Odorant binding protein 69a connects social interaction to modulation of social responsiveness in Drosophila

Abstract

Living in a social environment requires the ability to respond to specific social stimuli and to incorporate information obtained from prior interactions into future ones. One of the mechanisms that facilitates social interaction is pheromone-based communication. In Drosophila melanogaster, the male-specific pheromone cis-vaccenyl acetate (cVA) elicits different responses in male and female flies, and functions to modulate behavior in a context and experience-dependent manner. Although it is the most studied pheromone in flies, the mechanisms that determine the complexity of the response, its intensity and final output with respect to social context, sex and prior interaction, are still not well understood. Here we explored the functional link between social interaction and pheromone-based communication and discovered an odorant binding protein that links social interaction to sex specific changes in cVA related responses. Odorant binding protein 69a (Obp69a) is expressed in auxiliary cells and secreted into the olfactory sensilla. Its expression is inversely regulated in male and female flies by social interactions: cVA exposure reduces its levels in male flies and increases its levels in female flies. Increasing or decreasing Obp69a levels by genetic means establishes a functional link between Obp69a levels and the extent of male aggression and female receptivity. We show that activation of cVA-sensing neurons is sufficeint to regulate Obp69a levels in the absence of cVA, and requires active neurotransmission between the sensory neuron to the second order olfactory neuron. The cross-talk between sensory neurons and non-neuronal auxiliary cells at the olfactory sensilla, represents an additional component in the machinery that promotes behavioral plasticity to the same sensory stimuli in male and female flies.

Social Context Enhances Hormonal Modulation of Pheromone Detection in Drosophila

“…To address how external social cues are integrated with internal state, we focused on the courtship-promoting Or47b olfactory receptor neurons (ORNs) to investigate the effects of age and housing condition on reproductive behavior in male Drosophila. ORNs are often required for the contextual modulation of social behaviors [6,8,16], and several lines of evidence suggest that age-dependent plasticity in Or47b ORNs underlies contextual modulation of courtship behavior [17,18]. Among the $50 ORN types in the adult olfactory system, Or47b neurons exhibit uncommon anatomical and physiological plasticity [17][18][19].…”

Robust olfactory responses in the absence of odorant binding proteins

“…The in vivo functions of many odorant receptors have been well established (Ai et al, 2010; Benton et al, 2009; Ha and Smith, 2006; Hallem and Carlson, 2006; Hallem et al, 2004; van der Goes van Naters and Carlson, 2007; Yao et al, 2005), but their structures are only now beginning to be solved, with the recent determination of a cryo-EM structure for an odor receptor co-receptor, Orco (Butterwick et al, 2018). Reciprocally, the structures of many Obps have been solved at high resolution (Brito et al, 2016; Kruse et al, 2003; Laughlin et al, 2008; Leite et al, 2009; Sandler et al, 2000), but their functions in vivo are much less clear (Bentzur et al, 2018; Gomez-Diaz et al, 2013; Kim et al, 1998; Larter et al, 2016; Sun et al, 2018b; Xu et al, 2005; Zhang et al, 2017).…”

Divergence of chemosensing during the early stages of speciation

“…Work on the silkmoth ( Bombyx mori ) homolog BmOBP20 underscores the importance of this gene in chemosensation ( 55 ). More recently, work on the Drosophila homolog ( OBP69a ) suggests that the expression of OBP69a is regulated by cis -vaccenyl acetate (a male-specific Drosophila pheromone) and experimentally demonstrates that expression levels of OBP69a modulate male-male aggression and female receptivity ( 56 ). Moreover, HmOBP20 was previously identified to be in a region of high divergence between Heliconius elevatus and Heliconius pardalinus ( 57 ), two other recently diverged species in the genus.…”