Abstract

Beneficial symbioses are widespread and diverse in the functions they provide to the host ranging from nutrition to protection. However, these partnerships with symbionts can be costly for the host. Such costs, so called “direct costs”, arise from a trade-off between allocating resources to symbiosis and other functions such as reproduction or growth. Ecological costs may also exist when symbiosis negatively affects the interactions between the host and other organisms in the environment. Although ecological costs can deeply impact the evolution of symbiosis, they have received little attention. The pea aphid Acyrthosiphon pisum benefits a strong protection against its main parasitoids from protective bacterial symbionts. The ecological cost of symbiont-mediated resistance to parasitism in aphids was here investigated by analyzing aphid behavior in the presence of predatory ladybirds. We showed that aphids harboring protective symbionts expressed less defensive behaviors, thus suffering a higher predation than symbiont-free aphids. Consequently, our study indicates that this underlined ecological cost may affect both the coevolutionary processes between symbiotic partners and the prevalence of such beneficial bacterial symbionts in host natural populations.

Highlights

  • IntroductionInterest divergence leads to the famous perpetual arms race between victims and enemies

  • Within antagonistic interactions, interest divergence leads to the famous perpetual arms race between victims and enemies

  • The fitness costs of defense can arise from both internal processes, when fitness-limiting resources are allocated to defenses at the expense of growth and reproduction, and external processes that occur when defense expression results in disrupting a beneficial interaction or in enhancing susceptibility toward enemies

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Summary

Introduction

Interest divergence leads to the famous perpetual arms race between victims and enemies. The victims establish diverse defensive strategies that are selected for the benefits they provide in case of enemy attack. The cost-benefit paradigm motivated most of the theory about the evolution of defense strategies against enemies (e.g., Strauss et al 2002 on plants; Kraaijeveld et al 2002 on animals), demonstrating the existence of fitness costs associated with defenses is a challenging task. Recent work on diverse invertebrates has revealed that heritable facultative symbionts can confer protection against a range of natural enemies (Oliver et al 2010). Apart from their essential nutrient-providing symbiont Buchnera aphidicola, many aphid species harbor several facultative bacterial symbionts influencing a 2014 The Authors.

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