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Journal of Heredity Advance Access originally published online on January 13, 2005
Journal of Heredity 2005 96(3):171-184; doi:10.1093/jhered/esi027
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© 2005 The American Genetic Association
THE WILHEMINE E. KEY 2004 INVITATIONAL LECTURE

New Perspectives on Eye Development and the Evolution of Eyes and Photoreceptors

W. J. Gehring

From the Department of Cell Biology, Biozentrum, University of Basel, Klingelbergstrasse 70, 4056 Basel, Switzerland

Address correspondence to Walter Gehring at the address above, or e-mail: walter.gehring{at}unibas.ch

Recent experiments on the genetic control of eye development have opened up a completely new perspective on eye evolution. The demonstration that targeted expression of one and the same master control gene, that is, Pax6 can induce the formation of ectopic eyes in both insects and vertebrates, necessitates a reconsideration of the dogma of a polyphyletic origin of the various eye types in all the animal phyla. The involvement of Pax6 and six1 and six3 genes, which encode highly conserved transcription factors, in the genetic control of eye development in organisms ranging from planarians to humans argues strongly for a monophyletic origin of the eye. Because transcription factors can control the expression of any target gene provided it contains the appropriate gene regulatory elements, the conservation of the genetic control of eye development by Pax6 among all bilaterian animals is not due to functional constraints but a consequence of its evolutionary history. The prototypic eyes postulated by Darwin to consist of two cells only, a photoreceptor and a pigment cell, were accidentally controlled by Pax6 and the subsequent evolution of the various eye types occurred by building onto this original genetic program. A hypothesis of intercalary evolution is proposed that assumes that the eye morphogenetic pathway is progressively modified by intercalation of genes between the master control genes on the top of the hierarchy and the structural genes like rhodopsin at the bottom. The recruitment of novel genes into the eye morphogenetic pathway can be due to at least two different genetic mechanisms, gene duplication and enhancer fusion.



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  		(Photograph by Ch. Scholz.)

Walter J. Gehring is Professor at the Biozentrum of the University of Basel, Switzerland. He obtained his Ph.D. at the University of Zurich in 1965 and after two years as a research assistant of Professor Ernst Hadorn he joined Professor Alan Garen's group at Yale University in New Haven as a postdoctoral fellow. In 1969 he was appointed as an associate professor at the Yale Medical School and 1972 he returned to Switzerland to become a professor of developmental biology and genetics at the Biozentrum of the University of Basel. He has served as Secretary General of the European Molecular Biology Organization and President of the International Society for Developmental Biologists. He was elected as a Foreign Associate of the US National Academy of Sciences, the Royal Swedish Academy of Science, the Leopoldina, a Foreign Member of the Royal Society of London for Improving Natural Knowledge and the French Académie des Sciences.

Walter Gehring has been involved in studies of Drosophila genetics and development, particularly in the analysis of cell determination in the embryo and transdetermination of imaginal discs. He has made significant contributions to the study of the heat shock genes, various transposons and the homeotic genes which are involved in the genetic control of development. He and his group have discovered the homeobox, a DNA segment characteristic for homeotic genes which is not only present in arthropods and their ancestors, but also in vertebrates up to man. He has been involved in the development and application of enhancer trapping methods. He and his collaborators have identified Pax 6 as a master control gene for eye development, which led to a new theory about the monophyletic origin of the eyes in evolution.

 
In tracing back the evolution of eyes beyond bilaterians, we find highly developed eyes in some box-jellyfish as well as in some Hydrozoans. In Hydrozoans the same orthologous six genes (six1 and six3) are required for eye regeneration as in planarians, and in the box jellyfish Tripedalia a pax B gene, which may be a precursor of Pax6, was found to be expressed in the eyes. In contrast to the adults, which have highly evolved eyes, the Planula larva of Tripedalia has single- celled photoreceptors similar to some unicellular protists.

For the origin of photoreceptor cells in metazoa, I propose two hypotheses, one based on cellular differentiation and a more speculative one based on symbiosis. The former assumes that photoreceptor cells originated from a colonial protist in which all the cells were photosensitive and subsequent cellular differentiation to give rise to photoreceptor cells. The symbiont hypothesis, which I call the Russian doll model, assumes that photosensitivity arose first in photosynthetic cyanobacteria that were subsequently taken up into red algae as primary chloroplasts. The red algae in turn were taken up by dinoflagellates as secondary chloroplasts and in some species evolved into the most sophisticated eye organelles, as found, for example, in some dinoflagellates like Erythropsis and Warnovia, which lack chloroplasts. Because dinoflagellates are commonly found as symbionts in cnidarians, the dinoflagellates may have transferred their photoreceptor genes to cnidarians. In cnidarians such as Tripedalia the step from photoreceptor organelles to multicellular eyes has occurred. These two hypotheses, the cellular differentiation and the symbiont hypothesis, are not mutually exclusive and are the subject of further investigations.


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