Phenological asynchrony between host plant and gypsy moth reduces insect gut microbiota and susceptibility to Bacillus thuringiensis

Abstract

The phenological synchrony between the emergence of overwintering herbivorous insects and the budding of host plants is considered a crucial factor in the population dynamics of herbivores. However, the mechanisms driving the interactions between the host plant, herbivores, and their pathogens are often obscure. In the current study, an artificially induced phenological asynchrony was used to investigate how the asynchrony between silver birch Betula pendula and gypsy moth Lymantria dispar affects the immunity of the insect to bacteria, its susceptibility to the entomopathogenic bacteria Bacillus thuringiensis, and the diversity in its midgut microbiota. The lysozyme‐like activity in both the midgut and hemolymph plasma and the nonspecific esterase activity and antimicrobial peptide gene expression in the midgut were studied in both noninfected and B. thuringiensis‐infected larvae. Our results provide the first evidence that phenologically asynchronous larvae are less susceptible to B. thuringiensis infection than phenologically synchronous larvae, and our results show that these effects are related to the high basic levels and B. thuringiensis‐induced levels of lysozyme‐like activities. Moreover, a 16S rRNA analysis revealed that dramatic decreases in the diversity of the larval gut bacterial consortia occurred under the effect of asynchrony. Larvae infected with B. thuringiensis presented decreased microbiota diversity if the larvae were reared synchronously with the host plant but not if they were reared asynchronously. Our study demonstrates the significant effect of phenological asynchrony on innate immunity‐mediated interactions between herbivores and entomopathogenic bacteria and highlights the role of nonpathogenic gut bacteria in these interactions.

Effects of phenological synchronization on caterpillar early-instar survival under a changing climate

“…Phenology can drive these relationships in similar ways as with multicellular natural enemies, as insect immunity can vary with host plant synchrony (Martemyanov et al 2015). The study of mycorrhizae (e.g., Tao et al 2016), phylloplane flora (e.g., Leong et al 1997), midgut biota (e.g., Mason and Raffa 2014;Martemyanov et al 2016), and pathogens (e.g., Hajek et al 1990;Leong et al 1997;van Frankenhuyzen et al 2007;Gowler et al 2015) in plant-herbivore systems is suggesting potentially important roles for multitrophic interactions with these poorly understood organisms. These relationships are only beginning to be identified and their phenologies or responses to climate have yet to be examined.…”

“…Recent work shows that late-emerging insects that are limited to feeeding on mature foliage (which contains higher tannin levels) are more susceptible to nuclear polyhedrosis virus (Martemyanov et al 2015) but less susceptible to Bacillus thuringiensis infection (Martemyanov et al 2016). The underlying mechanisms are not understood but could be related to effects on midgut biota: late-emerging larvae show dramatic decreases in the diversity of the midgut bacterial community (Martemyanov et al 2016). The relationship between pathogens and foliar chemistry, notably phenology and induced defenses following defoliation, in their effects on gypsy moth outbreak dynamics remains difficult to establish (Cory and Hoover 2006).…”

Ambient temperature‐mediated enzymic activities and intestinal microflora in Lymantria dispar larvae

“…The previous study suggested that intestinal microflora was involved in human's physical and mental health (Petersen, Skov, Thyssen, & Jensen, ; Stricoff & Robinson, ). Similarly, intestinal microflora plays diverse functions in invertebrate, such as olfactory behavior regulation (Qiao, Keesey, Hansson, & Knaden, ), metabolism (Ayayee, Muñoz‐Garcia, & Keeney, ; B. Chen et al, ), and immune (Lee, Lee, & Lee, ; Martemyanov et al, ; Xia et al, ). In addition, consistent changes of gut microbial community and host development indicated that the gut microbiota might be involved in the entomic development (B. Chen et al, ).…”

Insect parasites in multicomponent systems and development of new bioinsecticides

“…Polenogova, unpublished). In other experiments, we demonstrated that the diversity of bacteria in the L. dispar midgut was decreased by the consumption of low-quality leaves and was associated with a decrease in the susceptibility of the insects to the entomopathogenic bacterium B. thuringiensis [23].…”