Conditional Reduction of Predation Risk Associated with a Facultative Symbiont in an Insect

Sarah Polin,Jean-Christophe Simon,Tsutomu Tsuchida,Yannick Outreman,Jean-François Le Gallic,Owain Rhys Edwards

doi:10.1371/journal.pone.0143728

Abstract

Symbionts are widespread among eukaryotes and their impacts on the ecology and evolution of their hosts are meaningful. Most insects harbour obligate and facultative symbiotic bacteria that can influence their phenotype. In the pea aphid Acyrthosiphon pisum, an astounding symbiotic-mediated phenotype has been recently observed: when infected with the symbiotic bacteria Rickettsiella viridis, young red aphid larvae become greener at adulthood and even darker green when co-infected with Rickettsiella viridis and Hamiltonella defensa. As body colour affects the susceptibility towards natural enemies in aphids, the influence of the colour change due to these facultative symbionts on the host survival in presence of predators was tested. Our results suggested that the Rickettsiella viridis infection may impact positively host survival by reducing predation risk. Due to results from uninfected aphids (i.e., more green ones attacked), the main assumption is that this symbiotic infection would deter the predatory ladybird feeding by reducing the profitability of their hosts rather than decreasing host detection through body colour change. Aphids co-infected with Rickettsiella viridis and Hamiltonella defensa were, however, more exposed to predation suggesting an ecological cost associated with multiple infections. The underlying mechanisms and ecological consequences of these symbiotic effects are discussed.

Highlights

While considered until recently as a marginal phenomenon, symbiotic associations are gaining recognition as a ubiquitous feature of animal life [1]
Four different A. pisum aphid types were defined according to their colour and symbiotic complement: (i) red aphid genotypes free of facultative bacterial symbionts, (ii) green aphid genotypes free of facultative bacterial symbionts, (iii) red genotypes harbouring Rickettsiella and becoming green at adulthood and (iv) red genotypes co-infected with Rickettsiella and Hamiltonella and becoming green at adulthood
The red individuals infected with Rickettsiella change their body colour becoming green at adulthood and our study showed that this symbiotic association influenced the survival rate of the host when exposed to predators

Summary

Introduction

While considered until recently as a marginal phenomenon, symbiotic associations are gaining recognition as a ubiquitous feature of animal life [1]. Because host species and their heritable symbionts share fates, but not necessarily common interests, inherited symbionts often exert phenotypical effects that can profoundly influence the ecology and the evolution of animal hosts [2]. These symbiont-mediated phenotypes can alter, negatively or positively, the interaction between the symbiont host and its natural enemies (i.e., pathogens, parasite and predators) [3]. Symbiont infection can be associated with an increased susceptibility to pathogens

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