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Abstract:
The hawkmoth Manduca sexta and one of its preferred hosts in the North American Southwest, Datura wrightii, share a model
insect–plant relationship based on mutualistic and antagonistic
life-history traits. D. wrightii is the innately preferred nectar source
and oviposition host for M. sexta. Hence, the hawkmoth is an important
pollinator while the M. sexta larvae are specialized herbivores
of the plant. Olfactory detection of plant volatiles plays a
crucial role in the behavior of the hawkmoth. In vivo, the odorant
receptor coreceptor (Orco) is an obligatory component for the function
of odorant receptors (ORs), a major receptor family involved in
insect olfaction. We used CRISPR-Cas9 targeted mutagenesis to
knock out (KO) the MsexOrco gene to test the consequences of a
loss of OR-mediated olfaction in an insect–plant relationship. Neurophysiological
characterization revealed severely reduced antennal
and antennal lobe responses to representative odorants emitted by
D. wrightii. In a wind-tunnel settingwith a flowering plant, Orco KO
hawkmoths showed disrupted flight orientation and an ablated
proboscis extension response to the natural stimulus. The Orco KO
gravid female displayed reduced attraction toward a nonflowering
plant. However, more than half of hawkmoths were able to use
characteristic odor-directed flight orientation and oviposit on the
host plant. Overall, OR-mediated olfaction is essential for foraging
and pollination behaviors, but plant-seeking and oviposition behaviors are sustained through additional OR-independent sensory cues.