Local Adaptation of Aboveground Herbivores towards Plant Phenotypes Induced by Soil Biota

Abstract

BackgroundSoil biota may trigger strong physiological responses in plants and consequently induce distinct phenotypes. Plant phenotype, in turn, has a strong impact on herbivore performance. Here, we tested the hypothesis that aboveground herbivores are able to adapt to plant phenotypes induced by soil biota.Methodology and Principal FindingsWe bred spider mites for 15 generations on snap beans with three different belowground biotic interactions: (i) no biota (to serve as control), (ii) arbuscular mycorrhizal fungi and (ii) root-feeding nematodes. Subsequently, we conducted a reciprocal selection experiment using these spider mites, which had been kept on the differently treated plants. Belowground treatments induced changes in plant biomass, nutrient composition and water content. No direct chemical defence through cyanogenesis was detected in any of the plant groups. Growth rates of spider mites were higher on the ecotypes on which they were bred for 15 generations, although the statistical significance disappeared for mites from the nematode treatment when corrected for all multiple comparisons.Conclusion/SignificanceThese results demonstrate that belowground biota may indeed impose selection on the aboveground insect herbivores mediated by the host plant. The observed adaptation was driven by variable quantitative changes of the different separately studied life history traits (i.e. fecundity, longevity, sex-ratio, time to maturity).

Dual benefit from a belowground symbiosis: nitrogen fixing rhizobia promote growth and defense against a specialist herbivore in a cyanogenic plant

“…In addition to variation in plant primary and secondary metabolites mediated by rhizobia, attractiveness of plants to herbivores is influenced by multiple factors, such as occupation by other herbivores or pathogens, presence of predators or parasitoids, microclimatic conditions, as well as by plant architecture, distribution and availability (e.g., Denno et al 1995;Rostás et al 2003;Bonte et al 2010). Under natural conditions belowground plantassociated species often show distinct spatial structure, although detailed knowledge on the scales of spatial variation in most natural systems is largely lacking (Ettema and Wardle 2002).…”

Plant-Mediated Systemic Interactions Between Pathogens, Parasitic Nematodes, and Herbivores Above- and Belowground

“…Studies testing systemic effects of sedentary RKNs on leaf-chewing herbivores generally show an increase in insect performance, whereas the migratory endoparasitic nematode Pratylenchus penetrans shows a reduction in performance. Likewise, the sedentary cyst nematode H. schachtii enhances the attractiveness of A. thaliana for the cell content-feeding spider mite Tetranynchus uricae and enhances its development (66), whereas the migratory root-feeding nematode P. penetrans reduces its fecundity on Phaseolus vulgaris (18). From such observations, it is tempting to speculate that sedentary nematodes have stronger facilitating effects on AG chewing herbivores than migratory nematodes.…”

Third-party mutualists have contrasting effects on host invasion under the enemy-release and biotic-resistance hypotheses

“…In tripartite interactions, the identity of all three interacting species is important and may influence the results of interactions (Bennett et al 2009;Kempel et al 2013;Zytynska et al 2014;Parker et al 2017). A recent study by Bonte et al (2010) found that spider mites adapted to the physiological change in snap beans induced by AMF in just fifteen generations. Schausberger et al (2012) found that Phytoseiulus persimilis, a predatory mite that is the natural enemy of the spider mite that attacks bean plants, was more strongly attracted by the volatiles of plants that were induced by the fungus Glomus mosseae.…”