Spotlight on the evolution of vision

1 Since the 1980s our understanding of the evolution of visual systems has undergone an explosion with the advent of technologies for molecular and genomic analyses. The revolutionary fi nding that put the evolution of vision into the spotlight was the demonstration that homeodomain-containing transcription factors controlling pattern formation and development in the fl y eye could also do so in mice and humans (Ton et al., 1991 ; Glaser et al., 1992 ; Quiring et al., 1994 ; Halder et al., 1995 ; Gehring & Ikeo, 1999 ). These landmark discoveries revealed that organisms with anatomically and morphologically different visual systems contain remarkably similar genes. This stimulated a proliferation of exciting work, prompting a reassessment of the evolution of eyes (Gehring & Ikeo, 1999 ; Arendt, 2003 ; Plachetzki et al., 2005 ; Nilsson & Arendt, 2008 ; Collin et al., 2009 ; Lamb et al., 2009 ; Nilsson, 2009 ; Yau & Hardie, 2009 ; Fain et al., 2010 ; Jacobs, 2010 ; Feuda et al., 2012 ; Porter et al., 2012 ). These similarities among organisms are not only limited to developmentally controlled genes. Studies in invertebrates have contributed to uncovering signal transduction mechanisms in our eyes. For example, an invertebrate-related r-opsin, melanopsin, was discovered in intrinsically photoreceptive ganglion cells (ipRGC) in the vertebrate eye (Provencio et al., 2000 ; Graham et al., 2008 ). Further reminiscent of the invertebrate signaling cascade, the transient receptor potential channels 6 and 7 (TRPC6 and TRPC7) function in the ipRGCs through a phospholipase C (PLC) signaling cascade, demonstrating that ipRGCs use an invertebrate-type phototransduction cascade. The discovery of additional invertebrate-related TRP channels (TRPM1) in ON-bipolar cells (Morgans et al., 2009 ; Shen et al., 2009 ) has lent further support to the recognition that studies on the visual systems of invertebrates offer powerful information about human eyes. TRP channels were fi rst discovered in Drosophila and mutations in the trp gene lead to retinal degeneration in fruit fl ies (Minke, 2010 ; Hardie, 2011 ; Montell, 2011 ). Likewise, mutations in TRPM1 are linked to autosomal-recessive congenital stationary night blindness in humans (Audo et al., 2009 ). Interestingly, it is estimated that 90% of the disease-causing genes in humans have counterparts in organisms that emerged very early in evolution, prior to the bilaterian radiation (about 520–540 million years ago during the Cambrian explosion) (Domazet-Loso & Tautz, 2008 ). Investigators continue to capitalize on a host of versatile genetic, electrophysiological, molecular, cell biological and biochemical techniques to dissect fundamental processes in a variety of experimental organisms. These studies are aimed at not only for understanding the evolution of vision and visual function but also for developing treatments and potential cures for human eye diseases (Fadool et al., 1997 ; Wang & Montell, 2007 ; Nilsson, 2009 ; Yau & Hardie, 2009 ; Colley, 2010 ; Fain et al., 2010 ; Jacobs, 2010 ; Hardie, 2011 ; Montell, 2012 ). For example, even the light-activated protein pumps used by microbes, channelrhodopsin and halorhodopsin, are providing a way to restore light sensitivity to retinas whose photoreceptors have degenerated. They have also proved useful in optogenetics technologies aimed at uncovering neural circuits (Deisseroth, 2011 ; Greenberg et al., 2011 ; Polosukhina et al., 2012 ). These examples underscore the importance of investigating all lightsensitive systems independent of their shedding light on the evolution of vision. A sequence of stages has been envisioned to explain how a primitive eyespot evolved to become a complex camera-type eye (Nilsson & Arendt, 2008 ; Nilsson, 2009 ). In multicellular organisms, these fl at eyespots can be simple single-cell photoreceptors, scattered on the surface. Some eyespots have no associated pigment cells and are unable to detect the direction of a light source. It is thought that the eyespot dimpled inward to form a pit or cup eye. This provides higher visual acuity by allowing the eye to sense the direction of light. Flatworms are an example of an organism with this type of eye, which can do little more than to detect movement. It is proposed that the eye then became constricted at the eye opening, forming a narrower aperture. This advance enabled sharper imaging abilities, and the chambered nautilus has such an eye. However, in order to further increase visual acuity, the aperture would need to be so small that it would shut out much light. So a lens was needed, and, subsequently, the image became sharper and sharper as eye evolution proceeded to produce the complex camera-type human eye (Nilsson & Arendt, 2008 ; Nilsson, 2009 ). Despite the perceived simplicity of microbes, jellyfi sh, worms, fruit fl ies and fi sh, they are remarkably complex creatures with genetic make-ups that are surprisingly similar to our own. In this issue, three articles are focused on our current knowledge of the evolution of vision from the earliest of known visual systems, consisting of simple eyespots, to pit eyes and cup eyes, to lowresolution eyes and fi nally to the complex high-resolution cameratype eye. In studying evolution, it is often found that molecular data point in one direction and morphological fi ndings in another (Nilsson & Arendt, 2008 ; Nilsson, 2009 ). First, Nilsson provides new details on how eye evolution is directed by the demands of visually guided behavior. He discusses how in evolution the progression of gradually more complex behaviors made demands for increasing the performance of photoreceptor organs. Nilsson proposes a sequence of four sensory tasks, beginning with nondirectional photoreception, followed by directional photoreception, low-resolution vision and culminating in high-resolution vision. To understand why certain morphological features, physiology and molecular make-up have evolved, he points out that it is important to understand the selection INTRODUCTION