Abstract

Ichthyosaurs are extinct marine reptiles that display a notable external similarity to modern toothed whales. Here we show that this resemblance is more than skin deep. We apply a multidisciplinary experimental approach to characterize the cellular and molecular composition of integumental tissues in an exceptionally preserved specimen of the Early Jurassic ichthyosaur Stenopterygius. Our analyses recovered still-flexible remnants of the original scaleless skin, which comprises morphologically distinct epidermal and dermal layers. These are underlain by insulating blubber that would have augmented streamlining, buoyancy and homeothermy. Additionally, we identify endogenous proteinaceous and lipid constituents, together with keratinocytes and branched melanophores that contain eumelanin pigment. Distributional variation of melanophores across the body suggests countershading, possibly enhanced by physiological adjustments of colour to enable photoprotection, concealment and/or thermoregulation. Convergence of ichthyosaurs with extant marine amniotes thus extends to the ultrastructural and molecular levels, reflecting the omnipresent constraints of their shared adaptation to pelagic life.

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Data availability

The Stenopterygius specimen examined in this study (MH 432) is permanently accessioned in the collections of Urweltmuseum Hauff, Holzmaden, Germany. The data supporting our findings are available from the corresponding author upon reasonable request.

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Acknowledgements

We thank E. R. Schroeter for scientific advice. S. M. Webb and C. Roach assisted during the SRS-XRF analysis. T. Wigren produced the artistic reconstructions. Financial support was provided by a Grant for Distinguished Young Researchers (642-2014-3773, Swedish Research Council) to J.L., as well as a National Science Foundation INSPIRE grant (EAR-1344198) to M.H.S. and W.Z., and donations from F. M. and S. P. Orr, and V. and G. Mullis. The Paul Scherrer Institute, Switzerland, provided beamtime at the TOMCAT beamline of the Swiss Light Source. SRS-XRF data were collected at the Stanford Synchrotron Radiation Lightsource using beamline 10-2. NanoSIMS measurements were obtained at the Chemical Imaging Infrastructure, Chalmers University of Technology and University of Gothenburg, which is supported by the Knut and Alice Wallenberg Foundation. Part of this work was performed at the Analytical Instrumentation Facility (AIF) of North Carolina State University. The AIF is supported by the State of North Carolina and the National Science Foundation (ECCS-1542015) and is a member of the North Carolina Research Triangle Nanotechnology Network, a site within the National Nanotechnology Coordinated Infrastructure.

Reviewer information

Nature thanks A. Houssaye, B. Kessler, S. Kiel and R. N. S. Sodhi for their contribution to the peer review of this work.

Author information

Affiliations

  1. Department of Geology, Lund University, Lund, Sweden

    • Johan Lindgren
    • , Carl Alwmark
    • , Mats E. Eriksson
    • , Martin Jarenmark
    •  & Mary H. Schweitzer
  2. RISE Research Institutes of Sweden, Chemistry and Materials, Borås, Sweden

    • Peter Sjövall
  3. Geobiology, Geoscience Centre, University of Göttingen, Göttingen, Germany

    • Volker Thiel
  4. Department of Biological Sciences, North Carolina State University, Raleigh, NC, USA

    • Wenxia Zheng
    •  & Mary H. Schweitzer
  5. Department of Chemistry, Fujita Health University School of Health Sciences, Toyoake, Japan

    • Shosuke Ito
    •  & Kazumasa Wakamatsu
  6. Urweltmuseum Hauff, Holzmaden, Germany

    • Rolf Hauff
  7. Museum of Evolution, Uppsala University, Uppsala, Sweden

    • Benjamin P. Kear
  8. MAX-IV laboratory, Lund University, Lund, Sweden

    • Anders Engdahl
  9. Naturkunde-Museum Bielefeld, Abteilung Geowissenschaften, Bielefeld, Germany

    • Sven Sachs
  10. Science for Life Laboratory, Uppsala University, Uppsala, Sweden

    • Per E. Ahlberg
  11. Department of Organismal Biology, Uppsala University, Uppsala, Sweden

    • Per E. Ahlberg
  12. Swiss Light Source, Paul Scherrer Institute, Villigen, Switzerland

    • Federica Marone
  13. Institute of Natural and Environmental Sciences, University of Hyogo, Hyogo, Japan

    • Takeo Kuriyama
  14. Wildlife Management Research Center, Hyogo, Japan

    • Takeo Kuriyama
  15. Department of Biology, Lund University, Lund, Sweden

    • Ola Gustafsson
  16. Department of Chemistry and Chemical Engineering, Chalmers University of Technology, Gothenburg, Sweden

    • Per Malmberg
  17. Department of Chemistry and Molecular Biology, University of Gothenburg, Gothenburg, Sweden

    • Aurélien Thomen
  18. Centre for Analysis and Synthesis, Department of Chemistry, Lund University, Lund, Sweden

    • Irene Rodríguez-Meizoso
  19. Chemical Physics, Department of Chemistry, Lund University, Lund, Sweden

    • Per Uvdal
  20. Department of Applied Biosciences, Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Japan

    • Makoto Ojika
  21. North Carolina Museum of Natural Sciences, Raleigh, NC, USA

    • Mary H. Schweitzer

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Contributions

J.L. conceived the project. The text was written by J.L. and B.P.K. with contributions from S.S., P.S., M.H.S. and P.E.A., and feedback from all authors. All figures were assembled by J.L. with input from all authors. R.H. collected and prepared MH 432. J.L., P.S. and M.J. recorded the SRS-XRF measurements; O.G., P.S., C.A., T.K. and J.L. conducted the FEG-SEM and TEM analyses; V.T. performed the Py-GC/MS experiments; S.I. and K.W. carried out the alkaline hydrogen peroxide oxidation analysis; M.H.S. and W.Z. conducted the immunohistochemistry investigation; P.S. and J.L. performed the ToF-SIMS experiments; A.T., P.M., J.L. and P.S. carried out the NanoSIMS analysis; A.E., J.L. and P.U. recorded the infrared microspectroscopic measurements; M.E.E. and F.M. acquired the SRXTM data; M.O. performed the amino acid analysis; and M.J. and I.R.-M. conducted the maturation experiments.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Johan Lindgren.

Extended data figures and tables

  1. Extended Data Fig. 1 Regular, ultraviolet light and SRS-XRF images of MH 432.

    a, Skin compressed onto the diagenetically flattened gastralia basket. b, Amorphous adipocere (arrows) external to the gastralia and liver residue (arrowheads) within the abdominal cavity. c, Fibrous muscle or connective tissue on the left side of the trunk. dm, Some of the anatomical features, and the stone putty used to reassemble the individual blocks, are enhanced under ultraviolet light. Note the differences in fluorescence between the putty (arrowheads in f), internal structures (arrowheads in g) and integument (arrowheads in i). n, SRS-XRF false-colour images showing the spatial distribution of silicon (magenta), phosphorous (green) and copper (blue). o, SRS-XRF false-colour images showing the spatial distribution of iron (red), sulfur (yellow) and zinc (blue). The lack of co-localization between copper, zinc and the preserved soft tissues might result from calcium phosphate overprinting.

  2. Extended Data Fig. 2 Light microscopy, TEM, EDX and NanoSIMS data from MH 432 integument.

    a, Transverse section through demineralized epidermis (sample 13a) showing epidermal ridges (arrowheads) and invasive sediments (dashed line). b, TEM micrograph through the stratified epidermis (sample 13). Stc, stratum corneum; sti/stg, stratum intermedium and/or stratum germinativum. c, Enlargement of a branched epidermal melanophore. d, Squamous keratinocytes from between the stratum intermedium and stratum corneum (sample 10); these become progressively flattened towards the exterior surface (top). Arrowheads, cellular envelopes. e, TEM section through the fibrous superficial dermis (sample 12a). f, Back-scattered electron micrograph and single-element EDX maps of untreated integument in external view. Coloured images illustrate the relative abundance of each element, with higher intensities indicating greater abundance. Note the enrichment of calcium and phosphorous in the fossilized epidermis and dermis. Intensities from carbon derive primarily from the underlying conductive tape. Al, aluminium (lime); C, carbon (red); Ca, calcium (blue); Fe, iron (violet); K, potassium (turquoise blue); O, oxygen (yellow); P, phosphorous (purple); S, sulfur (orange); Si, silicon (turquoise). g, Back-scattered electron micrograph and single-element EDX maps of untreated integument in internal view (colours as in f). Note high levels of carbon (arrows) and localized enrichment of calcium (arrowheads) in the blubber and subjacent fibrous tissue. Intensities from silicon and oxygen derive primarily from authigenic silica minerals. h, High-resolution NanoSIMS images acquired from demineralized skin showing the distribution of CH, CN, P, S and CaO (sample 13a). CN-rich microbodies are melanosomes (see Extended Data Fig. 3e).

  3. Extended Data Fig. 3 Three-dimensional visualization and chemistry of MH 432 melanophores.

    a, SRXTM renderings of branched melanophores (sample 18). b, FEG-SEM micrograph of a dermal melanophore and adjacent organic matter recovered from demineralized integument (sample 13a). Note the remnant cell body (arrow) and external moulds of disrupted pigment organelles in the polymerized matrix of one dendrite (arrowheads). c, FEG-SEM micrograph of a dermal melanophore and adjacent organic matter from demineralized integument (sample 13). Note the clustered melanosomes that represent the cell body (arrow), and dendritic extensions packed with pigment organelles (arrowheads). d, Back-scattered electron micrograph and single-element EDX maps of the melanophore in Fig. 3e–g. Coloured images illustrate the relative abundance of each element, with higher intensities indicating greater abundance. Note the enrichment of carbon and, to a lesser extent, sulfur and oxygen in the fossil pigment cell. Intensities from calcium and fluoride derive from the underlying spectrophotometric window (see g). Al, aluminium (lime); C, carbon (red); Ca, calcium (blue); Cu, copper (dark red); F, fluoride (green); O, oxygen (yellow); P, phosphorous (purple); S, sulfur (orange); Si, silicon (turquoise). e, High-resolution NanoSIMS images of the melanophore in Fig. 3h–k showing the distribution of CH, CN, P, S and CaO. Note the relatively high levels of CN and S in the melanosomes, whereas the surrounding matrix also contains measurable amounts of CH and P. f, The alkaline hydrogen peroxide oxidation products PTCA, PDCA and PTeCA (Fig. 3r) from samples 7a (two batches), 10a (two batches), 10b, 13a, 13d and 14a (two batches). g, Infrared spectrum from the melanophore in Fig. 3e–g (arrowhead in the inset light microscopy image) showing peaks attributed to hydrocarbons and phosphate.

  4. Extended Data Fig. 4 Pyrolysis data collected at 560 °C for 10 s, from the soft tissues of MH 432.

    a, Py-GC/MS chromatograms obtained from MH 432 (TIC, total ion currents). The prominent peak series in each sample represents homologous n-alkenes and n-alkanes; chromatograms are normalized to the highest of these peaks. Inset ion chromatograms (m/z 217) illustrate the distribution of eukaryote-derived steranes, with 27 and 29 denoting carbon numbers. S and R denote (20S)-5α,14α,17α(H) and (20R)-5α,14α,17α(H) isomers, respectively. Abundant C27-steranes (cholestanes) in the integument constitute diagenetic products of ichthyosaur cholesterol. The predominant 20R isomer is also indicated in the TICs to illustrate its abundance among the total pyrolysates. C29-steranes (stigmastanes) reflect background sedimentation from algae and/or terrestrial plants. Note the high amount of cholestanes in the integument and greater abundance of stigmastanes in the host rock. Also note the higher intensities of aromatics (relative to aliphatics), diasteranes (relative to regular steranes) and a stronger unresolved complex mixture in the liver, reflecting original compositional differences and/or enhanced biodegradation. b, Py-GC/MS ion chromatograms (m/z 250, normalized to sample weight) showing a compound tentatively identified as n-octadecadiene (arrowheads, n-C18:2). This molecule is interpreted as a pyrolysis product of kerogen-bound n-octadecenyl (n-C18:1) moieties potentially originating from oleic acid (C18:1ω9c), the most abundant monoenoic fatty acid in extant vertebrates. Note the localized occurrence within the flank integument (where the blubber is best preserved). Replicate sample measurements (denoted by i and ii) are provided to demonstrate reproducibility.

  5. Extended Data Fig. 5 ToF-SIMS images and spectra from MH 432 integument.

    a, Images of positive ions (sample 2) that are characteristic of (from left to right) peptides/proteins (C4H8N+, m/z 70), polyaromatic hydrocarbons (C9H7+, m/z 115; C10H8+, m/z 128; C11H7+, m/z 139; C11H9+, m/z 141; C12H8+, m/z 152; C13H9+, m/z 165; C14H10+, m/z 178; C15H9+, m/z 189; and C16H10+, m/z 202) and the sedimentary matrix (Al+, m/z 27; Si+, m/z 28; and K+, m/z 39), along with a three-colour overlay image of these ions in which green represents proteinaceous matter, red represents polyaromatic hydrocarbons and blue represents sediment. b, Positive ion spectra from selected regions of interest indicated in the three-colour overlay image in a (green demarcations highlight areas dominated by proteinaceous matter; red lines frame regions rich in polyaromatic hydrocarbons). Characteristic aliphatic and polyaromatic hydrocarbon peaks are indicated by triangles and circles, respectively, in the top spectrum (red regions of interest), whereas typical protein fragment ions are denoted by stars in the bottom spectrum (green regions of interest; see Supplementary Information). c, Negative ion images of sample 13a (see Fig. 5m) representing (top row, from left to right) sulfur-containing materials (SO3, m/z 80 and C4HS, m/z 81), phosphate (PO2, m/z 63 and PO3, m/z 79) and the sedimentary matrix (SiO3, m/z 76; SiHO3, m/z 77; and AlSiO4, m/z 119), together with a three-colour overlay image of these ions in red, green and blue, respectively. The bottom row shows the spatial distribution of ions representing eumelanin (C3N, m/z 50; C3NO, m/z 66; and C5N, m/z 74) and epoxy (C2H3O2, m/z 59 and C3H3O2, m/z 71), along with a five-colour overlay image featuring sulfur-containing ions (red), phosphate (green), eumelanin (yellow), epoxy (cyan) and sediment (blue); the total ion image is shown on the far right.

  6. Extended Data Fig. 6 Amino acid analysis data from MH 432.

    ad, Liquid chromatography condition I. a, Standard amino acids (200 pmol per 4 μl). b, Sample 7a, liver (a 4-μl portion of 8.51 mg per 170 μl). c, Sample 13d, integument (a 4-μl portion of 10.27 mg per 206 μl). d, Sample 14a, sediment (a 4-μl portion of 10.05 mg per 201 μl). eh, Liquid chromatography condition II. e, Standard amino acids (200 pmol per 4 μl). f, Sample 7a, liver (a 5-μl portion of 8.51 mg per 340 μl). g, Sample 13d, integument (a 5-μl portion of 10.27 mg per 411 μl). h, Sample 14a, sediment (a 5-μl portion of 10.05 mg per 402 μl). Chromatograms for the unstable amino acids asparagine, cysteine, glutamine and tryptophan were omitted from the figure. Additionally, aspartic acid, methionine and tyrosine were not detected (either owing to their low ionization efficacy or lability). Peaks with retention times similar to those of glycine and serine in the condition-II chromatograms derive from impurities (as demonstrated by the corresponding amino acid peaks in the condition-I chromatograms). Data from condition I were used for alanine, glutamic acid, glycine and serine; data from condition II were used for all other amino acids. The solvent for standard amino acids and extracted samples was 0.1 M HCl. hSer, homoserine. ‘x’ denotes an impurity.

  7. Extended Data Fig. 7 Immunoreactivity of fossil ichthyosaur and extant leatherback sea turtle skin.

    at, Immunohistochemical staining and immunogold labelling of demineralized MH 432 skin (samples 8 and 12a) (ah) versus experimentally treated D. coriacea skin (it), exposed to antibodies raised against Bos taurus elastin (a, b), G. domesticus actin (c, d), A. mississippiensis collagen (e, f, k, l), G. domesticus feathers (indicative of β-keratin) (g, h), G. domesticus tropomyosin (i, j), A. mississippiensis haemoglobin (m, n), S. camelus haemoglobin (o, p) and G. domesticus α-keratin (qt). Images in a, c, e, g, i, k, m, o, q show where the antibodies bind to tissue (green) superimposed on transmitted light images. Fluorescein isothiocyanate fluorescence in b, d, f, h, j, l, n, p, r indicates binding for all antibodies except β-keratin. In D. coriacea, the migration from the epidermis to underlying tissues of compounds derived from α-keratin probably reflects the combined effects of decay, compaction and maturation. De/hy, dermis and hypodermis (corresponding to blubber in adult D. coriacea); epi, epidermis. s, t, Low-resolution (s) and high-resolution (t) localization of anti-α-keratin antibody tagged with gold to fibrous matter in D. coriacea skin. Note the filamentous structures (arrowhead).

  8. Extended Data Fig. 8 Ultrastructure and chemistry of the liver of MH 432.

    a, Polygonal surface structure of the red-brown organ trace (arrowheads). Note the irregular patches of phosphatized adipocere (A) overlying the mineralized internal structure, and a vertebral centrum (vert) that has penetrated the decomposing tissue before fossilization. b, Light microscopy section through demineralized liver matrix (sample 1), which reveals its layered architecture that is probably produced by diagenetic compaction. c, FEG-SEM micrograph of pliable organic matter released via treatment with EDTA (sample 1). d, Enlargement showing a degraded and somewhat fibrous (arrowheads) biomass. eh, Overlay (e, g) and fluorescent (f, h) images of demineralized liver material (sample 7) exposed to antibodies raised against A. mississippiensis (e, f) and S. camelus haemoglobin (g, h). i, TEM micrograph of probable cellular membranes (arrowheads). j, TEM micrograph showing a dense melanosome cluster (sample 1). k, Positive ion ToF-SIMS spectrum with peaks characteristic of aliphatics (triangles) and polyaromatics (circles; sample 1).

  9. Extended Data Fig. 9 Experimental maturation of extant skin and subcutis to simulate the effects of diagenesis.

    a, Stained light microscopy section through the scaly carapace integument from a juvenile D. coriacea. Bm, basement membrane; de, dermis; mel, melanophore; stc, stratum corneum; stg, stratum germinativum; and sti, stratum intermedium. b, Autoclave-treated carapace integument from a juvenile D. coriacea showing flattened keratinocytes and melanophores (arrowheads). c, Scaleless carapace integument of an adult D. coriacea revealing multiple layers of stratified squamous keratinocytes. Note the greater thickness of the stratum intermedium in the adult relative to the juvenile individual (compare with a). d, Enlargement of the stratum corneum and stratum intermedium. e, Melanized P. phocoena body integument. B, blubber (dermis and subcutis); epi, epidermis; s, outer skin surface (in oblique aspect). f, Side (top) and internal (bottom) views of artificially compressed P. phocoena integument. g, Light microscopy section through artificially compressed P. phocoena integument showing the condensed blubber layer (compare with e). Er, epidermal ridge. h, Side (top) and internal (bottom) views of P. phocoena integument following autoclave experiments. i, Stained light microscopy section through autoclave-treated integument of P. phocoena. j, Enlargement of the loosely packed superficial blubber (Bs)—a possible entry for microbes (compare Extended Data Fig. 10d)—and dense deeper blubber (Bd). k, Melanosomes in experimentally treated epidermis of P. phocoena. l, m, Shrunken, membrane-bound (arrowheads) adipocytes (or lipid vesicles) in experimentally treated blubber of P. phocoena (compare Extended Data Fig. 10g). nq, Overlay (n, p) and fluorescent (o, q) images of experimentally treated integument of P. phocoena, exposed to antibodies raised against G. domesticus α-keratin (n, o) and G. domesticus tropomyosin (p, q).

  10. Extended Data Fig. 10 Taphonomy of MH 432.

    a, Cross-section through the main rock slab (left side of posterior termination) in original geological orientation, showing sediment infill between the integument (arrow) and a sectioned vertebra (vert). Saturated mud (arrowheads) encased the carcass following gravitational collapse of the backbone. b, Natural break through the main slab (centre of posterior termination) exposing intrusive sediment infill into the body cavity before disarticulation of the vertebral column. Arrowheads indicate the liver residue. c, Cross-section through the main slab (right side of posterior termination). Note the invasive sediment covering the residual soft parts (arrows) and dorsal ribs from the right side of the body (arrowheads). d, Light microscopy section through demineralized integument (sample 13a) with clay minerals and inferred bacteria (delimited by dashed line) penetrating between the phosphatized epidermis and/or dermis (Epi/de) and polymerized blubber (B). Skin (stars) and melanophores (arrowheads) occur along with hollow structures interpreted as bacterial cellular bodies (circles) and massed melanosomes (arrows). e, TEM micrograph of sample 13a showing clay minerals (arrowheads) and bacterial cells (arrows). f, Enlarged melanosome concentration produced by microbially mediated skin reduction. g, Adipocyte or lipid vesicle (compare Extended Data Fig. 9l, m), or microbe (compare with i), with well-developed cellular membrane (arrow) and adjacent melanosomes (arrowheads). h, Collapsed thick-walled bacterial cells (arrowheads) that suggest microorganismal infestation before fossilization and diagenetic compaction (sample 13a). i, Comparative image of extant bone-boring bacteria (arrows) showing retention of cellular membranes (arrowheads) after removal of internal contents. j, Decomposed skin of MH 432 (sample 13).

Supplementary information

  1. Supplementary Information

    This file contains Supplementary text Part A-J which includes Supplementary Tables S1 and S2.

  2. Reporting Summary

  3. Video 1: Three-Dimensional Structure of a MH 432 Melanophore

    Volume rendering of a SRXTM dataset showing a melanophore with long dendritic processes (Sample 18).

  4. Video 2: Elasticity of MH 432 Fibrous Tissue

    Free-floating (in Milli-Q water) fibrous tissue (Sample 21) liberated from the enclosing phosphatic matrix by treatment with EDTA. Note flexibility upon manipulation.

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DOI

https://doi.org/10.1038/s41586-018-0775-x

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