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Vision and the diversification of Phanerozoic marine invertebrates

Published online by Cambridge University Press:  08 April 2016

Martin Aberhan ,
Sabine Nürnberg  and
Wolfgang Kiessling
Martin Aberhan
Affiliation:
Museum für Naturkunde, Leibniz Institute for Research on Evolution and Biodiversity at the Humboldt University Berlin, Invalidenstraße 43, D-10115 Berlin, Germany. E-mail: [email protected]
Sabine Nürnberg
Affiliation:
Museum für Naturkunde, Leibniz Institute for Research on Evolution and Biodiversity at the Humboldt University Berlin, Invalidenstraße 43, D-10115 Berlin, Germany. E-mail: [email protected]
Wolfgang Kiessling
Affiliation:
Museum für Naturkunde, Leibniz Institute for Research on Evolution and Biodiversity at the Humboldt University Berlin, Invalidenstraße 43, D-10115 Berlin, Germany. E-mail: [email protected]
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Abstract

Identifying biological traits that promote evolutionary success is fundamental for understanding biodiversity dynamics and for assessing the evolutionary response of organisms to global change. We tested the hypothesis that image-forming eyes have contributed to the diversification of taxa in the geological past. Using fossil occurrences in the Paleobiology Database, we analyzed the diversity and evolutionary rates of more than 17,000 Phanerozoic genera of marine invertebrates living on or above the shallow-water seafloor according to their visual capabilities. Analysis of the complete data set shows a peak in the proportional diversity of sighted genera early in the Phanerozoic, and their continuance at a relatively low and stable level after the Ordovician. As an explanation of this pattern we suggest that selection pressure to develop eyes rose in the Cambrian, and that behavioral constraints had a balancing effect thereafter. In contrast to the pooled data, a clade-level study of those subgroups that contain both sighted and blind genera revealed that—in trilobites, all epifaunal bivalves, pectinoid bivalves, gastropods, and echinoderms—sighted genera diversified more strongly than blind genera. This difference is controlled by significantly raised extinction rates of blind genera. These more finely resolved patterns support the hypothesis that good vision is a key trait that promoted preferential diversification.

Type
Featured Article
Information
Paleobiology , Volume 38 , Issue 2 , Spring 2012 , pp. 187 - 204
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Aberhan, M., and Kiessling, W. 2011. Phanerozoic marine biodiversity: a fresh look at data, methods, patterns and processes. InTalent, J., ed. Extinction intervals and biogeographic perturbations through time. Springer, Berlin(in press).Google Scholar
Aberhan, M., Weidemeyer, S., Kiessling, W., Scasso, R. A., and Medina, F. A. 2007. Faunal evidence for reduced productivity and uncoordinated recovery in Southern Hemisphere Cretaceous/Paleogene boundary sections. Geology 35:227–230.Google Scholar
Adrain, J. M., Fortey, R. A., and Westrop, S. R. 1998. Post-Cambrian trilobite diversity and evolutionary faunas. Science 280:1922–1925.Google Scholar
Alroy, J. 2008. Dynamics of origination and extinction in the marine fossil record. Proceedings of the National Academy of Sciences USA 105:11536–11542.Google Scholar
Alroy, J., Aberhan, M., Bottjer, D. J., Foote, M., Fürsich, F. T., Hendy, A. J. W., Holland, S. M., Ivany, L. C., Kiessling, W., Kosnik, M. A., Marshall, C. R., McGowan, A. J., Miller, A. I., Olszewski, T. D., Patzkowsky, M. E., Wagner, P. J., Bonuso, N., Borkow, P. S., Brenneis, B., Clapham, M. E., Ferguson, C. A., Hanson, V. L., Jamet, C. M., Krug, A. Z., Layou, K. M., Leckey, E. H., Nürnberg, S., Peters, S. E., Sessa, J. A., Simpson, C., Tomasovych, A., and Visaggi, C. C. 2008. Phanerozoic trends in the diversity of marine invertebrates. Science 321:97–100.Google Scholar
Alvarez, L. W., Alvarez, W., Asaro, F., and Michel, H. V. 1980. Extraterrestrial causes for the Cretaceous-Tertiary extinction. Science 208:1095–1108.Google Scholar
Bambach, R. K., Knoll, A. H., and Sepkoski, J. J. Jr. 2002. Anatomical and ecological constraints on Phanerozoic animal diversity in the marine realm. Proceedings of the National Academy of Sciences USA 99:6854–6859.Google Scholar
Clarkson, E., Levi-Setti, R., and Horváth, G. 2006. The eyes of trilobites: the oldest preserved visual system. Arthropod Structure and Development 35:247–259.Google Scholar
Dall, S. R. X., Giraldeau, L.-A., Olsson, O., McNamara, J. M., and Stephens, D. W. 2005. Information and its use by animals in evolutionary biology. Trends in Ecology and Evolution 20:187–193.Google Scholar
de Queiroz, A. 1999. Do image-forming eyes promote evolutionary diversification? Evolution 53:1654–1664.Google Scholar
de Queiroz, A. 2002. Contingent predictability in evolution: key traits and diversification. Systematic Biology 51:917–929.Google Scholar
Droser, M. L., Bottjer, D. J., and Sheehan, P. M. 1997. Evaluating the ecological architecture of major events in the Phanerozoic history of marine invertebrate life. Geology 25:167–170.Google Scholar
Feist, R. 1995. Effect of paedomorphosis in eye reduction on patterns of evolution and extinction in trilobites. Pp.225–244inMcNamara, K. J., ed. Evolutionary change and heterochrony. Wiley, Chichester, U.K.Google Scholar
Feist, R. 2002. Trilobites from the latest Frasnian Kellwasser Crisis in North Africa (Mrirt, central Moroccan Meseta). Acta Palaeontologica Polonica 47:203–210.Google Scholar
Fernald, R. D. 2006. Casting a genetic light on the evolution of eyes. Science 313:1914–1918.Google Scholar
Foote, M. 1988. Survivorship analysis of Cambrian and Ordovician trilobites. Paleobiology 14:258–271.Google Scholar
Foote, M. 2000. Origination and extinction components of taxonomic diversity: general problems. Paleobiology 26:74–102.Google Scholar
Foote, M., and Miller, A. I. 2007. Principles of paleontology. W. H. Freeman, New York.Google Scholar
Heard, S. B., and Hauser, D. L. 1995. Key evolutionary innovations and their ecological mechanisms. Historical Biology 10:151–173.Google Scholar
Hendler, G. 2004. An echinoderm's eye view of photoreception and vision. Pp.339–350inHeinzeller, T.and Nebelsick, J. H., eds. Echinoderms: München. Taylor and Francis, London.Google Scholar
Jablonski, D. 2005. Evolutionary innovations in the fossil record: the intersection of ecology, development, and macroevolution. Journal of Experimental Zoology B 304:504–519.Google Scholar
Jablonski, D. 2008. Species selection: theory and data. Annual Review of Ecology, Evolution, and Systematics 39:501–524.Google Scholar
Kiessling, W., and Aberhan, M. 2007. Environmental determinants of marine benthic biodiversity dynamics through Triassic–Jurassic time. Paleobiology 33:414–434.Google Scholar
Knoll, A. H., Bambach, R. K., Payne, J. L., Pruss, S., and Fischer, W. W. 2007. Paleophysiology and end-Permian mass extinction. Earth and Planetary Science Letters 256:295–313.Google Scholar
Land, M. F., and Nilsson, D.-E. 2002. Animal eyes. Oxford University Press, Oxford.Google Scholar
Land, M. F., and Nilsson, D-E. 2006. General-purpose and special-purpose visual systems. Pp.167–210inWarrant, E.and Nilsson, D.-E., eds. Invertebrate vision. Cambridge University Press, Cambridge.Google Scholar
Madin, J. S., Alroy, J., Aberhan, M., Fürsich, F. T., Kiessling, W., Kosnik, M. A., and Wagner, P. J. 2006. Statistical independence of escalatory ecological trends in Phanerozoic marine invertebrates. Science 312:897–900.Google Scholar
Marcotte, B. M. 1999. Turbidity, arthropods and the evolution of perception: toward a new paradigm of marine Phanerozoic diversity. Marine Ecology Progress Series 191:267–288.Google Scholar
Morton, B. 2001. The evolution of eyes in the Bivalvia. Oceanography and Marine Biology: an Annual Review 39:165–205.Google Scholar
Morton, B. 2008. The evolution of eyes in the Bivalvia: new insights. American Malacological Bulletin 26:35–45.Google Scholar
Muntz, W. R. A. 1987. Visual behavior and visual sensitivity of Nautilus pompilius. Pp.231–244inSaunders, W. B.and Landman, N. H., eds. Nautilus: the biology and paleobiology of a living fossil. Plenum, New York.Google Scholar
Nilsson, D.-E. 2009. The evolution of eyes and visually guided behaviour. Philosophical Transactions of the Royal Society of London B 364:2833–2847.Google Scholar
O'Connor, M., Garm, A., and Nilsson, D-E. 2009. Structure and optics of the eyes of the box jellyfish Chiropsella bronzie. Journal of Comparative Physiology A 195:557–569.Google Scholar
Packard, A. 1988. Visual tactics and evolutionary strategies. Pp.89–103inWiedmann, J.and Kullmann, J., eds. Cephalopods—present and past. Schweizerbart, Stuttgart.Google Scholar
Parker, A. R. 2003. In the blink of an eye: how vision sparked the big bang of evolution. Basic Books, New York.Google Scholar
Parsons, P. A. 2005. Environments and evolution: interactions between stress, resource inadequacy and energetic efficiency. Biological Reviews 80:589–610.Google Scholar
Passamaneck, Y. J., Furchheim, N., Hejnol, A., Martindale, M. Q., and Lüter, C. 2011. Ciliary photoreceptors in the cerebral eyes of a protostome larva. EvoDevo 2011, 2:6.Google Scholar
Plotnick, R. E., Dornbos, S. Q., and Chen, J. 2010. Information landscapes and sensory ecology of the Cambrian Radiation. Paleobiology 36:303–317.Google Scholar
Raup, D. M, and Sepkoski, J. J. Jr. 1982. Mass extinctions in the marine fossil record. Science 215:1501–1503.Google Scholar
Salvini-Plawen, L. V., and Mayr, E. 1977. On the evolution of photoreceptors and eyes. Evolutionary Biology 10:207–263.Google Scholar
Schoenemann, B., and Clarkson, E. N. K. 2011. Eyes and vision in the Chengjiang arthropod Isoxys indicating adaptation to habitat. Lethaia 44:223–230.Google Scholar
Seyer, J.-O. 1994. Structure and optics of the eye of the hawk-wing conch, Strombus raninus (L.). Journal of Experimental Zoology 268:200–207.Google Scholar
Smith, M. R., and Caron, J.-B. 2010. Primitive soft-bodied cephalopods from the Cambrian. Nature 465:469–472.Google Scholar
Wagner, P. J., Kosnik, M. A., and Lidgard, S. 2006. Abundance distributions imply elevated complexity of post-Paleozoic marine ecosystems. Science 314:1289–1292.Google Scholar
Waller, T. R. 2006. Phylogeny of families in the Pectinoidea (Mollusca: Bivalvia): importance of the fossil record. Zoological Journal of the Linnean Society 148:313–342.Google Scholar
Yerramilli, D., and Johnsen, S. 2010. Spatial vision in the purple sea urchin Strongylocentrotus purpuratus (Echinoidea). Journal of Experimental Biology 213:249–255.Google Scholar
Zuker, C. S. 1994. On the evolution of eyes: would you like it simple or compound? Science 265:742–743.Google Scholar