Simultaneous evolution of competitiveness and defense: induced switching in Arabis drummondii

Abstract

Optimality theory for plant defense against herbivores predicts an evolutionary tradeoff between the abilities to compete and defend. We tested this hypothesis by studying the effects of genetic variation in competitiveness on defense expression. Two closely related and differentially competitive congeners were compared for levels of resistance, tolerance, and secondary metabolite production. In a growth room experiment, plants of Arabis drummondii and A. holboellii were grown in the presence and absence of the common bunch grass Boutelloua gracilis, the specialist herbivore Plutella xylostella, and generalist herbivore Trichoplusia ni. Tolerance to competition, measured as growth next to the grass relative to controls in the absence of grass, was greatest for A. drummondii, the species that occurred in communities with higher densities of inter-specific neighbors. Measures of defense (resistance to herbivores, tolerance to damage, and concentrations of glucosinolates) varied inconsistently between the Arabis, species, depending on type of herbivore, competition level, and type of defense. The better competitor A. drummondii was more resistant to specialist herbivores, as in the field, and exhibited greater herbivoreand competition-induced changes in glucosinolate profiles. Further, when plants of A. drummondii were fed upon in competitive environments, the induced glucosinolate response was reduced while tolerance levels increased in an apparent switching of induced strategies. We suggest that competitiveness and defense responses are sometimes positively correlated because some defensive traits also function as competitive traits. A competitive function for defenses may also explain why defenses were affected by competition. Alternatively, since the induced response did not increase estimates of total glucosinolate content significantly, minimal defense costs might also allow the simultaneous evolution of competitiveness and defense. Finally, when faced with both herbivory and competition, some competitive species, such as A. drummondii, may switch to growth-based rather than toxin-based strategies as recent theoretical models predict.

Induced responses to competition and herbivory: natural selection on multi‐trait phenotypic plasticity

“…Thus, by being activated by herbivores, signaling molecules could enhance responses to plant competition. In addition, secondary metabolites induced by herbivores could also have allelopathic properties (Inderjit 1996, Lankau andStrauss 2007), reducing the costs of defense under competitive environments, as has been found for Arabis perennans (Siemens et al 2003) and A. drummondii (Jones et al 2006). The benefits of an increased realized resistance in the competitive environment was also suggested by the positive selection gradient observed for this response.…”

“…For example, abscisic acid, which is an important hormone regulator of responses to water and salt stress, has been found to enhance the jasmonate-induced defenses against herbivores in tomato plants (Thaler and Bostock 2004). Moreover, increased resistance, and/or other functions sharing metabolic pathways with such response, can provide some benefits to plants growing under competition (Cipollini 2004, Jones et al 2006. For example, the signaling role of jasmonic acid induced after herbivore attack has been reported to be associated with responses of plants to water (Reymond et al 2000) and salt (Wang et al 2001) stress.…”

“…The present study, however, shows the opposite trend and rather adds to the evidence supporting the recently proposed Defense Stress Benefit Hypothesis (Siemens et al 2003), suggesting that, in fact, resistance can be enhanced in competitive environments. Overall, the accumulation of studies supporting both hypotheses suggests that the interactive effects of competition and herbivory on plant resistance may be driven not only by resource trade-offs, but by more complex dynamics given the putative multiple functions of such responses (Jones et al 2006) and may also depend on which resources are depleted by competition (Agrawal 2004, Wise andAbrahamson 2005) and their influence on both constitutive and induced resistance traits. Notes: Directional selection gradients were obtained from a selection analysis using a contextual analysis approach, which included all five induced responses and their means per patch as independent variables in a multiple regression on relative fitness values.…”

Comparative Genetic Mapping inBoechera stricta, a Close Relative of Arabidopsis

“…Numerous studies have analyzed molecular and phenotypic diversity of Boechera species. This includes the molecular evolutionary analysis of gene families (Bishop et al, 2000;Schein et al, 2004;Benderoth et al, 2006), the phylogeography of haplotypes (Dobeš et al, 2004b;Song et al, 2006), the occurrence of supernumary B chromosomes (Böcher, 1951;Sharbel et al, 2004), variation in breeding systems and ploidy (Sharbel and MitchellOlds, 2001;Schranz et al, 2005;Schranz et al, 2006a), drought tolerance (Knight et al, 2006), morphological and taxonomical diversity (Rollins, 1993;Al-Shehbaz, 2003;Windham and Al-Shehbaz, 2006), and the evolved responses to pathogen or insect pests (Roy, 1993;Roy and Kirchner, 2000;Jones et al, 2006). The further elucidation of these and other patterns of variation would be greatly aided by the creation and analysis of segregating genetic stocks.…”

Optimal defense in plants: assessment of resource allocation costs

“…Combinations included ratios between glucosinolates that may have precursor or other biosynthetic relationships (Heidel et al 2006), and principal component analysis, which may reflect aspects of variation in glucosinolate profiles (Jones et al 2006). Previously, for example, we have detected an herbivore-induced glucosinolate response using these glucosinolate ratios (D.H. Siemens unpublished data: the induced response was detected at 24 and 48 h post feeding, but not earlier at 2 h-damage-by-time interaction, F 6,142 = 2.393, P = 0.031).…”