Towards a Better Understanding of the Origins of Microlens Arrays in Mesozoic Ophiuroids and Asteroids

Abstract

Echinoderms are characterized by a calcite endoskeleton with a unique microstructure, which is optimized for multiple functions. For instance, some light-sensitive ophiuroids (Ophiuroidea) and asteroids (Asteroidea) possess skeletal plates with multi-lens arrays that are thought to act as photosensory organs. The origins of these lens-like microstructures have long been unclear. It was recently proposed that the complex photosensory systems in certain modern ophiuroids and asteroids could be traced back to at least the Late Cretaceous (ca. 79 Ma). Here, we document similar structures in ophiuroids and asteroids from the Early Cretaceous of Poland (ca. 136 Ma) that are approximately 57 million years older than the oldest asterozoans with lens-like microstructures described thus far. We use scanning electron microscopy, synchrotron tomography, and electron backscatter diffraction combined with focused ion beam microscopy to describe the morphology and crystallography of these structures in exceptional detail. The results indicate that, similar to Recent light-sensitive ophiuroids, putative microlenses in Cretaceous ophiuroids and asteroids exhibit a shape and crystal orientation that would have minimized spherical aberration and birefringence. We suggest that these lens-like microstructures evolved by secondary deposition of calcite on pre-existing porous tubercles that were already present in ancestral Jurassic forms.

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References

  1. Aizenberg, J., & Hendler, G. (2004). Designing efficient microlens arrays: lessons from nature. Journal of Materials Chemistry, 14, 2066–2072.

    CAS  Article  Google Scholar 

  2. Aizenberg, J., Tkachenko, A., Weiner, S., Addadi, L., & Hendler, G. (2001). Calcitic microlenses as part of the photoreceptor system in brittlestars. Nature, 412, 819–822.

    CAS  Article  PubMed  Google Scholar 

  3. Aronson, R. B. (1987). Predation on fossil and Recent ophiuroids. Paleobiology, 13, 187–192.

    Article  Google Scholar 

  4. Aronson, R. B. (1989). A community-level test of the Mesozoic marine revolution theory. Paleobiology, 15, 20–25.

    Article  Google Scholar 

  5. Aronson, R. B. (1991). Predation, physical disturbance and sub-lethal arm damage in ophiuroids: A Jurassic-Recent comparison. Marine Ecology Progress Series, 74, 91–97.

    Article  Google Scholar 

  6. Blake, D.B., Tintori, A., & Hagdorn, H. (2000). A new asteroid (Echinodermata) from the Norian (Triassic) Calcare di Zorzino of northern Italy: Its stratigraphic occurrence and phylogenetic significance. Rivista Italiana di Paleontologia e Stratigrafia, 106, 141–156.

    Google Scholar 

  7. Cunningham, J. A., Rahman, I. A., Lautenschlager, S., Rayfield, E. J., & Donoghue, P.C.J. (2014). A virtual world of palaeontology. Trends in Ecology & Evolution, 29, 347–357.

    Article  Google Scholar 

  8. Delroisse, J., Mallefet, J., & Flammang, P. (2016). De novo adult transcriptomes of two European brittle stars: Spotlight on opsin-based photoreception. PLoS ONE, 11, e0152988. doi:10.1371/journal.pone.0152988.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Döderlein, L. (1898). Ueber “Krystallkörper” bei Seesternen. Denkschriften der Medizinisch Naturwissenschaftlichen Gesellschaft zu Jena, 8, 491–494.

    Google Scholar 

  10. Dubois, P., & Hayt, S. (1990). Ultrastructure des ossicules d’échinodermes à stéréome non perforé. In C. De Ridder, P. Dubois; M.C. Lahaye & M. Jangoux (Eds.), Echinoderm research (pp. 217–223). Rotterdam: Balkema.

    Google Scholar 

  11. Gale, A. (2011). Asteroidea (Echinodermata) from the Oxfordian (Late Jurassic) of Savigna, Départment [sic!] du Jura, France. Swiss Journal of Palaeontology, 130, 69–89.

    Article  Google Scholar 

  12. Garm, A., & Nilsson, D. E. (2014). Visual navigation in starfish: first evidence for the use of vision and eyes in starfish. Proceedings of the Royal Society B: Biological Sciences, 281, 2013–3011.

    Article  Google Scholar 

  13. Głuchowski, E. (1987). Jurassic and Early Cretaceous articulate Crinoidea from the Pieniny Klippen Belt and Tatra Mts. Poland. Studia Geologica Polonica, 94, 1–102.

    Google Scholar 

  14. Gorzelak, P., & Salamon, M. A. (2009). Signs of benthic predation on Late Jurassic stalked crinoids, preliminary data. Palaios, 24, 70–73.

    Article  Google Scholar 

  15. Gorzelak, P., Salamon. M. A., & Baumiller, T. K. (2012). Predator-induced macroevolutionary trends in Mesozoic crinoids. Proceedings of the National Academy of Sciences of the United States of America, 109, 7004–7007.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. Gorzelak, P., Salamon, M. A., Lach, R., Loba, M., & Ferré, B. (2014). Microlens arrays in the complex visual system of Cretaceous echinoderms. Nature Communications, 5, 3576. doi:10.1038/ncomms4576.

    Article  PubMed  Google Scholar 

  17. Heatfield, B. M. (1971). Growth of the calcareous skeleton during regeneration of spines of the sea urchin Strongylocentrotus purpuratus (Stimpson); a light and scanning electron microscope study. Journal of Morphology, 134, 57–90.

    Article  Google Scholar 

  18. Hendler, G. (1984). Brittlestar color-change and phototaxis (Echinodermata: Ophiuroidea: Ophiocomidae). Marine Ecology, 5, 379–401.

    Article  Google Scholar 

  19. Hendler, G. (2004). An echinoderm’s eye view of photoreception and vision. In T. Heinzeller, & J. Nebelsick (Eds.), Echinoderms; Munchen; Proceedings of the 11th International Echinoderm Conference. (pp. 339–350). Leiden: A.A. Balkema Publishers.

    Google Scholar 

  20. Hendler, G., & Byrne, M. (1987). Fine structure of the dorsal arm plate of Ophiocoma wendti (Echinodermata, Ophiuroidea). Zoomorphology, 107, 261–272.

    Article  Google Scholar 

  21. Hess, H., Salamon, M. A., & Gorzelak, P. (2011). Late Jurassic-Early Cretaceous (Tithonian-Berriasian) cyrtocrinids from south-eastern Poland. Neues Jahrbuch für Geologie und Paläontologie, Abhandlungen, 260, 119–128.

    Article  Google Scholar 

  22. Kaim, A. (2001). Faunal dynamics of juvenile gastropods and associated organisms across the Valanginian transgression-regression cycle in central Poland. Cretaceous Research, 22, 333–351.

    Article  Google Scholar 

  23. Killian, C. E., & Wilt, F. H. (2008). Molecular aspects of biomineralization of the echinoderm endoskeleton. Chemical Reviews, 108, 4463–4474.

    CAS  Article  PubMed  Google Scholar 

  24. Mah, C. L. (2005). A phylogeny of Iconaster and Glyphodiscu s (Goniasteridae; Valvatida; Asteroidea) with descriptions of four new species. Zoosystema, 27, 131–167.

    Google Scholar 

  25. Politi, Y., Arad, T., Klein, E., Weiner, S., & Addadi, L. (2004). Sea urchin spine calcite forms via a transient amorphous calcium phase. Science, 306, 1161–1164.

    CAS  Article  PubMed  Google Scholar 

  26. Raup, D. M. (1966). The endoskeleton. In R. A. Boolootian (Ed.), Physiology of echinodermata (pp. 379–395). New York: Interscience.

    Google Scholar 

  27. Salamon, M. A. (2007). First record of bourgueticrinid crinoids from the Cenomanian of southern Poland. Cretaceous Research, 28, 459–499.

    Article  Google Scholar 

  28. Salamon, M. A. (2008). The Callovian (Middle Jurassic) crinoids from northern Lithuania. Paläontologische Zeitschrift, 82, 269–278.

    Article  Google Scholar 

  29. Salamon, M. A. (2009). Early Cretaceous (Valanginian) sea lilies (Echinodermata, Crinoidea) from Poland. Swiss Journal of Geosciences, 102, 77–88.

    CAS  Article  Google Scholar 

  30. Salamon, M. A., & Gorzelak, P. (2010a). Cyrtocrinids (Echinodermata, Crinoidea) from Upper Jurassic Štramberk-type limestones in southern Poland. Palaeontology, 53, 869–885.

    Article  Google Scholar 

  31. Salamon, M. A., & Gorzelak, P. (2010b). Late Cretaceous crinoids (Crinoidea) from Eastern Poland. Palaeontographica Abt. A, 291, 1–43.

    Article  Google Scholar 

  32. Salamon, M. A., Niedźwiedzki, R., Lach, R., Brachaniec, T., & Gorzelak, P. (2012). Ophiuroids discovered in the Middle Triassic hypersaline environment. PLoS ONE, 7(11), e49798. doi:10.1371/journal.pone.0049798.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. Salamon, M. A., & Zatoń, M. (2007). Late Bajocian through Callovian (Middle Jurassic) crinoid fauna from the epicontinental deposits of Poland. Swiss Journal of Geosciences, 100, 153–164.

    Article  Google Scholar 

  34. Smith, A. B. (1990). Biomineralization in echinoderms. In J. G. Carter (Ed.), Skeletal biomineralization: Patterns, processes, and evolutionary trends (pp. 413–443). New York: Van Nostrand Reinhold.

    Google Scholar 

  35. Stampanoni, M., et al. (2007). TOMCAT: A beamline for tomographic microscopy and coherent radiology experiments. AIP Conference Proceedings, 879, 848.

    CAS  Article  Google Scholar 

  36. Sutton, M. D., Rahman, I. A., & Garwood, R. J. (2014). Techniques for virtual palaeontology. New York: Wiley.

    Google Scholar 

  37. Sweatman, H.P.A. (1995). A field study of fish predation on juvenile crown-of-thorns starfish. Coral Reefs, 14(1), 47–53.

    Article  Google Scholar 

  38. Torney, C., Lee, M. R., & Owen, A. W. (2014). Microstructure and growth of the lenses of schizochroal trilobite eyes. Palaeontology, 57, 783–799.

    Article  Google Scholar 

  39. Ullrich-Lüter, E.M., Dupont, S., Arboleda, E., Hausen, H., & Arnone, M.I. (2011). Unique system of photoreceptors in sea urchin tube feet. Proceedings of the National Academy of Sciences of the United States of America, 108, 8367–8372.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Vermeij, G. J. (1977). The Mesozoic marine revolution; evidence from snails, predators and grazers. Paleobiology, 3, 245–258.

    Article  Google Scholar 

  41. Villier, L. (2008). Sea star ossicles from the Callovian black clays of the Łuków area, eastern Poland. Neues Jahrbuch für Geologie und Paläontologie, Abh, 247, 147–160.

    Article  Google Scholar 

  42. Villier, L., Charbonnier, S., & Riou, B. (2009). Sea stars from Middle Jurassic Lagerstätte of La Volute sur Rhône (Ardèche, France). Journal of Paleontology, 83, 389–398.

    Article  Google Scholar 

  43. Villier, L., Kutscher, M., & Mah, C.H.L. (2004). Systematics and palaecology of middle Toarcian Asteroidea (Echinodermata) from the ‘Seuil du Poitou’, Western France. Geobios, 37, 807–825.

    Article  Google Scholar 

  44. Vinogradova, E., Ruíz-Zepeda, F., Plascencia-Villa, G., & José-Yacamán, M. (2016). Calcitic microlens arrays in Archaster typicus: Microstructural evidence for an advanced photoreception system in modern starfish. Zoomorphology, 135, 83–87.

    Article  Google Scholar 

  45. Walker, M. H. (1978). Food and feeding habits of Lethrinus chrysostomus Richardson (Pisces: Perciformes) and other Lethrinids on the Great Barrier Reef. Australian Journal of Marine & Freshwater Research, 29(5), 623–630.

    Article  Google Scholar 

  46. Wei, T., Sun, Y., Zhang, B., Wang, R., & Xu, T. (2014). A mitogenomic perspective on the phylogenetic position of the Hapalogenys genus (Acanthopterygii: Perciformes) and the evolutionary origin of perciformes. PLoS ONE, 9(7), e103011. doi:10.1371/journal.pone.0103011.

    Article  PubMed  PubMed Central  Google Scholar 

  47. Yamamoto, M., & Yoshida, M. (1978). Fine structure of the ocelli of a synaptid holothurian,Opheodesoma spectabilis, and the effects of light and darkness. Zoomorphologie, 90, 1–17.

    Article  Google Scholar 

  48. Yoshida, M. (1966). Photosensitivity. In R. A. Boolootian (Ed.), Physiology of echinodermata (pp. 435–464). New York: Wiley.

    Google Scholar 

  49. Zatoń, M., Salamon, M. A., Boczarowski, A., & Sitek, S. (2008a). Taphonomy of dense ophiuroid accumulations from the Middle Triassic of Poland. Lethaia, 41(1), 47–58.

    Article  Google Scholar 

  50. Zatoń, M., Salamon, M. A., & Kaźmierczak, J. (2008b). Cyrtocrinids (Crinoidea) and associated stalked crinoids from the Lower/Middle Oxfordian (Upper Jurassic) shelfal deposits of southern Poland. Geobios, 41, 559–569.

    Article  Google Scholar 

  51. Zhang, S. (2003). Fabrication of novel biomaterials through molecular self-assembly. Nature Biotechnology, 21, 1171–1178.

    CAS  Article  PubMed  Google Scholar 

  52. Zhao, F., Bottjer, D. J., Hu, S., Yin, Z., & Zhu, M. (2013). Complexity and diversity of eyes in Early Cambrian ecosystems. Scientific Reports, 3, 2751. doi:10.1038/srep02751.

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was completed while the first author was a recipient of a grant from the Polish National Science Centre (NCN) Grant number DEC-2011/03/N/ST10/04798 and was performed in part in the NanoFun laboratory co-financed by the European Regional Development Fund within the Innovation Economy Operational Programme POIG.02.02.00-00-025/09. IAR was funded by an 1851 Royal Commission Research Fellowship. SZ was funded by grants RYC-2012-10576 and CGL2013-48877 from the Spanish MINECO. We acknowledge the Paul Scherrer Institut, Villigen, Switzerland for the provision of synchrotron radiation beamtime on the TOMCAT beamline at the Swiss Light Source and thank Professor Charles G Messing (Nova Southeastern University) for providing the extant ophiuroid specimen. We also thank two anonymous reviewers for their supportive comments.

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Gorzelak, P., Rahman, I.A., Zamora, S. et al. Towards a Better Understanding of the Origins of Microlens Arrays in Mesozoic Ophiuroids and Asteroids. Evol Biol 44, 339–346 (2017). https://doi.org/10.1007/s11692-017-9411-1

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Keywords

  • Echinoderms
  • Photosensitivity
  • Cretaceous
  • Microlenses
  • Calcite
  • Tomography