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Title: Hierarchical biota-level and taxonomic controls on the chemistry of fossil melanosomes revealed using synchrotron X-ray fluorescence

Abstract

Fossil melanosomes, micron-sized granules rich in melanin in vivo, provide key information for investigations of the original coloration, taxonomy and internal anatomy of fossil vertebrates. Such studies rely, in part, on analysis of the inorganic chemistry of preserved melanosomes and an understanding of melanosome chemical taphonomy. The extent to which the preserved chemistry of fossil melanosomes is biased by biotic and abiotic factors is, however, unknown. Here we report the discovery of hierarchical controls on the inorganic chemistry of melanosomes from fossil vertebrates from nine biotas. The chemical data are dominated by a strong biota-level signal, indicating that the primary taphonomic control is the diagenetic history of the host sediment. This extrinsic control is superimposed by a biological, tissue-level control; tissue-specific chemical variation is most likely to survive in fossils where the inorganic chemistry of preserved melanosomes is distinct from that of the host sediment. Comparative analysis of our data for fossil and modern amphibians reveals that most fossil specimens show tissue-specific melanosome chemistries that differ from those of extant analogues, strongly suggesting alteration of original melanosome chemistry. Collectively, these findings form a predictive tool for the identification of fossil deposits with well-preserved melanosomes amenable to studies of fossil colour andmore » anatomy.« less

Authors:
 [1];  [2];  [1]
  1. Univ. College Cork (Ireland). School of Biological, Earth and Environmental Sciences
  2. SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
Publication Date:
Research Org.:
SLAC National Accelerator Lab., Menlo Park, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities Division; European Research Council (ERC)
OSTI Identifier:
1817156
Grant/Contract Number:  
AC02-76SF00515; ERC-2014-StG-637691
Resource Type:
Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Biogeochemistry; Evolution

Citation Formats

Rossi, Valentina, Webb, Samuel M., and McNamara, Maria E. Hierarchical biota-level and taxonomic controls on the chemistry of fossil melanosomes revealed using synchrotron X-ray fluorescence. United States: N. p., 2020. Web. doi:10.1038/s41598-020-65868-3.
Rossi, Valentina, Webb, Samuel M., & McNamara, Maria E. Hierarchical biota-level and taxonomic controls on the chemistry of fossil melanosomes revealed using synchrotron X-ray fluorescence. United States. https://doi.org/10.1038/s41598-020-65868-3
Rossi, Valentina, Webb, Samuel M., and McNamara, Maria E. Tue . "Hierarchical biota-level and taxonomic controls on the chemistry of fossil melanosomes revealed using synchrotron X-ray fluorescence". United States. https://doi.org/10.1038/s41598-020-65868-3. https://www.osti.gov/servlets/purl/1817156.
@article{osti_1817156,
title = {Hierarchical biota-level and taxonomic controls on the chemistry of fossil melanosomes revealed using synchrotron X-ray fluorescence},
author = {Rossi, Valentina and Webb, Samuel M. and McNamara, Maria E.},
abstractNote = {Fossil melanosomes, micron-sized granules rich in melanin in vivo, provide key information for investigations of the original coloration, taxonomy and internal anatomy of fossil vertebrates. Such studies rely, in part, on analysis of the inorganic chemistry of preserved melanosomes and an understanding of melanosome chemical taphonomy. The extent to which the preserved chemistry of fossil melanosomes is biased by biotic and abiotic factors is, however, unknown. Here we report the discovery of hierarchical controls on the inorganic chemistry of melanosomes from fossil vertebrates from nine biotas. The chemical data are dominated by a strong biota-level signal, indicating that the primary taphonomic control is the diagenetic history of the host sediment. This extrinsic control is superimposed by a biological, tissue-level control; tissue-specific chemical variation is most likely to survive in fossils where the inorganic chemistry of preserved melanosomes is distinct from that of the host sediment. Comparative analysis of our data for fossil and modern amphibians reveals that most fossil specimens show tissue-specific melanosome chemistries that differ from those of extant analogues, strongly suggesting alteration of original melanosome chemistry. Collectively, these findings form a predictive tool for the identification of fossil deposits with well-preserved melanosomes amenable to studies of fossil colour and anatomy.},
doi = {10.1038/s41598-020-65868-3},
journal = {Scientific Reports},
number = 1,
volume = 10,
place = {United States},
year = {Tue Jun 02 00:00:00 EDT 2020},
month = {Tue Jun 02 00:00:00 EDT 2020}
}

Works referenced in this record:

An Exceptionally Preserved Three-Dimensional Armored Dinosaur Reveals Insights into Coloration and Cretaceous Predator-Prey Dynamics
journal, August 2017


Direct chemical evidence for eumelanin pigment from the Jurassic period
journal, May 2012

  • Glass, K.; Ito, S.; Wilby, P. R.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 26
  • DOI: 10.1073/pnas.1118448109

What's the use of generating melanin?
journal, April 1999


T HE R OLE OF D ECAY AND M INERALIZATION IN THE P RESERVATION OF S OFT -B ODIED F OSSILS
journal, May 2003


Infrared mapping resolves soft tissue preservation in 50 million year-old reptile skin
journal, March 2011

  • Edwards, N. P.; Barden, H. E.; van Dongen, B. E.
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 278, Issue 1722
  • DOI: 10.1098/rspb.2011.0135

The association of zinc and other metals with melanin and a melanin-protein complex
journal, March 1953

  • Bowness, J. M.; Morton, R. A.
  • Biochemical Journal, Vol. 53, Issue 4
  • DOI: 10.1042/bj0530620

Phosphatization of soft-tissue in experiments and fossils
journal, November 1993

  • Briggs, D. E. G.; Kear, A. J.; Martill, D. M.
  • Journal of the Geological Society, Vol. 150, Issue 6
  • DOI: 10.1144/gsjgs.150.6.1035

Tissue-specific geometry and chemistry of modern and fossilized melanosomes reveal internal anatomy of extinct vertebrates
journal, August 2019

  • Rossi, Valentina; McNamara, Maria E.; Webb, Sam M.
  • Proceedings of the National Academy of Sciences, Vol. 116, Issue 36
  • DOI: 10.1073/pnas.1820285116

Skin pigmentation provides evidence of convergent melanism in extinct marine reptiles
journal, January 2014

  • Lindgren, Johan; Sjövall, Peter; Carney, Ryan M.
  • Nature, Vol. 506, Issue 7489
  • DOI: 10.1038/nature12899

Binding of Metal Ions to Melanin and Their Effects on the Aerobic Reactivity¶
journal, January 2004


Molecular preservation of the pigment melanin in fossil melanosomes
journal, January 2012

  • Lindgren, Johan; Uvdal, Per; Sjövall, Peter
  • Nature Communications, Vol. 3, Issue 1
  • DOI: 10.1038/ncomms1819

Melanosomes: Biogenesis, Properties, and Evolution of an Ancient Organelle
journal, January 2019


High-performance liquid chromatography estimation of cross-linking of dihydroxyindole moiety in eumelanin
journal, March 2013

  • Ito, Shosuke; Wakamatsu, Kazumasa; Glass, Keely
  • Analytical Biochemistry, Vol. 434, Issue 2
  • DOI: 10.1016/j.ab.2012.12.005

The colour of fossil feathers
journal, July 2008

  • Vinther, Jakob; Briggs, Derek E. G.; Prum, Richard O.
  • Biology Letters, Vol. 4, Issue 5
  • DOI: 10.1098/rsbl.2008.0302

Dietary mineral content influences the expression of melanin-based ornamental coloration
journal, October 2006


Melanin Chemistry and the Ecology of Stress
journal, May 2015

  • Galván, Ismael; Solano, Francisco
  • Physiological and Biochemical Zoology, Vol. 88, Issue 3
  • DOI: 10.1086/680362

Ion-Exchange and Adsorption of Fe(III) by Sepia Melanin
journal, June 2004


The role of the calcium carbonate-calcium phosphate switch in the mineralization of soft-bodied fossils
journal, September 1996

  • Briggs, Derek E. G.; Wilby, Philip R.
  • Journal of the Geological Society, Vol. 153, Issue 5
  • DOI: 10.1144/gsjgs.153.5.0665

The mapping and differentiation of biological and environmental elemental signatures in the fossil remains of a 50 million year old bird
journal, January 2015

  • Egerton, Victoria M.; Wogelius, Roy A.; Norell, Mark A.
  • Journal of Analytical Atomic Spectrometry, Vol. 30, Issue 3
  • DOI: 10.1039/C4JA00395K

Experimental maturation of feathers: implications for reconstructions of fossil feather colour
journal, June 2013

  • McNamara, Maria E.; Briggs, Derek E. G.; Orr, Patrick J.
  • Biology Letters, Vol. 9, Issue 3
  • DOI: 10.1098/rsbl.2013.0184

The eyes of Tullimonstrum reveal a vertebrate affinity
journal, April 2016

  • Clements, Thomas; Dolocan, Andrei; Martin, Peter
  • Nature, Vol. 532, Issue 7600
  • DOI: 10.1038/nature17647

Fossilized melanosomes and the colour of Cretaceous dinosaurs and birds
journal, January 2010

  • Zhang, Fucheng; Kearns, Stuart L.; Orr, Patrick J.
  • Nature, Vol. 463, Issue 7284
  • DOI: 10.1038/nature08740

The MicroAnalysis Toolkit: X-ray Fluorescence Image Processing Software
conference, January 2011

  • Webb, S. M.; McNulty, Ian; Eyberger, Catherine
  • THE 10TH INTERNATIONAL CONFERENCE ON X-RAY MICROSCOPY, AIP Conference Proceedings
  • DOI: 10.1063/1.3625338

Chemical, experimental, and morphological evidence for diagenetically altered melanin in exceptionally preserved fossils
journal, September 2015

  • Colleary, Caitlin; Dolocan, Andrei; Gardner, James
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 41
  • DOI: 10.1073/pnas.1509831112

Natural melanin pigments and their interfaces with metal ions and oxides: emerging concepts and technologies
journal, May 2017

  • Di Mauro, Eduardo; Xu, Ri; Soliveri, Guido
  • MRS Communications, Vol. 7, Issue 2
  • DOI: 10.1557/mrc.2017.33

A bony-crested Jurassic dinosaur with evidence of iridescent plumage highlights complexity in early paravian evolution
journal, January 2018


Synchrotron-based chemical imaging reveals plumage patterns in a 150 million year old early bird
journal, January 2013

  • Manning, Phillip. L.; Edwards, Nicholas P.; Wogelius, Roy A.
  • Journal of Analytical Atomic Spectrometry, Vol. 28, Issue 7
  • DOI: 10.1039/c3ja50077b

Non-random decay of chordate characters causes bias in fossil interpretation
journal, January 2010

  • Sansom, Robert S.; Gabbott, Sarah E.; Purnell, Mark A.
  • Nature, Vol. 463, Issue 7282
  • DOI: 10.1038/nature08745

Countershading and Stripes in the Theropod Dinosaur Sinosauropteryx Reveal Heterogeneous Habitats in the Early Cretaceous Jehol Biota
journal, November 2017


3D Camouflage in an Ornithischian Dinosaur
journal, September 2016

  • Vinther, Jakob; Nicholls, Robert; Lautenschlager, Stephan
  • Current Biology, Vol. 26, Issue 18
  • DOI: 10.1016/j.cub.2016.06.065

Pheomelanin pigment remnants mapped in fossils of an extinct mammal
journal, May 2019

  • Manning, Phillip L.; Edwards, Nicholas P.; Bergmann, Uwe
  • Nature Communications, Vol. 10, Issue 1
  • DOI: 10.1038/s41467-019-10087-2

Current Understanding of the Binding Sites, Capacity, Affinity, and Biological Significance of Metals in Melanin
journal, July 2007

  • Hong, Lian; Simon, John D.
  • The Journal of Physical Chemistry B, Vol. 111, Issue 28
  • DOI: 10.1021/jp071439h

Trace Metals as Biomarkers for Eumelanin Pigment in the Fossil Record
journal, June 2011


Molecular composition and ultrastructure of Jurassic paravian feathers
journal, August 2015

  • Lindgren, Johan; Sjövall, Peter; Carney, Ryan M.
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep13520

Interpreting melanin-based coloration through deep time: a critical review
journal, August 2015

  • Lindgren, Johan; Moyer, Alison; Schweitzer, Mary H.
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 282, Issue 1813
  • DOI: 10.1098/rspb.2015.0614

Taphonomic experiments resolve controls on the preservation of melanosomes and keratinous tissues in feathers
journal, September 2019

  • Slater, Tiffany S.; McNamara, Maria E.; Orr, Patrick J.
  • Palaeontology, Vol. 63, Issue 1
  • DOI: 10.1111/pala.12445

Occurrence of the potent mutagens 2- nitrobenzanthrone and 3-nitrobenzanthrone in fine airborne particles
journal, January 2019

  • Santos, Aldenor G.; da Rocha, Gisele O.; de Andrade, Jailson B.
  • Scientific Reports, Vol. 9, Issue 1
  • DOI: 10.1038/s41598-018-37186-2

Fossilization of melanosomes via sulfurization
journal, April 2016

  • McNamara, Maria E.; van Dongen, Bart E.; Lockyer, Nick P.
  • Palaeontology, Vol. 59, Issue 3
  • DOI: 10.1111/pala.12238

Impact of diagenesis and maturation on the survival of eumelanin in the fossil record
journal, November 2013


Soft-Tissue Preservation in Miocene Frogs from Libros, Spain: Insights into the Genesis of Decay Microenvironments
journal, February 2009


Melanosomes or Microbes: Testing an Alternative Hypothesis for the Origin of Microbodies in Fossil Feathers
journal, March 2014

  • Moyer, Alison E.; Zheng, Wenxia; Johnson, Elizabeth A.
  • Scientific Reports, Vol. 4, Issue 1
  • DOI: 10.1038/srep04233

A multiplatform code for the analysis of energy-dispersive X-ray fluorescence spectra
journal, January 2007

  • Solé, V. A.; Papillon, E.; Cotte, M.
  • Spectrochimica Acta Part B: Atomic Spectroscopy, Vol. 62, Issue 1
  • DOI: 10.1016/j.sab.2006.12.002

Non-integumentary melanosomes can bias reconstructions of the colours of fossil vertebrates
journal, July 2018

  • McNamara, Maria E.; Kaye, Jonathan S.; Benton, Michael J.
  • Nature Communications, Vol. 9, Issue 1
  • DOI: 10.1038/s41467-018-05148-x

Synchrotron X-ray absorption spectroscopy of melanosomes in vertebrates and cephalopods: implications for the affinity of Tullimonstrum
journal, October 2019

  • Rogers, Christopher S.; Astrop, Timothy I.; Webb, Samuel M.
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 286, Issue 1913
  • DOI: 10.1098/rspb.2019.1649