Role of retinal movements in visual perception during courtship in Drosophila

Abstract

Courtship in Drosophila melanogaster is a highly stereotyped and precisely executed behavior that leads to successful mating. Vision plays an important role in this process by guiding male orientation, tracking of the moving female, regulation of proximity with the female and positioning during singing to ensure optimal alignment. Although their compound eyes were considered fixed structures, recent work revealed that Drosophila have retinal movements guided by two muscles. While these retinal movements are similar to vertebrate eye movements in many ways, their behavioral relevance still remains to be explored. To investigate their role in visually guided courtship behavior, we genetically silenced retinal motor neurons using three independent driver lines expressing tetanus toxin (TNT), thereby inhibiting or reducing retinal movements. Males with silenced or reduced retinal movements retained the ability to perform basic courtship maneuvers like orienting, following, circling and singing, indicating that courtship as a whole was executed without any hindrance. However, mating success was reduced and copulation latency was increased and despite normal locomotion speed, they maintained a greater mean distance from the females. Moreover, they failed to maintain precise spatial alignment with the female during singing which is critical for effective courtship. They showed a higher frequency of singing bouts initiated outside the stereotypical alignment region, as well as increased instances in which alignment was lost during the course of a singing bout. These findings show that retinal movements are not required for the basic courtship behavior but help for precise spatial estimation and fine-tuning spatial alignment during singing, showing that retinal movements enhance visual perception during courtship in Drosophila melanogaster.