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

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.

[1]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[2]  Steven D. Prager,et al.  The dynamics of animal social networks: analytical, conceptual, and theoretical advances , 2014 .

[3]  R. Safran,et al.  Signaling stress? An analysis of phaeomelanin-based plumage color and individual corticosterone levels at two temporal scales in North American barn swallows, Hirundo rustica erythrogaster , 2013, Hormones and Behavior.

[4]  R. Boonstra,et al.  Stress and the microbiome: linking glucocorticoids to bacterial community dynamics in wild red squirrels , 2016, Biology Letters.

[5]  J. Tung,et al.  Social behavior and the microbiome , 2015, Current Opinion in Behavioral Sciences.

[6]  David M. Zonana,et al.  An integrative view of the signaling phenotype: Dynamic links between signals, physiology, behavior and social context , 2014 .

[7]  J. Adelman,et al.  Sexual signal exaggeration affects physiological state in male barn swallows , 2008, Current Biology.

[8]  Michael L. Wilson,et al.  Social behavior shapes the chimpanzee pan-microbiome , 2016, Science Advances.

[9]  R. Safran,et al.  Plumage coloration, not length or symmetry of tail-streamers, is a sexually selected trait in North American barn swallows , 2004 .

[10]  P. Sharp,et al.  Endocrine phenotype, reproductive success and survival in the great tit, Parus major , 2013, Journal of evolutionary biology.

[11]  Richard James,et al.  Calibrating animal‐borne proximity loggers , 2015, Methods in ecology and evolution.

[12]  Jenny Tung,et al.  Social networks predict gut microbiome composition in wild baboons , 2015, eLife.

[13]  William A. Walters,et al.  Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms , 2012, The ISME Journal.

[14]  Se Jin Song,et al.  Cohabiting family members share microbiota with one another and with their dogs , 2013, eLife.

[15]  S. Dowd,et al.  Exposure to a social stressor alters the structure of the intestinal microbiota: Implications for stressor-induced immunomodulation , 2011, Brain, Behavior, and Immunity.

[16]  Rupert G. Miller The jackknife-a review , 1974 .

[17]  H. Fritz,et al.  Linear social dominance hierarchy and corticosterone responses in male mallards and pintails , 2005, Hormones and Behavior.

[18]  Iris I. Levin,et al.  Performance of Encounternet Tags: Field Tests of Miniaturized Proximity Loggers for Use on Small Birds , 2015, PloS one.

[19]  M. Keeling,et al.  Networks and epidemic models , 2005, Journal of The Royal Society Interface.

[20]  E. Tibbetts The evolution of honest communication: integrating social and physiological costs of ornamentation. , 2014, Integrative and comparative biology.

[21]  R. Safran,et al.  Patterns and ecological predictors of age-related performance in female North American barn swallows, Hirundo rustica erythrogaster , 2014, Behavioral Ecology and Sociobiology.

[22]  S. Kulkarni,et al.  Social and sexual behaviours aid transmission of bacteria in birds , 2007, Behavioural Processes.

[23]  I. Lovette,et al.  Dynamic Paternity Allocation as a Function of Male Plumage Color in Barn Swallows , 2005, Science.

[24]  Damien R. Farine,et al.  Developmental stress predicts social network position , 2014, Biology Letters.