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Stress response, gut microbial diversity and sexual signals correlate with social interactions.

ABSTRACT: Theory predicts that social interactions are dynamically linked to phenotype. Yet because social interactions are difficult to quantify, little is known about the precise details on how interactivity is linked to phenotype. Here, we deployed proximity loggers on North American barn swallows (Hirundo rustica erythrogaster) to examine intercorrelations among social interactions, morphology and features of the phenotype that are sensitive to the social context: stress-induced corticosterone (CORT) and gut microbial diversity. We analysed relationships at two spatial scales of interaction: (i) body contact and (ii) social interactions occurring between 0.1 and 5 m. Network analysis revealed that relationships between social interactions, morphology, CORT and gut microbial diversity varied depending on the sexes of the individuals interacting and the spatial scale of interaction proximity. We found evidence that body contact interactions were related to diversity of socially transmitted microbes and that looser social interactions were related to signalling traits and CORT.

SUBMITTER: Levin II

PROVIDER: S-EPMC4938059 | biostudies-literature | 2016 Jun

REPOSITORIES: biostudies-literature

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Stress response, gut microbial diversity and sexual signals correlate with social interactions.

Levin Iris I II Zonana David M DM Fosdick Bailey K BK Song Se Jin SJ Knight Rob R Safran Rebecca J RJ

Biology letters 20160601 6

Theory predicts that social interactions are dynamically linked to phenotype. Yet because social interactions are difficult to quantify, little is known about the precise details on how interactivity is linked to phenotype. Here, we deployed proximity loggers on North American barn swallows (Hirundo rustica erythrogaster) to examine intercorrelations among social interactions, morphology and features of the phenotype that are sensitive to the social context: stress-induced corticosterone (CORT) ...[more]

PMID: 27354713

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Project description:BackgroundThe human gut contains approximately 1014 bacteria, belonging to hundreds of different species. Together, these microbial species form a complex food web that can break down nutrient sources that our own digestive enzymes cannot handle, including complex polysaccharides, producing short chain fatty acids and additional metabolites, e.g., vitamin K. Microbial diversity is important for colonic health: Changes in the composition of the microbiota have been associated with inflammatory bowel disease, diabetes, obesity and Crohn's disease, and make the microbiota more vulnerable to infestation by harmful species, e.g., Clostridium difficile. To get a grip on the controlling factors of microbial diversity in the gut, we here propose a multi-scale, spatiotemporal dynamic flux-balance analysis model to study the emergence of metabolic diversity in a spatial gut-like, tubular environment. The model features genome-scale metabolic models (GEM) of microbial populations, resource sharing via extracellular metabolites, and spatial population dynamics and evolution.ResultsIn this model, cross-feeding interactions emerge readily, despite the species' ability to metabolize sugars autonomously. Interestingly, the community requires cross-feeding for producing a realistic set of short-chain fatty acids from an input of glucose, If we let the composition of the microbial subpopulations change during invasion of adjacent space, a complex and stratified microbiota evolves, with subspecies specializing on cross-feeding interactions via a mechanism of compensated trait loss. The microbial diversity and stratification collapse if the flux through the gut is enhanced to mimic diarrhea.ConclusionsIn conclusion, this in silico model is a helpful tool in systems biology to predict and explain the controlling factors of microbial diversity in the gut. It can be extended to include, e.g., complex nutrient sources, and host-microbiota interactions via the intestinal wall.

Project description:Reciprocity plays a key role maintaining cooperation in society. However, little is known about the neural process that underpins human reciprocity during social interactions. Our neuroimaging study manipulated partner identity (computer, human) and strategy (random, tit-for-tat) in repeated prisoner's dilemma games and investigated the neural correlate of reciprocal interaction with humans. Reciprocal cooperation with humans but exploitation of computers by defection was associated with activation in the left amygdala. Amygdala activation was also positively and negatively correlated with a preference change for human partners following tit-for-tat and random strategies, respectively. The correlated activation represented the intensity of positive feeling toward reciprocal and negative feeling toward non-reciprocal partners, and so reflected reciprocity in social interaction. Reciprocity in social interaction, however, might plausibly be misinterpreted and so we also examined the neural coding of insight into the reciprocity of partners. Those with and without insight revealed differential brain activation across the reward-related circuitry (i.e., the right middle dorsolateral prefrontal cortex and dorsal caudate) and theory of mind (ToM) regions [i.e., ventromedial prefrontal cortex (VMPFC) and precuneus]. Among differential activations, activation in the precuneus, which accompanied deactivation of the VMPFC, was specific to those without insight into human partners who were engaged in a tit-for-tat strategy. This asymmetric (de)activation might involve specific contributions of ToM regions to the human search for reciprocity. Consequently, the intensity of emotion attached to human reciprocity was represented in the amygdala, whereas insight into the reciprocity of others was reflected in activation across the reward-related and ToM regions. This suggests the critical role of mentalizing, which was not equated with reward expectation during social interactions.

Project description:BACKGROUND:The gut microbiome can influence life history traits associated with host fitness such as fecundity and longevity. In most organisms, these two life history traits are traded-off, while they are positively linked in social insects. In ants, highly fecund queens can live for decades, while their non-reproducing workers exhibit much shorter lifespans. Yet, when fertility is induced in workers by death or removal of the queen, worker lifespan can increase. It is unclear how this positive link between fecundity and longevity is achieved and what role the gut microbiome and the immune system play in this. To gain insights into the molecular regulation of lifespan in social insects, we investigated fat body gene expression and gut microbiome composition in workers of the ant Temnothorax rugatulus in response to an experimental induction of fertility and an immune challenge. RESULTS:Fertile workers upregulated several molecular repair mechanisms, which could explain their extended lifespan. The immune challenge altered the expression of several thousand genes in the fat body, including many immune genes, and, interestingly, this transcriptomic response depended on worker fertility. For example, only fertile, immune-challenged workers upregulated genes involved in the synthesis of alpha-ketoglutarate, an immune system regulator, which extends the lifespan in Caenorhabditis elegans by down-regulating the TOR pathway and reducing oxidant production. Additionally, we observed a dramatic loss in bacterial diversity in the guts of the ants within a day of the immune challenge. Yet, bacterial density did not change, so that the gut microbiomes of many immune challenged workers consisted of only a single or a few bacterial strains. Moreover, the expression of immune genes was linked to the gut microbiome composition, suggesting that the ant host can regulate the microbiome in its gut. CONCLUSIONS:Immune system flare-ups can have negative consequence on gut microbiome diversity, pointing to a previously underrated cost of immunity. Moreover, our results provide important insights into shifts in the molecular regulation of fertility and longevity associated with insect sociality.

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Stress response, gut microbial diversity and sexual signals correlate with social interactions.

Publications

Stress response, gut microbial diversity and sexual signals correlate with social interactions.

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