Strategies for managing rival bacterial communities: Lessons from burying beetles

Abstract

The role of bacteria in animal development, ecology and evolution is increasingly well understood, yet little is known of how animal behaviour affects bacterial communities. Animals that benefit from defending a key resource from microbial competitors are likely to evolve behaviours to control or manipulate the animal's associated external microbiota.We describe four possible mechanisms by which animals could gain a competitive edge by disrupting a rival bacterial community: “weeding,” “seeding,” “replanting” and “preserving.” By combining detailed behavioural observations with molecular and bioinformatic analyses, we then test which of these mechanisms best explains how burying beetles, Nicrophorus vespilloides, manipulate the bacterial communities on their carcass breeding resource.Burying beetles are a suitable species to study how animals manage external microbiota because reproduction revolves around a small vertebrate carcass. Parents shave a carcass and apply antimicrobial exudates on its surface, shaping it into an edible nest for their offspring. We compared bacterial communities in mice carcasses that were either fresh, prepared by beetles or unprepared but buried underground for the same length of time. We also analysed bacterial communities in the burying beetle's gut, during and after breeding, to understand whether beetles could be “seeding” the carcass with particular microbes.We show that burying beetles do not “preserve” the carcass by reducing bacterial load, as is commonly supposed. Instead, our results suggest they “seed” the carcass with bacterial groups which are part of the Nicrophorus core microbiome. They may also “replant” other bacteria from the carcass gut onto the surface of their carrion nest. Both these processes may lead to the observed increase in bacterial load on the carcass surface in the presence of beetles. Beetles may also “weed” the bacterial community by eliminating some groups of bacteria on the carcass, perhaps through the production of antimicrobials themselves.Whether these alterations to the bacterial community are adaptive from the beetle's perspective, or are simply a by‐product of the way in which the beetles prepare the carcass for reproduction, remains to be determined in future work. In general, our work suggests that animals might use more sophisticated techniques for attacking and disrupting rival microbial communities than is currently appreciated.

Phoretic Poecilochirus mites specialize on their burying beetle hosts

“…However, the beetles in our experiments were nematode‐free so that any influence of nematode variation on our results is unlikely. Finally, the beetles manipulate the microbiota growing on the carcass (Arce et al, ; Cotter & Kilner, ; Duarte et al, ; Vogel et al., ). If microbiotic communities caused by different beetle species would differ, the two mite species may have evolved different strategies to deal with them.…”

“…The effects need not necessarily be caused directly by the mites themselves, but may result from third parties. If the mites carried specific microbes, for example, beetle anal secretions may be specifically targeted at these (Cotter & Kilner, ; Duarte et al., ). In any case, the potential for beetle adaptations to mites deserves to be studied with specifically designed experiments.…”

Gut microbiota in the burying beetle, Nicrophorus vespilloides, provide colonization resistance against larval bacterial pathogens

“…Parents protect larvae and provide nutrition in the form of regurgitated food (Eggert et al., ). In addition, they transfer their gut microbiome to larvae by direct feeding and via contamination of the carcass surface (Duarte et al., ; Shukla et al., ; Wang & Rozen, ). The present results indicate that larvae benefit directly from the acquisition of these bacteria (Figures and b) and suggest that two of the key members of the N. vespilloides microbiome are mutualists.…”

“…The present results indicate that larvae benefit directly from the acquisition of these bacteria (Figures and b) and suggest that two of the key members of the N. vespilloides microbiome are mutualists. Thus, while Nicrophorus adults ensure transmission of these and other species (Duarte et al., ; Vogel et al., ) from generation to generation, the bacteria provide direct benefits to beetles within the highly contaminated carcass environment (Vogel et al., ). It remains possible that other advantages exist, for example, improved nutrient acquisition (Wilkinson, Koga, & Fukatsu, ) or changes in the composition of the decomposer microbial community on the carcass (Duarte et al., ), but as yet these possibilities have not been measured.…”

“…Thus, while Nicrophorus adults ensure transmission of these and other species (Duarte et al., ; Vogel et al., ) from generation to generation, the bacteria provide direct benefits to beetles within the highly contaminated carcass environment (Vogel et al., ). It remains possible that other advantages exist, for example, improved nutrient acquisition (Wilkinson, Koga, & Fukatsu, ) or changes in the composition of the decomposer microbial community on the carcass (Duarte et al., ), but as yet these possibilities have not been measured. In addition, it is important to note that parents may transmit other factors, besides microbes, to offspring during development that may directly or indirectly affect their parental abilities.…”