Evolution of vision

List of participants

Heinz Arnheiter, Ernst Bamberg, Nicolas Franceschini, Walter Gehring (organizer), Roger Hardie, David Klein, Zbynek Kozmik, Dan-Eric Nilsson, Francesca Pignoni, Claudio Punzo, Steven Reppert, Botond Roska, Hiroshi Suga, Veronica van Heyningen, Eric Warrant, Heinz Wassle, Rüdiger Wehner (organizer)





Evolution of vision
by Hiroshi Suga & Nicholas Franceschini
8 – 13 June 2009


The meeting was held from 8 to 13 June 2009, with 17 interdisciplinary experts from Europe and USA in order to explore the developmental, evolutionary, physiological, engineering, and clinical aspect of vision.


Walter J. Gehring (Biozentrum, University of Basel, Switzerland) started the meeting with his talk titled “The Evolution of Eyes and Photoreceptors”. For Charles Darwin it was difficult to explain the evolution of the eye simply by variation and selection; but he found a possible solution by proposing a simple prototypic eye consisting of two cells only a photoreceptor and a pigment cell. Such a simple eye would allow directional vision with a great selective advance. By modification and selection the various more elaborate eye could evolve. Whereas the Neodarwinists assumed a polyphyletic origin of the various eye-types in the different animal phyla, his group’s molecular genetic data favor Darwins hypothesis: a master control gene, Pax6, was identified which is shared by all bilateria and is capable of inducing eyes in both insects and vertebrates. He concluded that these findings argue strongly for a monophyletic origin of the eyes.


Francesca Pignoni (Harvard Medical School, Boston, USA) then discussed about the evolutionary conserved transcription factors in Drosophila eye development. The regulation of the proneural gene for photoreceptors, atonal, in the three visual organs of the fruit fly (eye, ocelli and Bolwig’s organ) is complex and relies on overlapping as well as distinct control regions. Direct control by the Pax6 pathway occurs through multiple sites and regulates ato expression in both retina and ocelli. The Microphthalmia-associated transcription factor (Mitf) controls RPE development in the mouse. Conflicting evidence for and against a role for Mitf in the fly eye epithelium was presented. Whether this reflects a conservation of Mitf function as a negative regulator of eye identity within the peripodial membrane of the eye disc or the ability of exogenous Mitf to tap into conserved aspects of Pax6 function remains to be determined.


Rüdiger Wehner (University of Zürich, Switzerland) presented data on how insects see the sky through their eyes. From the outside the compound eye of the Saharan desert ant Cataglyphis gives the impression of being a homogeneous array of about one thousand identical subunits, the ommatidia. But neuroanatomical, neurophysiological and behavioral analyses show that the eye and the underlying neural circuits consist of a set of distinct visual subsystems subsurving different functions in the ant’s long-distance navigation behavior such as perceiving polarized skylight (dorsal rim area), and spectral gradients in the sky (adjacent dorsal retina), or taking visual“snapshots” of landmark sceneries (20-30 degree wide visual streak along the equator of the eye). In navigation then different visual subsystems are employed, either simultaneously or successively, in path integration and landmark guidance routines.


After the lunch, Eric J. Warrant (University of Lund, Sweden) continued on the topic of insect’s vision in darkness. Nocturnal insects have recently revealed themselves to have formidable visual abilities despite the difficulties and limitations imposed by living in very dim light. Many have colour vision, can orientate using the dim polarisation pattern of the moon, and navigate using visual landmarks. He described how these remarkable abilities are supported by highly sensitive eyes and a neural strategy of spatial and temporal summation, adaptations that are currently being used to create artificial seeing systems for use in very dim light.


Nicolas Franceschini (CNRS, Marseille, France) presented his “biorobotic” approach to study the operation of the insect compound eye, which is a jewel of microoptics and microcircuits that evolved from the eye of the cambrian trilobites. To better grasp the complex problems that insects’ eyes and brains had to solve, Franceschini’s group has been attempting for 25 years to reconstruct visuo-motor systems using optics and electronics, after analyzing in particular the mechanism involved in motion sensitive neurons in the housefly, using single neuron recording and single photoreceptor stimulations. Meanwhile, motion sensitive “electronic neurons” have equipped many terrestrial and aerial robots in the group, which are able to behave autonomously and avoid obstacles by sensing the optic flow generated by their own locomotion. This novel approach has already shed new light on neural circuits and enigmatic behavioral patterns described in insects over the last 70 years, while providing air- and space technologies with novel autopilot principles.


On the morning of June 10, Heinz Wässle (Max Plank Institute for Brain Research, Germany) discussed on evolution of color vision in mammals. Most mammals are dichromats and have S-cones and M-cones, which represent the primordial color vision system. Old world primates and humans are trichromats and their color vision is based on S-cones, M-cones and L-cones. The question was addressed, how trichromatic vision is supported by the common mammalian retinal circuitry.


After the coffee break, Roger C. Hardie (Cambridge University, UK) presented his study on the phototransduction in microvillar photoreceptors. Two classes of photoreceptors have emerged during animal evolution: ciliary (eg vertebrate rods) and microvillar (eg rhabdomeric photoreceptors of most invertebrates). Microvillar photoreceptors in Drosophila, generate larger and faster responses to single photons than rods, but can nevertheless light adapt to cover the entire range of environmental illuminance. This performance is achieved using a phospholipase C based cascade culminating in the activation of Ca selective TRP channels. Key features which enable this performance include ultracompartmentalization afforded by the tiny microvilli, a lipid, membrane delimited second messenger which restricts activation by a single photon to channels in a single microvillus, and rapid Ca-dependent positive and negative feedbacks mediated by Ca influx via TRP channels.


Heinz Arnheiter (NIH, Bethsda, USA) then described the transcription regulation in the retinal pigment epithelium (RPE). The optic vesicles of the developing vertebrate embryo initially express a set of transcription factors which later in development are sorted into, and selectively used in, its principal derivatives, the future retina and the retinal pigment epithelium. Pax6, however, remains expressed in both retina and RPE. Using genetically sensitized backgrounds, i.e. mutant alleles of the microphthalmia transcription factor, his group shows that Pax6 has anti-retinogenic properties in the future RPE, in contrast to its well-known pro-retinogenic activities in the future retina. This phenomenon underscores the transcriptional versatility of Pax6.


After the lunch, Ernst Bamberg (Max-Planck Institute of Biophysics, Germany) talked about his groundbreaking work on channelrhodopsins discovered originally in Chlamydomonas. The molecular mechanisms and their applications were discussed. The most promising medical applications of channelrhodopsins were also discussed by Botond Roska, the next speaker.

Botond Roska (Friedrich Miescher Institute for Biomedical Research, Basel, Switzerland) presented his work on the retinal neural circuits and medical applications of his group’s study. The first part of his talk focuses on how neural circuits of the retina extract relevant visual features from the visual scene. He introduced a neural circuit that is sensitive to looming motion and discussed the mechanism that makes it looming sensitive. Next, he showed how transsynaptic viruses in combination with a genetic address book of retinal cell types can be used to highlight neural connectivity in a retinal circuit that entrains the circadian rhythm. Finally, he demonstrated circuit specific optogenetic techniques to restore visual function in blind mice.


After dinner, the participants were kindly invited to a concert performed by a singer who is supported by the foundation.


As the first speaker on June 11, Veronica van Heyningen (MRC Human Genetics Unit, UK) presented her study on genetics of eye disease and its evolutionary implication. Heterozygous loss of function mutations in three interacting transcription factors, PAX6, SOX2 and OTX2 lead to aniridia, microphthalmia and anophthalmia in humans. Chromosomal breakpoints 150 kb downstream of PAX6 also cause loss of function, suggesting a requirement for a large cis-regulatory region. Such regulatory elements, tested in mouse or zebrafish reporter systems, suggest that each expressing tissue requires multiple elements to regulate gene expression and each element has multiple targets; how they work together remains to be deciphered. However, it is clear that complex auto-regulatory and co-regulatory circuits contribute to the essential network architectures for successful development and tissue maintenance. Target specificity is finely tuned. Regulatory changes frequently drive evolutionary alteration, as illustrated by subfunctionalisation observed following gene duplication, for example in zebrafish.


Claudio Punzo (Harvard Medical School, Boston, USA) continued the focus on eye disease. Retinitis Pigmentosa (RP) is an incurable retinal disease that leads to blindness. One puzzling aspect concerns the progression of the disease. While most mutations that cause RP are in rod photoreceptor-specific genes, cone photoreceptors die as well. Understanding this non-autonomous cone death is important for the development of therapeutic strategies. His group’s data suggest that this non-autonomous death of cones is due to slow starvation caused by the morphological changes of the retina due to the loss of rods


David C. Klein (NIH, Bethesda, USA) next discussed the evolution of the pineal gland. He developed a novel hypothesis which claims that the pineal gland and retina evolved from a common photodetector. This is supported by convincing genetic, anatomical and functional evidences. According to him, functions shared by both tissues were active in the same cell, but were in conflict because the melatonin precursor serotonin inactivated retinaldehyde. The conflict was resolved by the evolutionary decision of cellular specialization – the pineal gland being dedicated to melatonin production and the retinal photoreceptor dedicated to light detection.


The afternoon was free; some of the participants were relaxed in the garden, some went for excursion, and others may have worked; the discussion continued in any case. At night, a lecture on astronomy was provided by a staff member from Les Treilles, who is also an enthusiastic astronomer, with a short practical course using his telescope.


The morning session of June 12 was dedicated to evo-devo studies on eyes. Dan-E. Nilsson (Lund University, Sweden) discussed on key inventions for eye evolution. It’s not the eyes and brains themselves that provide the selective advantage driving evolution of their visual systems. Rather, it is the ability to perform visual tasks that drive the evolution of vision. Naturally, early stages in the evolution of visual organs must have been simple, and served only few visual tasks. Hence, eye evolution is driven by a consecutive accumulation of visual tasks. Each task adds to the requirements on eye structure, making it gradually more complex. To understand the requirements on eye structure in a phylogenetically basal animal, his group have investigated vision in box jellyfish. Behavioural experiments indicate that these animals use vision primarily for positioning in the habitat, and for negotiating obstacles. To serve these tasks, the eyes are tuned for low spatial frequencies and are colour blind. The findings indicate that low resolution is not just sufficient, but in fact desirable in early stages of eye evolution. On the basis of his findings in box jellyfish he continued to reconstruct the sequence of acquisition of visual tasks in general. He identifies four key innovations that, one after the other, paved the way for the evolution of efficient eyes. These innovations are (i) efficient photopigments, (ii) directionality through screening pigment, (iii) photoreceptor membrane folding and (iv) focusing optics. A corresponding evolutionary sequence is suggested, starting at non-directional monitoring of ambient luminance, and leading to comparisons of luminances within a scene, first by a scanning mode and later by parallel spatial channels in imaging eyes.


Hiroshi Suga (Barcelona Science Park, University of Barcelona, Spain) then continued the topic on evolution of eye and vision, presenting his work on a hydrozoan jellyfish with eyes.


In order to know the molecular basis of photoreception and development of cnidarian eye, he and his colleagues studied the opsin and Pax genes of a hydrozoan jellyfish with eyes, Cladonema radiatum. His study provided the audiences with some new insights on cnidarian vision, eye development and diverse photic behavior. The study strongly argues for the hypothesis of animal eye monophyly including those of cnidarians.


In addition, he introduced his new challenge in establishing new pre-metazoan model organisms to know the molecular innovations at the transition from protists to multi-cellular organisms.


The morning session was closed by Zbynek Kozmik’s (Institute of Molecular Genetics, Prague, Czech Republic) talk about his hypothesis on eye evolution. The evolution of the eye requires involvement of several distinct components – photoreceptors, screening pigment and genes orchestrating their proper temporal and spatial organization. His group’s studies indicate that vertebrate and cubozoan eyes arose by independent recruitment of orthologous genes. Multiple examples of co-option of crystallins, Gα-protein subunits and screening pigments contrast with the conserved role of opsins and a small set of transcription factors governing eye development in distantly related animals. The direct regulation of essential photoreceptor genes by these factors suggest that this regulatory relationship might have been already established in the ancestral photoreceptor cell.

In the last lecture of the meeting, Steven Reppert (University of Massachusetts Medical School, Worcester, USA) summarized his recent works on animal magnetoreception by cryotochromes. He discussed a novel circadian clock mechanism in the monarch butterfly, which provides the timing component for time-compensated sun compass orientation used during their spectacular fall migration. The butterfly clock mechanism uses two distinct cryptochromes, with one functioning as a circadian photoreceptor and the other as a major transcriptional repressor of the clockwork. He also discussed recent behavioral and genetic studies showing that cryptochrome mediates light-dependent magnetosensitivity in Drosophila.


All the lectures were followed by extensive discussion, which in most of the cases continued during lunch, dinner, and excursion.


The meeting was closed on June 12 and most of the participants left on the next day.

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