On the capacity for rapid adaptation and plastic responses to herbivory and intraspecific competition in insular populations of Plectritis congesta

A capacity for rapid adaptation should enhance the persistence of populations subject to temporal and spatial heterogeneity in natural selection, but examples from nature remain scarce. Plectritis congesta (Caprifoliaceae) is a winter annual that exhibits local adaptation to browsing by ungulates and hypothesized to show context‐dependent trade‐offs in traits affecting success in competition versus resistance or tolerance to browsing. We grew P. congesta from 44 insular populations historically exposed or naïve to ungulates in common gardens to (1) quantify genetic, plastic and competitive effects on phenotype; (2) estimate a capacity for rapid adaptation (evolvability); and (3) test whether traits favoured by selection with ungulates present were selected against in their absence. Plants from browsed populations bolted and flowered later, had smaller inflorescences, were less fecund and half as tall as plants from naïve populations on average, replicating patterns in nature. Estimated evolvabilities (3–36%) and narrow‐sense heritabilities (h2; 0.13–0.32) imply that differences in trait values as large as reported here can arise in 2–18 generations in an average population. Phenotypic plasticity was substantial, varied by browsing history and fruit phenotype and increased with competition. Fecundity increased with plasticity in flowering height given competition (0.47 ± 0.02 florets/cm, β ± se), but 23–77% faster in naïve plants bearing winged fruits (0.53 ± 0.04) than exposed‐wingless plants (0.43 ± 0.03) or exposed‐winged and naïve‐wingless plants (0.30 ± 0.03, each case). Our results support the hypothesis that context‐dependent variation in natural selection in P. congesta populations has conferred a substantial capacity for adaptation in response to selection in traits affecting success in competition versus resistance or tolerance to browsing in the absence versus presence of ungulates, respectively. Theory suggests that conserving adaptive capacity in P. congesta will require land managers to maintain spatial heterogeneity in natural selection, prevent local extinctions and maintain gene flow.