Avoid, attack or do both? Behavioral and physiological adaptations in natural enemies faced with novel hosts

Corinne Vacher,Sam P Brown,Michael E Hochberg

doi:10.1186/1471-2148-5-60

Abstract

BackgroundConfronted with well-defended, novel hosts, should an enemy invest in avoidance of these hosts (behavioral adaptation), neutralization of the defensive innovation (physiological adaptation) or both? Although simultaneous investment in both adaptations may first appear to be redundant, several empirical studies have suggested a reinforcement of physiological resistance to host defenses with additional avoidance behaviors. To explain this paradox, we develop a mathematical model describing the joint evolution of behavioral and physiological adaptations on the part of natural enemies to their host defenses. Our specific goals are (i) to derive the conditions that may favor the simultaneous investment in avoidance and physiological resistance and (ii) to study the factors that govern the relative investment in each adaptation mode.ResultsOur results show that (i) a simultaneous investment may be optimal if the fitness costs of the adaptive traits are accelerating and the probability of encountering defended hosts is low. When (i) holds, we find that (ii) the more that defended hosts are rare and/or spatially aggregated, the more behavioral adaptation is favored.ConclusionDespite their interference, physiological resistance to host defensive innovations and avoidance of these same defenses are two strategies in which it may be optimal for an enemy to invest in simultaneously. The relative allocation to each strategy greatly depends on host spatial structure. We discuss the implications of our findings for the management of invasive plant species and the management of pest resistance to new crop protectants or varieties.

Highlights

Confronted with well-defended, novel hosts, should an enemy invest in avoidance of these hosts, neutralization of the defensive innovation or both? simultaneous investment in both adaptations may first appear to be redundant, several empirical studies have suggested a reinforcement of physiological resistance to host defenses with additional avoidance behaviors
When (i) holds, we find that (ii) the more that defended hosts are rare and/or spatially aggregated, the more behavioral adaptation is favored
What conditions favor the simultaneous investment in physiological and behavioral adaptations to host defenses? Accelerating fitness costs of adaptations We find that the fitness costs of physiological and behavioral adaptations to novel host defenses can have an important effect on the optimal enemy strategy (Fig. 1)

Summary

Introduction

Simultaneous investment in both adaptations may first appear to be redundant, several empirical studies have suggested a reinforcement of physiological resistance to host defenses with additional avoidance behaviors To explain this paradox, we develop a mathematical model describing the joint evolution of behavioral and physiological adaptations on the part of natural enemies to their host defenses. BMC Evolutionary Biology 2005, 5:60 http://www.biomedcentral.com/1471-2148/5/60 hosts and preferentially avoid defended ones (behavioral adaptation), or develop a direct counter-adaptation allowing the successful attack of defended hosts (physiological adaptation). Both adaptation modes have been extensively studied and reviewed, especially in arthropod systems [25]

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