Survival of the choosiest: females prefer to oviposit on rare tolerant plants

Most larvae of phytophagous insects have little mobility, so they must complete their development on those plants 'chosen' by their mothers, even if this does not always increase the performance of her offspring. Here, we tested the hypothesis that the defence strategy expressed by host plants and the frequency at which they are represented within populations can condition both the preference of the female and the performance of her offspring. Using the plant Datura stramonium and its specialist insect Lema daturaphila, we conducted an experiment in which the frequency of resistant and tolerant genotypes within cages was manipulated, and the initial density of herbivorous adults was controlled. Results provide conclusive evidence of negative frequency-dependent oviposition preference for tolerant plants and differential density-dependent effect between resistant and tolerant plants on larval survival. Female oviposition preference also changed larval density, which in turn fed back to influence larval survival. Moreover, we found that oviposition preference for rare tolerant plants resulted, indeed, in lower plant fitness. Thus, the evolution of phytophagous insects' oviposition preference can be shaped by the frequency in which different plant defensive strategies are represented within the population and can create evolutionary feedback on their host plants. This article is part of the theme issue 'Exploring negative frequency dependent selection across levels: from genetics to ecology and back again'.