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

Abstract

Background: Confronted 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.

Results: Our 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.

Conclusion: Despite 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.

Figure 1

Null clines for physiological (solid line) and behavioral (dotted line) adaptation to host defenses as a function of the shape of the cost function. Black points are stable steady states. Arrows represent schematic phase trajectories. k_R = 0.1, k_B = 0.1, e = 0.1, a = 0.4, f = 20%.

Figure 2

Co-equilibrium (R*, B*) between physiological (solid line) and behavioral (dotted line) adaptation to host defenses as a function of the frequency f and the spatial aggregation level a of well-defended hosts. Equilibrium is polymorphic in the white plane and monomorphic in the gray plane ((R*, B*) = (1,0) or (0,1)). k_R = 0.1, k_B = 0.1, e = 0.1, x = 2

Figure 3

Total investment in adaptation to host defenses (R*+B*) and relative allocation to behavioral adaptation B*/(R*+B*) as a function of the frequency f and the spatial aggregation level a of defended hosts in the case of a polymorphic equilibrium (R*, B*). Model parameters are the same than in Figure 2.

Figure 4

Co-equilibrium (R*, B*) between physiological (solid line) and behavioral (dotted line) adaptation to host defenses as a function of the search cost coefficient e and the spatial aggregation level a of well-defended hosts. Equilibrium is polymorphic. k_R = 0.1, k_B = 0.1, x = 2, f = 20%

Figure 5

Enemy life cycle. Parameters W₀, H and S are defined in Table 1.