Vision and the diversification of Phanerozoic marine invertebrates

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.

[1]  W. Kiessling,et al.  Phanerozoic Marine Biodiversity: A Fresh Look at Data, Methods, Patterns and Processes , 2012 .

[2]  E. Clarkson,et al.  Eyes and vision in the Chengjiang arthropod Isoxys indicating adaptation to habitat , 2011 .

[3]  M. Martindale,et al.  Ciliary photoreceptors in the cerebral eyes of a protostome larva , 2011, EvoDevo.

[4]  Martin R. Smith,et al.  Primitive soft-bodied cephalopods from the Cambrian , 2010, Nature.

[5]  R. Plotnick,et al.  Information landscapes and sensory ecology of the Cambrian Radiation , 2010, Paleobiology.

[6]  S. Johnsen,et al.  Spatial vision in the purple sea urchin Strongylocentrotus purpuratus (Echinoidea) , 2010, Journal of Experimental Biology.

[7]  W. R. A. Muntz Visual Behavior and Visual Sensitivity of Nautilus pompilius , 2010 .

[8]  Dan-Eric Nilsson,et al.  The evolution of eyes and visually guided behaviour , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[9]  Anders Garm,et al.  Structure and optics of the eyes of the box jellyfish Chiropsella bronzie , 2009, Journal of Comparative Physiology A.

[10]  B. Morton The Evolution of Eyes in the Bivalvia: New Insights* , 2008 .

[11]  David Jablonski,et al.  Species Selection: Theory and Data , 2008 .

[12]  J. Alroy Dynamics of origination and extinction in the marine fossil record , 2008, Proceedings of the National Academy of Sciences.

[13]  Karen M. Layou,et al.  Phanerozoic Trends in the Global Diversity of Marine Invertebrates , 2008, Science.

[14]  W. Kiessling,et al.  Environmental determinants of marine benthic biodiversity dynamics through Triassic–Jurassic time , 2007 .

[15]  A. Knoll,et al.  Paleophysiology and End-Permian Mass Extinction , 2007 .

[16]  W. Kiessling,et al.  Faunal evidence for reduced productivity and uncoordinated recovery in Southern Hemisphere Cretaceous-Paleogene boundary sections , 2007 .

[17]  G. Horváth,et al.  The eyes of trilobites: The oldest preserved visual system. , 2006, Arthropod structure & development.

[18]  M. Kosnik,et al.  Abundance Distributions Imply Elevated Complexity of Post-Paleozoic Marine Ecosystems , 2006, Science.

[19]  T. Waller Phylogeny of families in the Pectinoidea (Mollusca: Bivalvia): importance of the fossil record , 2006 .

[20]  M. Land,et al.  Gereral purpose and special purpose visual systems , 2006 .

[21]  Joshua S Madin,et al.  Statistical Independence of Escalatory Ecological Trends in Phanerozoic Marine Invertebrates , 2006, Science.

[22]  J. Lupovitch In the Blink of an Eye: How Vision Sparked the Big Bang of Evolution , 2006 .

[23]  R. Fernald Casting a genetic light on the evolution of eyes. , 2006, Science.

[24]  D. Jablonski Evolutionary innovations in the fossil record: the intersection of ecology, development, and macroevolution. , 2005, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[25]  P. Parsons Environments and evolution: interactions between stress, resource inadequacy and energetic efficiency , 2005, Biological reviews of the Cambridge Philosophical Society.

[26]  Sasha R. X. Dall,et al.  Information and its use by animals in evolutionary ecology. , 2005, Trends in ecology & evolution.

[27]  G. Hendler An echinoderm‚Äôs eye view of photoreception and vision , 2004 .

[28]  A. Queiroz Contingent predictability in evolution: key traits and diversification. , 2002 .

[29]  A. Knoll,et al.  Anatomical and ecological constraints on Phanerozoic animal diversity in the marine realm , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[30]  R. Feist Trilobites from the latest Frasnian Kellwasser crisis in North Africa [Mrirt, Central Moroccan Meseta] , 2002 .

[31]  A. de Queiroz Contingent predictability in evolution: key traits and diversification. , 2002, Systematic biology.

[32]  B. Morton The evolution of eyes in the Bivalvia , 2001 .

[33]  M. Foote Origination and extinction components of taxonomic diversity: general problems , 2000, Paleobiology.

[34]  B. Marcotte Turbidity, arthropods and the evolution of perception: toward a new paradigm of marine phanerozoic diversity , 1999 .

[35]  A. Queiroz DO IMAGE‐FORMING EYES PROMOTE EVOLUTIONARY DIVERSIFICATION? , 1999 .

[36]  A. de Queiroz DO IMAGE-FORMING EYES PROMOTE EVOLUTIONARY DIVERSIFICATION? , 1999, Evolution; international journal of organic evolution.

[37]  R. Fortey,et al.  Post-cambrian trilobite diversity and evolutionary faunas , 1998, Science.

[38]  Mary L. Droser,et al.  Evaluating the ecological architecture of major events in the Phanerozoic history of marine invertebrate life , 1997 .

[39]  S. Heard,et al.  Key evolutionary innovations and their ecological mechanisms , 1995 .

[40]  C. Zuker,et al.  On the evolution of eyes: would you like it simple or compound? , 1994, Science.

[41]  J. Seyer Structure and optics of the eye of the hawk-wing conch, Strombus raninus (L.) , 1994 .

[42]  M. Foote Survivorship analysis of Cambrian and Ordovician trilobites , 1988, Paleobiology.

[43]  D. Raup,et al.  Mass Extinctions in the Marine Fossil Record , 1982, Science.

[44]  L. W. Alvarez,et al.  Extraterrestrial Cause for the Cretaceous-Tertiary Extinction , 1980, Science.

[45]  David M. Raup,et al.  Principles Of Paleontology , 1978 .

[46]  E. Mayr,et al.  On the evolution of photoreceptors and eyes , 1977 .

[47]  K. Corbett The Late Cambrian to Early Ordovician sequence on the Denison Range, southwest Tasmania , 1975, Papers and Proceedings of The Royal Society of Tasmania.

[48]  M. Wiener,et al.  Animal eyes. , 1957, The American orthoptic journal.