Foliar-feeding insects acquire microbiomes from the soil rather than the host plant

Abstract

Microbiomes of soils and plants are linked, but how this affects microbiomes of aboveground herbivorous insects is unknown. We first generated plant-conditioned soils in field plots, then reared leaf-feeding caterpillars on dandelion grown in these soils, and then assessed whether the microbiomes of the caterpillars were attributed to the conditioned soil microbiomes or the dandelion microbiome. Microbiomes of caterpillars kept on intact plants differed from those of caterpillars fed detached leaves collected from plants growing in the same soil. Microbiomes of caterpillars reared on detached leaves were relatively simple and resembled leaf microbiomes, while those of caterpillars from intact plants were more diverse and resembled soil microbiomes. Plant-mediated changes in soil microbiomes were not reflected in the phytobiome but were detected in caterpillar microbiomes, however, only when kept on intact plants. Our results imply that insect microbiomes depend on soil microbiomes, and that effects of plants on soil microbiomes can be transmitted to aboveground insects feeding later on other plants.

Bacterial communities of herbivores and pollinators that have co-evolved Cucurbita spp

“…The high number of rare, low abundance OTUs in Acalymma herbivores is consistent with accumulating evidence that the local environment – ie , the variable and diverse microbial communities that colonize plants or the surrounding soil – are the most significant source of microbial exposure for most non-social and non-sap feeding insects (Moran 2003, Kwong and Moran 2016, Hammer et al 2017, McFrederick et al 2017, Hammer et al 2019, Hannula et al 2019). The lower average number of OTUs per insect in bees compared to beetles may reflect that bees exclusively feed on Cucurbita floral resources, while Acalymma beetles are often found feeding on other introduced cucurbit crop plants (most notably muskmelon and cucumbers, both Cucumis spp.…”

Gut microbiota metabolic potential correlates with body size between mulberry‐feeding lepidopteran pest species

“…44 For example, the caterpillar Mamestra brassicae (Lepidoptera; Noctuidae) actively acquires additional species of beneficial microbes from its soil environment. 45 In our case, considering that these mulberry pests in the final larval instar were collected from the same host plant species at the same site, host phylogeny thus appears to be a major driver shaping gut microbiota. Species differences in host physiology and local gut environment, such as pH, oxygen levels and redox conditions, can wileyonlinelibrary.com/journal/ps contribute to variation in microbiotas.…”

“…Insect gut bacterial diversity can be determined by multiple factors, including environmental habitat, diet, developmental stage and the phylogeny of the host . For example, the caterpillar Mamestra brassicae (Lepidoptera; Noctuidae) actively acquires additional species of beneficial microbes from its soil environment . In our case, considering that these mulberry pests in the final larval instar were collected from the same host plant species at the same site, host phylogeny thus appears to be a major driver shaping gut microbiota.…”

The microbiome of theMelitaea cinxiabutterfly shows marked variation but is only little explained by the traits of the butterfly or its host plant

“…In our study, we did not consider the soil below the host plant. The microbial communities of the soil have been previously highlighted as a potential source of microorganisms for the foliar caterpillar Mamestra brassicae (Hannula et al, 2019). However, if the soil was the microbiota source, we would expect caterpillars from the same host plant growing on the same soil to carry a more similar microbiota.…”