Genetic Dissection of Behavior: Modulation of Locomotion by Light in theDrosophila melanogasterLarva Requires Genetically Distinct Visual System Functions

Abstract

The Drosophila larva modulates its pattern of locomotion when exposed to light. Modulation of locomotion can be measured as a reduction in the distance traveled and by a sharp change of direction when the light is turned on. When the light is turned off this change of direction, albeit significantly smaller than when the light is turned on, is still significantly larger than in the absence of light transition. Mutations that disrupt adult phototransduction disrupt a subset of these responses. In larvae carrying these mutations the magnitude of change of direction when the light is turned on is reduced to levels indistinguishable from that recorded when the light is turned off, but it is still significantly higher than in the absence of any light transition. Similar results were obtained when these responses were measured in strains where the larval photoreceptor neurons were ablated by mutations in the glass (gl) gene or by the targeted expression of the cell death gene head involution defective (hid). A mutation in the homeobox gene sine oculis (so) that ablates the larval visual system, or the targeted expression of the reaper (rpr) cell death gene, abolishes all responses to light detected as a change of direction. We propose the existence of an extraocular light perception that does not use the same phototransduction cascade as the adult photoreceptors. Our results indicate that this novel visual function depends on the blue-absorbing rhodopsin Rh1 and is specified by the so gene.

Sensorimotor structure of Drosophila larva phototaxis

“…Because of the limits of the projector's dynamic range, we could not increase the steepness of the gradient without significantly reducing the size of the experimental arena, so we turned to temporal gradients using triangle waveforms to mimic the stimulus received by larvae moving in straight lines on illumination patterns with a steeper linear spatial gradient. In our previous studies of spatial and temporal gradients of temperature (3)(4)(5)(6)(7)(8)(9)14), odor, and carbon dioxide (10, 11), we found that temporal triangle waves evoked the same behavioral responses as linear spatial gradients.…”

“…2C). We presented larvae with a temporal analog of the checkerboard, a temporal squarewave light stimulus (8,16) (17). The temporal square-wave setup also revealed a distinct photosensory behavior: pausing in response to an abrupt decrease in light intensity (cessation of forward movement without initiation of head-sweeps) ( Fig.…”

“…However, temporal comparisons performed by moving animals, also known as klinotaxis, also can encode spatial information (2). Like most fly larvae, Drosophila larvae are negatively phototactic during most of their development (3)(4)(5)(6)(7)(8)(9). To navigate away from light, the Drosophila larva uses two sets of photosensors, the Rhodopsin-expressing Bolwig's organs (BO) that mediate phototaxis at low light levels and the non-Rhodopsin-expressing class IV multidendritic (md) neurons that respond to intense light levels comparable to direct sunlight (10).…”

Evolution of Insect Eyes: Tales of Ancient Heritage, Deconstruction, Reconstruction, Remodeling, and Recycling

“…The Drosophila larva performs light-oriented behavior using a pair of photoreceptor bundles that attach to each side of the cephalopharyngeal head skeleton of the maggot and constitute the Bolwig's organs (BO; Fig. 6d) (Busto et al 1999). Originally discovered by Niels Bolwig in the closely related house fly (Bolwig 1946), the BOs had at first not been related to the compound eye.…”

“…Since species with primitive ommatidium-type larval eyes are known in both Coleoptera and Diptera (Gilbert 1994), one has to conclude that the reduction of accessory cells occurred independently in the lineages leading to Drosophila and Tribolium. It is noteworthy that in both of these groups, the ecology of larvae appears to render vision less important (Busto et al 1999;Park 1934). The reduction may therefore be the result of evolution against costly visual organs.…”