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Evolution of color and motion vision

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Like the human retina, the Drosophila retina contains randomly distributed color photoreceptor cells that are defined by the expression of different color sensitive Rhodopsins. In Drosophila, two types of individual unit eyes (ommatidia) are specified by stochastic expression of the transcription factor Spineless. This decision is controlled by a two-step process: First, each allele of spineless randomly makes a cell-intrinsic ON/OFF expression decision governed by global activation coupled with stochastic repression. When the expression decisions disagree (one allele ON and one allele OFF ), interchromosal communication coordinates expression state between the two alleles. This effect does not depend on chromosomal pairing or endogenous spineless chromosomal position but instead requires specific DNA elements to mediate regulatory interactions. This mechanism couples stochastic repression with interallelic coordination and contrasts starkly with the noisy activation mechanisms seen in bacteria, and the mono-allelic, stochastic activation mechanisms observed in the mouse olfactory and human color vision systems. Many vertebrate and invertebrate eyes also have retinal mosaics that contain different stochastically specified types of photoreceptors. At least one group, the butterflies, make a three-way stochastic choice between three ommatidial types. However, it remains unclear how much of the regulatory network that specifies photoreceptor subtypes is retained or has evolved in other insects, and whether they use stochastic Spineless expression to diversify their sometimes more complex retinal mosaics. We will present evidence that a conserved regulatory code defines and expands photoreceptor subtypes between flies (Drosophila) and butterflies (Papilio xuthus and Vanessa cardui). We used CRISPR /Cas9 to knock out Spineless in butterflies and provide functional evidence that there is deep evolutionary conservation of stochastic patterning mechanisms. Furthermore, butterflies have two R7 photoreceptors that allow for the specification of three types of ommatidia instead of two. This in turn allowed for the evolution and deployment of additional opsins, tetrachromacy, and improved color vision, important features of butterfly life history and ecology. Our extensive knowledge of patterning in the Drosophila visual system applies to other groups, and adaptation for specific visual requirements can occur through modification of this network. There are other instances where instead, the animal has sacrificed its color vision in order to improve its ability to track flying prey or females. The most dramatic example is the ‘love spot’ observed in males of several dipteran species. For instance, in the dorso-frontal region of the Musca (house fly) male eye, which faces the flying female being chased, R7 cells are transformed from color detectors into motion sensitive photoreceptors. This completely disrupts color vision but adds a seventh ‘outer’ photoreceptor that improves the ability of the male to track the female. This R7 now expresses the broad spectrum Rh1 instead of a UV opsin; it also projects to the lamina part of the optic lobe where motion is processed instead of reaching directly into the medulla where R7 normally compares its output with R8 for color discrimination. We have shown that this drastic change in wiring pattern is due to loss of expression of the runt gene in R7. We suggest that similar changes occur in both males and females of ‘killer’ flies that rely on in-flight chases of other insects. Therefore, these two examples in the insect world illustrate the flexibility of the visual system to adapt to specific circumstances that fit the lifestyle of the animal. These changes rely on molecular variations that can be explained in simple evolutionary steps.

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