ReviewEcological costs of induced resistance
Introduction
Plant resistance against herbivores and pathogens is subject to extensive phenotypic plasticity: many resistance traits are expressed only, or to a higher degree, in response to a first ‘eliciting’ attack. De novo synthesis of phytoalexins and pathogenesis-related (PR) proteins, and changes in cell wall composition, are associated with induced systemic resistance (ISR) or systemic acquired resistance (SAR) against pathogens 1•., 2., 3.. Increased or de novo production of secondary compounds is correlated with induced resistance against herbivores (IR) 4., 5.. IR can also be achieved indirectly by the attraction of ‘enemies of the plant's enemies’ [6] by volatile organic compounds (VOCs) [7] or extrafloral nectar [8•]. Recent studies have demonstrated the defensive effects of VOCs [9••] and the induction of extrafloral nectar flow [8•] under natural conditions. Most resistance traits can be artificially induced by the application of ‘elicitors’, and plants can be genetically engineered to express these traits constitutively, particularly those that are correlated with ISR. Induced defences are therefore receiving increasing attention, especially in the context of crop protection.
To explain the evolution of induced defences, as distinct from constitutive (i.e. constant) resistance, costs of induced resistance have been postulated: resistance traits are assumed to reduce the fitness of the plant when expressed under enemy-free conditions [10]. ‘Just-in-time’ mechanisms such as induced resistance are believed to have evolved, at least in part, to ‘save’ costs when defence is not required. Different forms of costs have been defined (Box 1), but they are by no means mutually exclusive. Recent studies have focused on ‘allocation costs’ and have revealed negative fitness effects of induced responses under enemy-free conditions 11., 12., 13., 14., 15••.. Most of these studies have used chemical elicitation of resistance, which may cause effects beyond those that are associated with induced resistance (Box 2). Yet, there is increasing agreement that inducing resistance does cause relevant allocation costs 16•., 17., 18..
The evolutionarily relevant costs of resistance include all of the negative effects on plant fitness that may be caused by a resistance trait under natural growing conditions 16•., 19.. Costs may result from ‘internal’ mechanisms (e.g. genetic costs, allocation costs, or autotoxicity), but can also result from ‘external’ mechanisms. ‘Ecological costs’ arise when one of the interactions between a plant and its biotic and abiotic environment is affected in a way that negatively affects plant fitness (Fig. 1). These costs are not apparent in experiments on isolated plants that are cultivated indoors under artificially optimised growing conditions, and thus are likely to be hidden in most of the studies conducted to far. To provide a starting point for further research, this review lists the few recent examples that have identified ecological costs of induced resistance and highlights some of the resistance traits that are likely to be associated with such costs.
Section snippets
Delayed flowering and impaired pollination
Several studies have identified reduced numbers of flowers [20], or delayed flowering, fruit set, or fruit ripening 11., 14., when plants were treated with jasmonic acid (JA) or methyljasmonate (MeJA) to induce IR. The fitness consequences of these manipulations were, however, inconsistent under the chosen experimental conditions. Though not inevitably reducing seed production, delays in flowering, fruit set, or fruit ripening can severely compromise plant fitness under natural conditions.
Allocation costs and reduced competitive ability
The allocation costs of chemically (i.e. MeJA-) induced nicotine production in native tobacco (Nicotiana attenuata and N. sylvestris) translate to fitness costs only when the plants compete with uninduced conspecific neighbours, when induced plants suffer from an impaired ability to compete for nitrogen [22]. Herbivore-induced Lepidium virginicum (Brassicaceae) plants showed reductions in root biomass when growing at high densities [23]. In wheat plants, the negative effects on seed set of
Negative effects on mutualists and positive effects on enemies
Strauss et al. [21] reported negative effects of induced herbivore resistance on pollinator visitation rates. Herbivore-induced volatiles may have deterrent effects on some of the plants’ insect mutualists, as the information provided by volatiles released from an infested plant is highly complex [7]. Moreover, indirect defence strategies involve a third partner that cannot be controlled perfectly by the plant. Mutualistic ants that inhabit obligate ant-plants (myrmecophytes) are highly mobile
Induced susceptibility
Further ecological costs occur when plant defence mechanisms cause resistance to one species but also result in susceptibility to other natural enemies. Herbivory-induced susceptibility to herbivores has rarely been reported (probably because of the lack of long-term studies such as that by Underwood [42]), but many studies have addressed the question of whether and how induced resistance against herbivores affects ISR against pathogens and vice versa (for reviews see 43., 44., 45., 46.).
Trade-offs between resistance and tolerance
Tolerance is a phenotypically plastic characteristic that has been defined as ‘a decrease in the per unit effect of herbivory on plant fitness’ [48], and thus is another strategy by which plants may cope with damage. Theoretical considerations show that highly resistant plants do not need to be tolerant, whereas highly tolerant plants are not forced to be resistant. Hence, negative correlations between resistance and tolerance are likely to have evolved [49]. Empirical data supporting this
Conclusions
Allocation costs may have an important opportunity aspect if they reduce a plant's future competitive ability. Even such ‘internal’ costs may therefore depend on — and affect — a plant's environment and thus are, in fact, ‘ecological’ costs. Such interactions point to the close linkage between ‘internal’ and ‘external’ mechanisms that give rise to costs of induced resistance. Yet, it is by no means true that ‘ecological costs are simply a special case of allocation costs’ (as stated in [48]).
Acknowledgements
I thank Wilhelm Boland, Ian T Baldwin, Thomas Mitchell-Olds and Jonathan Gershenzon (all of the Max Planck Institute of Chemical Ecology, Jena) for their critical reading of earlier versions of this manuscript, and Karsten Mody (Zoologie III, University of Würzburg) for sharing unpublished data. Financial support from the German Research Foundation (DFG, grant He 3169/1-4) and the Max-Planck-Gesellschaft is gratefully acknowledged.
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
• of special interest
•• of outstanding interest
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