Letter | Published:

The eyes of Tullimonstrum reveal a vertebrate affinity

Nature volume 532, pages 500503 (28 April 2016) | Download Citation

Abstract

Tullimonstrum gregarium is an iconic soft-bodied fossil from the Carboniferous Mazon Creek Lagerstätte (Illinois, USA)1. Despite a large number of specimens and distinct anatomy, various analyses over the past five decades have failed to determine the phylogenetic affinities of the ‘Tully monster’, and although it has been allied to such disparate phyla as the Mollusca2, Annelida3,4 or Chordata5, it remains enigmatic1,2,3,4,5. The nature and phylogenetic affinities of Tullimonstrum have defied confident systematic placement because none of its preserved anatomy provides unequivocal evidence of homology, without which comparative analysis fails. Here we show that the eyes of Tullimonstrum possess ultrastructural details indicating homology with vertebrate eyes. Anatomical analysis using scanning electron microscopy reveals that the eyes of Tullimonstrum preserve a retina defined by a thick sheet comprising distinct layers of spheroidal and cylindrical melanosomes. Time-of-flight secondary ion mass spectrometry and multivariate statistics provide further evidence that these microbodies are melanosomes. A range of animals have melanin in their eyes, but the possession of melanosomes of two distinct morphologies arranged in layers, forming retinal pigment epithelium, is a synapomorphy of vertebrates. Our analysis indicates that in addition to evidence of colour patterning6, ecology7 and thermoregulation8, fossil melanosomes can also carry a phylogenetic signal. Identification in Tullimonstrum of spheroidal and cylindrical melanosomes forming the remains of retinal pigment epithelium indicates that it is a vertebrate; considering its body parts in this new light suggests it was an anatomically unusual member of total group Vertebrata.

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References

  1. 1.

    Wormlike fossil from the Pennsylvanian of Illinois. Science 151, 75–76 (1966)

  2. 2.

    in Mazon Creek Fossils (ed. ) 269–301 (Academic, 1979)

  3. 3.

    & Pennsylvanian invertebrates of the Mazon Creek Area, Illinois: the morphology and affinities of Tullimonstrum. Fieldiana Geol. 12, 119–149 (1969)

  4. 4.

    in The Early Evolution of Metazoa and The Significance of Problematic Taxa (eds & ) 35–46 (Cambridge Univ. Press, 1991)

  5. 5.

    in The Early Evolution of Metazoa and The Significance of Problematic Taxa (eds & ) 271–286 (Cambridge Univ. Press, 1991)

  6. 6.

    , , & The colour of fossil feathers. Biol. Lett. 4, 522–525 (2008)

  7. 7.

    et al. Fossil evidence for evolution of the shape and color of penguin feathers. Science 330, 954–957 (2010)

  8. 8.

    et al. Skin pigmentation provides evidence of convergent melanism in extinct marine reptiles. Nature 506, 484–488 (2014)

  9. 9.

    & Distinguishing heat from light in debate over controversial fossils. BioEssays 31, 178–189 (2009)

  10. 10.

    & Similarity. Biol. J. Linn. Soc. 75, 59–82 (2002)

  11. 11.

    Key characters uniting hemichordates and chordates: homologies or homoplasies? Can. J. Zool. 83, 8–23 (2005)

  12. 12.

    et al. Chemical, experimental, and morphological evidence for diagenetically altered melanin in exceptionally preserved fossils. Proc. Natl Acad. Sci. USA 112, 12592–12597 (2015)

  13. 13.

    & Pohlsepia mazonensis, an early ‘octopus’ from the Carboniferous of Illinois, USA. Palaeontology 43, 919–926 (2000)

  14. 14.

    First fossil hagfish (Myxinoidea): a record from the Pennsylvanian of Illinois. Science 254, 701–703 (1991)

  15. 15.

    & First fossil lamprey: a record from the Pennsylvanian of Illinois. Science 162, 1265–1267 (1968)

  16. 16.

    & The long-rostrumed elasmobranch Bandringa zangerl, 1969, and taphonomy within a Carboniferous shark nursery. J. Vertebr. Paleontol. 34, 22–33 (2014)

  17. 17.

    & Richardson’s Guide to The Fossil Fauna of Mazon Creek (eds & ) (Northeastern Illinois Univ., 1997)

  18. 18.

    , & Decay of vertebrate characters in hagfish and lamprey (Cyclostomata) and the implications for the vertebrate fossil record. Proc. R. Soc. B 278, 1150–1157 (2011)

  19. 19.

    , & Atlas of vertebrate decay: a visual and taphonomic guide to fossil interpretation. Palaeontology 56, 457–474 (2013)

  20. 20.

    & Photoreceptors, Their Role in Vision Vol. 5 (Cambridge Univ. Press, 1982)

  21. 21.

    & Eye evolution: common use and independent recruitment of genetic components. Phil. Trans. R. Soc. B 364, 2819–2832 (2009)

  22. 22.

    et al. Characterization of the pigment produced by the planarian, Dugesia ryukyuensis. Pigment Cell Res. 19, 248–249 (2006)

  23. 23.

    et al. Assembly of the cnidarian camera-type eye from vertebrate-like components. Proc. Natl Acad. Sci. USA 105, 8989–8993 (2008)

  24. 24.

    & Development of pigment cells in the brain of ascidian tadpole larvae: insights into the origins of vertebrate pigment cells. Pigment Cell Res. 14, 428–436 (2001)

  25. 25.

    , & The shell-eyes of the chiton Acanthopleura granulata (Mollusca, Polyplacophora) use pheomelanin as a screening pigment. J. Nat. Hist. 48, 2899–2911 (2014)

  26. 26.

    et al. Comparisons of the structural and chemical properties of melanosomes isolated from retinal pigment epithelium, iris and choroid of newborn and mature bovine eyes. Photochem. Photobiol. 81, 510–516 (2005)

  27. 27.

    & New agnathous fishes from the Pennsylvanian of Illinois. Fieldiana Geol. 33, 489–510 (1977)

  28. 28.

    & Stalked eyes as an adaptation towards more efficient foraging in marine fish larvae. Bull. Mar. Sci. 31, 31–36 (1981)

  29. 29.

    , , , & Fine structure and development of the retina of the grenadier anchovy Coilia nasus (Engraulididae, Clupeiformes). J. Morphol. 248, 41–55 (2001)

  30. 30.

    , , & Maximizing information obtained from secondary ion mass spectra of organic thin films using multivariate analysis. Surf. Sci. 570, 78–97 (2004)

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Acknowledgements

W. Simpson, P. Mayer, S. Williams, D. Rudkin and K. Seymour are thanked for specimen access and loans. Funding was through a Natural Environment Research Council studentship P14DF19 (to T.C.) and grant NE/K004557/1 (to M.A.P. and S.E.G.). We also acknowledge the National Science Foundation grant DMR-0923096 used to purchase the TOF–SIMS instrument at Texas Materials Institute, UTA. D. Murdock, C. Nedza, S. Wentges and A. Clements are thanked for proofreading. S. Furzeland is thanked for scanning electron microscope optimization. P. Smith is thanked for Adobe Illustrator tutorials.

Author information

Affiliations

  1. Department of Geology, University of Leicester, Leicester LE1 7RH, UK

    • Thomas Clements
    • , Mark A. Purnell
    •  & Sarah E. Gabbott
  2. Texas Materials Institute, The University of Texas at Austin, Austin, Texas 78712, USA

    • Andrei Dolocan
  3. School of Earth Sciences, University of Bristol, Bristol BS8 1RJ, UK

    • Peter Martin
    •  & Jakob Vinther
  4. Interface Analysis Centre, HH Wills Physics Laboratory, University of Bristol, Bristol BS8 1TQ, UK

    • Peter Martin
  5. School of Biological Sciences, University of Bristol, Bristol BS8 1TQ, UK

    • Jakob Vinther

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Contributions

S.E.G. and M.A.P. conceived the research programme of which this work is part. S.E.G., J.V. and T.C. designed and performed research. S.E.G., T.C., J.V., M.A.P. and A.D. wrote the manuscript. A.D. and J.V. undertook TOF–SIM analyses and interpretation. J.V., A.D. and M.A.P. conducted PCA. S.E.G., T.C., J.V. and P.M. operated and optimized the scanning electron microscope.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Jakob Vinther or Sarah E. Gabbott.

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https://doi.org/10.1038/nature17647

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