Gut microbiota of dung beetles correspond to dietary specializations of adults and larvae

Abstract

Vertebrate dung is central to the dung beetle life cycle, constituting food for adults and a protective and nutritive refuge for their offspring. Adult dung beetles have soft mandibles and feed primarily on nutritionally rich dung particles, while larvae have sclerotized mandibles and consume coarser dung particles with a higher C/N ratio. Here, using the dung beetles Euoniticellus intermedius and E. triangulatus, we show that these morphological adaptations in mandibular structure are also correlated with differences in basic gut structure and gut bacterial communities between dung beetle life stages. Metagenome functional predictions based on 16S rDNA characterization further indicated that larval gut communities are enriched in genes involved in cellulose degradation and nitrogen fixation compared to adult guts. Larval gut communities are more similar to female gut communities than they are to those of males, and bacteria present in maternally provisioned brood balls and maternal 'gifts' (secretions deposited in the brood ball along with the egg) are also more similar to larval gut communities than to those of males. Maternal secretions and maternally provisioned brood balls, as well as dung, were important factors shaping the larval gut community. Differences between gut microbiota in the adults and larvae are likely to contribute to differences in nutrient assimilation from ingested dung at different life history stages.

Host dietary specialization and neutral assembly shape gut bacterial communities of wild dragonflies

“…In contrast, a 78 generalist host is more likely to stochastically sample a wider range of environmental microbes 79 associated with its variable diet. For example, scavengers and omnivores tend to have richer 80 gut communities (Yun et al 2014;Yadav et al 2015; Shukla et al 2016); and we expect to find 81 a positive correlation between host diet diversity and gut microbial diversity (Engel & Moran 82 2013; Yun et al 2014). Given this disruptive effect of dietary variation, strong host-imposed 83 selection should stabilize gut bacterial community composition, and minimize the impact of 84 stochastic or deterministic events.…”

What do we know about biological nitrogen fixation in insects? Evidence and implications for the insect and the ecosystem

“…For example, the broad‐headed bug, Riptortus clavatus , was shown to acquire the potential diazotroph Burkholderia from the environment at every generation (Kikuchi et al ., ). Indeed, evidence for the potential vertical transmission of diazotrophs is limited (e.g., Lauzon et al ., ; Ayayee et al ., ; Shukla et al ., ). In some cases, specialized regions and pouches in the insect's digestive system (especially in the hindgut) were characterized as “incubators” for beneficial bacteria, including potential diazotrophs, for example, in termites (Breznak, ), beetles (Ceja‐Navarro et al ., ; Shukla et al ., ), stinkbugs (Kikuchi et al ., ), and ants (van Borm et al ., ).…”

Developmental bias in horned dung beetles and its contributions to innovation, adaptation, and resilience

“…Microbes have long been hypothesized to play a critical role in enabling both juvenile and adult Onthophagus to subsist and diversify upon dung, which is primarily composed of complex polysaccharides such as cellulose and relatively low in amino acids (Flachowsky & Hennig, 1990;Frank, Brückner, Hilpert, Heethoff, & Blüthgen, 2017;Halffter & Edmonds, 1982;Holter, 2016;Muller, 1980). Recent work on O. taurus and the closely related genus Euoniticellus now shows that pedestal microbiota are enriched for genes implicated in cellulose degradation and nitrogen fixation (Estes et al, 2013;Shukla, Sanders, Byrne, & Pierce, 2016). Additional experimental support for this hypothesis derives from the demonstration that Onthophagus larvae forced to develop without their pedestal microbiota require more time to complete development and metamorphose into smaller adults compared to larvae that are provided with their pedestal microbes.…”