Drosophila males require the longitudinal stretch receptors to tremulate their abdomen and produce substrate-borne signals during courtship

Abstract

Substrate-borne cues are important species-specific signals that are widely used during courtship of many animals, from arthropods to vertebrates. They allow mating partners to communicate with, recognise and choose one another. Animals often produce substrate-borne signals by vibrating a body part, such as the abdomen. During Drosophila courtship, species-specific substrate-borne vibrations are generated by the males regular up-and-down abdominal tremulations and these must be precisely controlled to produce an effective and specific signal. The vibrations immobilise the female, therefore facilitating copulation. It is not known how the males nervous system regulates this abdominal tremulation. Here, we demonstrate a role for the dorsal abdominal longitudinal stretch receptors (LSR), which include the dorsal bipolar dendritic (dbd) neurons. These neurons are a set of conserved proprioceptors found throughout Insecta. We show that impairing the function of dbd neurons through general inhibition results in males exhibiting high level of arhythmic abdominal movements (referred to as bobbing) and decreased level of tremulation. Strikingly, this causes a failure in the females response during courtship. We show that depleting the mechanosensitive ion channel TRPA1 (but not Piezo) in the dbd neurons leads to a similar increase in bobbing movements. Thus, we identify neurons and a key molecular player necessary for males to perform this important mode of communication.