Understanding the reciprocal adaptation that occurs between plant and herbivores is a central topic in Eco-evolutionary research. Over the past decades a growing body of literature has demonstrated the importance of soil biota to understand aboveground plant-herbivore interactions. Paradoxically, although the significance of such plant-mediated indirect interactions is well acknowledged from a community ecology perspective, the consequences in plant-herbivore evolutionary dynamics, although suggested, have been scarcely addressed. In order to tackle this issue, we first developed an individual-based simulation model in which we studied the effect of community structure (i.e. the presence/absence of soil biota) on the evolution of toxin production in a plant and the resistance to the plant toxin of an aboveground herbivore. Secondly, and in order to validate some of the conclusions obtained from the model, we addressed the topic experimentally. To do so, we created three selection lines out of a population of the foliar herbivore Tetranychus urticae by rearing for 15 generations individuals on bean plants grown in three different soils: (i) sterile soil, (ii) sterile soil inoculated with mycorrhiza and (iii) sterile soil inoculated with root-feeding nematodes. Afterwards, in a reciprocal breeding experiment we investigated whether local adaptation of herbivores towards the beans grown with different soil organisms occurred. We took females from each selection line and compared their performance on bean leaves from the three different soil treatments by monitoring a series of life history parameters: mortality, developmental time, fecundity and gender of the offspring.

Results/Conclusions

The outcome of the model indicated that the level of toxin produced by plants, and of the resistance to plant toxins of the aboveground herbivore was strongly influenced by the community structure, i.e. the presence or absence of soil organisms. The reciprocal breeding experiment showed that growth rates of T. urticae females were significantly higher on plants with soil conditions similar to the experienced during the selection phase compared to the growth rates on leaves from the other soil treatments; which demonstrates local adaptation of aboveground herbivores towards different plant phenotypes induced by soil biota. The results of these two studies suggest that soil biotic interactions may be important to understand the evolutionary ecology of aboveground plant-insect herbivore interactions.