Dinosaur egg colour had a single evolutionary origin

Protoporphyrin (PP) and biliverdin (BV) give rise to the enormous diversity in avian egg coloration. Egg color serves several ecological purposes, including post-mating signaling and camouflage. Egg camouflage represents a major character of open-nesting birds which accomplish protection of their unhatched offspring against visually oriented predators by cryptic egg coloration. Cryptic coloration evolved to match the predominant shades of color found in the nesting environment. Such a selection pressure for the evolution of colored or cryptic eggs should be present in all open nesting birds and relatives. Many birds are open-nesting, but protect their eggs by continuous brooding, and thus exhibit no or minimal eggshell pigmentation. Their closest extant relatives, crocodiles, protect their eggs by burial and have unpigmented eggs. This phylogenetic pattern led to the assumption that colored eggs evolved within crown birds. The mosaic evolution of supposedly avian traits in non-avian theropod dinosaurs, however, such as the supposed evolution of partially open nesting behavior in oviraptorids, argues against this long-established theory. Using a double-checking liquid chromatography ESI-Q-TOF mass spectrometry routine, we traced the origin of colored eggs to their non-avian dinosaur ancestors by providing the first record of the avian eggshell pigments protoporphyrin and biliverdin in the eggshells of Late Cretaceous oviraptorid dinosaurs. The eggshell parataxon Macroolithus yaotunensis can be assigned to the oviraptor Heyuannia huangi based on exceptionally preserved, late developmental stage embryo remains. The analyzed eggshells are from three Late Cretaceous fluvial deposits ranging from eastern to southernmost China. Reevaluation of these taphonomic settings, and a consideration of patterns in the porosity of completely preserved eggs support an at least partially open nesting behavior for oviraptorosaurs. Such a nest arrangement corresponds with our reconstruction of blue-green eggs for oviraptors. According to the sexual signaling hypothesis, the reconstructed blue-green eggs support the origin of previously hypothesized avian paternal care in oviraptorid dinosaurs. Preserved dinosaur egg color not only pushes the current limits of the vertebrate molecular and associated soft tissue fossil record, but also provides a perspective on the potential application of this unexplored paleontological resource. How to cite this article Wiemann et al. (2017), Dinosaur origin of egg color: oviraptors laid blue-green eggs. PeerJ 5:e3706; DOI 10.7717/peerj.3706

Open-nesting birds use biological pigments in eggshell to camouflage their unhatched offspring, varying the colour to account for the nesting environment and location. The tetrapyrrolic pigments protoporphyrin (PP) and biliverdin (BV), which both participate in the haem metabolism, are responsible for the reddish brown of chicken eggs and the brilliant blue of robin and emu eggs. However, eggshell pigmentation correlates with the nest type in a wide range of avian species and suggests that coloured eggs are basal to the avian lineage, extending back to their non-avian dinosaur origins. Detecting preserved eggshell pigments could thus shed light on dinosaur nesting behaviour. Using HPLC separation coupled to ESI-Q-TOF mass spectrometry, we here provide the first record of the eggshell pigments PP and BV preserved in fossils from three different localities, in 66 million year-old oviraptorid eggshell (Macroolithus yaotunensis). These eggs were presumably laid in at least partially open nests by the oviraptorid Heyuannia huangi and camouflaged by an originally blue-greenish egg colouration. Such a blue-greenish eggshell pigmentation hints at increased paternal care in Heyuannia. Shell porosity measurements, preserved clutches and parental animals support an open nesting behaviour for oviraptorid dinosaurs. Furthermore, the detection of PP, together with supporting microscopic observations, represents the first evidence for cuticle preservation in fossil eggshell. Our study demonstrates that molecular biomarkers, such as preserved metabolites, can be used to trace the evolution of modern avian traits, and to provide insights into dinosaur reproductive biology and the preservation of endogenous organic matter in fossil vertebrates.

Scientific Reports

Chemoecology, 2010

The known chemical basis of diverse avian eggshell coloration is generated by the same two classes of tetrapyrrole pigments in most living birds. We aimed to extend the evolutionary scope of these patterns by detecting pigments from extinct birds’ eggs. In our samples biliverdin was successfully extracted from subfossil shell fragments of the blue-green egg-laying upland moa Megalapteryx didinus, while protoporphyrin was extracted from the beige eggs of two other extinct moa species. Our data on pigment detection from eggshells of other extant paleognath birds, together with published information on other modern lineages, confirm tetrapyrroles as ubiquitous and conserved pigments contributing to diverse eggshell colours throughout avian evolution.

Science, 2010

Nature communications, 2018

The Jurassic Yanliao theropods have offered rare glimpses of the early paravian evolution and particularly of bird origins, but, with the exception of the bizarre scansoriopterygids, they have shown similar skeletal and integumentary morphologies. Here we report a distinctive new Yanliao theropod species bearing prominent lacrimal crests, bony ornaments previously known from more basal theropods. It shows longer arm and leg feathers than Anchiornis and tail feathers with asymmetrical vanes forming a tail surface area even larger than that in Archaeopteryx. Nanostructures, interpreted as melanosomes, are morphologically similar to organized, platelet-shaped organelles that produce bright iridescent colours in extant birds. The new species indicates the presence of bony ornaments, feather colour and flight-related features consistent with proposed rapid character evolution and significant diversity in signalling and locomotor strategies near bird origins.

PloS one, 2010

Background: The exceptional diversity of coloration found in avian eggshells has long fascinated biologists and inspired a broad range of adaptive hypotheses to explain its evolution. Three main impediments to understanding the variability of eggshell appearance are: (1) the reliable quantification of the variation in eggshell colours; (2) its perception by birds themselves, and (3) its relation to avian phylogeny. Here we use an extensive museum collection to address these problems directly, and to test how diversity in eggshell coloration is distributed among different phylogenetic levels of the class Aves.

Nature, 2014

Inference of colour patterning in extinct dinosaurs 1-3 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 vertebrates 4 , and may therefore support a significant physiological shift in maniraptoran dinosaurs.

Archaeopteryx has been regarded as an icon of evolution ever since its discovery from the Late Jurassic limestone deposits of solnhofen, Germany in 1861. Here we report the first evidence of colour from Archaeopteryx based on fossilized colour-imparting melanosomes discovered in this isolated feather specimen. using a phylogenetically diverse database of extant bird feathers, statistical analysis of melanosome morphology predicts that the original colour of this Archaeopteryx feather was black, with 95% probability. Furthermore, reexamination of the feather’s morphology leads us to interpret it as an upper primary covert, contrary to previous interpretations. Additional findings reveal that the specimen is preserved as an organosulphur residue, and that barbule ultrastructure identical to that of modern bird feathers had evolved as early as the Jurassic. As in extant birds, the extensive melanization would have provided structural advantages to the Archaeopteryx wing feather during this early evolutionary stage of dinosaur flight.

Palaeogeography Palaeoclimatology Palaeoecology, 2006

Although dinosaur eggs were first discovered and identified in the late 1800s, limited attention was given to the scientific value of oological fossils in contrast to observations based on skeletal features. Here, we offer a review of Mesozoic saurischian egg materials, in comparison with extant crocodilians and avians, and their paleobiological interpretation based either on the presence of embryos in ovo or brooding adults on egg clutches. Our study focuses on the eggs of the oviraptorid Citipati osmolka (Mongolia), the troodontid Troodon formosus (North America), the theropod oospecies Macroelongatoolithus xixiaensis (China), the ornithothoracine bird (Argentina), an indeterminate theropod (Thailand), and titanosaurs (Argentina). Results show that (1) many oological characters and reproductive behaviors associated with modern birds are rooted among non-avian theropods, (2) there is a reproductive evolutionary cline from crocodilians to modern birds with (3) a noticeable pattern of coeval development between the accretion of eggshell layers, origination and size increased of larger air cells (inferred from egg polar asymmetry), and brooding/incubating behaviors. Most of these pre-adaptations are grouped in two main clades of the saurischian cladogram: one at the level of Oviraptorosauridae and the other at Troodontidae. Although undeniably these two theropod taxa seem to represent two important phases for the evolution of avian reproduction, the phylogenetic distance between these clades and Titanosauria cannot be ignored. As such, the reproductive features that appeared in concert in oviraptorids might have gradually evolved across more basal theropod clades. Although Troodon formosus by its egg shape and nesting behavior seems to be in this study the precursors of modern avian reproduction, the importance of smallbodied theropods such as those who laid the Phu Phok eggs cannot be dismissed and the eggs of such dinosaurs could suggest a closer phylogenetic ties to Aves than troodontids. At a higher level of inferences, there is a strong possibility that the evolution of these reproductive features is concurrent with profound physiological and metabolic changes that occurred in saurischian dinosaurs throughout their evolution. D 2006 Published by Elsevier B.V.