Increased susceptibility to fungal disease accompanies adaptation to drought in Brassica rapa

Abstract

Recent studies have demonstrated adaptive evolutionary responses to climate change, but little is known about how these responses may influence ecological interactions with other organisms, including natural enemies. We used a resurrection experiment in the greenhouse to examine the effect of evolutionary responses to drought on the susceptibility of Brassica rapa plants to a fungal pathogen, Alternaria brassicae. In agreement with previous studies in this population, we found an evolutionary shift to earlier flowering postdrought, which was previously shown to be adaptive. Here, we report the novel finding that postdrought descendant plants were also more susceptible to disease, indicating a rapid evolutionary shift to increased susceptibility. This was accompanied by an evolutionary shift to increased specific leaf area (thinner leaves) following drought. We found that flowering time and disease susceptibility displayed plastic responses to experimental drought treatments, but that this plasticity did not match the direction of evolution, indicating that plastic and evolutionary responses to changes in climate can be opposed. The observed evolutionary shift to increased disease susceptibility accompanying adaptation to drought provides evidence that even if populations can rapidly adapt in response to climate change, evolution in other traits may have ecological effects that could make species more vulnerable.

Keywords: Alternaria brassicae; drought; flowering time; rapid evolution; resurrection approach.

Fig. 1

Evolutionary changes in a natural B. rapa population between pre-drought ancestors (dark bars) and post-drought descendants (light bars). We found a significant evolutionary shift to (A) earlier flowering, (B) greater disease susceptibility, and (C) increased specific leaf area (SLA). There was also evidence for plasticity in these traits, with the direction of the response opposite to the evolutionary response (A–B) except for SLA (C). The plants were grown under well-watered (wet) or drought stressed (dry) treatments and were inoculated (fungus) or mock inoculated (none) with fungal spores. A three-way ANOVA (two-way for disease susceptibility) was conducted on transformed data (Table S1) with population, inoculation, and watering treatments as fixed-effects, followed by specific pairwise comparisons within treatments conducted using one-way ANOVAs. Untransformed means are shown with standard errors. Statistics are provided in Table 1 (two- and three- way ANOVAs) and the text (one-way ANOVAs). Sample sizes are shown above each bar.