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. 2018 May 25;9(1):2072.
doi: 10.1038/s41467-018-04443-x.

Fossilized skin reveals coevolution with feathers and metabolism in feathered dinosaurs and early birds

Maria E McNamara  1 , Fucheng Zhang  2 , Stuart L Kearns  3 , Patrick J Orr  4 , André Toulouse  5 , Tara Foley  5 , David W E Hone  6 , Chris S Rogers  7 , Michael J Benton  3 , Diane Johnson  8 , Xing Xu  9 , Zhonghe Zhou  10
Affiliations

Fossilized skin reveals coevolution with feathers and metabolism in feathered dinosaurs and early birds

Maria E McNamara et al. Nat Commun. .

Abstract

Feathers are remarkable evolutionary innovations that are associated with complex adaptations of the skin in modern birds. Fossilised feathers in non-avian dinosaurs and basal birds provide insights into feather evolution, but how associated integumentary adaptations evolved is unclear. Here we report the discovery of fossil skin, preserved with remarkable nanoscale fidelity, in three non-avian maniraptoran dinosaurs and a basal bird from the Cretaceous Jehol biota (China). The skin comprises patches of desquamating epidermal corneocytes that preserve a cytoskeletal array of helically coiled α-keratin tonofibrils. This structure confirms that basal birds and non-avian dinosaurs shed small epidermal flakes as in modern mammals and birds, but structural differences imply that these Cretaceous taxa had lower body heat production than modern birds. Feathered epidermis acquired many, but not all, anatomically modern attributes close to the base of the Maniraptora by the Middle Jurassic.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1
Phosphatised soft tissues in non-avian maniraptoran dinosaurs and a basal bird. a–h Backscatter electron images of tissue in Confuciusornis (IVPP V 13171; a, e, f), Beipiaosaurus (IVPP V STM31-1; b, g), Sinornithosaurus (IVPP V 12811; c, h) and Microraptor (IVPP V 17972A; d). a–d Small irregularly shaped patches of tissue. e Detail of tissue surface showing polygonal texture. f Focused ion beam-milled vertical section through the soft tissue showing internal fibrous layer separating two structureless layers. g, h Fractured oblique section through the soft tissues, showing the layers visible in f
Fig. 2
Fig. 2
Ultrastructure of the soft tissues in Confuciusornis (IVPP V 13171). a, b Backscatter electron micrographs; all other images are secondary electron micrographs. a, b Closely packed polygons. c Detail of polygons showing fibrous contents, with d interpretative drawing. e–g Polygon (e) with detail of regions indicated showing tonofibrils bridging (f) and abutting at (g) junction between polygons. h, i Helical coiling in tonofibrils. h Oblique view of polygon with central tonofibrils orientated perpendicular to the polygon surface. j, k Polygons showing stretching-like deformation
Fig. 3
Fig. 3
Corneocytes in extant birds. a–d Scanning electron micrographs of shed skin in extant zebra finch (Taeniopygia guttata (n = 1); a–d). a Corneocytes defining polygonal texture. b Central depression (arrow) marks position of pycnotic nucleus. c, d Shed skin flakes entrained within feathers
Fig. 4
Fig. 4
Schematic phylogeny, scaled to geological time, of selected coelurosaurs showing the pattern of acquisition of key modifications of the skin. The phylogeny is the most likely of the maximum likelihood models, based on minimum-branch lengths (mbl) and transitions occurring as all-rates-different (ARD). Claws and footpads are considered primitive in coelurosaurs. Available data indicate that modified keratinocytes, and continuous shedding, originated close to the base of the Maniraptora; this is predicted to shift based on future fossil discoveries towards the base of the Coelurosauria to include other feathered taxa
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