The chemical signatures underlying host plant discrimination by aphids

David P Hopkins,Roger K Butlin,Duncan D Cameron

doi:10.1038/s41598-017-07729-0

David P Hopkins, Roger K Butlin + Show 1 more

Open Access

https://doi.org/10.1038/s41598-017-07729-0

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Journal: Scientific Reports	Publication Date: Aug 17, 2017
Citations: 21	License type: open-access

Affiliation: University of Sheffield

Abstract

The diversity of phytophagous insects is largely attributable to speciation involving shifts between host plants. These shifts are mediated by the close interaction between insects and plant metabolites. However, there has been limited progress in understanding the chemical signatures that underlie host preferences. We use the pea aphid (Acyrthosiphon pisum) to address this problem. Host-associated races of pea aphid discriminate between plant species in race-specific ways. We combined metabolomic profiling of multiple plant species with behavioural tests on two A. pisum races, to identify metabolites that explain variation in either acceptance or discrimination. Candidate compounds were identified using tandem mass spectrometry. Our results reveal a small number of compounds that explain a large proportion of variation in the differential acceptability of plants to A. pisum races. Two of these were identified as L-phenylalanine and L-tyrosine but it may be that metabolically-related compounds directly influence insect behaviour. The compounds implicated in differential acceptability were not related to the set correlated with general acceptability of plants to aphids, regardless of host race. Small changes in response to common metabolites may underlie host shifts. This study opens new opportunities for understanding the mechanistic basis of host discrimination and host shifts in insects.

Highlights

Phytophagous insects are extremely diverse and often feed on restricted ranges of host plants[1]
Both LD1 and E2 profiles from the electrical penetration graphs (EPG) showed a continuum in overall acceptability and discrimination across the 19 host plant species (Fig. 1, Supplementary Fig. S2) and these measures were uncorrelated (E2 r = 0.18, P = 0.46; LD1 r = 0.13, P = 0.58)
There were significant correlations between aphid performance variation across plant species, measured as fecundity of single adults over seven days, and acceptability measured as either E2 (MS aphids r = 0.76, P < 0.001; TP aphids r = 0.79, P < 0.001) or LD1 profile (MS aphids r = 0.80, P < 0.001, TP aphids r = 0.76, P < 0.001) (Supplementary Fig. S2)

Summary

Introduction

Phytophagous insects are extremely diverse and often feed on restricted ranges of host plants[1]. While insects may utilise a variety of cues when making feeding decisions, chemical cues (either volatiles detected before feeding or compounds detected during feeding initiation) are very frequently involved[9] This focuses attention on the insect chemosensory system, including chemosensory receptors, and on differences in plant chemistry among potential hosts. Feeding stimulants and repellents have been identified in many insect-plant interactions[10, 11] and show a wide range of chemistry[12] These interactions are of interest in pest control but in most cases they do not explain insect specificity, i.e. why insects of closely-related species or host races accept distinct ranges of host species. Whatever the mechanism for chemical recognition, it leads to performance differences and assortative mating[22] These conditions result in reproductive isolation and genetic differentiation among races[22]

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Conclusion