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Title: Synchrotron X-ray absorption spectroscopy of melanosomes in vertebrates and cephalopods: implications for the affinity of Tullimonstrum

Abstract

Screening pigments are essential for vision in animals. Vertebrates use melanins bound in melanosomes as screening pigments, whereas cephalopods are assumed to use ommochromes. In this work, preserved eye melanosomes in the controversial fossil Tullimonstrum (Mazon Creek, IL, USA) are partitioned by size and/or shape into distinct layers. These layers resemble tissue-specific melanosome populations considered unique to the vertebrate eye. Here, we show that extant cephalopod eyes also show tissue-specific size- and/or shape-specific partitioning of melanosomes; these differ from vertebrate melanosomes in the relative abundance of trace metals and in the binding environment of copper. Chemical signatures of melanosomes in the eyes of Tullimonstrum more closely resemble those of modern cephalopods than those of vertebrates, suggesting that an invertebrate affinity for Tullimonstrum is plausible. Melanosome chemistry may thus provide insights into the phylogenetic affinities of enigmatic fossils where melanosome size and/or shape are equivocal.

Authors:
ORCiD logo [1];  [1];  [2];  [3];  [3]; ORCiD logo [1]
  1. Univ. College Cork, Distillery Fields, Cork (Republic of Ireland)
  2. SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
  3. Fujita Health Univ. Toyoake, Aichi (Japan). School of Health Sciences
Publication Date:
Research Org.:
SLAC National Accelerator Lab., Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); European Research Starting Grant
OSTI Identifier:
1604749
Grant/Contract Number:  
AC02-76SF00515; ERC-2014-StG-637691-ANIVOLEVO
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the Royal Society B: Biological Sciences
Additional Journal Information:
Journal Volume: 286; Journal Issue: 1913; Journal ID: ISSN 0962-8452
Publisher:
The Royal Society Publishing
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; fossil soft tissues; Konservat-Lagerstätten; melanosomes; trace metals

Citation Formats

Rogers, Christopher S., Astrop, Timothy I., Webb, Samuel M., Ito, Shosuke, Wakamatsu, Kazumasa, and McNamara, Maria E. Synchrotron X-ray absorption spectroscopy of melanosomes in vertebrates and cephalopods: implications for the affinity of Tullimonstrum. United States: N. p., 2019. Web. doi:10.1098/rspb.2019.1649.
Rogers, Christopher S., Astrop, Timothy I., Webb, Samuel M., Ito, Shosuke, Wakamatsu, Kazumasa, & McNamara, Maria E. Synchrotron X-ray absorption spectroscopy of melanosomes in vertebrates and cephalopods: implications for the affinity of Tullimonstrum. United States. https://doi.org/10.1098/rspb.2019.1649
Rogers, Christopher S., Astrop, Timothy I., Webb, Samuel M., Ito, Shosuke, Wakamatsu, Kazumasa, and McNamara, Maria E. Wed . "Synchrotron X-ray absorption spectroscopy of melanosomes in vertebrates and cephalopods: implications for the affinity of Tullimonstrum". United States. https://doi.org/10.1098/rspb.2019.1649. https://www.osti.gov/servlets/purl/1604749.
@article{osti_1604749,
title = {Synchrotron X-ray absorption spectroscopy of melanosomes in vertebrates and cephalopods: implications for the affinity of Tullimonstrum},
author = {Rogers, Christopher S. and Astrop, Timothy I. and Webb, Samuel M. and Ito, Shosuke and Wakamatsu, Kazumasa and McNamara, Maria E.},
abstractNote = {Screening pigments are essential for vision in animals. Vertebrates use melanins bound in melanosomes as screening pigments, whereas cephalopods are assumed to use ommochromes. In this work, preserved eye melanosomes in the controversial fossil Tullimonstrum (Mazon Creek, IL, USA) are partitioned by size and/or shape into distinct layers. These layers resemble tissue-specific melanosome populations considered unique to the vertebrate eye. Here, we show that extant cephalopod eyes also show tissue-specific size- and/or shape-specific partitioning of melanosomes; these differ from vertebrate melanosomes in the relative abundance of trace metals and in the binding environment of copper. Chemical signatures of melanosomes in the eyes of Tullimonstrum more closely resemble those of modern cephalopods than those of vertebrates, suggesting that an invertebrate affinity for Tullimonstrum is plausible. Melanosome chemistry may thus provide insights into the phylogenetic affinities of enigmatic fossils where melanosome size and/or shape are equivocal.},
doi = {10.1098/rspb.2019.1649},
journal = {Proceedings of the Royal Society B: Biological Sciences},
number = 1913,
volume = 286,
place = {United States},
year = {2019},
month = {10}
}

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Cited by: 8 works
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Figures / Tables:

Figure 1 Figure 1: Anatomy of extant cephalopod and vertebrate eyes. Schematic illustrations of ($a$) cephalopod eye and ($b$) vertebrate eye with, inset, detail of tissue layers. ($c$) Histological sections and scanning electron micrographs (SEM) of eyes in Loligo, Octopus, Sepia and Petromyzon. Sections are stained with Warthin-Starry; melanin appears black. Allmore » tissues show melanosome-like microbodies. C. choroid; I/black arrows, iris; L, lens; 0, optic nerve; OG, optic nerve ganglia; R, retina; RPE/*, retinal pigment epithelium; RPL/arrowheads, retinal pigmented layer; S/white arrow, sclera; SCL, subciliary layer; V, vitreous humour.« less

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