Evolution of Mixed Strategies of Plant Defense Allocation Against Natural Enemies

Abstract

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...

Heritable variation in the foliar secondary metabolite sideroxylonal in Eucalyptus confers cross-resistance to herbivores

“…Average narrow-sense heritability (with standard errors in parentheses), estimated using the same provenances are shown italicized and on the diagonal. The genetic correlation of height and DBH was estimated using Fisher optimisation to obtain model convergence In addition to resistance, plants may employ alternative or additional strategies to limit the costs of herbivory, such as tolerance (Fornoni et al 2004) or escaping herbivory through faster growth (Kursar and Coley 2003). We found some support for the latter in E. tricarpa, as overall insect damage was related to both sideroxylonal concentration and growth.…”

Protein storage and root:shoot reallocation provide tolerance to damage in a hybrid willow system

“…Even if not fixed, as observed in several studies (Weinig et al 2003;Fornoni et al 2004;Boege et al 2007;Stevens et al 2007), selection should reduce variation in tolerance. Thus, studies exploring a single species may provide limited insight regarding the traits that confer tolerance to damage.…”

“…Ecologists have also intensively studied tolerance to damage. Studies have probed issues centering on the evolution of tolerance (Simms and Triplett 1994;Agrawal et al 1999;Juenger and Bergelson 2000;Fornoni et al 2003Fornoni et al , 2004Weinig et al 2003;Stevens et al 2007;Fornoni 2011) and the implications of the environment on the expression of tolerance (Siemens et al 2003;Katjiua and Ward 2006;Hódar et al 2008;Vandenberghe et al 2008). In a complementary framework to these evolutionary questions, research has also started to detail mechanisms that provide tolerance to herbivore damage (van der Meijden et al 2000;Stevens et al 2008;Eyles et al 2009;Fornoni 2011); however, our understanding of the mechanistic basis of tolerance is still underdeveloped.…”

“…Studies on annuals and short-lived, monocarpic herbs provide better estimates of lifetime fitness, so research on plant tolerance to damage has focused on these plants (Fineblum and Rausher 1995;Rosenthal and Welter 1995;Lennartsson et al 1998;Mauricio et al 1997;Juenger and Bergelson 2000;van der Meijden et al 2000;Fornoni et al 2003Fornoni et al , 2004Weinig et al 2003). Even though some studies have examined tolerance in perennial herbs and in woody plants (Hochwender et al 2000b; Rogers and Siemann 2002;Myers and Kitajima 2007;Stevens et al 2007Stevens et al , 2008Eyles et al 2009), studies of woody plants have usually not incorporated reproductive fitness into their evaluation of tolerance (but see Kaitaniemi et al 1999;Pratt et al 2005).…”

Impact of attack by Gnorimoschema gallmakers on their ancestral and novel Solidago hosts

“…data), and Lau (2008, working with Lotus wrangelianus) showed that selection on tolerance weakens when insect attack is sparse. It is even possible that low attack rates on S. gigantea reflect the evolution of increased resistance after G. gallaesolidaginis's host shift-and if resistance and tolerance trade off (Fornoni et al 2004;Núñez-Farfán et al 2007;Agrawal 2011; but see Jokela et al 2000) then a response to selection in resistance might pre-empt a response in tolerance. We have not measured resistance to G. gallaesolidaginis by S. altissima/gigantea, although Hakes and Cronin (2011) found selection against resistance to leaf-chewing herbivores in S. altissima (and no evidence for resistance-tolerance tradeoffs).…”