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2.
Palaeontology ; 63(1): 103-115, 2020 Jan.
Article in English | MEDLINE | ID: mdl-32025055

ABSTRACT

Fossils are a key source of data on the evolution of feather structure and function through deep time, but their ability to resolve macroevolutionary questions is compromised by an incomplete understanding of their taphonomy. Critically, the relative preservation potential of two key feather components, melanosomes and keratinous tissue, is not fully resolved. Recent studies suggesting that melanosomes are preferentially preserved conflict with observations that melanosomes preserve in fossil feathers as external moulds in an organic matrix. To date, there is no model to explain the latter mode of melanosome preservation. We addressed these issues by degrading feathers in systematic taphonomic experiments incorporating decay, maturation and oxidation in isolation and combination. Our results reveal that the production of mouldic melanosomes requires interactions with an oxidant and is most likely to occur prior to substantial maturation. This constrains the taphonomic conditions under which melanosomes are likely to be fossilized. Critically, our experiments also confirm that keratinous feather structures have a higher preservation potential than melanosomes under a range of diagenetic conditions, supporting hitherto controversial hypotheses that fossil feathers can retain degraded keratinous structures.

3.
Nat Ecol Evol ; 3(1): 24-30, 2019 01.
Article in English | MEDLINE | ID: mdl-30568282

ABSTRACT

Pterosaurs were the first vertebrates to achieve true flapping flight, but in the absence of living representatives, many questions concerning their biology and lifestyle remain unresolved. Pycnofibres-the integumentary coverings of pterosaurs-are particularly enigmatic: although many reconstructions depict fur-like coverings composed of pycnofibres, their affinities and function are not fully understood. Here, we report the preservation in two anurognathid pterosaur specimens of morphologically diverse pycnofibres that show diagnostic features of feathers, including non-vaned grouped filaments and bilaterally branched filaments, hitherto considered unique to maniraptoran dinosaurs, and preserved melanosomes with diverse geometries. These findings could imply that feathers had deep evolutionary origins in ancestral archosaurs, or that these structures arose independently in pterosaurs. The presence of feather-like structures suggests that anurognathids, and potentially other pterosaurs, possessed a dense filamentous covering that probably functioned in thermoregulation, tactile sensing, signalling and aerodynamics.


Subject(s)
Dinosaurs/anatomy & histology , Feathers/anatomy & histology , Integumentary System/anatomy & histology , Animals , Fossils , Melanosomes
4.
Nat Commun ; 9(1): 2878, 2018 07 23.
Article in English | MEDLINE | ID: mdl-30038333

ABSTRACT

The soft tissues of many fossil vertebrates preserve evidence of melanosomes-micron-scale organelles that inform on integumentary coloration and communication strategies. In extant vertebrates, however, melanosomes also occur in internal tissues. Hence, fossil melanosomes may not derive solely from the integument and its appendages. Here, by analyzing extant and fossil frogs, we show that non-integumentary melanosomes have high fossilization potential, vastly outnumber those from the skin, and potentially dominate the melanosome films preserved in some fossil vertebrates. Our decay experiments show that non-integumentary melanosomes usually remain in situ provided that carcasses are undisturbed. Micron-scale study of fossils, however, demonstrates that non-integumentary melanosomes can redistribute through parts of the body if carcasses are disturbed by currents. Collectively, these data indicate that fossil melanosomes do not always relate to integumentary coloration. Integumentary and non-integumentary melanosomes can be discriminated using melanosome geometry and distribution. This is essential to accurate reconstructions of the integumentary colours of fossil vertebrates.


Subject(s)
Anura/physiology , Color , Fossils , Melanosomes/metabolism , Xenopus/physiology , Animals , Biological Evolution , Feathers , Iguanas/physiology , Melanins/chemistry , Pigmentation , Skin/metabolism , Vertebrates , Xenopus laevis
5.
Nat Commun ; 9(1): 2072, 2018 05 25.
Article in English | MEDLINE | ID: mdl-29802246

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.


Subject(s)
Biological Coevolution , Birds/physiology , Dinosaurs/physiology , Epidermis/physiology , Feathers/physiology , Animals , Epidermis/ultrastructure , Feathers/ultrastructure , Fossils , Microscopy, Electron, Scanning , Phylogeny
7.
Palaeontology ; 59(3): 337-350, 2016 May.
Article in English | MEDLINE | ID: mdl-27499556

ABSTRACT

Fossil melanin granules (melanosomes) are an important resource for inferring the evolutionary history of colour and its functions in animals. The taphonomy of melanin and melanosomes, however, is incompletely understood. In particular, the chemical processes responsible for melanosome preservation have not been investigated. As a result, the origins of sulfur-bearing compounds in fossil melanosomes are difficult to resolve. This has implications for interpretations of original colour in fossils based on potential sulfur-rich phaeomelanosomes. Here we use pyrolysis gas chromatography mass spectrometry (Py-GCMS), fourier transform infrared spectroscopy (FTIR) and time of flight secondary ion mass spectrometry (ToF-SIMS) to assess the mode of preservation of fossil microstructures, confirmed as melanosomes based on the presence of melanin, preserved in frogs from the Late Miocene Libros biota (NE Spain). Our results reveal a high abundance of organosulfur compounds and non-sulfurized fatty acid methyl esters in both the fossil tissues and host sediment; chemical signatures in the fossil tissues are inconsistent with preservation of phaeomelanin. Our results reflect preservation via the diagenetic incorporation of sulfur, i.e. sulfurization (natural vulcanization), and other polymerization processes. Organosulfur compounds and/or elevated concentrations of sulfur have been reported from melanosomes preserved in various invertebrate and vertebrate fossils and depositional settings, suggesting that preservation through sulfurization is likely to be widespread. Future studies of sulfur-rich fossil melanosomes require that the geochemistry of the host sediment is tested for evidence of sulfurization in order to constrain interpretations of potential phaeomelanosomes and thus of original integumentary colour in fossils.

8.
Curr Biol ; 26(8): 1075-82, 2016 04 25.
Article in English | MEDLINE | ID: mdl-27040775

ABSTRACT

Evidence of original coloration in fossils provides insights into the visual communication strategies used by ancient animals and the functional evolution of coloration over time [1-7]. Hitherto, all reconstructions of the colors of reptile integument and the plumage of fossil birds and feathered dinosaurs have been of melanin-based coloration [1-6]. Extant animals also use other mechanisms for producing color [8], but these have not been identified in fossils. Here we report the first examples of carotenoid-based coloration in the fossil record, and of structural coloration in fossil integument. The fossil skin, from a 10 million-year-old colubrid snake from the Late Miocene Libros Lagerstätte (Teruel, Spain) [9, 10], preserves dermal pigment cells (chromatophores)-xanthophores, iridophores, and melanophores-in calcium phosphate. Comparison with chromatophore abundance and position in extant reptiles [11-15] indicates that the fossil snake was pale-colored in ventral regions; dorsal and lateral regions were green with brown-black and yellow-green transverse blotches. Such coloration most likely functioned in substrate matching and intraspecific signaling. Skin replicated in authigenic minerals is not uncommon in exceptionally preserved fossils [16, 17], and dermal pigment cells generate coloration in numerous reptile, amphibian, and fish taxa today [18]. Our discovery thus represents a new means by which to reconstruct the original coloration of exceptionally preserved fossil vertebrates.


Subject(s)
Carotenoids/metabolism , Colubridae/physiology , Fossils , Skin Pigmentation/physiology , Animals , Chromatophores/physiology , Melanins/metabolism
9.
J R Soc Interface ; 11(100): 20140736, 2014 Nov 06.
Article in English | MEDLINE | ID: mdl-25185581

ABSTRACT

Nature's most spectacular colours originate in integumentary tissue architectures that scatter light via nanoscale modulations of the refractive index. The most intricate biophotonic nanostructures are three-dimensional crystals with opal, single diamond or single gyroid lattices. Despite intense interest in their optical and structural properties, the evolution of such nanostructures is poorly understood, due in part to a lack of data from the fossil record. Here, we report preservation of single diamond (Fd-3m) three-dimensional photonic crystals in scales of a 735,000 year old specimen of the brown Nearctic weevil Hypera diversipunctata from Gold Run, Canada, and in extant conspecifics. The preserved red to green structural colours exhibit near-field brilliancy yet are inconspicuous from afar; they most likely had cryptic functions in substrate matching. The discovery of pristine fossil examples indicates that the fossil record is likely to yield further data on the evolution of three-dimensional photonic nanostructures and their biological functions.


Subject(s)
Biological Evolution , Diamond , Fossils , Plants , Canada
10.
Biol Lett ; 9(3): 20130184, 2013 Jun 23.
Article in English | MEDLINE | ID: mdl-23536445

ABSTRACT

Fossil feathers often preserve evidence of melanosomes-micrometre-scale melanin-bearing organelles that have been used to infer original colours and patterns of the plumage of dinosaurs. Such reconstructions acknowledge that evidence from other colour-producing mechanisms is presently elusive and assume that melanosome geometry is not altered during fossilization. Here, we provide the first test of this assumption, using high pressure-high temperature autoclave experiments on modern feathers to simulate the effects of burial on feather colour. Our experiments show that melanosomes are retained despite loss of visual evidence of colour and complete degradation of other colour-producing structures (e.g. quasi-ordered arrays in barbs and the keratin cortex in barbules). Significantly, however, melanosome geometry and spatial distribution are altered by the effects of pressure and temperature. These results demonstrate that reconstructions of original plumage coloration in fossils where preserved features of melanosomes are affected by diagenesis should be treated with caution. Reconstructions of fossil feather colour require assessment of the extent of preservation of various colour-producing mechanisms, and, critically, the extent of alteration of melanosome geometry.


Subject(s)
Color , Feathers , Fossils , Animals
11.
Proc Biol Sci ; 279(1731): 1114-21, 2012 Mar 22.
Article in English | MEDLINE | ID: mdl-21957131

ABSTRACT

Structural colours, the most intense, reflective and pure colours in nature, are generated when light is scattered by complex nanostructures. Metallic structural colours are widespread among modern insects and can be preserved in their fossil counterparts, but it is unclear whether the colours have been altered during fossilization, and whether the absence of colours is always real. To resolve these issues, we investigated fossil beetles from five Cenozoic biotas. Metallic colours in these specimens are generated by an epicuticular multi-layer reflector; the fidelity of its preservation correlates with that of other key cuticular ultrastructures. Where these other ultrastructures are well preserved in non-metallic fossil specimens, we can infer that the original cuticle lacked a multi-layer reflector; its absence in the fossil is not a preservational artefact. Reconstructions of the original colours of the fossils based on the structure of the multi-layer reflector show that the preserved colours are offset systematically to longer wavelengths; this probably reflects alteration of the refractive index of the epicuticle during fossilization. These findings will allow the former presence, and original hue, of metallic structural colours to be identified in diverse fossil insects, thus providing critical evidence of the evolution of structural colour in this group.


Subject(s)
Coleoptera/anatomy & histology , Color , Animals , Coleoptera/ultrastructure , Microscopy, Electron, Scanning , Microscopy, Electron, Transmission , Models, Biological , Nanostructures/chemistry , Nanostructures/ultrastructure
12.
PLoS Biol ; 9(11): e1001200, 2011 Nov.
Article in English | MEDLINE | ID: mdl-22110404

ABSTRACT

Structural colors are generated by scattering of light by variations in tissue nanostructure. They are widespread among animals and have been studied most extensively in butterflies and moths (Lepidoptera), which exhibit the widest diversity of photonic nanostructures, resultant colors, and visual effects of any extant organism. The evolution of structural coloration in lepidopterans, however, is poorly understood. Existing hypotheses based on phylogenetic and/or structural data are controversial and do not incorporate data from fossils. Here we report the first example of structurally colored scales in fossil lepidopterans; specimens are from the 47-million-year-old Messel oil shale (Germany). The preserved colors are generated by a multilayer reflector comprised of a stack of perforated laminae in the scale lumen; differently colored scales differ in their ultrastructure. The original colors were altered during fossilization but are reconstructed based upon preserved ultrastructural detail. The dorsal surface of the forewings was a yellow-green color that probably served as a dual-purpose defensive signal, i.e. aposematic during feeding and cryptic at rest. This visual signal was enhanced by suppression of iridescence (change in hue with viewing angle) achieved via two separate optical mechanisms: extensive perforation, and concave distortion, of the multilayer reflector. The fossils provide the first evidence, to our knowledge, for the function of structural color in fossils and demonstrate the feasibility of reconstructing color in non-metallic lepidopteran fossils. Plastic scale developmental processes and complex optical mechanisms for interspecific signaling had clearly evolved in lepidopterans by the mid-Eocene.


Subject(s)
Fossils , Moths , Nanostructures/ultrastructure , Pigmentation , Animals , Biological Evolution , Microscopy, Electron, Scanning , Moths/ultrastructure , Nanostructures/chemistry , Phylogeny , Wings, Animal/ultrastructure
13.
Nature ; 465(7295): 215-8, 2010 May 13.
Article in English | MEDLINE | ID: mdl-20463737

ABSTRACT

The renowned soft-bodied faunas of the Cambrian period, which include the Burgess Shale, disappear from the fossil record in the late Middle Cambrian, after which the Palaeozoic fauna dominates. The disappearance of faunas of Burgess Shale type curtails the stratigraphic record of a number of iconic Cambrian taxa. One possible explanation for this loss is a major extinction, but more probably it reflects the absence of preservation of similar soft-bodied faunas in later periods. Here we report the discovery of numerous diverse soft-bodied assemblages in the Lower and Upper Fezouata Formations (Lower Ordovician) of Morocco, which include a range of remarkable stem-group morphologies normally considered characteristic of the Cambrian. It is clear that biotas of Burgess Shale type persisted after the Cambrian and are preserved where suitable facies occur. The Fezouata biota provides a link between the Burgess Shale communities and the early stages of the Great Ordovician Biodiversification Event.


Subject(s)
Biodiversity , Fossils , Marine Biology , Animals , Extinction, Biological , Morocco
14.
Nature ; 463(7284): 1075-8, 2010 Feb 25.
Article in English | MEDLINE | ID: mdl-20107440

ABSTRACT

Spectacular fossils from the Early Cretaceous Jehol Group of northeastern China have greatly expanded our knowledge of the diversity and palaeobiology of dinosaurs and early birds, and contributed to our understanding of the origin of birds, of flight, and of feathers. Pennaceous (vaned) feathers and integumentary filaments are preserved in birds and non-avian theropod dinosaurs, but little is known of their microstructure. Here we report that melanosomes (colour-bearing organelles) are not only preserved in the pennaceous feathers of early birds, but also in an identical manner in integumentary filaments of non-avian dinosaurs, thus refuting recent claims that the filaments are partially decayed dermal collagen fibres. Examples of both eumelanosomes and phaeomelanosomes have been identified, and they are often preserved in life position within the structure of partially degraded feathers and filaments. Furthermore, the data here provide empirical evidence for reconstructing the colours and colour patterning of these extinct birds and theropod dinosaurs: for example, the dark-coloured stripes on the tail of the theropod dinosaur Sinosauropteryx can reasonably be inferred to have exhibited chestnut to reddish-brown tones.


Subject(s)
Birds/anatomy & histology , Color , Dinosaurs/anatomy & histology , Feathers/cytology , Fossils , Melanosomes , Pigmentation , Animals , Birds/classification , China , Dinosaurs/classification , Extinction, Biological , Feathers/anatomy & histology , Feathers/ultrastructure , Integumentary System/anatomy & histology , Melanosomes/physiology , Melanosomes/ultrastructure , Phylogeny , Pigmentation/physiology
15.
Proc Biol Sci ; 277(1680): 423-7, 2010 Feb 07.
Article in English | MEDLINE | ID: mdl-19828545

ABSTRACT

The very labile (decay-prone), non-biomineralized, tissues of organisms are rarely fossilized. Occurrences thereof are invaluable supplements to a body fossil record dominated by biomineralized tissues, which alone are extremely unrepresentative of diversity in modern and ancient ecosystems. Fossil examples of extremely labile tissues (e.g. muscle) that exhibit a high degree of morphological fidelity are almost invariably replicated by inorganic compounds such as calcium phosphate. There is no consensus as to whether such tissues can be preserved with similar morphological fidelity as organic remains, except when enclosed inside amber. Here, we report fossilized musculature from an approximately 18 Myr old salamander from lacustrine sediments of Ribesalbes, Spain. The muscle is preserved organically, in three dimensions, and with the highest fidelity of morphological preservation yet documented from the fossil record. Preserved ultrastructural details include myofilaments, endomysium, layering within the sarcolemma, and endomysial circulatory vessels infilled with blood. Slight differences between the fossil tissues and their counterparts in extant amphibians reflect limited degradation during fossilization. Our results provide unequivocal evidence that high-fidelity organic preservation of extremely labile tissues is not only feasible, but likely to be common. This is supported by the discovery of similarly preserved tissues in the Eocene Grube Messel biota.


Subject(s)
Fossils , Muscles , Paleontology , Preservation, Biological/methods , Sulfur/physiology , Urodela , Animals , Microscopy/methods , Microscopy, Electron, Scanning , Muscles/physiology , Muscles/ultrastructure , Spain , Urodela/anatomy & histology , Urodela/physiology
16.
Proc Biol Sci ; 269(1497): 1195-203, 2002 Jun 22.
Article in English | MEDLINE | ID: mdl-12065034

ABSTRACT

The small, non-biomineralized, three-dimensionally preserved arthropod Offacolus kingi Orr et al. from the Wenlock Series (Silurian) of Herefordshire, England, is re-evaluated, and the new family Offacolidae erected. This new study is based on specimens which have been serially ground, reconstructed by computer and rendered in the round as coloured models. Offacolus possesses a prosomal appendage array similar to that of Limulus, but also bears robust and setose exopods on appendages II-V which are unlike those found in any other arthropods. Opisthosomal appendages are similar in number and morphology to the book-gills of Limulus. Cladistic analysis places Offacolus basally within the Chelicerata, as a sister taxon to the eurypterids and extant chelicerates, but more derived than the Devonian Weinbergina.


Subject(s)
Arthropods/anatomy & histology , Arthropods/classification , Computer Simulation , Fossils , Phylogeny , Animals , England , Models, Anatomic
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