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      Taphonomic experiments resolve controls on the preservation of melanosomes and keratinous tissues in feathers

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          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.

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          Most cited references58

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          Keratin: Structure, mechanical properties, occurrence in biological organisms, and efforts at bioinspiration

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            Melanins: Skin Pigments and Much More—Types, Structural Models, Biological Functions, and Formation Routes

            F. Solano (2014)
            This review presents a general view of all types of melanin in all types of organisms. Melanin is frequently considered just an animal cutaneous pigment and is treated separately from similar fungal or bacterial pigments. Similarities concerning the phenol precursors and common patterns in the formation routes are discussed. All melanins are formed in a first enzymatically-controlled phase, generally a phenolase, and a second phase characterized by an uncontrolled polymerization of the oxidized intermediates. In that second phase, quinones derived from phenol oxidation play a crucial role. Concerning functions, all melanins show a common feature, a protective role, but they are not merely photoprotective pigments against UV sunlight. In pathogenic microorganisms, melanization becomes a virulence factor since melanin protects microbial cells from defense mechanisms in the infected host. In turn, some melanins are formed in tissues where sunlight radiation is not a potential threat. Then, their redox, metal chelating, or free radical scavenging properties are more important than light absorption capacity. These pigments sometimes behave as a double-edged sword, and inhibition of melanogenesis is desirable in different cells. Melanin biochemistry is an active field of research from dermatological, biomedical, cosmetical, and microbiological points of view, as well as fruit technology.
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              Chemistry of mixed melanogenesis--pivotal roles of dopaquinone.

              Melanins can be classified into two major groups-insoluble brown to black pigments termed eumelanin and alkali-soluble yellow to reddish-brown pigments termed pheomelanin. Both types of pigment derive from the common precursor dopaquinone (ortho-quinone of 3,4-dihydroxyphenylalanine) which is formed via the oxidation of l-tyrosine by the melanogenic enzyme tyrosinase. Dopaquinone is a highly reactive ortho-quinone that plays pivotal roles in the chemical control of melanogenesis. In the absence of sulfhydryl compounds, dopaquinone undergoes intramolecular cyclization to form cyclodopa, which is then rapidly oxidized by a redox reaction with dopaquinone to give dopachrome (and dopa). Dopachrome then gradually and spontaneously rearranges to form 5,6-dihydroxyindole and to a lesser extent 5,6-dihydroxyindole-2-carboxylic acid, the ratio of which is determined by a distinct melanogenic enzyme termed dopachrome tautomerase (tyrosinase-related protein-2). Oxidation and subsequent polymerization of these dihydroxyindoles leads to the production of eumelanin. However, when cysteine is present, this process gives rise preferentially to the production of cysteinyldopa isomers. Cysteinyldopas are subsequently oxidized through redox reaction with dopaquinone to form cysteinyldopaquinones that eventually lead to the production of pheomelanin. Pulse radiolysis studies of early stages of melanogenesis (involving dopaquinone and cysteine) indicate that mixed melanogenesis proceeds in three distinct stages-the initial production of cysteinyldopas, followed by their oxidation to produce pheomelanin, followed finally by the production of eumelanin. Based on these data, a casing model of mixed melanogenesis is proposed in which a preformed pheomelanic core is covered by a eumelanic surface.
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                Author and article information

                Contributors
                tiffany.slater@ucc.ie
                maria.mcnamara@ucc.ie
                patrick.orr@ucd.ie
                t.foley@ucc.ie
                sito@fujita-hu.ac.jp
                kwaka@fujita-hu.ac.jp
                Journal
                Palaeontology
                Palaeontology
                10.1111/(ISSN)1475-4983
                PALA
                Palaeontology
                John Wiley and Sons Inc. (Hoboken )
                0031-0239
                19 September 2019
                January 2020
                : 63
                : 1 ( doiID: 10.1111/pala.v63.1 )
                : 103-115
                Affiliations
                [ 1 ] School of Biological, Earth & Environmental Sciences University College Cork Cork Ireland
                [ 2 ] UCD School of Earth Sciences University College Dublin Dublin Ireland
                [ 3 ] Department of Anatomy & Neuroscience University College Cork Cork Ireland
                [ 4 ] Department of Chemistry Fujita Health University School of Health Sciences Toyoake Aichi Japan
                Author information
                https://orcid.org/0000-0003-1475-8376
                Article
                PALA12445
                10.1111/pala.12445
                6988486
                32025055
                5778c66b-d663-410c-bf4f-cebd9ca84d6a
                © The Authors. Palaeontology published by John Wiley & Sons Ltd on behalf of The Palaeontological Association

                This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc-nd/4.0/ License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non‐commercial and no modifications or adaptations are made.

                History
                : 04 February 2019
                : 15 May 2019
                Page count
                Figures: 7, Tables: 1, Pages: 13, Words: 7425
                Funding
                Funded by: European Research Council Starting Grant , open-funder-registry 10.13039/100010663;
                Award ID: 2014‐ERC‐StG‐637691‐ANICOLEVO
                Categories
                Original Article
                Original Articles
                Custom metadata
                2.0
                January 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.5 mode:remove_FC converted:21.01.2020

                mouldic melanosome,fossil colour,fossil feather,experimental taphonomy,melanin,keratin

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