Gustatory sensitivity and food acceptance in two phylogenetically closely related papilionid species: Papilio hospiton and Papilio machaon.

Giorgia Sollai,Carla Masala,Paolo Solari,Iole Tomassini Barbarossa,Roberto Crnjar

doi:10.1371/journal.pone.0100675

Abstract

In herbivorous insects, food selection depends on sensitivity to specific chemical stimuli from host-plants as well as to secondary metabolites (bitter) and to sugars (phagostimulatory). Bitter compounds are noxious, unpalatable or both and evoke an aversive feeding response. Instead, sugars and sugar alcohols play a critical role in determining and enhancing the palatability of foods. We assumed that peripheral taste sensitivity may be related to the width of the host selection. Our model consists of two closely phylogenetically related Papilionid species exhibiting a difference in host plant choice: Papilio hospiton and Papilio machaon. The spike activity of the lateral and medial maxillary styloconic taste sensilla was recorded following stimulation with several carbohydrates, nicotine and NaCl, with the aim of characterizing their gustatory receptor neurons and of comparing their response patterns in the light of their different acceptability in feeding behaviour. The results show that: a) each sensillum houses phagostimulant and phagodeterrent cells; b) the spike activity of the gustatory neurons in response to different taste stimuli is higher in P. hospiton than in P. machaon; c) sugar solutions inhibit the spike activity of the deterrent and salt cells, and the suppression is higher in P. machaon than in P. hospiton. In conclusion, we propose that the different balance between the phagostimulant and phagodeterrent inputs from GRNs of maxillary sensilla may contribute in determining the difference in food choice and host range.

Highlights

All animals have taste chemoreceptor cells that respond to different food chemicals and the integrated activity of these cells plays a role in the balance between appetitive or aversive behaviour to foods
To test for a dose-response relationship, we analyzed the spike activity evoked in the first second of the discharge for each gustatory receptor neurons (GRNs) (‘‘L’’, ‘‘M1’’, ‘‘M2’’ and ‘‘S’’) to increasing concentrations of nicotine, several carbohydrates and NaCl, in both sensilla and species, by using a repeated-measures ANOVA
For the lateral styloconic sensillum (Fig. 5), repeated-measures ANOVA showed for both species a significant effect of concentration on the spike frequency of the ‘‘L’’ GRN in response to nicotine (F[2,96] = 117.44; p,0.00001), and post-hoc comparisons showed that the spike frequency in response to each concentration was higher than in response to the lower concentration (p, 0.0001; Duncan’s test)

Summary

Introduction

All animals have taste chemoreceptor cells that respond to different food chemicals and the integrated activity of these cells plays a role in the balance between appetitive or aversive behaviour to foods. Herbivorous insects, and in particular the larvae of Lepidoptera, represent a suitable model to study the relationship between sensory input and behavioural output in the choice of food, as they exhibit clear food preferences and possess a limited number of gustatory neurons, housed within sensilla in the maxillae and epipharynx [12,13]. Most of the electrophysiological studies have been focused on the two styloconic sensilla of each maxillary galea, since they are readily accessible. Both of these sensilla contain four gustatory receptor neurons (GRNs), the axons of which project directly to the central nervous system [4]. Each lateral and medial sensillum has at least one sugar sensitive and one deterrent cell; the specific stimuli for the other cells are species dependent and include inositol, aminoacids, water and/or salts, as reviewed by Schoonhoven and van Loon [13]

Methods

Results

Conclusion