds. J. Paleontol. 88, 99–108 (2014).

    Google Scholar 

  20. 20.

    Wang, M., Hu, H. & Li, Z. A new small enantiornithine bird from the Jehol Biota, with implications for early evolution of avian skull morphology. J. Syst. Palaeontol. 14, 481–497 (2016).

    Google Scholar 

  21. 21.

    Wang, M., O’Connor, J. K. & Zhou, Z. A new robust enantiornithine bird from the Lower Cretaceous of China with scansorial adaptations. J. Vertebr. Paleontol. 34, 657–671 (2014).

    Google Scholar 

  22. 22.

    Rogers, R. R., Hartman, J. H. & Krause, D. W. Stratigraphic analysis of Upper Cretaceous rocks in the Mahajanga Basin, northwestern Madagascar: implications for ancient and modern faunas. J. Geol. 108, 275–301 (2000).

    CAS  PubMed  ADS  Google Scholar 

  23. 23.

    Gauthier, J. A. & de Queiroz, K. in New Perspectives on the Origin and Early Evolution of Birds: Proceedings of the International Symposium in Honor of John H. Ostrom (eds Gauthier, J. & Gall, L. F.). 7–41 (Peabody Museum of Natural History, Yale Univ., 2001).

  24. 24.

    Chiappe, L. M., Norell, M. A. & Clark, J. M. A new skull of Gobipteryx minuta (Aves: Enantiornithes) from the Cretaceous of the Gobi Desert. Am. Mus. Novit. 3346, 1–15 (2001).

    Google Scholar 

  25. 25.

    Wang, M. & Zhou, Z. A new enantiornithine (Aves: Ornithothoraces) with completely fused premaxillae from the Early Cretaceous of China. J. Syst. Palaeontol. 17, 1299–1312 (2019).

    Google Scholar 

  26. 26.

    Hieronymus, T. L. & Witmer, L. M. Homology and evolution of avian compound Rhamphothecae. Auk 127, 590–604 (2010).

    Google Scholar 

  27. 27.

    Wang, M., Zhou, Z.-H., O’Connor, J. K. & Zelenkov, N. V. A new diverse enantiornithine family (Bohaiornithidae fam. nov.) from the Lower Cretaceous of China with information from two new species. Vert. Palasiat. 52, 31–76 (2014).

    Google Scholar 

  28. 28.

    Wang, M. & Hu, H. A comparative morphological study of the jugal and quadratojugal in early birds and their dinosaurian relatives. Anat. Rec. 300, 62–75 (2017).

    Google Scholar 

  29. 29.

    Wang, Y. et al. A previously undescribed specimen reveals new information on the dentition of Sapeornis chaoyangensis. Cretac. Res. 74, 1–10 (2017).

    Google Scholar 

  30. 30.

    Hu, H., O’Connor, J. K., Wang, M., Wroe, S. & McDonald, P. G. New anatomical information on the bohaiornithid Longusunguis and the presence of a plesiomorphic diapsid skull in Enantiornithes. J. Syst. Palaeontol. 18, 1481–1495 (2020).

    Google Scholar 

  31. 31.

    Hu, H. et al. Evolution of the vomer and its implications for cranial kinesis in Paraves. Proc. Natl Acad. Sci. USA 116, 19571–19578 (2019).

    CAS  PubMed  Google Scholar 

  32. 32.

    Felice, R. N. & Goswami, A. Developmental origins of mosaic evolution in the avian cranium. Proc. Natl Acad. Sci. USA 115, 555–560 (2018).

    CAS  PubMed  Google Scholar 

  33. 33.

    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).

    PubMed  Google Scholar 

  34. 34.

    Mallarino, R. et al. Closely related bird species demonstrate flexibility between beak morphology and underlying developmental programs. Proc. Natl Acad. Sci. USA 109, 16222–16227 (2012).

    CAS  PubMed  ADS  Google Scholar 

  35. 35.

    Tokita, M., Yano, W., James, H. F. & Abzhanov, A. Cranial shape evolution in adaptive radiations of birds: comparative morphometrics of Darwin’s finches and Hawaiian honeycreepers. Phil. Trans. R. Soc. Lond. B 372, 20150481 (2017).

    Google Scholar 

  36. 36.

    Bell, A. & Chiappe, L. M. Statistical approaches for inferring ecology in Mesozoic birds. J. Syst. Palaeontol. 9, 119–133 (2011).

    Google Scholar 

  37. 37.

    O’Connor, J. K. The trophic habits of early birds. Palaeogeogr. Palaeoclimatol. Palaeoecol. 513, 178–195 (2019).

    Google Scholar 

  38. 38.

    Rogers, R. R. Fine-grained debris flows and extraordinary vertebrate burials in the Late Cretaceous of Madagascar. Geology 33, 297–300 (2005).

    ADS  Google Scholar 

  39. 39.

    Rogers, R. R., Krause, D. W., Curry Rogers, K., Rasoamiaramanana, A. H. & Rahantarisoa, L. Paleoenvironment and paleoecology of Majungasaurus crenatissimus (Theropoda: Abelisauridae) from the Late Cretaceous of Madagascar. J. Vertebr. Paleontol. 27, 21–31 (2007).

    Google Scholar 

  40. 40.

    Brusatte, S. L., Lloyd, G. T., Wang, S. C. & Norell, M. A. Gradual assembly of avian body plan culminated in rapid rates of evolution across the dinosaur–bird transition. Curr. Biol. 24, 2386–2392 (2014).

    CAS  PubMed  Google Scholar 

  41. 41.

    Turner, A. H., Makovicky, P. J. & Norell, M. A. A review of dromaeosaurid systematics and paravian phylogeny. Bull. Am. Mus. Nat. Hist. 371, 1–206 (2012).

    Google Scholar 

  42. 42.

    Ronquist, F. et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61, 539–542 (2012).

    PubMed  PubMed Central  Google Scholar 

  43. 43.

    Lewis, P. O. A likelihood approach to estimating phylogeny from discrete morphological character data. Syst. Biol. 50, 913–925 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Clarke, J. A. & Middleton, K. M. Mosaicism, modules, and the evolution of birds: results from a Bayesian approach to the study of morphological evolution using discrete character data. Syst. Biol. 57, 185–201 (2008).

    PubMed  Google Scholar 

  45. 45.

    Rambaut, A., Suchard, M. A., Xie, D. & Drummond, A. J. Tracer v.1.6. http://beast.community/tracer (2014).

  46. 46.

    O’Reilly, J. E. & Donoghue, P. C. J. The efficacy of consensus tree methods for summarizing phylogenetic relationships from a posterior sample of trees estimated from morphological data. Syst. Biol. 67, 354–362 (2018).

    PubMed  Google Scholar 

  47. 47.

    Goloboff, P. A., Farris, J. & Nixon, K. TNT, a free program for phylogenetic analysis. Cladistics 24, 774–786 (2008).

    Google Scholar 

  48. 48.

    Goloboff, P. A., Farris, J. S. & Nixon, K. C. TNT: tree analysis using new technology. version 1.1 (Willi Hennig Society Edition) http://www.lillo.org.ar/phylogeny/tnt/ (2008).

  49. 49.

    Goloboff, P. A. & Catalano, S. A. TNT version 1.5, including a full implementation of phylogenetic morphometrics. Cladistics 32, 221–238 (2016).

    Google Scholar 

Download references

Acknowledgements

We thank the Université d’Antananarivo, the Mahajanga Basin Project field teams and the villagers of the Berivotra Study Area for support; the ministries of Mines, Higher Education and Culture of the Republic of Madagascar for permission to conduct field research; the National Geographic Society (8597-09) and the US National Science Foundation (EAR–0446488, EAR–1525915, EAR–1664432) for funding; and M. Witton for drafting the line drawings used in Fig. 1 and Extended Data Figs. 1, 2. Collection of avian three-dimensional morphometric data was funded by European Research Council grant no. STG-2014-637171 (to A. Goswami). Full acknowledgments are provided in the Supplementary Information.

Author information

Affiliations

Authors

Contributions

P.M.O., A.H.T. and J.R.G. designed the project; P.M.O., A.H.T., J.R.G., R.R.R., D.W.K. and L.J.R. conducted the fieldwork. J.R.G. performed the mechanical preparation of the specimen; J.R.G. and P.M.O. conducted the digital preparation and interpretation of the specimen using microcomputed tomography and carried out the rapid prototyping of UA 10015; R.R.R. and L.J.R. provided geological data and taphonomic interpretation; P.M.O., A.H.T., J.R.G. and R.N.F. completed the laboratory work on and digital representation of the fossil and provided input on descriptions and comparisons; A.H.T. and P.M.O. contributed to the character coding and phylogenetic analysis; R.N.F. completed the morphometric analyses; P.M.O., A.H.T. and J.R.G. developed the manuscript, with contributions and/or editing from all authors.

Corresponding author

Correspondence to Patrick M. O’Connor.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature thanks Bhart-Anjan Bhullar and Daniel Field for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data figures and tables

Extended Data Fig. 1 Rostrum of the Cretaceous enantiornithine bird Falcatakely (UA 10015, holotype).

a, Reconstruction (not to scale) illustrating the preserved (in white) elements of the cranium. b, Digital polygon surface reconstruction (from microcomputed tomography scans) of the right nasal in rostrodorsal view (caudal to the top) highlighting the midline depression and dimpled surface texture. c, Digital polygon surface reconstruction of the right nasal in dorsal view illustrating the dimpled architecture on the frontal and rostral portions, which extends laterally onto the lacrimal. d, Digital polygon surface reconstruction of the right facial elements in right lateral view to illustrate the shape and inter-element relationships of the nasal, maxilla and lacrimal (note the surface texture of the right maxilla with neurovascular sulci broadly expressed over the lateral surface, deep to the inferred keratinous covering (that is, beak)). e, Digital polygon surface reconstruction of the lower lateral face to highlight arrangement of the maxilla, lacrimal, jugal and postorbital (all elements from the right side). f, Digital polygon surface reconstruction of left maxilla and premaxilla articulation (rostral to the left). AOF, antorbital fenestra; cdp, caudodorsal process of the lacrimal; cp, choanal process of the palatine; ect, ectopterygoid; EN, external nares; ITF, infratemporal fenestra; fpn, frontal process of the nasal; inb, internarial bar; jpmx, jugal process of the maxilla; ju, jugal; lbo, lacrimal boot; lc, lacrimal; ld, lacrimal dimpling; le, lacrimal excavation; lf, lacrimal foramen; mpmx, midline premaxilla; mx, maxilla; mxpj, maxillary process of the jugal; na, nasal; nd, nasal dimpling; nf, nasal fossa; nvs, neurovascular sulci; pal, palatine; pmpm, premaxillary process of the maxilla; pmx, premaxilla; po, postorbital; qj, quadratojugal; rdp, rostrodorsal process of the lacrimal; rpn, rostral process of the nasal; tm, tomial margin; to, tooth; vr, ventral ramus of the lacrimal.

Extended Data Fig. 2 Palatal and lateral facial regions of the Cretaceous enantiornithine bird Falcatakely (UA 10015, holotype).

a, Digital polygon surface reconstruction (from microcomputed tomography scans) of the palate and lateral face in ventral view. b, Reconstructed outline drawing of Falcatakely in palatal view (shaded regions are not preserved). c, Digital polygon surface reconstruction of internal aspect of left facial skeleton (premaxilla, maxilla and nasal) and palate in right lateral view. The left and right sides are indicated as (l) and (r), respectively. The dashed line in c represents the approximate contour of the caudal margin (that is, the ventral ramus of the lacrimal) of the antorbital fenestra. Scale bar, 5 mm; the scale bar is representative for a and c; the reconstruction in b is not to the same scale. AOF, antorbital fenestra; bs, basisphenoid rostrum; cp, choanal process of the (right) palatine; ect, ectopterygoid; EN, external nares; jpmx, jugal process of the maxilla; mpmx, midline premaxilla; mx, maxilla; na, nasal; pal, palatine; pmx, premaxilla; pter, pterygoid; to, tooth; up, uncinate process of the ectopterygoid; vm, vomers.

Extended Data Fig. 3 Majority- rule tree of Falcatakely among coelurosaurians from the Bayesian analysis of the TWiG matrix.

Clades outside of the Avialae are collapsed for brevity. Posterior probabilities are placed above the nodes.

Extended Data Fig. 4 Majority -rule tree of Falcatakely among avialans from the Bayesian analysis of a modified matrix that was previously published.

A matrix modified from a previous study25 was used. Posterior probabilities are placed above the nodes.

Extended Data Fig. 5 Geometric morphometric analysis of rostrum shape in Falcatakely among avians.

Plot of the first two principal components of the three-dimensional landmark analysis of total rostrum shape of Falcatakely and extant avian taxa. Whereas the unique configuration of the maxilla and premaxilla in Falcatakely is more similar to those of non-avialan paravians (Fig. 3), the overall three-dimensional rostrum phenotype occupies the morphospace that is converged on by subsequent radiations of neornithine birds (Supplementary Data). See Supplementary Information for analytical protocols.

Extended Data Fig. 6 Landmarking procedure for three-dimensional geometric morphometric analysis in dorsal and lateral views.

a, Dorsal view. b, Lateral view. Red spheres represent anatomical (type I) landmarks; yellow spheres are sliding semi-landmarks.

Supplementary information

Supplementary Information

This file includes details related to the provenance of the specimens, preparation (mechanical and digital) of the specimen, and the parameters of both the geometric morphometric and phylogenetic analyses undertaken for the publication. Location:NPG website and DRYAD.

Reporting Summary

Supplementary Data

An interactive morphopace plot of Falcatakely forsterae and extant avian taxa (HTML format). Also available at https://doi.org/10.5061/dryad.mkkwh70wg.

Video 1

Polygon surface model reconstruction (from CT data) of Falcatakely forsterae, as preserved, with rotation around a dorsoventral axis (relative to left maxilla). Location: NPG Website and DRYAD.

Video 2

Polygon surface model reconstruction (from CT data) of Falcatakely forsterae, Beauchêne-style, with rotation around a dorsoventral axis axis (relative to left maxilla). Location: NPG Website and DRYAD.

Video 3

Polygon surface model reconstruction (from CT data) of Falcatakely forsterae, as preserved, with rotation around a mediolateral axis (relative to left maxilla). Location: NPG Website and DRYAD.

Video 4

Polygon surface model reconstruction (from CT data) of Falcatakely forsterae, Beauchêne-style, with rotation around a mediolateral axis (relative to left maxilla). Location: NPG Website and DRYAD.

Video 5

Polygon surface model reconstruction (from CT data) of Falcatakely forsterae, as preserved, with rotation around a rostrocaudal axis (relative to left maxilla). Location: NPG Website and DRYAD.

Video 6

Polygon surface model reconstruction (from CT data) of Falcatakely forsterae, Beauchêne-style, with rotation around a rostrocaudal axis (relative to left maxilla). Location: NPG Website and DRYAD.

Video 7

Animation of in-situ to Beauchêne-style state changes in polygon reconstructions (relative to left maxilla). Location: NPG Website and DRYAD.

Video 8

Montage highlighting stages of data recovery used for study of Falcatakely forsterae. Location: NPG Website and DRYAD.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

O’Connor, P.M., Turner, A.H., Groenke, J.R. et al. Late Cretaceous bird from Madagascar reveals unique development of beaks. Nature 588, 272–276 (2020). https://doi.org/10.1038/s41586-020-2945-x

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing