Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Melanosome evolution indicates a key physiological shift within feathered dinosaurs

Subjects

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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Melanosome length observed in extant feathers, lepidosaur, testudine and archosaur skin, and mammalian hair.
Figure 2: SEM images of melanosomes from extant taxa representing the lowest-aspect-ratio and highest-aspect-ratio forms for each integumentary type.
Figure 3: Melanosomes from Jehol Group fossils.
Figure 4: Melanosome diversity across Amniota.

References

  1. 1

    Zhang, F. et al. Fossilized melanosomes and the colour of Cretaceous dinosaurs and birds. Nature 463, 1075–1078 (2010)

    ADS  CAS  Article  Google Scholar 

  2. 2

    Li, Q. et al. Plumage color patterns of an extinct dinosaur. Science 327, 1369–1372 (2010)

    ADS  CAS  Article  Google Scholar 

  3. 3

    Li, Q. et al. Reconstruction of Microraptor and the evolution of iridescent plumage. Science 335, 1215–1219 (2012)

    ADS  CAS  Article  Google Scholar 

  4. 4

    Ducrest, A.-L., Keller, L. & Roulin, A. Pleiotropy in the melanocortin system, coloration and behavioural syndromes. Trends Ecol. Evol. 23, 502–510 (2008)

    Article  Google Scholar 

  5. 5

    Stoddard, M. C. & Prum, R. O. How colorful are birds? Evolution of the avian plumage color gamut. Behav. Ecol. 22, 1042–1052 (2011)

    Article  Google Scholar 

  6. 6

    McGraw, K. J. in Bird Coloration. 1. Mechanisms and Measurements (eds Hill, G. E. & McGraw, K. J. ) 243–294 (Harvard Univ. Press, 2006)

    Google Scholar 

  7. 7

    Mills, M. G. & Patterson, L. B. Not just black and white: pigment pattern development and evolution in vertebrates. Semin. Cell Dev. Biol. 20, 72–81 (2009)

    CAS  Article  Google Scholar 

  8. 8

    Bagnara, J. T. & Hadley, M. E. Chromatophores and Color Change: The Comparative Physiology of Animal Pigmentation (Prentice-Hall, 1973)

    Google Scholar 

  9. 9

    Snyder, H. K. et al. Iridescent colour production in hairs of blind golden moles (Chrysochloridae). Biol. Lett. 8, 393–396 (2012)

    Article  Google Scholar 

  10. 10

    Clarke, J. A. et al. Fossil evidence for evolution of the shape and color of penguin feathers. Science 330, 954–957 (2010)

    ADS  CAS  Article  Google Scholar 

  11. 11

    Spearman, R. I. C. The Integument (Cambridge Univ. Press, 1973)

    Google Scholar 

  12. 12

    Xu, X., Zhou, Z. & Prum, R. O. Branched integumental structures in Sinornithosaurus and the origin of feathers. Nature 410, 200–204 (2001)

    ADS  CAS  Article  Google Scholar 

  13. 13

    Xu, X. et al. Basal tyrannosauroids from China and evidence for protofeathers in tyrannosauroids. Nature 431, 680–684 (2004)

    ADS  CAS  Article  Google Scholar 

  14. 14

    Ji, Q., Norell, M. A., Gao, K.-Q., Ji, S.-A. & Ren, D. The distribution of integumentary structures in a feathered dinosaur. Nature 410, 1084–1088 (2001)

    ADS  CAS  Article  Google Scholar 

  15. 15

    Zheng, X.-T., You, H.-L., Xu, X. & Dong, Z.-M. An Early Cretaceous heterodontosaurid dinosaur with filamentous integumentary structures. Nature 458, 333–336 (2009)

    ADS  CAS  Article  Google Scholar 

  16. 16

    Mayr, G., Peters, D. S., Plodowski, G. & Vogel, O. Bristle-like integumentary structures at the tail of the horned dinosaur Psittacosaurus. Naturwissenschaften 89, 361–365 (2002)

    ADS  CAS  Article  Google Scholar 

  17. 17

    Kellner, A. W. A. et al. The soft tissue of Jeholopterus (Pterosauria, Anurognathidae, Batrachognathinae) and the structure of the pterosaur wing membrane. Proc. R. Soc. Lond. B 277, 321–329 (2010)

    Google Scholar 

  18. 18

    Carney, R., Vinther, J., Shawkey, M. D., D’Alba, L. & Ackermann, J. New evidence on the colour and nature of the isolated Archaeopteryx feather. Nature Comm. 3, 637 (2012)

    ADS  Article  Google Scholar 

  19. 19

    R Development Core Team. R: A language and environment for statistical computing. (R Foundation for Statistical Computing, 2008)

  20. 20

    McNamara, M. E., Briggs, D. E. G., Orr, P. J., Field, D. J. & Wang, Z. Experimental maturation of feathers: implications for reconstructions of fossil feather colour. Biol. Lett. 9, 20130184

  21. 21

    Greenwold, M. H. & Sawyer, R. H. Linking the molecular evolution of avian beta (β) keratins to the evolution of feathers. J. Exp. Zool. Mol. Dev. Evol. 316, 609–616 (2011)

    CAS  Article  Google Scholar 

  22. 22

    Ito, S. & Wakamatsu, K. Quantitative analysis of eumelanin and pheomelanin in humans, mice, and other animals. Pigment Cell Res. 16, 523–531 (2003)

    Article  Google Scholar 

  23. 23

    Wolnicka-Glubisz, A., Peclo, A., Podkowa, D., Kolodziejczyk, L. M. & Plonka, P. M. Pheomelanin in the skin of Hymenochirus boettgeri (Amphibia:Anura:Pipidae). Exp. Dermatol. 21, 537–540 (2012)

    CAS  Article  Google Scholar 

  24. 24

    Roulin, A., Mafli, A. & Wakamatsu, K. Reptiles produce pheomelanin: evidence in the Eastern Hermann’s Tortoise. J. Herpetol. 47, 258–261 (2013)

    Article  Google Scholar 

  25. 25

    Yoshihara, C. et al. Elaborate color patterns of individual chicken feathers may be formed by the agouti signaling protein. Gen. Comp. Endocrinol. 175, 495–499 (2012)

    CAS  Article  Google Scholar 

  26. 26

    Manceau, M., Domingues, V. S., Mallarino, R. & Hoekstra, H. E. The developmental role of agouti in color pattern evolution. Science 331, 1062–1065 (2011)

    ADS  CAS  Article  Google Scholar 

  27. 27

    Hubbard, J. K., Uy, J. A. C., Hauber, M. E., Hoekstra, H. E. & Safran, R. J. Vertebrate pigmentation: from underlying genes to adaptive function. Trends Genet. 26, 231–239 (2010)

    CAS  Article  Google Scholar 

  28. 28

    Emaresi, G. et al. Pleiotropy in the melanocortin system: expression levels of this system are associated with melanogenesis and pigmentation in the tawny owl (Strix aluco). Mol. Ecol. 22, 4915–4930 (2013)

    CAS  Article  Google Scholar 

  29. 29

    Yabuuchi, M., Bando, K., Hiramatsu, M., Takahashi, S. & Takeuchi, S. Local agouti signaling protein/melanocortin signaling system that possibly regulates lipid metabolism in adipose tissues of chickens. J. Poult. Sci. 47, 176–182 (2010)

    CAS  Article  Google Scholar 

  30. 30

    Calder, W. A., III & Dawson, T. J. Resting metabolic rates of ratite birds: the kiwis and the emu. Biochem. Physiol. A 60, 479–481 (1978)

    Article  Google Scholar 

Download references

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

Authors

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.

Corresponding authors

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

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

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 figures and tables

Extended Data Figure 1 Sampling map of an unnamed turtle fossil, PKUP V1070 (top) and a lizard fossil, Yabeinosaurus sp. PKUP V1059 (bottom).

Numbers indicate integument sampling sites; melanosome data from all sites are presented in Fig. 4 and pooled for the per-taxon values given in Supplementary Table 2.

Extended Data Figure 2 Sampling map of a gliding lizard fossil, Xianglong zhaoi, PMOL 000666, counterpart (top) and the basal avialan, Confuciusornis sanctus, CUGB G20070001 (bottom).

Integument sampling sites are numbered. Numbers indicate integument sampling sites; melanosome data from all sites are presented in Fig. 4 and pooled for the per-taxon values given in Supplementary Table 2.

Extended Data Figure 3 Skin sample from the ornithischian dinosaur, Psittacosaurus lujiatunensis, PKUP V1050 (top) and from the ornithischian dinosaur, Psittacosaurus lujiatunensis, PKUP V1051 (bottom).

Numbers indicate integument sampling sites; melanosome data from all sites are presented in Fig. 4 and pooled for the per-taxon values given in Supplementary Table 2.

Extended Data Figure 4 Sampling map for two pterosaurs, PMOL AP00022 (top) and BMNHC PH000988 (bottom).

Numbers indicate integument sampling sites; melanosome data from all sites are presented in Fig. 4 and pooled for the per-taxon values given in Supplementary Table 2.

Extended Data Figure 5 Samples from filaments preserved in the neck region of a skeleton of the theropod dinosaur, Beipiaosaurus, BMNHC PH000911 (counter slab).

Numbers indicate integument sampling sites; melanosome data from all sites are presented in Fig. 4 and pooled for the per-taxon values given in Supplementary Table 2.

Extended Data Figure 6 Sampling map of the feathered maniraptoran dinosaur, Caudipteryx zoui, PMOL AD00020.

Numbers indicate integument sampling sites; melanosome data from all sites are presented in Fig. 4 and pooled for the per-taxon values given in Supplementary Table 2.

Extended Data Figure 7 Sampling map of (top) an unnamed enantiornithine bird, CUGB G20120001 and (bottom) an undescribed enantiornithine bird, CUGB P1201.

Numbers indicate integument sampling sites; melanosome data from all sites are presented in Fig. 4 and pooled for the per-taxon values given in Supplementary Table 2.

Extended Data Figure 8 Sampling map of an undescribed ornithurine bird, CUGB G20100053.

Numbers indicate integument sampling sites; melanosome data from all sites are presented in Fig. 4 and pooled for the per-taxon values given in Supplementary Table 2.

Extended Data Figure 9 Melanosome diameters and aspect ratios observed in extant feathers, lepidosaur, testudine and archosaur skin, and mammalian hair.

Melanosome diameters are shown in a, and aspect ratios are shown in b. Boxplot colours correspond with integument colour: black, brown, grey. For feathers, ‘penguin-like’ is shown in blue and iridescent is shown in purple. Lines are median values, boxes are quartiles, lines are range. Boxplots sharing the same letter (v, w, x, y, z) are not significantly different from one another.

Extended Data Figure 10 Exploration of the potential effects of taphonomy and sampling on the observed differences in melanosomes in skin, hair, filaments and feathers.

Top, melanosome diversity is adjusted to model taphonomic shrinkage of melanosomes suggested from experimental studies. Values for all fossil samples were adjusted (enlarged by 20%) based on the findings of ref. 18 (Supplementary Methods). Original data points are shown in colours and adjusted data are shown in grey. Grey regions indicate the extent of the total melanosome morphospace from the primary analyses. The pattern reported (i.e., increased diversity and higher-aspect-ratio forms only in Maniraptora and Mammalia) is not affected (Fig. 4, main text; n for each integumentary type is identical to the primary analysis). Bottom, to consider the effect of sampling on the observed pattern samples from near the thoracic region were removed from the database. Although there was no evidence to suggest that these samples were from internal organs, or that such organs were preserved, because melanosomes are present in some internal organs in extant taxa, the sensitivity of the results to removal these samples was explored. There was no effect on the pattern reported from the primary analysis (compare Fig. 4). Samples 1 and 2 from Yabeinosaurus sp. (PKUP V1059), sample 1 from Psittacosaurus lujiatunensis (PKUP V1050), samples 121, 122 and 123 from Caudipteryx zoui (PMOL AD00020), samples 11, 13 and 14 from an undescribed enantiornithine (CUGB P1201), samples 30 and 33 from an undescribed enantiornithine (CUGB G20120001), and samples 64–69, 89 and 90 from an undescribed ornithurine bird (CUGB G20100053) were removed from the database. Samples are colour coded as in Fig. 4, main text and adjusted n for subsampling analysis follows: extant mammal hair (blue, n = 719), skin from extant (dark green, n = 742) and extinct (light green, n = 605) lepidosaurian, testudine and archosaurian species, feathers in basal Paraves (yellow, n = 1,212), Confuciusornis and crown-ward extinct avialan taxa (orange, n = 1,376), extant Aves (bright red, n = 3,294) and flightless palaeognath birds (dark red, n = 107). Colours of silhouettes correspond with colours in scatterplots. Black indicated unsampled taxa or integumentary type (e.g., bristle structures on the tail of Psittacosaurus).

Related audio

Supplementary information

Supplementary Information

This file contains Supplementary Methods, Supplementary Tables 1-3 and additional references. (PDF 321 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Li, Q., Clarke, J., Gao, KQ. et al. Melanosome evolution indicates a key physiological shift within feathered dinosaurs. Nature 507, 350–353 (2014). https://doi.org/10.1038/nature12973

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