Evolving eyes RUSSELL D. FERNALD* Biological Sciences and Neuroscience Program, Stanford University, Stanford, CA, USA ABSTRACT Despite the incredible diversity among extant eyes, laws of physics constrain how light can be collected resulting in only eight known optical systems in animal eyes. Surprisingly, all animal eyes share a common molecular strategy using opsin for catching photons, but there are a diverse collection of mechanisms with proteins unrelated to each other used to focus light for vision. However, opsin is expressed in either one of two types of photoreceptor that differ fundamentally in their structure and tissue of origin. Taken together, this collection of observa- tions strongly suggests that eyes have had multiple origins with remarkable convergence due to physics and molecular conservation of the opsin protein. Yet recent work has shown that a family of conserved genes are involved in eye formation despite substantial differences in their structure and origin, leading to a controversy over whether eyes evolved once or repeatedly. A likely resolution of this discussion is that particular genes and genetic programs have become associ- ated with specific features needed for eyes and such suites of genes have been recruited as new eyes evolve. Since specific genes and their products are used repeatedly, it is somewhat difficult to conceptualize their causal relationships relative to evolutionary processes. However, detailed comparison of developmental programs may offer clues about multiple origins. KEY WORDS: vertebrate eye, development, eye evolution, eye variety Int. J. Dev. Biol. 48: 701-705 (2004) doi: 10.1387/ijdb.041888rf 0214-6282/2004/$25.00 © UBC Press Printed in Spain www.ijdb.ehu.es *Address correspondence to: Dr. Russell D. Fernald. Department of Biological Sciences, Gilbert Hall, Stanford University, Stanford CA 94305, USA. Fax: +1-650-723-0881. e-mail: rfernald@stanford.edu Introduction Light has been the dominant selective force on our planet, resulting in circadian rhythms and the ubiquitous biological clock as well as the most important organ, the eye. Scientists have always been fascinated by eyes, wondering about their remarkable variety, their exquisite functional properties, their development and ultimately their evolutionary origin. As a result, we know a lot about variety in eyes, morphological sources of ocular tissue, some molecular actors responsible for eye development and even about how eyes might have evolved. This review will present highlights of these topics along with some ideas about how to think about the evolution of eyes. Eye Variety In his landmark book, Walls (1942) showed that the variety of eyes is quite astonishing and included a staggering range of adaptations produced by selective pressures for vision in different visual habitats. However, there are several features common to all eyes as a result of constraints on their construction. Since eyes collect and focus light, limits on their structure depend on the physical properties of light, which, in turn, sets limits on the optical features of eyes (c.f., Fernald, 1988, Fig. 1). For example, eyes have evolved to be sensitive to a narrow range of wavelengths relative to the broad spectrum of energy produced by sunlight. This is likely because early evolution occurred in water which strongly filters light (Fernald 1988). So the narrow range of sensitivity probably resulted from selection for biochemical mechanisms sensitive to the range of wavelengths that could penetrate water and set the stage for wavelength sensitivity during evolution. Many animal species have long since moved onto land and are exposed to the broader spectrum of EM radiation from the sun, but most animal eyes remain limited to seeing within this narrow band. Insects and some species of fish and birds later evolved receptors in ultraviolet region (e.g. Viltala et al., 1995) but the limited range of wavelength sensitivity reflects our aquatic origins, an evolutionary adaptation that persists. Of ca. 33 phyla, about a third have no specialized organ for detecting light, a third have light sensitive organs and the remainder have animals with what we would consider eyes (Land & Nilsson, 2002). Image-forming eyes evolved in six of the 33 extant metazoan phyla (Cnidaria, Mollusca, Annelida, Onychophora, Arthropoda, and Chordata), and these six contribute about 96% of the known species alive today (Land and Fernald, 1992), suggesting eyes are indeed useful. Existing eyes reflect diverse solutions to the problem of obtaining an image and range in size from a fraction of a millimeter to tens of centimeters in diameter. The range of eye