Effects of an odor background on moth pheromone communication: constituent identity matters more than blend complexity

Abstract

Olfaction allows insects to communicate with pheromones even in complex olfactory landscapes. It is generally admitted that, due to the binding selectivity of the receptors, general odorants should weakly interfere with pheromone detection. However, laboratory studies show that volatile plant compounds (VPCs) modulate responses to the pheromone in male moths. We used extracellular electrophysiology and calcium imaging to measure the responses to the pheromone of receptor and central neurons in males Agrotis ipsilon while exposed to simple or composite backgrounds of VPCs. Maps of activities were built using calcium-imaging to visualize which areas in antennal lobes (ALs) were affected by VPCs. To mimic a natural olfactory landscape short pheromone puffs were delivered over VPC backgrounds. We chose a panel of VPCs with different chemical structures and physicochemical properties representative of the odorant variety encountered by a moth. We evaluated the intrinsic activity of each VPC and compared the impact of VPC backgrounds at antenna and antennal lobe levels. Then, we prepared binary, ternary and quaternary combinations to determine whether blend activity could be deduced from that of its components. Our data confirm that a VPC background interfere with the moth pheromone system in a dose-dependent manner. Interference with the neuronal coding of pheromone signal starts at the periphery. VPCs showed differences in their capacity to elicit Phe-ORN firing response that cannot be explained by differences in stimulus intensities because we adjusted the source concentrations to vapor pressures. Thus, these differences must be attributed to the selectivity of ORs or any other olfactory proteins. The neuronal network in the ALs, which reformats the ORN-input, did not improve pheromone salience. We postulate that the AL network might have evolved to increase sensitivity and encode for fast changes over a wide range of concentrations, possibly at some cost for selectivity. Comparing three- or four-component blends to binary blends or single compound indicated that a blend showed the activity of its most active compound. Thus, although the diversity of a background might increase the probability of including a VPC interacting with the pheromone system, chemical diversity does not seem to be a prominent factor per se. Global warming is significantly affecting plant metabolism so that the emissions of VPCs and resulting odorscapes are modified. Increase in atmospheric mixing rates of VPCs will change olfactory landscapes which, as confirmed in our study, might impact pheromone communication.