Adaptive change in a genetically diverse plant population: Aphids as drivers of natural selection

Background/Question/Methods

Selection pressures exerted by natural enemies are invoked in recent biodiversity theory to explain high levels of diversity. Herbivores can potentially maintain genetic diversity within a plant community if plant genotypes differ in their resistance towards herbivores, and if resistance traits trade-off with plant fitness. At the meta-population scale, fluctuations in the abundance of an herbivore community could locally favour resistant genotypes, where in the absence of herbivores the most competitive genotype would dominate. However, the strength and specificity of such selective pressures remain largely untested and the existence of such trade-offs has been repeatedly challenged. We used a multi-generational experiment to quantify a) the selective pressures exerted by three different aphid species on populations of Arabidopsis thaliana and b) the costs of leaf hairs and glucosinolates (a group of defensive plant metabolites) in the absence of aphids. We established identical populations from a set of Arabidopsis genotypes and exposed these populations for five subsequent generations to the three aphid species or a no-aphid control, each treatment being replicated six times.

Results/Conclusions

The relative impact of aphids on plant biomass became smaller over time as a result of adaptive change in population composition. Average hair density was strongly reduced in the absence of herbivores, while aphid feeding maintained hair density at ancestral levels. This difference was linked to a competitive genotype with few leaf hairs that was dominant in controls but absent from all aphid treatments. Regardless of the treatment, mainly two groups of genotypes with distinctly different glucosinolate profiles dominated the final generation. However, these two groups were differentially favoured by the aphid species, with one of the species inverting the order of dominance between the two groups. These results provide clear experimental evidence that herbivores can exert strong, but specific selective pressure on plant populations and that at least some resistance traits carry a cost. A diverse, fluctuating herbivore community is therefore likely to maintain higher genetic diversity than would be predicted by classical niche-based theories, which is an important insight for diversity conservation.