Female Olfactory Sensitivity Is Temporally Asynchronous with Male Courtship in a Butterfly

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Abstract
Signal efficacy is crucial to communicative behaviours. To be effective, a signal once broadcast must be capable of being received and interpreted by a receiver or receivers. In addition to maximizing the amount that a signal stimulates receptive organs, optimally the timing of when a signal is broadcast would synchronize with a receiver’s peak receptivity. Here, we investigated whether peak timing of male courtship, which includes release of a pheromone required for copulation to occur, is synchronized with female pheromone sensitivity in the butterfly Bicyclus anynana (Lepidoptera: Nymphalidae). To do this, we performed behavioural and electrophysiological assays at dawn, noon, and dusk. We also investigated the circadian rhythmicity of antennae gene expression by performing RNA-Sequencing on antennal tissues collected at dawn, noon and dusk. We found that although males court most often near dusk, females are more sensitive to odorants in the morning. Furthermore, antennae exhibited differential and diurnally rhythmic expression of odorant receptors and genes associated with learning and sexual receptivity, as well as gene ontology (GO) terms related to fatty acid metabolism and trehalose biosynthesis, supporting our circadian electrophysiological results. Previous literature indicates females form both positive and negative mate preference associations with male pheromones in the morning, regardless of whether males court females. Thus, this asynchrony may enable female B. anynana to learn mate preferences before they are courted by conspecific (or potentially heterospecific) males. Summary: Male Bicyclus anynana butterflies court more at dusk while females are more sensitive to odorants in the morning. Patterns of antenna gene expression also suggest circadian rhythmicity of odorant sensitivity.
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