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Abstract and Figures

Birds are the only living amniotes with coloured eggs1-4, which have long been considered to be an avian innovation1,3. A recent study has demonstrated the presence of both red-brown protoporphyrin IX and blue-green biliverdin5-the pigments responsible for all the variation in avian egg colour-in fossilized eggshell of a nonavian dinosaur6. This raises the fundamental question of whether modern birds inherited egg colour from their nonavian dinosaur ancestors, or whether egg colour evolved independently multiple times. Here we present a phylogenetic assessment of egg colour in nonavian dinosaurs. We applied high-resolution Raman microspectroscopy to eggshells that represent all of the major clades of dinosaurs, and found that egg colour pigments were preserved in all eumaniraptorans: egg colour had a single evolutionary origin in nonavian theropod dinosaurs. The absence of colour in ornithischian and sauropod eggs represents a true signal rather than a taphonomic artefact. Pigment surface maps revealed that nonavian eumaniraptoran eggs were spotted and speckled, and colour pattern diversity in these eggs approaches that in extant birds, which indicates that reproductive behaviours in nonavian dinosaurs were far more complex than previously known3. Depth profiles demonstrated identical mechanisms of pigment deposition in nonavian and avian dinosaur eggs. Birds were not the first amniotes to produce coloured eggs: as with many other characteristics7,8 this is an attribute that evolved deep within the dinosaur tree and long before the spectacular radiation of modern birds.
| Egg colour reconstruction. a, Top, eggshell-pigment surface maps. n = 8; selection criteria were pigment presence (Fig. 1) and sufficient surface exposure. Protoporphyrin was mapped (1,350 cm −1 ± 2 cm −1 , 2 accumulations, 5 s of exposure) with three independent repetitions, which yielded similar results. Increased signal intensity (yellow) is relative to the lowest signal intensity (black, which equals background noise in the absence of protoporphyrin IX). Bottom, egg reconstructions that combine information from panels above, b and Fig. 1 into a range of potential colours for the fossil eggshells. From left to right: H. huangi, Mongolian microtroodontid (MAE 14-40), Mongolian troodontid (AMNH FARB 6631), Mongolian troodontid (IGM 100/1003), D. antirrhopus, Mongolian enantiornithine, D. novaehollandiae and G. domesticus. b, Pigment depth profiles across vertical sections of eggs from A. mississipiensis, plus the taxa shown in a (n = 9 specimens). Depth profiles were repeated three times independently, which yielded similar results. Photographs and depth profiles are not at the same scale. The distribution of protoporphyrin IX (red), biliverdin (blue) and proteinaceous matter (grey) is based on Raman point measurements and line maps (1,166 cm −1 ± 2 cm −1 ). Droplet icons indicate pigment elution. oc, organic cuticle; mc, mineralized cuticle; pz, prismatic zone; mt, membrana testacea. c, Visualization of gradual colour change of eggshell pigments and proteinaceous matter through time, based on observations of eggshells (D. novaehollandiae and Casuarius casuarius) and on a previous study 26 .
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LETTER https://doi.org/10.1038/s41586-018-0646-5
Dinosaur egg colour had a single evolutionary origin
Jasmina Wiemann1*, Tzu-Ruei Yang2 & Mark A. Norell3
Birds are the only living amniotes with coloured eggs
1–4
, which have
long been considered to be an avian innovation
1,3
. A recent study
has demonstrated the presence of both red-brown protoporphyrin
IX and blue-green biliverdin5—the pigments responsible for
all the variation in avian egg colour—in fossilized eggshell of
a nonavian dinosaur6. This raises the fundamental question of
whether modern birds inherited egg colour from their nonavian
dinosaur ancestors, or whether egg colour evolved independently
multiple times. Here we present a phylogenetic assessment of egg
colour in nonavian dinosaurs. We applied high-resolution Raman
microspectroscopy to eggshells that represent all of the major clades
of dinosaurs, and found that egg colour pigments were preserved
in all eumaniraptorans: egg colour had a single evolutionary
origin in nonavian theropod dinosaurs. The absence of colour in
ornithischian and sauropod eggs represents a true signal rather
than a taphonomic artefact. Pigment surface maps revealed that
nonavian eumaniraptoran eggs were spotted and speckled, and
colour pattern diversity in these eggs approaches that in extant birds,
which indicates that reproductive behaviours in nonavian dinosaurs
were far more complex than previously known3. Depth profiles
demonstrated identical mechanisms of pigment deposition in
nonavian and avian dinosaur eggs. Birds were not the first amniotes
to produce coloured eggs: as with many other characteristics7,8 this
is an attribute that evolved deep within the dinosaur tree and long
before the spectacular radiation of modern birds.
The huge diversity of avian egg colour
9
has previously been attributed
to the exploration of empty ecological niches after the extinction of
nonavian dinosaurs at the terminal Cretaceous event1. Different nesting
environments, as well as nesting behaviours, are thought to influence
egg colour1012. Egg colour may reflect selective pressure as a result of
an ecological interaction between the egg producer and an egg pred-
ator (camouflage) or parasite (egg recognition). Avian egg colour has
previously been shown to react in a plastic fashion to changes in the
incubation strategy or climate, or even in mating behaviour
1,10,1218
.
However, all previously proposed selective factors rely on the fact that
the eggs are exposed to the environment
10,11
and, with scant exception,
not buried or covered. More-recent research suggests that egg colour
may have co-evolved with (partially) open nesting habits in nonavian
dinosaurs6 but offers only a single data point of egg colour outside
crown birds, in open-nesting oviraptorid dinosaurs. Information on
eggshell pigments in a larger sample of nonavian dinosaurs is required
to understand the evolution of egg colour.
Both eggshell pigments—biliverdin and protoporphyrin IX—are
tetrapyrroles with minor structural differences that affect their chemi-
cal properties and their distribution across the eggshell
1922
. In contrast
to the more hydrophilic biliverdin, which extends deep into the pris-
matic zone of the eggshell, the more hydrophobic protoporphyrin—
which causes spots and speckles—is restricted to the waxy cuticle21,23.
The different solubility properties of biliverdin and protoporphyrin
appear to be key to their preservation potential
6,21,22,24
. Protoporphyrin
is more resilient to elution than biliverdin but both pigments are
preserved in detectable trace amounts
6,24
. Eggshell pigments appear to
be restricted, if not bound, to the proteinaceous scaffold of the eggshell
matrix25.
Proteins transform during diagenesis into pyrrole-, pyridine- and
imidazole-rich polymers through oxidative crosslinking
26
; the resulting
protein fossilization products (PFPs) appear similar to biliverdin and
protoporphyrin IX in their chemical composition. Raman spectros-
copy distinguishes between true egg-colour pigments and pigment-like
PFPs
26
(Extended Data Fig.1), and identifies and maps out pigments
over eggshell surfaces and across vertical egg sections to characterize
colour patterns and pigment deposition in fossil eggs. Placing this
information in a phylogenetic context offers insights into whether
egg colour evolved once within nonavian dinosaurs or multiple times
independently, and might help to identify selective factors.
In our sample of nineteen archosaur eggshells, egg colour pigments
are absent in eggshells of Alligator mississipiensis, the North American
hadrosaurid Maiasaura peeblesorum, the South American saltasaurid,
the French titanosaurid and the North American troodontid (Fig.1,
Extended Data Figs.2, 3). Egg colour pigments are preserved in
eggshells from the oviraptorid Heyuannia huangi, Mongolian micro
-
troodontids, the Chinese and Mongolian troodontids, the dromaeo-
saurid Deinonychus antirrhopus, the Mongolian enantiornithine,
Psammornis rothschildi, Rhea americana, the North American ratite,
Dromaius novaehollandiae and Gallus domesticus (Fig.1, Extended
Data Figs.2, 3).
Only biliverdin was detected in D. novaehollandiae, whereas only
protoporphyrin IX was present in the eggshells of the Mongolian
microtroodontid (MAE 14-40(specimen codes in parentheses)), the
Chinese and Mongolian troodontids, the Mongolian enantiornithine,
P. rothschildi and G. domesticus. Both egg colour pigments were
detected in eggshells from H. huangi, the Mongolian microtroodon-
tid (IGM 100/1323) and macrotroodontid (AMNH FARB 6631),
D. antirrhopus, R. americana and the North American ratite. The
presence of eggshell pigments corresponds to (partially) open nesting
habits (Fig.1).
All eggshell and associated sediment samples were plotted on a whole
spectra-based principal component analysis (PCA) (Extended Data
Fig.4 and its Source Data). Principal component 1 (PC1, 57.118%)
represents variability in pigment type, concentration and mode of egg
-
shell alteration, whereas principal component 2 (PC2, 23.841%) sep-
arates samples into unpigmented and pigmented eggshells (Extended
Data Fig.5). The PCA (Extended Data Fig.4a) revealed that eggshell
biomolecules are distinct from organic material in the sediment, with
both clusters separating across PC1 (73.116%). Within the eggshell
cluster, extant and fossil materials are separated across PC2 (10.977%)
(Extended Data Fig.4a). A separate PCA (Extended Data Fig.4b) based
on the spectral fingerprint region of biliverdin and protoporphyrin IX
(1,500cm
1
–1,650cm
1
± 2cm
1
) included all fossil eggshell sam-
ples: the resulting chemo-space identified a characteristic cluster of
pigmented eggshells, distinct from a separate cluster of unpigmented
eggshells. Mapping protoporphyrin IX on the eggshell surface (Fig.2a)
demonstrated that the eggs of H. huangi were spotted, as were those
of the Mongolian microtroodontids and troodontids, D. antirrhopus,
and the Mongolian enantiornithine. Reconstructions of the egg colours
are shown in Fig.2a.
Depth profiles (Fig.2b) across vertical eggshell sections show that
pigments are absent in all layers of the A. mississipiensis eggshell as
1Department of Geology & Geophysics, Yale University, New Haven, CT, USA. 2Steinmann Institute for Geology, Mineralogy, and Paleontology, University of Bonn, Bonn, Germany. 3Division of
Vertebrate Paleontology, American Museum of Natural History, New York, NY, USA. *e-mail: jasmina.wiemann@yale.edu
22 NOVEMBER 2018 | VOL 563 | NATURE | 555
© 2018 Springer Nature Limited. All rights reserved.
Content courtesy of Springer Nature, terms of use apply. Rights reserved
... Further studies on fossils use chemical imaging techniques such as Fourier transform infrared spectroscopy (FTIR) and Raman spectroscopy to search for chemical signals, e.g., of functional groups (e.g., amide or carbonyl group) in the samples [9,21,32]. FTIR excites the vibrations of chemical bonds using infrared irradiation. Each type of chemical bond will absorb infrared (IR) waves in a distinct wave number range in the near-IR (12,500-4000 cm −1 ), mid-IR (4000-400 cm −1 ), or far-IR (400-10 cm −1 ) regions. ...
... The produced signals are weak, often requiring prolonged periods of intense irradiation [48], which can lead to a degradation of thermolabile compounds due to the heat produced by the laser [32,49]. Raman spectroscopy has been used for the detection of heme in dinosaur bones [18] and for the detection of the heme degradation product biliverdin and of its precursor protoporphyrin IX in dinosaur eggshells [21]. ...
... (I) Djadokhta Formation, Mongolia [23]. (J) Hell Creek Formation, eastern Montana, USA [18][19][20] (K) Chinese provinces (Henan, Jiangxi, and Guangdong) [21,22]. Concept adapted from reference [76]. ...
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This review provides an overview of organic compounds detected in non-avian dinosaur fossils to date. This was enabled by the development of sensitive analytical techniques. Non-destructive methods and procedures restricted to the sample surface, e.g., light and electron microscopy, infrared (IR) and Raman spectroscopy, as well as more invasive approaches including liquid chromatography coupled to tandem mass spectrometry (LC-MS/MS), time-of-flight secondary ion mass spectrometry, and immunological methods were employed. Organic compounds detected in samples of dinosaur fossils include pigments (heme, biliverdin, protoporphyrin IX, melanin), and proteins, such as collagens and keratins. The origin and nature of the observed protein signals is, however, in some cases, controversially discussed. Molecular taphonomy approaches can support the development of suitable analytical methods to confirm reported findings and to identify further organic compounds in dinosaur and other fossils in the future. The chemical properties of the various organic compounds detected in dinosaurs, and the techniques utilized for the identification and analysis of each of the compounds will be discussed.
... [1,2] Applications of non-destructive, in situ Raman microspectroscopy have resulted in rapid progress in understanding biomolecule fossilization and the detection of biosignatures based on comparative statistical analyses of fossil organic matter. [3][4][5][6][7][8][9][10][11][12][13][14][15][16][17][18] The in situ approach facilitates rapid non-destructive analysis of surface-cleaned samples without requiring time-consuming extractions of the organic matter that may alter fossil molecular compounds. Raman spectroscopy not only characterizes molecular functional groups (small molecular units with distinct chemical properties), but also provides insights into higher-level structural organization by detecting intermolecular and organo-mineral interactions. ...
... [19,[24][25][26][27] A number of advantages, including time-efficient non-destructive analysis, availability and low operating cost of equipment, and the utility of results, make Raman and complementary types of light spectroscopy ideal for molecular tests of hypotheses based on the composition of paleontological and geological materials. [3][4][5][6][7][8][9][10][11][12][13][14][15][16][17][18][20][21][22][23] A diversity of studies conducted by different laboratories have recovered similar patterns in the molecular makeup of fossil organic matter in independently acquired in situ Raman spectra. [3][4][5][6][7][8][9][10][11][12][13][14][15][16][17][18][20][21][22][23] However, a recent Perspective by Alleon et al. [28] concluded that the biological results of a selected subset of these studies [3,4,6,11,12,15] are compromised, based on their detection of sinusoidal edge filter ripples, i.e., instrumental artefacts, in the Raman data. ...
... [3][4][5][6][7][8][9][10][11][12][13][14][15][16][17][18][20][21][22][23] A diversity of studies conducted by different laboratories have recovered similar patterns in the molecular makeup of fossil organic matter in independently acquired in situ Raman spectra. [3][4][5][6][7][8][9][10][11][12][13][14][15][16][17][18][20][21][22][23] However, a recent Perspective by Alleon et al. [28] concluded that the biological results of a selected subset of these studies [3,4,6,11,12,15] are compromised, based on their detection of sinusoidal edge filter ripples, i.e., instrumental artefacts, in the Raman data. [28] The results in the disputed studies are based on the statistical evaluation of in situ Raman spectra obtained in the organic fingerprint region (500-1800 cm −1 ) for a diversity of modern, experimentally matured, and fossil tissues covering all major branches of extinct and modern invertebrates and vertebrates, as well as sedimentary host rocks, and represent the first large-scale explorative studies of their kind in the geosciences. ...
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... Raman spectroscopy is a well-established method in taphonomy (Bernard et al., 2007;Jehlička, Jorge Villar & Edwards, 2004;Marshall et al., 2012;Thomas et al., 2007;Thomas et al., 2011;Wiemann, Yang & Norell, 2018;Witke et al., 2004). It is useful for assessing the degree of diagenetic alteration to bone (Thomas et al., 2007;Thomas et al., 2011) and Table 1 Materials used in this study. ...
... We also sampled fragments of associated gastralia (not pictured here) (B) Vessel containing spheres as well as non-spherical amorphous vessel fill (grey bracket) in thin section LJ98B-1 (sample area 1; originally prepared for (Yao, Zhang & Tang, 2002)). evaluating the origin of compounds and structures in fossil material (Marshall et al., 2012;Thomas et al., 2014;Wiemann, Yang & Norell, 2018). We employed Raman spectroscopy to test the alternative interpretation of the putative red blood cells as framboids of iron minerals (Martill & Unwin, 1997), and to assess the quality of bone preservation from a diagenetic perspective. ...
... The specimens used herein are accessioned at the IVPP in Beijing with the holotype under the museum number IVPP-V11559. The slide numbers are 2018-X1, 2018-X2, 2018-L1, 2018-L2, 2018-L3, 2018-L4, 2018-L5, HO-9601, HO-9602, LJ98B-1, and LJ98B-4, 2018-1, and 2018. The modern alligator bone sample is from un-accessioned material stored in the Virginia Tech osteology collection. ...
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... Meanwhile, Raman spectroscopy, as a non-destructive test, has drawn much attention in fossil egg researchers. For example, Raman spectroscopy can be used to identify the chemical composition of fossil eggshell [25], such as the hydroxyapatite (HAP) preserved in the cuticle layer [26], phosphate in the membrane [27], and color-producing pigments [28][29][30], S-to N-heterocycles [31], and amorphous carbon [32]. Moreover, Raman spectroscopy with the deconvolution technique can be used to detect the maximum paleotemperature recorded in eggshells [33]. ...
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