Local adaptation of aboveground herbivores towards plant phenotypes induced by soil biota

Abstract

Background: Soil 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 findings: We 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/significance: These 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).

Figure 1. Effects of the soil treatment on plant performance.

A): plant dry biomass; B: shoot water content; C: N and P-content. Equal notations indicate non-significant contrast for the respective plant performance measurements. Values marked with the same letter symbol do not differ significantly (P>0.05) after Tukey correction.

Figure 2. Effects of soil treatment on the selected life history parameters (mean values ± SE) for mites of the three selection lines.

Green bars: mites developed on AMF-treated plants; Red bars: mites developed on Nematode-treated plants; Grey bars: mites developed on Control plants (no belowground biota). A: time to maturity (females), B: survival rate of females, C: daily fecundity, D: sex ratio (females/total clutch size). Statistical significant differences within selection lines after Tukey-corrections: *: P<0.05; **: P<0.01; ***: P<0.001.

Figure 3. Effects of the soil treatment on measure growth rate r_m.

The mean integrated fitness measure growth rate r_m relates to the number of female offspring by one female per generation for mites from each of the three selection lines. Green bars: AMF-treatment; Red bars: Nematode-treatment Grey bars: Control treatment (no belowground biota). Error bars represent the 99% CI for each of the selection line x treatment combinations. *ns: differences between nematode and AMF treatment are not significant after correction for multiple testing (pairwise difference: P = 0.01).