Melanosome evolution indicates a key physiological shift within feathered dinosaurs

Abstract

Inference of colour patterning in extinct dinosaurs 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 vertebrates, and may therefore support a significant physiological shift in maniraptoran dinosaurs.

Interpreting melanin-based coloration through deep time: a critical review

“…This is critical for evaluating the many published accounts on presumed melanosomes in fossils, because the majority of those specimens where expressed colour, physiology, behaviour or evolutionary significance have been proposed do not illustrate three-dimensional bodies, but rather derive data from ovoid to elongate imprints within an uncharacterized matrix (e.g. [8][9][10]54]). This observation implies that the microbodies decay more rapidly than does the surrounding matrix, thus challenging the idea that melanin confers decay resistance to the bodies.…”

“…[6,50,51]), yet the search for ancient melanic pigments only began in earnest in the late 2000s following the proposal that feather traces might infer evidence of original hues and shades [7,52]. Since then, a number of investigations have used chemical markers and presumed fossil melanosomes to explore aspects of the biology and ecology of extinct animals, including colour [8,9,[53][54][55][56][57], behaviour [8,56] and physiology [10]. However, studies reporting remnant melanosomes have been met with controversy, and an alternative hypothesis has been put forth favouring a more conservative interpretation of the fossil microbodies as microbes colonizing the degrading tissues prior to burial [12,58].…”

“…They further suggested that the shape and arrangement of fossil melanosomes could be used to deduce plumage colours in ancient birds and non-avian dinosaurs [7], which led to inferences about ecology and behaviour that have since been adopted by numerous studies (e.g. [8][9][10]). …”

Rhetoric vs. reality: A commentary on “Bird Origins Anew” by A. Feduccia

“…obs. ), and in various other dinosaurian and non-dinosaurian taxa from the Jehol Group (Li et al 2012(Li et al , 2014a. Moreover, Lingham-Soliar does not provide a feasible alternative explanation for the observed color banding along the tail of Sinosauropteryx (Lingham-Soliar 2011.…”

“…Details and lengthy analyses have often been made freely available as online supplements (e.g., Xu et al 2009b, .100 pages of supplementary material). Moreover, the pace of discovery and description of new fossil specimens has steadily increased across a variety of journals and the appearance of in-depth papers on early birds and closely related non-avian theropods (many with feathers) is ever more frequent , 2008, 2014, Currie and Chen 2001, Clarke and Norell 2002, Hwang et al 2002, Norell and Xu 2005, Clarke et al 2006, Lamanna et al 2006, Li et al 2012, 2014a, O'Connor et al 2012, Chinsamy et al 2013. Undoubtedly, studies on the diversity of non-avian dinosaurs and early birds from the Daohugou and Jehol Biotas have resulted in a wealth of novel information about the anatomy of these animals and its relevance for understanding the origin of birds and of their flight.…”