Tolerance and resistance are two different plant defense strategies against herbivores. Empirical evidence in natural populations reveals that individual plants allocate resources simultaneously to both strategies, thus plants exhibit a mixed pattern of defense. In this review we examine the conditions that promote the evolutionary stability of mixed defense strategies in the light of available empirical and theoretical evidence. Given that plant tolerance and resistance are heritable and subject to environmentally dependent selection and genetic constraints, the joint evolution of tolerance and resistance is analyzed, with consideration of multiple species interactions and the plant mating system. The existence of mixed defense strategies in plants makes it necessary to re-explore the coevolutionary process between plants and herbivores, which centered historically on resistance as the only defensive mechanism. In addition, we recognize briefly the potential use of plant tolerance for pest management. Finally, we highlight unresolved issues for future development in this field of evolutionary ecology.
This study assessed the role of leaf trichome density as a component of resistance to herbivores, in six populations of Datura stramonium. Phenotypic selection on plant resistance was estimated for each population. A common garden experiment was carried out to determine if population differences in leaf trichome density are genetically based. Among population differences in leaf trichome density, relative resistance and fitness were found. Leaf trichome density was strongly positively correlated to resistance across populations. In 5 out of 6 populations, trichome density was related to resistance, and positive directional selection on resistance to herbivores was detected in three populations. Differences among populations in mean leaf trichome density in the common garden suggest genetic differentiation for this character in Datura stramonium. The results are considered in the light of the adaptive role of leaf trichomes as a component of defence to herbivores, and variable selection among populations.
In this study we present a simple optimization model for the evolution of defensive strategies (tolerance and resistance) of plants against their natural enemies. The model specifically evaluates the consequences of introducing variable costs and benefits of tolerance and resistance and nonlinear cost-and-benefit functions for tolerance and resistance. Incorporating these assumptions, the present model of plant defense predicts different evolutionary scenarios, not expected by previous work. Basically, the presence of an adaptive peak corresponding to intermediate levels of allocation to tolerance and resistance can arise when the shape parameter of the cost function is higher than the corresponding of the benefit function. The presence of two alternatives peaks of maximum tolerance and maximum resistance occurs only when benefits of tolerance and resistance interact less than additive. Finally, the presence of one peak of maximum resistance or maximum tolerance depends on the relative values of the magnitude of costs for tolerance and resistance. An important outcome of our model is that under a plausible set of conditions, variable costs of tolerance and resistance can represent an important aspect involved in the maintenance of intermediate levels of tolerance and resistance, and in favoring adaptive divergence in plant defensive strategies among populations. The model offers a framework for future theoretical and empirical work toward understanding spatial variation in levels of allocation to different defensive strategies.
In this study we examine the hypothesis that divergent natural selection produces genetic differentiation among populations in plant defensive strategies (tolerance and resistance) generating adaptive variation in defensive traits against herbivory. Controlled genetic material (paternal half-sib families) from two populations of the annual Datura stramonium genetically differentiated in tolerance and resistance to herbivory were used. This set of paternal half-sib families was planted at both sites of origin and the pattern of genotypic selection acting on tolerance and resistance was determined, as well as the presence and variation in the magnitude of allocational costs of tolerance. Selection analyses support the adaptive differentiation hypothesis. Tolerance was favored at the site with higher average level of tolerance, and resistance was favored at the site with higher average level of resistance. The presence of significant environmentally dependent costs of tolerance was in agreement with site variation in the adaptive value of tolerance. Our results support the expectation that environmentally dependent costs of plant defensive strategies can generate differences among populations in the evolutionary trajectory of defensive traits and promote the existence of a selection mosaic. The pattern of contrasting selection on tolerance suggests that, in some populations of D. stramonium, tolerance may alter the strength of reciprocal coevolution between plant resistance and natural enemies.
This study evaluated how natural selection act upon two proposed alternatives of defence (growth and resistance) against natural enemies in a common garden experiment using genetic material (full-sibs) from three populations of the annual plant Datura stramonium. Genetic and phenotypic correlations were used to search for a negative association between both alternatives of defence. Finally, the presence ⁄ absence of natural enemies was manipulated to evaluate the selective value of growth as a response against herbivory. Results indicated the presence of genetic variation for growth and resistance (1 -relative damage), whereas only population differentiation for resistance was detected. No correlation between growth and resistance was detected either at the phenotypic or the genetic level. Selection analysis revealed the presence of equal fitness benefits of growth and resistance among populations. The presence ⁄ absence of natural herbivores revealed that herbivory did not alter the pattern of selection on growth. The results indicate that both strategies of defence can evolve simultaneously within populations of D. stramonium.
Abstract. In this study we present a simple optimization model for the evolution of defensive strategies (tolerance and resistance) of plants against their natural enemies. The model specifically evaluates the consequences of introducing variable costs and benefits of tolerance and resistance and nonlinear cost-and-benefit functions for tolerance and resistance. Incorporating these assumptions, the present model of plant defense predicts different evolutionary scenarios, not expected by previous work. Basically, the presence of an adaptive peak corresponding to intermediate levels of allocation to tolerance and resistance can arise when the shape parameter of the cost function is higher than the corresponding of the benefit function. The presence of two alternatives peaks of maximum tolerance and maximum resistance occurs only when benefits of tolerance and resistance interact less than additive. Finally, the presence of one peak of maximum resistance or maximum tolerance depends on the relative values of the magnitude of costs for tolerance and resistance. An important outcome of our model is that under a plausible set of conditions, variable costs of tolerance and resistance can represent an important aspect involved in the maintenance of intermediate levels of tolerance and resistance, and in favoring adaptive divergence in plant defensive strategies among populations. The model offers a framework for future theoretical and empirical work toward understanding spatial variation in levels of allocation to different defensive strategies.Key words. Evolutionarily stable strategy, host-pathogen interaction, plant-herbivore interaction, resistance, tolerance. During the last decade, the understanding of plant-enemy interactions has benefited by the incorporation into models of a ubiquitous type of defense (i.e., tolerance). Tolerance has been defined as the ability of a plant genotype to reduce the negative effects of consumers (e.g., herbivores, pathogens) on plant fitness (Rosenthal and Kotanen 1994;Strauss and Agrawal 1999;Stowe et al. 2000;Fornoni et al. 2003a). Unlike resistance (i.e., the ability of a plant to reduce the attack of natural enemies), tolerance is not believed to negatively affect the success of herbivore or pathogen populations (Rosenthal and Kotanen 1994;Fay et al. 1996; Roy and Kichner 2000;Tiffin 2000a;Restif and Koella 2003; but see Stinchcombe 2002). Consequently, the evolution of tolerance can limit antagonistic coevolution between plants and their enemies, whereas the evolution of resistance prolongs such coevolutionary outcome (Rausher 2001).The joint evolution of plant tolerance and resistance to natural enemies has attracted substantial theoretical attention over the last decade (Rosenthal and Kotanen 1994;Fineblum and Rausher 1995;Strauss and Agrawal 1999;Mauricio 2000;Roy and Kirchner 2000;Stowe et al. 2000;Tiffin 2000a;Restif andKoella 2003, 2004;Fornoni et al. 2003a). Several experimental studies have tested some of the predictions made by these theoretical analyses (Simms and T...
Because most species are collections of genetically variable populations distributed to habitats differing in their abiotic/biotic environmental factors and community composition, the pattern and strength of natural selection imposed by species on each other's traits are also expected to be highly spatially variable. Here, we used genomic and quantitative genetic approaches to understand how spatially variable selection operates on the genetic basis of plant defenses to herbivores. To this end, an F 2 progeny was generated by crossing Datura stramonium (Solanaceae) parents from two populations differing in their level of chemical defense. This F 2 progeny was reciprocally transplanted into the parental plants' habitats and by measuring the identity by descent (IBD) relationship of each F 2 plant to each parent, we were able to elucidate how spatially variable selection imposed by herbivores operated on the genetic background (IBD) of resistance to herbivory, promoting local adaptation. The results highlight that plants possessing the highest total alkaloid concentrations (sum of all alkaloid classes) were not the most well-defended or fit. Instead, specific alkaloids and their linked loci/alleles were favored by selection imposed by different herbivores. This has led to population differentiation in plant defenses and thus, to local adaptation driven by plant-herbivore interactions.
.–In this study we examine the hypothesis that divergent natural selection produces genetic differentiation among populations in plant defensive strategies (tolerance and resistance) generating adaptive variation in defensive traits against herbivory. Controlled genetic material (paternal half‐sib families) from two populations of the annual Datura stramonium genetically differentiated in tolerance and resistance to herbivory were used. This set of paternal half‐sib families was planted at both sites of origin and the pattern of genotypic selection acting on tolerance and resistance was determined, as well as the presence and variation in the magnitude of allocational costs of tolerance. Selection analyses support the adaptive differentiation hypothesis. Tolerance was favored at the site with higher average level of tolerance, and resistance was favored at the site with higher average level of resistance. The presence of significant environmentally dependent costs of tolerance was in agreement with site variation in the adaptive value of tolerance. Our results support the expectation that environmentally dependent costs of plant defensive strategies can generate differences among populations in the evolutionary trajectory of defensive traits and promote the existence of a selection mosaic. The pattern of contrasting selection on tolerance suggests that, in some populations of D. stramonium, tolerance may alter the strength of reciprocal coevolution between plant resistance and natural enemies.
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