Aphids harbouring different endosymbionts exhibit differences in cuticular hydrocarbon profiles that can be recognized by ant mutualists

Corinne Hertaeg,Mark C Mescher,Christoph Vorburger,Marion Risse,Consuelo M De Moraes

doi:10.1038/s41598-021-98098-2

Corinne Hertaeg, Mark C Mescher + Show 3 more

Open Access

https://doi.org/10.1038/s41598-021-98098-2

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Abstract

Cuticular hydrocarbons (CHCs) have important communicative functions for ants, which use CHC profiles to recognize mutualistic aphid partners. Aphid endosymbionts can influence the quality of their hosts as ant mutualists, via effects on honeydew composition, and might also affect CHC profiles, suggesting that ants could potentially use CHC cues to discriminate among aphid lines harbouring different endosymbionts. We explored how several strains of Hamiltonella defensa and Regiella insecticola influence the CHC profiles of host aphids (Aphis fabae) and the ability of aphid-tending ants (Lasius niger) to distinguish the profiles of aphids hosting different endosymbionts. We found significant compositional differences between the CHCs of aphids with different infections. Some endosymbionts changed the proportions of odd-chain linear alkanes, while others changed primarily methyl-branched compounds, which may be particularly important for communication. Behavioural assays, in which we trained ants to associate CHC profiles of endosymbiont infected or uninfected aphids with food rewards, revealed that ants readily learned to distinguish differences in aphid CHC profiles associated with variation in endosymbiont strains. While previous work has documented endosymbiont effects on aphid interactions with antagonists, the current findings support the hypothesis that endosymbionts also alter traits that influence communicative interactions with ant mutualists.

Highlights

Cuticular hydrocarbons (CHCs) have important communicative functions for ants, which use cuticular hydrocarbons (CHCs) profiles to recognize mutualistic aphid partners
Our results demonstrate that facultative endosymbiotic bacteria can change the composition of aphid CHCs in ways that are perceivable by tending ants
Both H. defensa and R. insecticola strains had significant, and sometimes divergent, effects on the CHC profiles of their aphid hosts, endosymbiont effects were smaller in A. fabae clone 405 than clone 407

Summary

Introduction

Cuticular hydrocarbons (CHCs) have important communicative functions for ants, which use CHC profiles to recognize mutualistic aphid partners. Aphid endosymbionts can influence the quality of their hosts as ant mutualists, via effects on honeydew composition, and might affect CHC profiles, suggesting that ants could potentially use CHC cues to discriminate among aphid lines harbouring different endosymbionts. While all aphids exhibit an obligate association with the primary endosymbiont Buchnera aphidicola, which synthesizes essential amino acids that are missing in the aphid d iet[12], they form facultative associations with a number of other endosymbionts Some of these have been shown to provide ecologically important benefits to aphids, including increased heat tolerance[13,14], enhanced performance on specific host p lants[15], protection against pathogenic fungi[16,17], and reduced susceptibility to parasitoid w asps[18,19]. It is plausible that different secondary endosymbionts could have variable effects on the quality of honeydew for aphid mutualists while simultaneously inducing changes in CHC profiles that might enable ants to reliably discriminate between aphids harbouring different endosymbionts

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