Australia: The Land Where Time Began

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Feathered Dinosaurs and Early Birds – Coevolution with Feathers and Metabolism Revealed by Fossilised Skin

The evolution of feathers in modern birds is associated with complex adaptations of the skin. Insights into the evolution of feathers in non-avian dinosaurs and basal birds have been provided by the discovery of fossilised feathers, though it is not clear how associated integumentary adaptations evolved. In this paper McNamara et al. report the discovery of fossil skin which was preserved with remarkable nanoscale fidelity, in 3 maniraptoran non-avian dinosaurs and a basal bird from the cretaceous Jehol biota of China. The skin is comprised of desquamating epidermal comeocytes that preserved the cytoskeletal array of α-keratin tonofibrils that were helically coiled. It is confirmed by this structure that basal birds and non-avian dinosaurs shed small epidermal flakes as in mammals and birds of the present, though it is implied by structural difference that these taxa from the Cretaceous had lower production of heat by the body than is the case in birds of the present. Many, though not all, anatomically modern attributes were acquired by feathered epidermis close to the base of Maniraptora by the Middle Jurassic.

In vertebrates the integument is a complex multilayered organ that functions in homoeostasis, resisting mechanical stress and preventing attack by pathogens (Sawyer et al., 1986). Recurrent anatomical innovation of novel tissue structures such as scales, feathers and hair, its evolution, characterise its evolution, that are linked to major evolutionary radiations (Landman, 1986). Feathers are associated with structural, biochemical and functional modifications of the skin (Landman, 1986), such as a lipid-rich corneous layer, which is characterised by continuous shedding (Menon, Brown & Elias, 1986). Aspects of early feather evolution have been illuminated by evo-devo studies (Prum & Brush, 2002) and fossilised feathers, though the way in which the skin of basal birds and feathered non-avian dinosaurs evolved in tandem with feathers has not received much attention. As is the case with mammals, the skin of birds is thinner than in most reptiles and is shed in millimetre-scale flakes, which are comprised of shed corneocytes, i.e., keratinocytes that are terminally differentiated,  that are smaller than large patches or a whole-skin moult (Landman, 1986). In crocodilians and chelonians there is also desquamation of small patches, and it is considered primitive to synchronised cyclical skin shedding in squamates (Alibardi & Gill, 2007). Crocodilians and birds are the groups that bracket phylogenetically non-avian-dinosaurs and birds, both possess the basal condition; it is suggested by parsimony that this mechanism of skin shedding was shared with non-avian dinosaurs.

The increase in metabolic rate towards a true endothermic physiology, as in modern birds, during the evolution of dinosaurs was associated with profound changes in the integumentary structure (Wu et al., 2004) that relate to a subcutaneous hydraulic skeletal system, an intricate dermo-muscle system, and a lipid-rich corneous layer that is characterised by continuous shedding (Menon, Brown & Elias, 1986). However, the pattern of timing of acquisition of these ultrastructural skin characters is not well resolved and there is no a priori reason to assume that the ultrastructure of the skin of feathered non-avian dinosaurs and early birds would have resembled that of their modern counterparts. It is usual for dinosaur skin to be preserved as an external mould (Martill, Batten & Loydell, 2000), and only rarely as organic remains (Lingham-Soliar & Plodowski, 2010; Martill, 1991) or in authentic minerals (Manning et al., 2009; Schweitzer, 2011; Chiappe et al., 1998). Dinosaur skin is only rarely investigated at the ultrastructural level (Schweitzer, 2011), though mineralised fossil skin can retain (sub-) cellular anatomical features (McNamara et al., 2016; Navalόn et al., 2015). Critically, in spite of reports of preserved epidermis in a non-feathered dinosaur (Martill, Batten & Loydell, 2000), there is no known evidence of the epidermis (Lucas & Strettenheim, 1972) in basal birds or of preserved skin in feathered non-avian dinosaurs. Therefore, the coevolutionary history of skin and feathers is to a large extent unknown.

In this paper McNamara et al. report the discovery of fossilised skin in the feathered non-avian maniraptoran dinosaurs Beipiaosaurus, Sinomithosaurus and Microraptor, and the bird Confuciusornis from the Jehol biota from the Early Cretaceous. It is revealed by the ultrastructure of the preserved tissues that feathered skin had evolved many, though not all, modern attributes by the origin of the Maniraptora in the Middle Jurassic.

Evolutionary implications of fossil corneocytes structure

Key adaptations that are found in the counterparts of corneocytes in extant birds and mammals are exhibited in fossil comeocytes, especially their flattened polygonal geometry and fibrous cell contents which are consistent with α-keratin tonofibrils (McNamara et al., 2016). Also, robust intercellular connections are shown in the fossil tonofibrils (as in extant examples (Ishida et al., 2002)) and form a continuous scaffold across the corneocytes sheet. Contrasting with this, in extant reptiles, corneocytes contain a homogenous mass of β-keratin, as well as additional proteins that are present within the cell envelope, and during development fuse to form mature β-layers that lack distinct cell boundaries (Alibardi & Toni, 2007). A distinctly avian feature that is not present in modern reptiles (but see Alibardi, 2003) is the retention of pycnotic nuclei in fossil corneocytes.

It is considered that epidermal morphogenesis and differentiation diverged in sauropsids and therapsids (Alibardi & Toni, 2006). The data of McNamara et al. support other evidence which suggests that shared epidermal features in birds and mammals indicate convergent evolution (Maderson & Alibardi, 2000), suggesting that lipid-rich corneocyte contents may be derived evolutionarily (Maderson & Alibardi, 2000) in birds and feathered non-avian maniraptorans. It has been suggested by evo-devo studies that the avian epidermis could have arisen from the expansion of hinge regions in ‘Protofeather’-bearing scaly skin (Alibardi, 2003). The data of McNamara et al. show that the epidermis of basal birds and non-avian maniraptoran dinosaurs had already developed a character that was decidedly modern, even in taxa that lacked the power of flight, though there is a lack of evidence for this transition. The possibility, that at least some of the epidermal features that are described here originated in modern basal theropods, especially where there is a lack evidence of scales on preserved skin, as is the case in Sciurumimus (Rauhut et al., 2012), Cannot be excluded. Refined genomic mechanisms for the modulation of the complex expression of keratin in the epidermis (Porter & Lane, 2003), terminal differentiation of keratinocytes and the partitioning α- and β-keratin synthesis in the skin of feathered animals (Fukuyama & Epstein, 1968) were probably modified in tandem with the evolution of feathers close to the base of the Maniraptora by the late Middle Jurassic. It is suggested by existing fossil data that this occurred following the evolution of the beak in Maniraptoriformes and prior to the evolution of forelimb patagia and pterylae; The first fossil occurrences of all these features span about 10-15 Ma, which suggests a burst in innovation in the evolution of feathered integument close to and across Lower-Middle Jurassic boundary. The earliest evidence of dermal musculature associated with feathers is about 30 Myr younger at 125 Ma in an ornithothoracean bird (Navalόn et al., 2015). Given the essential role played by this dermal network in the support of feathers and control of the orientation of feathers (Lucas & Strettenheim, 1972), a taphonomic bias may be reflected in its absence in feathered non-avian maniraptorans.

The fossil corneocytes are distinctly non-avian in certain aspects and indicate that feathered dinosaurs and early birds had a unique integumentary anatomy and physiology that was transitional between that of modern birds and non-feathered dinosaurs. Corneocyte tonofibrils are dispersed loosely among intracellular lipids (Menon & Menon, 2000); this facilitates evaporative cooling in response to heat production during flight and insulation by plumage (Menon et al., 1996) in modern birds. Contrasting with this, the fossil tonofibrils are packed densely and fill the interior of the cell. In fossil corneocytes there is no evidence of post-mortem shrinkage: the size range is consistent with those in modern birds, and there is no evidence of diagenetic wrinkling, contortion or separation of individual cells. This strongly suggests that the density of tonofibrils that have been preserved in the fossil corneocytes is a reflection of the original higher densities than in extant birds. According to McNamara et al. this is not a function of body size: extant birds of disparate size, such as the zebra finch and the ostrich, exhibit tonofibrils that are loosely dispersed (Xu et al., 2014). Therefore, the fossil birds are likely to have had a lower physical requirement for evaporative cooling and, in turn, lower production of heat by the body related to the activity of flight (Menon et al., 1996) than is the case in modern birds. This is consistent with other evidence that has been found for non-avian maniraptoran dinosaurs (Xu et al., 2014; Nudds & Dyke, 2010) and basal birds (Xu et al., 2014) having low basal metabolic rates, and with hypotheses that Microraptor feathers (Dyke et al. 2013) and, potentially, Confuciusornis (Nudds & Dyke, 2010), (though see Falk et al., 2016) were not adapted for powered flight, at least for extended periods (Falk et al., 2016).

McNamara, M. E., et al. (2018). "Fossilized skin reveals coevolution with feathers and metabolism in feathered dinosaurs and early birds." Nature Communications 9(1): 2072.