Olfactory Learning Supports an Adaptive Sugar-Aversion Gustatory Phenotype in the German Cockroach

An association of food sources with odors prominently guides foraging behavior in animals. To understand the interaction of olfactory memory and food preferences, we used glucose-averse (GA) German cockroaches. Multiple populations of cockroaches evolved a gustatory polymorphism where glucose is per...

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Main Authors: Ayako Wada-Katsumata, Coby Schal
Format: Article
Language:English
Published: MDPI AG 2021-08-01
Series:Insects
Subjects:
Online Access:https://www.mdpi.com/2075-4450/12/8/724
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author Ayako Wada-Katsumata
Coby Schal
author_facet Ayako Wada-Katsumata
Coby Schal
author_sort Ayako Wada-Katsumata
collection DOAJ
description An association of food sources with odors prominently guides foraging behavior in animals. To understand the interaction of olfactory memory and food preferences, we used glucose-averse (GA) German cockroaches. Multiple populations of cockroaches evolved a gustatory polymorphism where glucose is perceived as a deterrent and enables GA cockroaches to avoid eating glucose-containing toxic baits. Comparative behavioral analysis using an operant conditioning paradigm revealed that learning and memory guide foraging decisions. Cockroaches learned to associate specific food odors with fructose (phagostimulant, reward) within only a 1 h conditioning session, and with caffeine (deterrent, punishment) after only three 1 h conditioning sessions. Glucose acted as reward in wild type (WT) cockroaches, but GA cockroaches learned to avoid an innately attractive odor that was associated with glucose. Olfactory memory was retained for at least 3 days after three 1 h conditioning sessions. Our results reveal that specific tastants can serve as potent reward or punishment in olfactory associative learning, which reinforces gustatory food preferences. Olfactory learning, therefore, reinforces behavioral resistance of GA cockroaches to sugar-containing toxic baits. Cockroaches may also generalize their olfactory learning to baits that contain the same or similar attractive odors even if they do not contain glucose.
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spelling doaj.art-7b174d672b334c41834c925c0f2365872023-11-22T08:07:37ZengMDPI AGInsects2075-44502021-08-0112872410.3390/insects12080724Olfactory Learning Supports an Adaptive Sugar-Aversion Gustatory Phenotype in the German CockroachAyako Wada-Katsumata0Coby Schal1Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC 27695, USADepartment of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC 27695, USAAn association of food sources with odors prominently guides foraging behavior in animals. To understand the interaction of olfactory memory and food preferences, we used glucose-averse (GA) German cockroaches. Multiple populations of cockroaches evolved a gustatory polymorphism where glucose is perceived as a deterrent and enables GA cockroaches to avoid eating glucose-containing toxic baits. Comparative behavioral analysis using an operant conditioning paradigm revealed that learning and memory guide foraging decisions. Cockroaches learned to associate specific food odors with fructose (phagostimulant, reward) within only a 1 h conditioning session, and with caffeine (deterrent, punishment) after only three 1 h conditioning sessions. Glucose acted as reward in wild type (WT) cockroaches, but GA cockroaches learned to avoid an innately attractive odor that was associated with glucose. Olfactory memory was retained for at least 3 days after three 1 h conditioning sessions. Our results reveal that specific tastants can serve as potent reward or punishment in olfactory associative learning, which reinforces gustatory food preferences. Olfactory learning, therefore, reinforces behavioral resistance of GA cockroaches to sugar-containing toxic baits. Cockroaches may also generalize their olfactory learning to baits that contain the same or similar attractive odors even if they do not contain glucose.https://www.mdpi.com/2075-4450/12/8/724gustationsugar aversionGerman cockroacholfactory learningmemoryforaging
spellingShingle Ayako Wada-Katsumata
Coby Schal
Olfactory Learning Supports an Adaptive Sugar-Aversion Gustatory Phenotype in the German Cockroach
Insects
gustation
sugar aversion
German cockroach
olfactory learning
memory
foraging
title Olfactory Learning Supports an Adaptive Sugar-Aversion Gustatory Phenotype in the German Cockroach
title_full Olfactory Learning Supports an Adaptive Sugar-Aversion Gustatory Phenotype in the German Cockroach
title_fullStr Olfactory Learning Supports an Adaptive Sugar-Aversion Gustatory Phenotype in the German Cockroach
title_full_unstemmed Olfactory Learning Supports an Adaptive Sugar-Aversion Gustatory Phenotype in the German Cockroach
title_short Olfactory Learning Supports an Adaptive Sugar-Aversion Gustatory Phenotype in the German Cockroach
title_sort olfactory learning supports an adaptive sugar aversion gustatory phenotype in the german cockroach
topic gustation
sugar aversion
German cockroach
olfactory learning
memory
foraging
url https://www.mdpi.com/2075-4450/12/8/724
work_keys_str_mv AT ayakowadakatsumata olfactorylearningsupportsanadaptivesugaraversiongustatoryphenotypeinthegermancockroach
AT cobyschal olfactorylearningsupportsanadaptivesugaraversiongustatoryphenotypeinthegermancockroach