Intracellular regulation of the insect chemoreceptor complex impacts odor localization in flying insects

Abstract

Flying insects are well known for airborne odour tracking and have evolved diverse chemoreceptors. While ionotropic receptors (IRs) are found across protostomes, insect odorant receptors (ORs) have only been identified in winged insects. We therefore hypothesized that the unique signal transduction of ORs offers an advantage for odour localization in flight. Using Drosophila, we found expression and increased activity of the intracellular signalling protein PKC in antennal sensilla following odour stimulation. Odour stimulation also enhanced phosphorylation of the OR co-receptor Orco in vitro, while site-directed mutation of Orco or mutations in PKC subtypes reduced the sensitivity and dynamic range of OR-expressing neurons in vivo, but not IR-expressing neurons. We ultimately show that these mutations reduce competence for odour localization of flies in flight. We conclude that intracellular regulation of OR sensitivity is necessary for efficient odour localization, which suggests a mechanistic advantage for the evolution of the OR complex in flying insects.

Transcriptome Surveys in Silverfish Suggest a Multistep Origin of the Insect Odorant Receptor Gene Family

“…(2) Ors may represent an adaptation to insect flight (Missbach et al, 2014), which is supported by the observation that Ors are typically more sensitive to their ligands than Irs, that Orexpressing sensory neurons respond more readily and reliably to short odor pulses typical for in-flight odor detection than their Ir-expressing counterparts, and that sensitivity of the Or/Orco complex can be adjusted by a variety of modulatory mechanisms (Sargsyan et al, 2011;Getahun et al, 2012Getahun et al, , 2016Mukunda et al, 2014;Guo et al, 2017).…”

Mutagenesis oforcoimpairs foraging but not oviposition in the hawkmothManduca sexta

“…In flight, odorant plumes are presented to the insect as intermittent packets of odor blends in a turbulent air stream (90) and OR-mediated olfaction is involved in directing plume tracking behaviors (91). Moth odor- guided flight behaviors are facilitated through the intermittency of odor packets in a visually aided up-wind flight path (90, 92).…”

Transcriptome Surveys in Silverfish Suggest a Multistep Origin of the Insect Odorant Receptor Gene Family

“…Two hypotheses have been proposed to explain the origin and expansion of the Or multigene family in insect genomes: (1) Ors may represent an adaptation to a terrestrial lifestyle (Brand et al, 2018;Robertson et al, 2003), which is supported by the tendency of Ors to detect hydrophobic compounds, whereas the more ancient Irs and Grs mostly detect hydrophilic substances. Moreover, Ors display, on average, a wider ligand spectrum than Irs, presumably allowing for the detection of a greater number of volatiles Ai et al, 2010;Hallem and Carlson, 2006;Min et al, 2013;Silbering et al, 2011); (2) Ors may represent an adaptation to insect flight (Missbach et al, 2014), which is supported by the observation that Ors are typically more sensitive to their ligands than Irs, that Or-expressing sensory neurons respond more readily and reliably to short odor pulses typical for in-flight odor detection than their Ir-expressing counterparts, and that sensitivity of the Or/Orco complex can be adjusted by a variety of modulatory mechanisms (Getahun et al, 2012(Getahun et al, , 2016Guo et al, 2017;Mukunda et al, 2014;Sargsyan et al, 2011). of the derived Orx/Orco system alongside the advent of insect flight (Missbach et al, 2014).…”