A deeper understanding of system interactions can explain contradictory field results on pesticide impact on honey bees

While there is widespread concern regarding the impact of pesticides on honey bees, well-replicated field experiments, to date, have failed to provide clear insights on pesticide effects. Here, we adopt a systems biology approach to gain insights into the web of interactions amongst the factors influencing honey bee health. We put the focus on the properties of the system that depend upon its architecture and not on the strength, often unknown, of each single interaction. Then we test in vivo, on caged honey bees, the predictions derived from this modelling analysis. We show that the impact of toxic compounds on honey bee health can be shaped by the concurrent stressors affecting bees. We demonstrate that the immune-suppressive capacity of the widespread pathogen of bees, deformed wing virus, can introduce a critical positive feed-back loop in the system causing bistability, i.e., two stable equilibria. Therefore, honey bees under similar initial conditions can experience different consequences when exposed to the same stressor, including prolonged survival or premature death. The latter can generate an increased vulnerability of the hive to dwindling and collapse. Our conclusions reconcile contrasting field-testing outcomes and have important implications for the application of field studies to complex systems

Honeybees use various criteria to select the site for performing the waggle dances on the comb

After returning to the hive, successful honeybee foragers dance on the surface of the comb, where they interact with dance followers. It has been shown that bees establish a specific site for their waggle dances that is likely marked with chemical signals. By recording the site where dances take place on the comb in a single-frame observation hive, we investigated the relative importance of three different criteria for the selection of the dance floor by bees, including the distance from the hive entrance, the cell filling, and the chemical marking by bees and found that all these criteria play a role, albeit their importance does not seem to be equal

Gene expression analysis of mite-infested pupae and adult bees.

Relative expression of the immune-related genes Apidaecin (a), Defensin-1 (b), Dorsal-1A (c) and of the RNAi related genes Argonaute-2 (d) and Dicer-like (e) of pupae and adult bees challenged with V. destructor. (Two-way ANOVA test. Apidaecin: mite: df = 1, F = 0.192, p = 0.66; age: df = 1, F = 1.179, p = 0.29; mite*age: df = 1, F = 1.237, p = 0.28; Defensin-1: mite: df = 1, F = 9.680, p df = 1, F = 294.82, p df = 1; F = 0.185, p = 0.67; Dorsal-1A: mite: df = 1, F = 2.156, p = 0.15; age: df = 1, F = 37.624, p 0.01; df = 1, F = 3.058, p = 0.09).; Ago-2: mite: df = 1, F = 2.99, p = 0.09; age: df = 1, F = 0.09, p = 0.75; mite*age: df = 1, F = 1.07, p = 0.31,; Dicer-like: mite: df = 1, F = 1.90, p = 0.18; age: df = 1, F = 5.23, p = 0.03; mite*age: df = 1, F = 0.93, p = 0.34. Uninfested pupae: n = 6, mite-infested pupae: n = 6, uninfested adults: n = 6, mite-infested adults: n = 5).</p

Survival of the honey bees DWV-infected during the pupal stage.

Survival curves of adult honey bees infected or not with 10^3 DWV copies at the larval stage and maintained under lab conditions (Wilcoxon test. Chi square = 6.42, df = 1, p = 0.01, uninfected bees: n = 52, DWV-infected bees: n = 50).</p

DWV genotypes.

Percentage of viral reads mapping on the two genomes, type A and B DWV.</p

DEGs bees infested during the pre-imaginal stages.

List of the genes differentially expressed between adult bees infested during the larval stage and uninfested. (DOCX)</p

Survival of the honey bees mite-infested at the adult stage.

Survival curves of the adult bees artificially infested or not with one Varroa mite at the emergence and maintained under lab conditions (Wilcoxon test. Chi square = 7.82; df = 1; p < 0.01, uninfested bees: n = 82, mite-infested bees: n = 83).</p

Survival of honey bees mite-infested during the pupal stage.

Survival curves of the adult bees artificially infested or not with one Varroa mite at the L5 stage and maintained under lab conditions (Wilcoxon test. Chi square = 6.4; df = 1; p < 0.01, uninfested bees: n = 103, mite-infested bees: n = 76).</p

Survival of the honey bees DWV-infected at the adult stage.

Survival curves of the adult honey bees infected or not with 10^3 DWV copies after the emergence (Wilcoxon test. Chi square = 22.29, df = 1, p < 0.01, uninfected bees: n = 99, DWV-infected bees: n = 98).</p