Thomas Dorey

Summary Temperature influences the distribution and performance of both plants and insect herbivores. Consequently, plant–herbivore interactions are likely to vary across thermal gradients, which could affect the evolution of plant defense. Furthermore, temperature fluctuations may elicit immediate changes in defense. To study the evolutionary and ecological aspects of plant antiherbivore defense depending on temperature, we conducted a transplant experiment on a mountain slope involving 30 Brassicaceae species varying in elevational distribution. Additionally, we carried out a climate‐chamber experiment on a subset of 12 species to assess the temperature dependence of constitutive and induced defenses. The transplant experiment revealed that species from higher elevations experienced less herbivory than those from lower elevations. The climate‐chamber experiment demonstrated that high‐elevation species mounted stronger induced defenses in physical properties of leaves and in phytochemical diversity. Plant responses to low temperature, compared to control temperature, were lower constitutive defense and increased defense induction limited to leaf toughness. By contrast, high temperature increased constitutive chemical defense and defense‐induced leaf toughness. Results suggest higher herbivory resistance in high‐elevation Brassicaceae species by the induced remodeling of chemical defense. Such defense indication may have been shaped by rare but hard‐to‐tolerate herbivory in the evolutionary past.

Abstract Although different ecological factors shape adaptative evolution in natural habitats, we know little about how their interactions impact local adaptation. Here we used eight generations of experimental evolution with outcrossing Brassica rapa plants as a model system, in eight treatment groups that varied in soil type, herbivory (with/without aphids), and pollination mode (hand- or bumblebee-pollination), to study how biotic interactions affect local adaptation to soil. First, we show that several plant traits evolved in response to biotic interactions in a soil-specific way. Second, using a reciprocal transplant experiment, we demonstrate that significant local adaptation to soil-type evolved in the “number of open flowers”, a trait used as a fitness proxy, but only in plants that evolved with herbivory and bee pollination. Whole genome re-sequencing of experimental lines revealed that biotic interactions caused a 10-fold increase in the number of SNPs across the genome with significant allele frequency change, and that alleles with opposite allele frequency change in different soil types (antagonistic pleiotropy) were most common in plants with an evolutionary history of herbivory and bee pollination. Our results demonstrate that the interaction with mutualists and antagonists can facilitate local adaptation to soil type through antagonistic pleiotropy.

Abstract Divergent evolution leads to variation among populations and thus promotes diversification. In plants, adaptation to different soils, pollinator guilds, and herbivores is thought to be a key ecological driver of adaptive divergence, but few studies have investigated this process experimentally. Here we use experimental evolution with fast cycling Brassica rapa plants to study the impact of soil, pollination, herbivory, and their interactions on divergent evolution in various traits during eight generations of selection. We found significant evolutionary changes in plant phenotypes caused by all three factors and their interactions. In the richer soil type, plants showed higher evolutionary rates, especially with bumblebee-pollination, which led to the evolution of increased attractiveness of plants to bumblebees. Plants that had experienced aphid-herbivory showed lower attractiveness. We found the strongest evolutionary divergence when plants evolved in different soils with bee-pollination rather than hand-pollination, irrespective of herbivory. This “soil-pollinator effect” impacted divergence in diverse suites of traits, for example leaf size, flowering time, flower petal length, some floral volatiles and leaf glucosinolates. We conclude that the interaction between soil and biotic pollination may be an important cause for divergent evolution of plants growing on different soil types, even without a shift in pollinator guilds.