Chemical characterization of pterosaur melanin challenges color inferences in extinct animals

Pinheiro, Felipe L.; Prado, Gustavo; Itô, Shôsuke; Simon, John D.; Wakamatsu, Kazumasa; Anelli, Luiz Eduardo; Andrade, José Artur Ferreira Gomes de; Glass, Keely

doi:10.1038/s41598-019-52318-y

Cited by 28 publications

(23 citation statements)

References 71 publications

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“…This suggests adaptive selection of color phenotypes dominated by more carboxylated melanin monomers, potentially linked to reduced oxidative stress during or after melanogenesis. This is supported by the inferred DHICA content of fossil melanosomes in a pterosaur [62]. Selection for different forms has implications for metal-melanosome associations, as DHI has a higher capacity for binding certain elements, such as Cu and Fe, at OH groups, relative to DHICA; conversely Ti has a higher capacity for binding to DHICA (at COOH groups).…”

Section: Box 2 Pheomelanin and Evolutionary Tradeoffsmentioning

confidence: 71%

Decoding the Evolution of Melanin in Vertebrates

McNamara

Rossi

Slater

et al. 2021

Trends in Ecology & Evolution

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Melanins are widespread pigments in vertebrates, with important roles in visual signaling, UV protection, and homeostasis. Fossil evidence of melanin and melanin-bearing organellesmelanosomesin ancient vertebrates may illuminate the evolution of melanin and its functions, but macroevolutionary trends are poorly resolved. Here, we integrate fossil data with current understanding of melanin function, biochemistry, and genetics. Mapping key genes onto phenotypic attributes of fossil vertebrates identifies potential genomic controls on melanin evolution. Taxonomic trends in the anatomical location, geometry, and chemistry of vertebrate melanosomes are linked to the evolution of endothermy. These shifts in melanin biology suggest fundamental links between melanization and vertebrate ecology. Tissue-specific and taxonomic trends in melanin chemistry support evidence for evolutionary tradeoffs between function and cytotoxicity. Melanin in Vertebrates Melanins (see Glossary) are dark to rufous pigments that are widespread in vertebrates and underpin critical functions in physiology and behavior [1]. Fossil evidence of melanin extending to over 300 million years ago has triggered a paradigm shift in paleobiology, prompting remarkable reconstructions of the coloration and behavior of extinct vertebrates [2-6]. New discoveries of internal melanins in vertebrate fossils have broadened our understanding of the functional diversity of ancient melanins [7-9] and invite a re-evaluation of the macroevolutionary history of melanin and its functions. Here, we synthesize trends in the fossil record of melanin and explore fossil evidence for the evolution of melanin function and the genetic basis of melanization. This highlights the value of the fossil record as a resource for tracking melanin evolution through deep time. Functions of Melanin in Ancient Vertebrates In extant vertebrates, melanin occurs as micron-sized organelles, melanosomes, in the integument, eyes and internal tissues and functions in photoprotection, visual signaling, thermoregulation, immunity, antioxidation, mechanical strengthening, and abrasion resistance [6,10,11] (Figure 1, Box 1). It is unclear which functions evolved first and which selection pressures dominate [11,12]. Fossils preserving evidence of melanin offer a unique temporal perspective. Melanin has been reported from fossil vertebrates from >25 localities from the Carboniferous to the Pliocene (Table S1 in the supplemental information online). The fossils include cyclostomes, fish, frogs, lizards, and other squamates, ichthyosaurs, plesiosaurs, turtles, pterosaurs, feathered and nonfeathered dinosaurs, birds, and mammals. This phylogenetically and temporally broad dataset yields evidence for ancient functions of melanin (Figure 2). Highlights In extant vertebrates melanin fulfils diverse roles including visual communication, photoprotection, antioxidation, and mechanical strengthening of tissues, but the evolution of these functions is debated. The discovery that melanosomes in fossil and modern ve...

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Section: Box 2 Pheomelanin and Evolutionary Tradeoffsmentioning

confidence: 71%

Decoding the Evolution of Melanin in Vertebrates

McNamara

Rossi

Slater

et al. 2021

Trends in Ecology & Evolution

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“…However, since PTeCA decreases less than PTCA, harsh maturation leads to an increased PTeCA/PTCA ratio for all melanins studied in this work. A PTeCA/PTCA ratio with a value greater than one, sometimes up to five, is characteristic of fossil eumelanins, because this ratio reflects the degree of cross-linking [ 4 , 6 , 23 , 25 , 26 , 34 ]. Thus, the harsh maturation experiments are, in this regard, consistent with fossilized eumelanins fossil melanin.…”

Section: Discussionmentioning

confidence: 99%

Chemical Evaluation of Eumelanin Maturation by ToF-SIMS and Alkaline Peroxide Oxidation HPLC Analysis

Jarenmark

Sjövall

Ito

et al. 2020

IJMS

Self Cite

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Residual melanins have been detected in multimillion-year-old animal body fossils; however, confident identification and characterization of these natural pigments remain challenging due to loss of chemical signatures during diagenesis. Here, we simulate this post-burial process through artificial maturation experiments using three synthetic and one natural eumelanin exposed to mild (100 °C/100 bar) and harsh (250 °C/200 bar) environmental conditions, followed by chemical analysis employing alkaline hydrogen peroxide oxidation (AHPO) and time-of-flight secondary ion mass spectrometry (ToF-SIMS). Our results show that AHPO is sensitive to changes in the melanin molecular structure already during mild heat and pressure treatment (resulting, e.g., in increased C-C cross-linking), whereas harsh maturation leads to extensive loss of eumelanin-specific chemical markers. In contrast, negative-ion ToF-SIMS spectra are considerably less affected by mild maturation conditions, and eumelanin-specific features remain even after harsh treatment. Detailed analysis of ToF-SIMS spectra acquired prior to experimental treatment revealed significant differences between the investigated eumelanins. However, systematic spectral changes upon maturation reduced these dissimilarities, indicating that intense heat and pressure treatment leads to the formation of a common, partially degraded, eumelanin molecular structure. Our findings elucidate the complementary nature of AHPO and ToF-SIMS during chemical characterization of eumelanin traces in fossilized organismal remains.

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“…et al, 2011). Os pterossauros são compostos por dois clados, "Rhamphorhynchoidea" (parafilético), de cauda longa, e os de cauda curta Pterodactyloidea (Pinheiro et al, 2019).…”

Section: A Fauna Mesozoica Não-dinossauriana E Os Achados De Estrutur...unclassified

Frequência De Preservação De Biomateriais Não Mineralizados No Registro Fóssil De Répteis Mesozoicos: Uma Abordagem Sobre Pterossauros E Répteis Marinhos

Alves¹,

Machado²

2021

BJD

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Nas últimas décadas, vários estudos encontraram preservação excepcional de diferentes biomoléculas originais em dinossauros. Porém, grupos distintos de répteis que dominaram ares, mares e oceanos na Era Mesozoica, como pterossauros, ictiossauros, mosassauros, notossauros e plesiossauros, apresentam dados escassos a respeito de achados de biomateriais não mineralizados e os que já foram identificados estão dispersos na literatura, associando a ideia das descobertas a fenômenos isolados. Este trabalho apresenta uma revisão da literatura publicada nas últimas duas décadas, a fim de compreender melhor a frequência dos achados reivindicados de biomateriais não mineralizados em fósseis de répteis do clado Pterosauria e de répteis marinhos do clado Lepidosauromorpha da Era Mesozóica, frequentemente confundidos com dinossauros pelo imaginário popular. Os resultados identificaram 3 estudos descrevendo materiais orgânicos preservados para representantes de Pterosauria. Para répteis marinhos do clado Lepidosauromorpha, foram encontrados 8 estudos com achados distribuídos entre Ichthyosauria, Mosasauria, Nothosauroidea e Plesiosauria. Em geral, os dados para tais grupos não se mostraram geográfica e taxonomicamente abrangentes nas rochas mesozóicas. No entanto, acredita-se que a frequência é subnotificada, e a partir do surgimento de novas tecnologias, a previsão é de que a bioquímica fóssil seja caracterizada em maior quantidade.

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Chemical characterization of pterosaur melanin challenges color inferences in extinct animals

Cited by 28 publications

References 71 publications

Decoding the Evolution of Melanin in Vertebrates

Decoding the Evolution of Melanin in Vertebrates

Chemical Evaluation of Eumelanin Maturation by ToF-SIMS and Alkaline Peroxide Oxidation HPLC Analysis

Frequência De Preservação De Biomateriais Não Mineralizados No Registro Fóssil De Répteis Mesozoicos: Uma Abordagem Sobre Pterossauros E Répteis Marinhos

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