Glucocorticoids coordinate changes in gut microbiome composition in wild North American red squirrels
Ley, R. E. et al. Evolution of mammals and their gut microbes. Science 320, 1647–1651 (2008).ADS
CAS
PubMed
PubMed Central
Google Scholar
Thaiss, C. A., Zmora, N., Levy, M. & Elinav, E. The microbiome and innate immunity. Nature 535, 65–74 (2016).ADS
CAS
PubMed
Google Scholar
Ezenwa, V. O., Gerardo, N. M., Inouye, D. W., Medina, M. & Xavier, J. B. Microbiology. Animal behavior and the microbiome. Science 338, 198–199 (2012).ADS
CAS
PubMed
PubMed Central
Google Scholar
Sampson, T. R. & Mazmanian, S. K. Control of brain development, function, and behavior by the microbiome. Cell Host Microbe. 17, 565–576 (2015).CAS
PubMed
PubMed Central
Google Scholar
Voigt, R. M., Forsyth, C. B., Green, S. J., Engen, P. A. & Keshavarzian, A. Circadian rhythm and the gut microbiome. Int. Rev. Neurobiol. 131, 193–205 (2016).CAS
PubMed
Google Scholar
Backhed, F. Programming of host metabolism by the gut microbiota. Endocr. Abstr. https://doi.org/10.1530/endoabs.32.s20.2 (2013).Article
Google Scholar
Mallott, E. K., Borries, C., Koenig, A., Amato, K. R. & Lu, A. Reproductive hormones mediate changes in the gut microbiome during pregnancy and lactation in Phayre’s leaf monkeys. Sci. Rep. 10, 9961 (2020).ADS
CAS
PubMed
PubMed Central
Google Scholar
Miller, E. A., Livermore, J. A., Alberts, S. C., Tung, J. & Archie, E. A. Ovarian cycling and reproductive state shape the vaginal microbiota in wild baboons. Microbiome. 5, 8 (2017).PubMed
PubMed Central
Google Scholar
Gomez-Arango, L. F. et al. Connections between the gut microbiome and metabolic hormones in early pregnancy in overweight and obese women. Diabetes 65, 2214–2223 (2016).CAS
PubMed
Google Scholar
Shin, J.-H. et al. Serum level of sex steroid hormone is associated with diversity and profiles of human gut microbiome. Res. Microbiol. 170, 192–201 (2019).CAS
PubMed
Google Scholar
Burokas, A., Moloney, R. D., Dinan, T. G. & Cryan, J. F. Microbiota regulation of the mammalian gut–brain axis. Adv. Appl. Microbiol. 91, 1–62. (2015).Sudo, N. The hypothalamic–pituitary–adrenal axis and gut microbiota. Gut–Brain Axis. https://doi.org/10.1016/b978-0-12-802304-4.00013-x (2016).Article
Google Scholar
Sapolsky, R. M., Romero, L. M. & Munck, A. U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 21, 55–89 (2000).CAS
PubMed
Google Scholar
Hau, M., Casagrande, S., Ouyang, J. Q. & Baugh, A. T. Glucocorticoid-mediated phenotypes in vertebrates: Multilevel variation and evolution. Adv. Stud. Behav. 48, 41–115 (2016).
Google Scholar
Sprague, R. S. & Breuner, C. W. Timing of fledging is influenced by glucocorticoid physiology in Laysan Albatross chicks. Horm. Behav. 58, 297–305 (2010).CAS
PubMed
Google Scholar
Fletcher, Q. E., Dantzer, B. & Boonstra, R. The impact of reproduction on the stress axis of free-living male northern red backed voles (Myodes rutilus). Gen. Comp. Endocrinol. 224, 136–147 (2015).CAS
PubMed
Google Scholar
Romero, L. M. & Wikelski, M. Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Nino events. Proc. Natl. Acad. Sci. USA. 98, 7366–7370 (2001).ADS
CAS
PubMed
PubMed Central
Google Scholar
Chevalier, C. et al. Gut microbiota orchestrates energy homeostasis during cold. Cell 163, 1360–1374 (2015).CAS
PubMed
Google Scholar
Amato, K. R. et al. Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME J. 7, 1344–1353 (2013).CAS
PubMed
PubMed Central
Google Scholar
Baniel, A. et al. Seasonal shifts in the gut microbiome indicate plastic responses to diet in wild geladas. Microbiome. 9, 26 (2021).PubMed
PubMed Central
Google Scholar
Kohl, K. D., Amaya, J., Passement, C. A., Dearing, M. D. & McCue, M. D. Unique and shared responses of the gut microbiota to prolonged fasting: A comparative study across five classes of vertebrate hosts. FEMS Microbiol. Ecol. 90, 883–894 (2014).CAS
PubMed
Google Scholar
Stecher, B. et al. Like will to like: Abundances of closely related species can predict susceptibility to intestinal colonization by pathogenic and commensal bacteria. PLoS Pathog. https://doi.org/10.1371/journal.ppat.1000711 (2010).Article
PubMed
PubMed Central
Google Scholar
Das, B. & Nair, G. B. Homeostasis and dysbiosis of the gut microbiome in health and disease. J. Biosci. 44(5), 1–8 (2019). https://www.ncbi.nlm.nih.gov/pubmed/31719226.CAS
Google Scholar
Noguera, J. C., Aira, M., Pérez-Losada, M., Domínguez, J. & Velando, A. Glucocorticoids modulate gastrointestinal microbiome in a wild bird. R. Soc. Open Sci. https://doi.org/10.1098/rsos.171743 (2018).Article
PubMed
PubMed Central
Google Scholar
UrenWebster, T. M., Rodriguez-Barreto, D., Consuegra, S. & GarciadeLeaniz, C. Cortisol-related signatures of stress in the fish microbiome. Front. Microbiol. 11, 1621 (2020).
Google Scholar
Stothart, M. R., Palme, R. & Newman, A. E. M. It’s what’s on the inside that counts: stress physiology and the bacterial microbiome of a wild urban mammal. Proc. Biol. Sci. 286, 20192111 (2019).PubMed
PubMed Central
Google Scholar
Vlčková, K. et al. Impact of stress on the gut microbiome of free-ranging western lowland gorillas. Microbiology 164, 40–44 (2018).PubMed
Google Scholar
Dantzer, B. et al. Density triggers maternal hormones that increase adaptive offspring growth in a wild mammal. Science 340, 1215–1217 (2013).ADS
CAS
PubMed
Google Scholar
Sarkar, A. et al. Microbial transmission in animal social networks and the social microbiome. Nat. Ecol. Evol. 4, 1020–1035 (2020).PubMed
Google Scholar
Kruuk, L. E. B., Merilä, J. & Sheldon, B. C. When environmental variation short-circuits natural selection. Trends Ecol. Evol. 18, 207–209 (2003).
Google Scholar
Stinchcombe, J. R. et al. Testing for environmentally induced bias in phenotypic estimates of natural selection: Theory and practice. Am. Nat. 160, 511–523 (2002).PubMed
Google Scholar
Rausher, M. D. The measurement of selection on quantitative traits: Biases due to environmental covariances between traits and fitness. Evolution 46, 616–626 (1992).PubMed
Google Scholar
Lamontagne, J. M. & Boutin, S. Local-scale synchrony and variability in mast seed production patterns of Picea glauca. J. Ecol. https://doi.org/10.1111/j.1365-2745.2007.01266.x (2007).Article
Google Scholar
Fletcher, Q. E. et al. Reproductive timing and reliance on hoarded capital resources by lactating red squirrels. Oecologia https://doi.org/10.1007/s00442-013-2699-3 (2013).Article
PubMed
Google Scholar
Fletcher, Q. E. et al. The functional response of a hoarding seed predator to mast seeding. Ecology 91, 2673–2683 (2010).PubMed
Google Scholar
Boutin, S. et al. Anticipatory reproduction and population growth in seed predators. Science 314, 1928–1930 (2006).ADS
CAS
PubMed
Google Scholar
Haines, J. A. et al. Sexually selected infanticide by male red squirrels in advance of a mast year. Ecology 99, 1242–1244 (2018).PubMed
Google Scholar
Dantzer, B., McAdam, A. G., Humphries, M. M., Lane, J. E. & Boutin, S. Decoupling the effects of food and density on life-history plasticity of wild animals using field experiments: Insights from the steward who sits in the shadow of its tail, the North American red squirrel. J. Anim. Ecol. 89, 2397–2414 (2020).PubMed
Google Scholar
Hestbeck, J. B. A Mathematical Model of Population Regulation in Cyclic Mammals. Population Biology 290–297 (Springer, 1983).
Google Scholar
Dantzer, B., Boutin, S., Humphries, M. M. & McAdam, A. G. Behavioral responses of territorial red squirrels to natural and experimental variation in population density. Behav. Ecol. Sociobiol. 66, 865–878 (2012).
Google Scholar
Siracusa, E. et al. Familiarity with neighbours affects intrusion risk in territorial red squirrels. Anim. Behav. 133, 11–20 (2017).
Google Scholar
Guindre-Parker, S. et al. Individual variation in phenotypic plasticity of the stress axis. Biol. Lett. 15, 20190260 (2019).PubMed
PubMed Central
Google Scholar
Laughlin, D. & Grace, J. Discoveries and novel insights in ecology using structural equation modeling. Ideas Ecol. Evol. https://doi.org/10.24908/iee.2019.12.5.c (2019).Article
Google Scholar
Pugesek, B. H., Tomer, A. & von Eye, A. Structural Equation Modeling: Applications in Ecological and Evolutionary Biology (Cambridge University Press, 2003).MATH
Google Scholar
Pearl, J. The causal foundations of structural equation modeling. (2012). https://doi.org/10.21236/ada557445Leftwich, P. T., Clarke, N. V. E., Hutchings, M. I. & Chapman, T. Gut microbiomes and reproductive isolation in Drosophila. Proc. Natl. Acad. Sci. USA. 114, 12767–12772 (2017).CAS
PubMed
PubMed Central
Google Scholar
Markle, J. G. M. et al. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 339, 1084–1088 (2013).ADS
CAS
PubMed
PubMed Central
Google Scholar
Reveles, K. R., Patel, S., Forney, L. & Ross, C. N. Age-related changes in the marmoset gut microbiome. Am. J. Primatol. https://doi.org/10.1002/ajp.22960 (2019).Article
PubMed
PubMed Central
Google Scholar
Dantzer, B. et al. Fecal cortisol metabolite levels in free-ranging North American red squirrels: Assay validation and the effects of reproductive condition. Gen. Comp. Endocrinol. 167, 279–286 (2010).CAS
PubMed
Google Scholar
Fletcher, Q. E. et al. Seasonal stage differences overwhelm environmental and individual factors as determinants of energy expenditure in free-ranging red squirrels. Funct. Ecol. https://doi.org/10.1111/j.1365-2435.2012.01975.x (2012).Article
Google Scholar
Lane, J. E., Boutin, S., Gunn, M. R., Slate, J. & Coltman, D. W. Female multiple mating and paternity in free-ranging North American red squirrels. Anim. Behav. 75, 1927–1937 (2008).
Google Scholar
Ren, T. et al. Seasonal, spatial, and maternal effects on gut microbiome in wild red squirrels. Microbiome. 5, 163 (2017).PubMed
PubMed Central
Google Scholar
Backhans, A., Fellström, C. & Lambertz, S. T. Occurrence of pathogenic Yersinia enterocolitica and Yersinia pseudotuberculosis in small wild rodents. Epidemiol. Infect. 139, 1230–1238 (2011).CAS
PubMed
Google Scholar
Bižanov, G. & Dobrokhotova, N. D. Experimental infection of ground squirrels (Citellus pygmaeus Pallas) with Yersinia pestis during hibernation. J. Infect. 54, 198–203 (2007).PubMed
Google Scholar
Stothart, M. R. et al. Stress and the microbiome: Linking glucocorticoids to bacterial community dynamics in wild red squirrels. Biol. Lett. 12, 20150875 (2016).PubMed
PubMed Central
Google Scholar
Costello, E. K., Stagaman, K., Dethlefsen, L., Bohannan, B. J. M. & Relman, D. A. The application of ecological theory toward an understanding of the human microbiome. Science 336, 1255–1262 (2012).ADS
CAS
PubMed
PubMed Central
Google Scholar
Rocca, J. D., Simonin, M., Bernhardt, E. S., Washburne, A. D. & Wright, J. P. Rare microbial taxa emerge when communities collide: Freshwater and marine microbiome responses to experimental mixing. Ecology https://doi.org/10.1002/ecy.2956 (2020).Article
PubMed
Google Scholar
Shade, A. et al. Conditionally rare taxa disproportionately contribute to temporal changes in microbial diversity. MBio https://doi.org/10.1128/mbio.01371-14 (2014).Article
PubMed
PubMed Central
Google Scholar
Dinan, T. G. & Cryan, J. F. The microbiome–gut–brain axis in health and disease. Gastroenterol. Clin. N. Am. 46, 77–89 (2017).
Google Scholar
Claus, S. P. et al. Colonization-induced host–gut microbial metabolic interaction. MBio 2, e00271-e310 (2011).PubMed
PubMed Central
Google Scholar
Bangsgaard Bendtsen, K. M. et al. Gut microbiota composition is correlated to grid floor induced stress and behavior in the BALB/c mouse. PLoS ONE 7, e46231 (2012).ADS
PubMed
PubMed Central
Google Scholar
Amato, K. R. et al. The gut microbiota appears to compensate for seasonal diet variation in the wild black howler monkey (Alouatta pigra). Microb. Ecol. 69, 434–443 (2015).CAS
PubMed
Google Scholar
McLaren, M. R. & Callahan, B. J. Pathogen resistance may be the principal evolutionary advantage provided by the microbiome. Philos. Trans. R Soc. Lond. B Biol. Sci. 375, 20190592 (2020).PubMed
PubMed Central
Google Scholar
Donohoe, D. R. et al. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metab. 13, 517–526 (2011).CAS
PubMed
PubMed Central
Google Scholar
Rivera-Chávez, F. et al. Depletion of butyrate-producing clostridia from the gut microbiota drives an aerobic luminal expansion of salmonella. Cell Host Microbe. 19, 443–454 (2016).PubMed
PubMed Central
Google Scholar
Meerburg, B. G. & Kijlstra, A. Role of rodents in transmission of Salmonella and Campylobacter. J. Sci. Food Agric. https://doi.org/10.1002/jsfa.3004 (2007).Article
Google Scholar
Jalal, M. S. et al. Antibiotic resistant zoonotic bacteria in Irrawaddy squirrel (Callosciurus pygerythrus). Vet. Med. Sci. 5, 260–268 (2019).CAS
PubMed
Google Scholar
Petrosus, E., Silva, E. B., Lay, D. Jr. & Eicher, S. D. Effects of orally administered cortisol and norepinephrine on weanling piglet gut microbial populations and Salmonella passage. J. Anim. Sci. 96, 4543–4551 (2018).PubMed
PubMed Central
Google Scholar
Lefcheck, J. S. piecewiseSEM: Piecewise structural equation modelling in r for ecology, evolution, and systematics. Methods Ecol. Evol. https://doi.org/10.1111/2041-210X.12512 (2016).Article
Google Scholar
Raulo, A. et al. Social networks strongly predict the gut microbiota of wild mice. ISME J. https://doi.org/10.1038/s41396-021-00949-3 (2021).Article
PubMed
PubMed Central
Google Scholar
Phillips, C. D. et al. Microbiome structural and functional interactions across host dietary niche space. Integr. Comp. Biol. 57, 743–755 (2017).CAS
PubMed
Google Scholar
Galley, J. D. et al. Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota. BMC Microbiol. 14, 189 (2014).PubMed
PubMed Central
Google Scholar
Wu, C.-S. et al. Age-dependent remodeling of gut microbiome and host serum metabolome in mice. Aging 13, 6330–6345 (2021).CAS
PubMed
PubMed Central
Google Scholar
Altmann, J., Gesquiere, L., Galbany, J., Onyango, P. O. & Alberts, S. C. Life history context of reproductive aging in a wild primate model. Ann. NY Acad. Sci. https://doi.org/10.1111/j.1749-6632.2010.05531.x (2010).Article
PubMed
Google Scholar
Sylvia, K. E., Jewell, C. P., Rendon, N. M., St John, E. A. & Demas, G. E. Sex-specific modulation of the gut microbiome and behavior in Siberian hamsters. Brain Behav. Immun. 60, 51–62 (2017).PubMed
Google Scholar
Grieneisen, L. E., Livermore, J., Alberts, S., Tung, J. & Archie, E. A. Group living and male dispersal predict the core gut microbiome in wild baboons. Integr. Comp. Biol. 57, 770–785 (2017).PubMed
PubMed Central
Google Scholar
Peckett, A. J., Wright, D. C. & Riddell, M. C. The effects of glucocorticoids on adipose tissue lipid metabolism. Metabolism 60, 1500–1510 (2011).CAS
PubMed
Google Scholar
Wu, T. et al. Chronic glucocorticoid treatment induced circadian clock disorder leads to lipid metabolism and gut microbiota alterations in rats. Life Sci. 192, 173–182 (2018).CAS
PubMed
Google Scholar
Deaver, J. A., Eum, S. Y. & Toborek, M. Circadian disruption changes gut microbiome taxa and functional gene composition. Front. Microbiol. 9, 737 (2018).PubMed
PubMed Central
Google Scholar
Schroeder, B. O. Fight them or feed them: How the intestinal mucus layer manages the gut microbiota. Gastroenterol. Rep. 7, 3–12 (2019).
Google Scholar
Huang, E. Y. et al. Using corticosteroids to reshape the gut microbiome: Implications for inflammatory bowel diseases. Inflamm. Bowel Dis. 21, 963–972 (2015).PubMed
Google Scholar
Carabotti, M., Scirocco, A., Maselli, M. A. & Severi, C. The gut–brain axis: Interactions between enteric microbiota, central and enteric nervous systems. Ann. Gastroenterol. Hepatol. 28, 203–209 (2015).
Google Scholar
de Weerth, C. Do bacteria shape our development? Crosstalk between intestinal microbiota and HPA axis. Neurosci. Biobehav. Rev. 83, 458–471 (2017).PubMed
Google Scholar
Luo, Y. et al. Gut microbiota regulates mouse behaviors through glucocorticoid receptor pathway genes in the hippocampus. Transl. Psychiatry. 8, 187 (2018).PubMed
PubMed Central
Google Scholar
Cryan, J. F. et al. The microbiota–gut–brain axis. Physiol. Rev. 99, 1877–2013 (2019).CAS
PubMed
Google Scholar
McAdam, A. G., Boutin, S., Sykes, A. K. & Humphries, M. M. Life histories of female red squirrels and their contributions to population growth and lifetime fitness. Ecoscience 14, 362–369 (2007).
Google Scholar
Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods. 7, 335–336 (2010).CAS
PubMed
PubMed Central
Google Scholar
Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200 (2011).CAS
PubMed
PubMed Central
Google Scholar
Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).CAS
Google Scholar
Sheriff, M. J., Dantzer, B., Delehanty, B., Palme, R. & Boonstra, R. Measuring stress in wildlife: Techniques for quantifying glucocorticoids. Oecologia 166, 869–887 (2011).ADS
PubMed
Google Scholar
Touma, C., Sachser, N., Möstl, E. & Palme, R. Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. Gen. Comp. Endocrinol. 130, 267–278 (2003).CAS
PubMed
PubMed Central
Google Scholar
Van Kesteren, F. et al. Experimental increases in glucocorticoids alter function of the HPA axis in wild red squirrels without negatively impacting survival and reproduction. Physiol. Biochem. Zool. 92, 445–458 (2019).PubMed
Google Scholar
Paradis, E., Claude, J. & Strimmer, K. APE: Analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004).CAS
PubMed
PubMed Central
Google Scholar
McMurdie, P. J. & Holmes, S. Package, “phyloseq”. Gan. 2, 7 (2013).
Google Scholar
Kembel, S. W. et al. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26, 1463–1464 (2010).CAS
Google Scholar
Zhang, X. & Yi, N. NBZIMM: Negative binomial and zero-inflated mixed models, with application to microbiome/metagenomics data analysis. BMC Bioinform. 21, 488 (2020).CAS
Google Scholar
Jones, S. E. & Lennon, J. T. Dormancy contributes to the maintenance of microbial diversity. Proc. Natl. Acad. Sci. USA. 107, 5881–5886 (2010).ADS
CAS
PubMed
PubMed Central
Google Scholar More