Costs of resistance and correlational selection in the multiple‐herbivore community of Solanum carolinense

Although a central assumption of most plant-defense theories is that resistance is costly, fitness costs have proven difficult to detect in the field. One useful, though labor-intensive, method to detect costs is to quantify stabilizing selection acting on resistance in field populations. Here, we report on an experimental field study of Solanum carolinense in which we employed a quadratic phenotypic-selection analysis on 12 types of resistance (defined operationally as one minus the proportion of tissue damaged) involving nine species of herbivores. For seven types of resistance, we found significant stabilizing selection and intermediate optimum levels, indicating the existence of fitness costs. These costs were greatest for resistance against frugivores, moderate for florivores, and lowest for folivores. In addition, significant correlational selection gradients were found for 10 pairs of resistance measures, which we interpret as evidence that the fitness impacts of these pairs of herbivores combined nonadditively. When the herbivores fed on the same type of tissue, their impact was synergistic (greater than additive), and when they fed on different tissues, their impact was antagonistic (less than additive). We suggest this may be a general pattern for correlational selection on resistance to different herbivores. Plants suffer attacks by a wide range of natural enemies, despite the fact that most plant populations apparently maintain genetic variation for the ability to resist these attacks (Maddox and Root 1987; Karban 1992; Kliebenstein 2014). Thus, a fundamental goal in the field of plant-herbivore evolutionary ecology is to elucidate factors that constrain plants from evolving higher levels of resistance when higher levels would appear to be within reach (Rausher 1996; Pilson 2000). One common explanation is that resistance comes at a cost, and plants are only likely to evolve resistance to the point at which the benefits of reduced damage do not exceed the costs of that resistance (Simms and Rausher 1987; Simms 1992; Bergelson and Purrington 1996; Koricheva 2002). The past few decades have seen extensive work identifying types of resistance costs and devising methods to detect these costs in plants (Rausher 1992b; Vila-Aiub et al. 2011; Cipollini et al. 2014). However, detecting costs of resistance in plant populations has often proved difficult (Bergelson and Purrington 1996; Agrawal 2011). It has been especially challenging to determine costs in a way that is ecologically and evolutionary relevant in natural populations (Cipollini et al. 2014). One method of detecting costs that is especially relevant to evolutionary ecologists is investigating the pattern of natural selection for resistance in field populations (Agrawal 2011; Cipollini et al. 2014). This method involves the measurement of damage levels (i.e., operational resistance) or candidate resistance traits, estimating plant fitness, and applying regression analysis of fitness on the resistance measurements (Lande and Arnold 1983). When such a selection analysis is run, a negative quadratic regression coefficient for a resistance measure suggests that stabilizing selection is acting on resistance. If stabilizing selection is detected, then it is likely that there is an intermediate optimum level of resistance, above which resistance is too costly and is thus selected against (Simms and Rausher 1987; Rausher 1992b). Although this selection analysis approach can provide powerful evidence of evolutionarily relevant costs of resistance, it is quite labor-intensive (Agrawal 2011). Thus, it has only been employed in a handful of plant-herbivore systems to date (e.g., Rausher and