The microbiome is now considered our ‘second genome’ with potentially comparable importance to the genome in determining human health. There is, however, a relatively limited understanding of the broader environmental factors, particularly social conditions, that shape variation in human microbial communities. Fulfilling the promise of microbiome research — particularly the microbiome’s potential for modification — will require collaboration between biologists and social and population scientists. For life scientists, the plasticity and adaptiveness of the microbiome calls for an agenda to understand the sensitivity of the microbiome to broader social environments already known to be powerful predictors of morbidity and mortality. For social and population scientists, attention to the microbiome may help answer nagging questions about the underlying biological mechanisms that link social conditions to health. We outline key substantive and methodological advances that can be made if collaborations between social and population health scientists and life scientists are strategically pursued.
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Clemente, J. C., Ursell, L. K., Parfrey, L. W. & Knight, R. The impact of the gut microbiota on human health: an integrative view. Cell 148, 1258–1270 (2012).
Grice, E. A. & Segre, J. A. The human microbiome: our second genome. Annu. Rev. Genomics Hum. Genet. 13, 151–170 (2012).
Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K. & Knight, R. Diversity, stability and resilience of the human gut microbiota. Nature 489, 220–230 (2012).
Cho, I. & Blaser, M. J. The human microbiome: at the interface of health and disease. Nat. Rev. Genet. 13, 260–270 (2012).
Sender, R., Fuchs, S. & Milo, R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 14, e1002533 (2016).
Foster, J. & Neufeld, K. A. Gut-brain axis: how the microbiome influences anxiety and depression. Int. J. Neuropsychopharmacol. 17, 27–27 (2014).
David, L. A. et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559–563 (2014).
Rothschild, D. et al. Environment dominates over host genetics in shaping human gut microbiota. Nature 555, 210–215 (2018).
Adams, R. I., Bateman, A. C., Bik, H. M. & Meadow, J. F. Microbiota of the indoor environment: a meta-analysis. Microbiome 3, 49 (2015).
Stilling, R. M., Bordenstein, S. R., Dinan, T. G. & Cryan, J. F. Friends with social benefits: host–microbe interactions as a driver of brain evolution and development? Front. Cell Infect. Microbiol. 4, 147 (2014).
Stamper, C. E. et al. The microbiome of the built environment and human behavior: implications for emotional health and well-being in postmodern Western societies. Int. Rev. Neurobiol. 131, 289–323 (2016).
Rook, G. A., Raison, C. L. & Lowry, C. A. Microbial ‘old friends’, immunoregulation and socioeconomic status. Clin. Exp. Immunol. 177, 1–12 (2014).
Finlay, B. B. & Arrietta, M. C. Let Them Eat Dirt: Saving Our Children from an Oversanitized World 304 (Greystone Books, New York, 2016).
McDade, T. W. The ecologies of human immune function. Annu. Rev. Anthropol. 21, 495–521 (2005).
Coe, C. L. & Laudenslager, M. L. Psychosocial influences on immunity, including effects on immune maturation and senescence. Brain Behav. Immun. 21, 1000–1008 (2007).
Fagundes, C. P., Glaser, R. & Kiecolt-Glaser, J. K. Stressful early life experiences and immune dysregulation across the lifespan. Brain Behav. Immun. 27, 8–12 (2013).
Dennis, C. L. Breastfeeding initiation and duration: a 1990–2000 literature review. J. Obstet. Gynecol. Neonatal Nurs. 31, 12–32 (2002).
Dominguez-Bello, M. G. et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl Acad. Sci. USA 107, 11971–11975 (2010).
Mueller, N. T. et al. Prenatal exposure to antibiotics, cesarean section and risk of childhood obesity. Int. J. Obes. 39, 665–670 (2015).
Kramer, M. S., Sequin, L., Lydon, J. & Goulet, L. Socio-economic disparities in pregnancy outcome: why do the poor fare so poorly? Paediatr. Perinat. Epidemiol. 14, 194–210 (2000).
Joseph, K. S., Liston, R. M., Dodds, L., Dahlgren, L. & Allen, A. C. Socioeconomic status and perinatal outcomes in a setting with universal access to essential health care services. CMAJ 177, 583–590 (2007).
van den Berg, G., van Eijsden, M., Vrijkotte, T. G. & Gemke, R. J. Educational inequalities in perinatal outcomes: the mediating effect of smoking and environmental tobacco exposure. PLoS ONE 7, e37002 (2012).
Anstey, E. H., Chen, J., Elam-Evans, L. D. & Perrine, C. G. Racial and geographic differences in breastfeeding — United States, 2011–2015. MMWR Morb. Mortal. Wkly Rep. 66, 723–727 (2017).
Codagnone, M. G. et al. Programming bugs: microbiota and the developmental origins of brain health and disease. Biol. Psychiatry https://doi.org/10.1016/j.biopsych.2018.06.014 (2018).
Blanton, L. V. et al. Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science 351, aad3311 (2016).
Yang, Y. C. et al. Social relationships and physiological determinants of longevity across the human life span. Proc. Natl Acad. Sci. USA 113, 578–583 (2016).
Moeller, A. H. et al. Social behavior shapes the chimpanzee pan-microbiome. Sci. Adv. 2, e1500997 (2016).
Bennett, G. et al. Host age, social group, and habitat type influence the gut microbiota of wild ring-tailed lemurs (Lemur catta). Am. J. Primatol. 78, 883–892 (2016).
Tung, J. et al. Social networks predict gut microbiome composition in wild baboons. Elife 4, e05224 (2015).
Amaral, W. Z. et al. Social influences on Prevotella and the gut microbiome of young monkeys. Psychosom. Med. 79, 888–897 (2017).
Lewin-Epstein, O., Aharonov, R. & Hadany, L. Microbes can help explain the evolution of host altruism. Nat. Commun. 8, 14040 (2017).
Archie, E. A. & Tung, J. Social behavior and the microbiome. Curr. Opin. Behav. Sci. 6, 28–34 (2015).
Johnson, K. V. & Foster, K. R. Why does the microbiome affect behaviour? Nat. Rev. Microbiol. 16, 647–655 (2018).
Lax, S. et al. Longitudinal analysis of microbial interaction between humans and the indoor environment. Science 345, 1048–1052 (2014).
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).
Rostron, B. L., Boies, J. L. & Arias, E. Education reporting and classification on death certificates in the United States. Vital Health Stat. 2, 1–21 (2010).
Perna, L., Thien-Seitz, U., Ladwig, K. H., Meisinger, C. & Mielck, A. Socio-economic differences in life expectancy among persons with diabetes mellitus or myocardial infarction: results from the German MONICA/KORA study. BMC Public Health 10, 135 (2010).
Ogden, C. L. et al. Prevalence of obesity among adults, by household income and education — United States, 2011–2014. MMWR Morb. Mortal. Wkly Rep. 66, 1369–1373 (2017).
Allen, A. P., Dinan, T. G., Clarke, G. & Cryan, J. F. A psychology of the human brain-gut-microbiome axis. Soc. Personal. Psychol. Compass 11, e12309 (2017).
Lach, G., Schellekens, H., Dinan, T. G. & Cryan, J. F. Anxiety, depression, and the microbiome: a role for gut peptides. Neurotherapeutics 15, 36–59 (2018).
Marmot, M. & Wilkinson, R. G. Psychosocial and material pathways in the relation between income and health: a response to Lynch. et al. BMJ 322, 1233–1236 (2001).
Kwong, W. K. & Moran, N. A. Gut microbial communities of social bees. Nat. Rev. Microbiol. 14, 374–384 (2016).
Bailey, M. T. et al. Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav. Immun. 25, 397–407 (2011).
Bailey, M. T. Influence of stressor-induced nervous system activation on the intestinal microbiota and the importance for immunomodulation. Adv. Exp. Med. Biol. 817, 255–276 (2014).
Bailey, M. T. & Coe, C. L. Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev. Psychobiol. 35, 146–155 (1999).
O’Mahony, S. M. et al. Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol. Psychiatry 65, 263–267 (2009).
Jasarevic, E., Howerton, C. L., Howard, C. D. & Bale, T. L. Alterations in the vaginal microbiome by maternal stress are associated with metabolic reprogramming of the offspring gut and brain. Endocrinology 156, 3265–3276 (2015).
Goyal, M. S., Venkatesh, S., Milbrandt, J., Gordon, J. I. & Raichle, M. E. Feeding the brain and nurturing the mind: linking nutrition and the gut microbiota to brain development. Proc. Natl Acad. Sci. USA 112, 14105–14112 (2015).
Xu, Z. & Knight, R. Dietary effects on human gut microbiome diversity. Br. J. Nutr. 113, S1–S5 (2015).
Nguyen, T. L., Vieira-Silva, S., Liston, A. & Raes, J. How informative is the mouse for human gut microbiota research? Dis. Model. Mech. 8, 1–16 (2015).
The Human Microbiome Project Consortium Structure, function and diversity of the healthy human microbiome. Nature 486, 207–214 (2012).
Yatsunenko, T. et al. Human gut microbiome viewed across age and geography. Nature 486, 222–227 (2012).
Zhernakova, A. et al. Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Science 352, 565–569 (2016).
Preliminary Characterization of the American Gut Population (American Gut Project, 2014); http://americangut.org/wp-content/uploads/2016/02/mod1_main.pdf
Falony, G. et al. Population-level analysis of gut microbiome variation. Science 352, 560–564 (2016).
Moayyeri, A., Hammond, C. J., Hart, D. J. & Spector, T. D. The UK Adult Twin Registry (TwinsUK Resource). Twin Res. Hum. Genet. 16, 144–149 (2013).
Goodrich, J. K. et al. Genetic determinants of the gut microbiome in UK twins. Cell Host Microbe 19, 731–743 (2016).
Jackson, M. A. et al. Signatures of early frailty in the gut microbiota. Genome Med. 8, 8 (2016).
Beaumont, M. et al. Heritable components of the human fecal microbiome are associated with visceral fat. Genome Biol. 17, 189 (2016).
Xie, H. et al. Shotgun metagenomics of 250 adult twins reveals genetic and environmental impacts on the gut microbiome. Cell Syst. 3, 572–584 (2016).
Goodrich, J. K. et al. Human genetics shape the gut microbiome. Cell 159, 789–799 (2014).
Menni, C. et al. Gut microbiome diversity and high-fibre intake are related to lower long-term weight gain. Int. J. Obes. 41, 1099–1105 (2017).
Fu, J. et al. The gut microbiome contributes to a substantial proportion of the variation in blood lipids. Circ. Res. 117, 817–824 (2015).
Falk, E. B. et al. What is a representative brain? Neuroscience meets population science. Proc. Natl Acad. Sci. USA 110, 17615–17622 (2013).
LeWinn, K. Z., Sheridan, M. A., Keyes, K. M., Hamilton, A. & McLaughlin, K. A. Sample composition alters associations between age and brain structure. Nat. Commun. 8, 874 (2017).
Morgan, S. L. & Winship, C. Counterfactuals and Causal Inference: Analytical Methods for Social Research. Social Research, 1st edn. (Cambridge Univ. Press, Cambridge, 2014).
Herd, P. et al. The influence of social conditions across the life course on the human gut microbiota: a pilot project with the Wisconsin Longitudinal Study. J. Gerontol. B Psychol. Sci. Soc. Sci. 73, 124–133 (2017).
Barker, D. J. P. Mothers, Babies, and Health in Later Life. 2nd edn. (Vol. ix, Churchill Livingstone, Edinburgh, 1998) .
Gluckman, P. & Hanson, M. The Fetal Matrix: Evolution, Development and Disease (Cambridge Univ. Press, Cambridge, 2004).
Langley-Evans, S. C. Fetal Nutrition and Adult Disease: Programming of Chronic Disease Through Fetal Exposure to Undernutrition (CABI Publishing, Wallingford, 2004).
Bateson, P. & Gluckman, P. Plasticity, Robustness, Development and Evolution (Cambridge Univ. Press, Cambridge, 2011).
Gluckman, P., Beedle, A., Buklijas, T., Low, F. & Hanson, M. Principles of Evolutionary Medicine 2nd edn, 400 (Oxford Univ. Press, Oxford, 2016).
Faith, J. J. et al. The long-term stability of the human gut microbiota. Science 341, 1237439 (2013).
Wamala, S. P., Lynch, J. & Kaplan, G. A. Women’s exposure to early and later life socioeconomic disadvantage and coronary heart disease risk: the Stockholm Female Coronary Risk Study. Int. J. Epidemiol. 30, 275–284 (2001).
Pensola, T. H. & Martikainen, P. Cumulative social class and mortality from various causes of adult men. J. Epidemiol. Community Health 57, 745–751 (2003).
Luo, Y. & Waite, L. J. The impact of childhood and adult SES on physical, mental, and cognitive well-being in later life. J. Gerontol. B Psychol. Sci. Soc. Sci. 60, S93–S101 (2005).
Lynch, J. W. et al. Childhood and adult socioeconomic status as predictors of mortality in Finland. Lancet 343, 524–527 (1994).
Cortese, R., Lu, L., Yu, Y., Ruden, D. & Claud, E. C. Epigenome–microbiome crosstalk: a potential new paradigm influencing neonatal susceptibility to disease. Epigenetics 11, 205–215 (2016).
Harris, R. A. et al. Colonic mucosal epigenome and microbiome development in children and adolescents. J. Immunol. Res. 2016, 9170162 (2016).
Indrio, F. et al. Epigenetic matters: the link between early nutrition, microbiome, and long-term health development. Front. Pediatr. 5, 178 (2017).
Monk, C., Spicer, J. & Champagne, F. A. Linking prenatal maternal adversity to developmental outcomes in infants: the role of epigenetic pathways. Dev. Psychopathol. 24, 1361–1376 (2012).
Barker, D. J., Eriksson, J. G., Forsen, T. & Osmond, C. Fetal origins of adult disease: strength of effects and biological basis. Int. J. Epidemiol. 31, 1235–1239 (2002).
Smith, M. I. et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science 339, 548–554 (2013).
Meaney, M. J. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 24, 1161–1192 (2001).
Mcewen, B. S. Protective and damaging effects of stress mediators: allostasis and allostatic load. N. Engl. J. Med. 338, 171–179 (1998).
Knudsen, E. I., Heckman, J. J., Cameron, J. L. & Shonkoff, J. P. Economic, neurobiological, and behavioral perspectives on building America’s future workforce. Proc. Natl Acad. Sci. USA 103, 10155–10162 (2006).
Forsdahl, A. Commentary: childhood deprivation and adult mortality. Int. J. Epidemiol. 31, 308–308 (2002).
Hayward, M. D. & Gorman, B. K. The long arm of childhood: the influence of early-life social conditions on men’s mortality. Demography 41, 87–107 (2004).
Bengtsson, T. & Lindstrom, M. Childhood misery and disease in later life: the effects on mortality in old age of hazards experienced in early life, southern Sweden, 1760–1894. Popul. Stud. 54, 263–277 (2000).
Almond, D. & Currie, J. Killing me softly: the fetal origins hypothesis. J. Econ. Perspect. 25, 153–172 (2011).
Finch, C. The Biology of Human Longevity: Inflammation, Nutrition, and Aging in the Evolution of Lifespans 1st edn (Academic Press, San Diego, 2007).
Fong, I. W. Emerging relations between infectious diseases and coronary artery disease and atherosclerosis. CMAJ 163, 49–56 (2000).
Kermack, W. O. & McKendrick, A. G. A contribution to the mathematical theory of epidemics. Proc. R. Soc. Lond. A: Math. Phys. Eng. Sci. 115, 700–721 (1927).
McDade, T. W., Rutherford, J., Adair, L. & Kuzawa, C. W. Early origins of inflammation: microbial exposures in infancy predict lower levels of C-reactive protein in adulthood. Proc. Biol. Sci. 277, 1129–1137 (2010).
Lumey, L. H. et al. Cohort profile: the Dutch Hunger Winter families study. Int. J. Epidemiol. 36, 1196–1204 (2007).
Li, C. & Lumey, L. H. Exposure to the Chinese famine of 1959–61 in early life and long-term health conditions: a systematic review and meta-analysis. Int. J. Epidemiol. 46, 1157–1170 (2017).
Tobi, E. W. et al. DNA methylation as a mediator of the association between prenatal adversity and risk factors for metabolic disease in adulthood. Sci. Adv. 4, eaao4364 (2018).
Roseboom, T., de Rooij, S. & Painter, R. The Dutch famine and its long-term consequences for adult health. Early Hum. Dev. 82, 485–491 (2006).
Painter, R. C. et al. Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG 115, 1243–1249 (2008).
Mother's money. The Economist (3 May 2018).
Rivera, J. A., Sotres-Alvarez, D., Habicht, J. P., Shamah, T. & Villalpando, S. Impact of the Mexican program for education, health, and nutrition (Progresa) on rates of growth and anemia in infants and young children: a randomized effectiveness study. JAMA 291, 2563–2570 (2004).
Behrman, J. R. & Todd, P. E. Randomness in the Experimental Samples of Progresa Working Paper 38. (International Food Policy Research Institute, Washington DC, 1999) .
Chetty, R. et al. The association between income and life expectancy in the United States, 2001–2014. JAMA 315, 1750–1766 (2016).
Crimmins, E., Jung, Ki,K. & Sarinnapha, V. Biodemography: new approaches to understanding trends and differences in population health and mortality. Demography 47, S41–S64 (2010).
McInerney, M., Mellor, J. M. & Nicholas, L. H. Recession depression: mental health effects of the 2008 stock market crash. J. Health Econ. 32, 1090–1104 (2013).
Glymour, M. M., Kawachi, I., Jencks, C. S. & Berkman, L. F. Does childhood schooling affect old age memory or mental status? Using state schooling laws as natural experiments. J. Epidemiol. Community Health 62, 532–537 (2008).
Davies, N. M., Dickson, M., Davey Smith, G., van den Berg, G. & Windmeijer, F. Preprint at bioRxiv https://doi.org/10.1101/074815 (2016).
Tillmann, T. et al. Education and coronary heart disease: Mendelian randomisation study. BMJ 358, j3542 (2017).
House, J. S., Landis, K. R. & Umberson, D. Social relationships and health. Science 241, 540–545 (1988).
Umberson, D., Crosnoe, R. & Reczek, C. Social relationships and health behavior across life course. Annu. Rev. Sociol. 36, 139–157 (2010).
Holt-Lunstad, J., Smith, T. B. & Layton, J. B. Social relationships and mortality risk: a meta-analytic review. PLoS Med. 7, e1000316 (2010).
Cao, X. Intestinal inflammation induced by oral bacteria. Science 358, 308–309 (2017).
Herd, P., Carr, D. & Roan, C. Cohort profile: Wisconsin Longitudinal Study (WLS). Int. J. Epidemiol. 43, 34–41 (2014).
Dill-McFarland, K. A. et al. Social relationships, social isolation, and the human gut microbiota. Preprint at bioRxiv https://doi.org/10.1101/428938 (2018).
Lawlor, D. A., Clark, H., Davey Smith, G. & Leon, D. A. Childhood intelligence, educational attainment and adult body mass index: findings from a prospective cohort and within sibling-pairs analysis. Int. J. Obes. 30, 1758–1765 (2006).
Meyler, D., Stimpson, J. P. & Peek, M. K. Health concordance within couples: a systematic review. Soc. Sci. Med. 64, 2297–2310 (2007).
The authors thank members of the Rey Laboratory for their insights and support. This work was supported by the National Institute of Food and Agriculture, US Department of Agriculture (2016-67017-24416, FER), the National Institute on Aging, National Institutes of Health (NIH) (AG041868, PH), the Center for the Demography of Health and Aging (AG017266, PH), and the Clinical and Translational Science Award (CTSA), NIH National Center for Advancing Translational Sciences (NCATS) (UL1TR000427, ZZT). Additional support was provided by the Vice Chancellor for Research and Graduate Education at the University of Wisconsin-Madison. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NIH.
The authors declare no competing interests.
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Herd, P., Palloni, A., Rey, F. et al. Social and population health science approaches to understand the human microbiome. Nat Hum Behav 2, 808–815 (2018). https://doi.org/10.1038/s41562-018-0452-y
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