Jasmonate-induced responses are costly but benefit plants under attack in native populations

Abstract

Herbivore attack is widely known to reduce food quality and to increase chemical defenses and other traits responsible for herbivore resistance. Inducible defenses are commonly thought to allow plants to forgo the costs of defense when not needed; however, neither their defensive function (increasing a plant's fitness) nor their cost-savings function have been demonstrated in nature. The root-produced toxin nicotine increases after herbivore attack in the native, postfire annual Nicotiana attenuata and is internally activated by the wound hormone, jasmonic acid. I treated the roots of plants with the methyl ester of this hormone (MeJA) to elicit a response in one member of each of 745 matched pairs of plants growing in native populations with different probabilities of attack from herbivores, and measured the lifetime production of viable seed. In populations with intermediate rates of attack, induced plants were attacked less often by herbivores and survived to produce more seed than did their uninduced counterparts. Previous induction did not significantly increase the fitness of plants suffering high rates of attack. However, if plants had not been attacked, induced plants produced less seed than did their uninduced counterparts. Jasmonate-induced responses function as defenses but are costly, and inducibility allows this species to forgo these costs when the defenses are unnecessary.

Figure 1

Mean (±1 SEM) shoot nicotine concentrations of N. attenuata plants (5/treatment) growing in a 2-year-old burn (population IIA) that had their roots treated with MeJA suspended in 10 ml of water by vigorous shaking or four of their leaves wounded with two rolls from a fabric tracing wheel (which produces a line of 4.5 punctures per cm of leaf lamina) 6 days before analysis. The amount of MeJA required to induce plants growing in the soil was approximately 10 times that required to induce plants growing in water culture (12). Controls were treated with 10 ml of water.

Figure 2

Lifetime capsule and viable seed production in matched pairs of N. attenuata plants growing in a 1-year-old burn (population IA) in which members of a pair were treated twice during the growing season with either methyl jasmonate (500 μg of MeJA suspended in water) or with 10 ml of water (see Fig. 1). (Left) The frequency distribution of differences in capsules produced per plant between treated and control plants in each pair. Seeds per capsule, mass per seed, and % viability of seeds did not differ significantly between plants in a pair (Table 2). Negative values reflect a cost of MeJA treatment (control member producing more capsules than its treated counterpart) and positive values reflect a benefit. (Middle) The mean (±1 SEM) capsules per plant for each treatment group (MeJA treatments, filled bars) and the statistical analysis of the differences between pairs. (Right) The mean (±1 SEM) lifetime viable seed production (calculated as described in Table 1) for each treatment group and the statistical analysis of the differences between pairs. Of the original 300 pairs, 241 survived to produce seed; of these survivors, both treated and control members of 160 pairs were attacked (losing 20% or more leaf area to herbivores by July). In 43 pairs both members escaped attack; in 13 pairs only the treated member was attacked; in 25 pairs only the control member of the pair was attacked.