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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.

SUBMITTER: Duarte A

PROVIDER: S-EPMC5836980 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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Strategies for managing rival bacterial communities: Lessons from burying beetles.

Duarte Ana A Welch Martin M Swannack Chris C Wagner Josef J Kilner Rebecca M RM

The Journal of animal ecology 20170821 2

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 ...[more]

PMID: 28682460

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Project description:Closely related species with overlapping geographic ranges encounter a significant challenge: they share many ecological traits and preferences but must partition resources to coexist. In Ontario, potentially eleven species of carrion beetles (Coleoptera: Silphidae) live together and require vertebrate carrion for reproduction. Their reliance on an ephemeral and uncommon resource that is unpredictable in space and time is thought to create intense intra- and interspecific competition. Evidence suggests that burying beetle species reduce competition by partitioning carrion for breeding across different habitats, temperatures, and seasons. Here, we test predictions of an alternative axis for partitioning carrion: vertical partitioning between the ground and forest canopy. We conducted a survey of carrion beetles from May to July 2016 at the Queen's University Biological Station across 50 randomly generated points using baited lethal traps at zero and six metres. Ground traps yielded more species and individuals compared to those in the canopy, and the number of individuals and species caught increased through the season in both trap types. Ground and canopy traps were accurately distinguished by the presence or absence of three species: ground traps contained more Nicrophorus orbicollis and Necrophila americana, while canopy traps contained more Nicrophorus pustulatus. We trapped 253 N. pustulatus in the canopy, but only 60 on the ground. N. pustulatus is thought to be rare across its geographic range, but our results suggest it is uniquely common in canopy habitats, demonstrating a vertical partitioning of habitat and resources. Our results are consistent with N. pustulatus having diverged into canopy habitats as a strategy to coexist with closely related sympatric species when competing for similar resources. We still, however, do not know the traits that allow N. pustulatus to flourish in the canopy, exactly how N. pustulatus uses canopy resources for breeding, or the factors that restrict the expansion of other burying beetles into this habitat.

Project description:BackgroundIn species with parental care, there is striking variation in offspring dependence at birth, ranging from feeding independence to complete dependency on parents for nutrition. Frequently, highly dependent offspring further evolve reductions or alterations of morphological traits that would otherwise promote self-sufficiency. Here, we examine evidence for morphological evolution associated with dependence in burying beetles (Nicrophorus spp.), in which dependence upon parents appears to have several independent origins. In many species, precocial first instar larvae can survive without parenting, but several altricial species die at this stage on their own. We focused specifically on the mandibles, which are expected to be related to feeding ability and therefore independence from parents.ResultsWe find no evidence that the size of the mandible is related to dependence on parents. However, we do find a developmental and phylogenetic correlation between independence and the presence of serrations on the inner edge of the mandible. Mandibles of independent species bear serrations at hatching, whereas dependent species hatch with smooth mandibles, only developing serrations in the second instar when these larvae gain the ability to survive on their own. Phylogenetic evidence suggests that serrations coincide with independence repeatedly. We note a single exception to this trend, a beetle with a serrated mandible that cannot survive without parents. However, this exception occurs in a species that has recently evolved the loss of independence.ConclusionsWe argue that the absence of mandible serrations occurs due to alternative selection pressures incurred in larvae dependent upon parents to survive. We suggest that this may have led to a variable function for mandibles, perhaps related to increased competitive ability among siblings or increased efficiency in receiving nutrition from parents. Furthermore, we propose that the phylogenetic pattern we see is consistent with the long-held evolutionary hypothesis that evolutionary change in behavior and physiology precede morphological change.

Project description:Asymmetric interference competition, where one species is behaviorally dominant over another, appears widespread in nature with the potential to structure ecological communities through trade-offs between competitive dominance and environmental tolerance. The details of how species interact and the factors that contribute to behavioral dominance, however, are poorly known for most species, yet such details are important for understanding when and why trade-offs occur. Here, we examine behavioral interactions between two species of burying beetles (Coleoptera: Silphidae) that compete for limited breeding resources (i.e., small vertebrate carcasses) in nature, to identify behaviors involved in interference competition and to test if large body size, species identity, or time of arrival best predict behavioral dominance among species. To test these ideas, we placed same-sex individuals of Nicrophorus orbicollis (early to mid-summer breeder) and N. tomentosus (late summer to fall breeder) into an enclosure together with a 25-30 g mouse carcass (Mus musculus). We then video-recorded all behaviors, including neutral and aggressive interactions, for 13 h per trial (N = 14 trials). For each interaction, we assigned a winner based on which beetle retained its position instead of fleeing or retained possession of the carcass; the overall behavioral dominant was determined as the individual that won the most interactions over the length of the trial. We found that large body size was the best predictor of behavioral dominance. In most interactions, N. orbicollis was larger and dominant over N. tomentosus; however, when N. tomentosus was larger they outcompeted smaller N. orbicollis, illustrating the importance of body size in aggressive contests. The order of arrival to the carcass (priority effects) did not predict behavioral dominance. The larger size and abundance of N. orbicollis in nature suggest a competitive asymmetry between the species, supporting the idea that N. orbicollis constrains the ability of N. tomentosus to breed earlier in the summer.

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Strategies for managing rival bacterial communities: Lessons from burying beetles.

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Strategies for managing rival bacterial communities: Lessons from burying beetles.

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