Letter | Published:

Melanosome evolution indicates a key physiological shift within feathered dinosaurs

Nature volume 507, pages 350353 (20 March 2014) | Download Citation

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Abstract

Inference of colour patterning in extinct dinosaurs1,2,3 has been based on the relationship between the morphology of melanin-containing organelles (melanosomes) and colour in extant bird feathers. When this relationship evolved relative to the origin of feathers and other novel integumentary structures, such as hair and filamentous body covering in extinct archosaurs, has not been evaluated. Here we sample melanosomes from the integument of 181 extant amniote taxa and 13 lizard, turtle, dinosaur and pterosaur fossils from the Upper-Jurassic and Lower-Cretaceous of China. We find that in the lineage leading to birds, the observed increase in the diversity of melanosome morphologies appears abruptly, near the origin of pinnate feathers in maniraptoran dinosaurs. Similarly, mammals show an increased diversity of melanosome form compared to all ectothermic amniotes. In these two clades, mammals and maniraptoran dinosaurs including birds, melanosome form and colour are linked and colour reconstruction may be possible. By contrast, melanosomes in lizard, turtle and crocodilian skin, as well as the archosaurian filamentous body coverings (dinosaur ‘protofeathers’ and pterosaur ‘pycnofibres’), show a limited diversity of form that is uncorrelated with colour in extant taxa. These patterns may be explained by convergent changes in the key melanocortin system of mammals and birds, which is known to affect pleiotropically both melanin-based colouration and energetic processes such as metabolic rate in vertebrates4, and may therefore support a significant physiological shift in maniraptoran dinosaurs.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (NSFC) grant 41272031, Fundamental Research Funds for Central Universities, Beijing Municipal Bureau of Human Resources, NSF grants EAR-1251895 and 1251922, Human Frontier Science Program (HFSP) grant RGY-0083, Air Force Office of Scientific Research (AFOSR) grant FA9550-13-1-0222, and the Jurassic Foundation. The Smithsonian Institution (J. F. Jacobs and A. Wynn) and San Diego Museum of Natural History (P. Unitt) provided extant samples. BMNHC PH000911 was photographed by M. Ellison.

Author information

Affiliations

  1. State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Beijing 100083, China

    • Quanguo Li
  2. Department of Geological Sciences, University of Texas at Austin, 1 University Station C1100, Austin, Texas 78712, USA

    • Julia A. Clarke
  3. School of Earth and Space Sciences, Peking University, Beijing 100871, China

    • Ke-Qin Gao
  4. Institute of Paleontology, Shenyang Normal University, Shenyang 110034, China

    • Chang-Fu Zhou
  5. Beijing Museum of Natural History, 126 Tianqiao South Street, Beijing 100050, China

    • Qingjin Meng
  6. Museum of China University of Geosciences (Beijing), 29 Xueyuan Road, 100083, China

    • Daliang Li
  7. Department of Biology and Integrated Bioscience Program, University of Akron, Akron, Ohio 44325-3908, USA

    • Liliana D’Alba
    •  & Matthew D. Shawkey

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Contributions

J.A.C., K.-Q.G., Q.L. and M.D.S. (listed alphabetically) jointly conceived the study and participated in manuscript preparation. Data for extant taxa were collected by L.D. and M.D.S. Data from fossil taxa were collected by Q.L., M.D.S., J.A.C., K.-Q.G., C.-F.Z., L.D. and Q.M. Data collection from fossils was supervised by Q.L., Q.M, C.-F.Z. and D.L.; J.A.C. and M.D.S. developed the analytical approach and assessed results jointly with Q.L. and K.-Q.G.; M.D.S, L.D. and Q.L. analysed the data.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Julia A. Clarke or Matthew D. Shawkey.

Specimens are permanently reposited at the public institutions indicated in the text and Supplementary Table 3; sampling is illustrated in the Extended Data Figures, and melanosome data are given in Supplementary Table 2 or have been made available previously3.

Extended data

Supplementary information

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  1. 1.

    Supplementary Information

    This file contains Supplementary Methods, Supplementary Tables 1-3 and additional references.

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DOI

https://doi.org/10.1038/nature12973

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