Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Microbial transmission in animal social networks and the social microbiome

Abstract

Host-associated microbiomes play an increasingly appreciated role in animal metabolism, immunity and health. The microbes in turn depend on their host for resources and can be transmitted across the host’s social network. In this Perspective, we describe how animal social interactions and networks may provide channels for microbial transmission. We propose the ‘social microbiome’ as the microbial metacommunity of an animal social group. We then consider the various social and environmental forces that are likely to influence the social microbiome at multiple scales, including at the individual level, within social groups, between groups, within populations and species, and finally between species. Through our comprehensive discussion of the ways in which sociobiological and ecological factors may affect microbial transmission, we outline new research directions for the field.

Your institute does not have access to this article

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Fig. 1: Social microbiomes as biological archipelagos.
Fig. 2: Processes at different scales influencing the social microbiome.
Fig. 3: Effect of dispersal on the social microbiome.

References

  1. McFall-Ngai, M. et al. Animals in a bacterial world, a new imperative for the life sciences. Proc. Natl Acad. Sci. USA 110, 3229–3236 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Charbonneau, M. R. et al. A microbial perspective of human developmental biology. Nature 535, 48–55 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Chung, H. et al. Gut immune maturation depends on colonization with a host-specific microbiota. Cell 149, 1578–1593 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Mazmanian, S. K., Liu, C. H., Tzianabos, A. O. & Kasper, D. L. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122, 107–118 (2005).

    CAS  PubMed  Google Scholar 

  5. Nicholson, J. K. et al. Host–gut microbiota metabolism interactions. Science 336, 1262–1267 (2012).

    CAS  PubMed  Google Scholar 

  6. Round, J. L. & Mazmanian, S. K. The gut microbiota shapes intestinal immune responses during health and disease. Nat. Rev. Immunol. 9, 313–323 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Flint, H. J., Bayer, E. A., Rincon, M. T., Lamed, R. & White, B. A. Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis. Nat. Rev. Microbiol. 6, 121–131 (2008).

    CAS  PubMed  Google Scholar 

  8. Gill, S. R. et al. Metagenomic analysis of the human distal gut microbiome. Science 312, 1355–1359 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Koppel, N., Rekdal, V. M. & Balskus, E. P. Chemical transformation of xenobiotics by the human gut microbiota. Science 356, eaag2770 (2017).

    PubMed  Google Scholar 

  10. Spanogiannopoulos, P., Bess, E. N., Carmody, R. N. & Turnbaugh, P. J. The microbial pharmacists within us: a metagenomic view of xenobiotic metabolism. Nat. Rev. Microbiol. 14, 273–287 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Sharon, G., Sampson, T. R., Geschwind, D. H. & Mazmanian, S. K. The central nervous system and the gut microbiome. Cell 167, 915–932 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Cryan, J. F. & Dinan, T. G. Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat. Rev. Neurosci. 13, 701–712 (2012).

    CAS  PubMed  Google Scholar 

  13. Diaz Heijtz, R. et al. Normal gut microbiota modulates brain development and behavior. Proc. Natl Acad. Sci. USA 108, 3047–3052 (2011).

    PubMed  Google Scholar 

  14. Johnson, K. V.-A. & Foster, K. R. Why does the microbiome affect behaviour? Nat. Rev. Microbiol. 16, 647–655 (2018).

    CAS  PubMed  Google Scholar 

  15. Sarkar, A. et al. The role of the microbiome in the neurobiology of social behaviour. Biol. Rev. https://doi.org/10.1111/brv.12603 (2020).

  16. Vuong, H. E., Yano, J. M., Fung, T. C. & Hsiao, E. Y. The microbiome and host behavior. Annu. Rev. Neurosci. 40, 21–49 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Carmody, R. N. et al. Diet dominates host genotype in shaping the murine gut microbiota. Cell Host Microbe 17, 72–84 (2015).

    CAS  PubMed  Google Scholar 

  18. Goodrich, J. K. et al. Human genetics shape the gut microbiome. Cell 159, 789–799 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Hill, C. J. et al. Evolution of gut microbiota composition from birth to 24 weeks in the INFANTMET Cohort. Microbiome 5, 4 (2017).

    PubMed  PubMed Central  Google Scholar 

  20. Jackson, M. A. et al. Gut microbiota associations with common diseases and prescription medications in a population-based cohort. Nat. Commun. 9, 2655 (2018).

    PubMed  PubMed Central  Google Scholar 

  21. Smits, S. A. et al. Seasonal cycling in the gut microbiome of the Hadza hunter-gatherers of Tanzania. Science 357, 802–806 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Rothschild, D. et al. Environment dominates over host genetics in shaping human gut microbiota. Nature 555, 210–215 (2018).

    CAS  PubMed  Google Scholar 

  23. Archie, E. A. & Tung, J. Social behavior and the microbiome. Curr. Opin. Behav. Sci. 6, 28–34 (2015).

    Google Scholar 

  24. Montiel-Castro, A. J., González-Cervantes, R. M., Bravo-Ruiseco, G. & Pacheco-López, G. The microbiota–gut–brain axis: neurobehavioral correlates, health and sociality. Front. Integr. Neurosci. 7, 70 (2013).

    PubMed  PubMed Central  Google Scholar 

  25. Münger, E., Montiel-Castro, A. J., Langhans, W. & Pacheco-López, G. Reciprocal interactions between gut microbiota and host social behaviour. Front. Integr. Neurosci. 12, 21 (2018).

    PubMed  PubMed Central  Google Scholar 

  26. Krause, J., Ruxton, G. D. & Ruxton, G. D. Living in Groups (Oxford Univ. Press, 2002).

  27. Leibold, M. A. et al. The metacommunity concept: a framework for multi‐scale community ecology. Ecol. Lett. 7, 601–613 (2004).

    Google Scholar 

  28. Clayton, J. B. et al. The gut microbiome of nonhuman primates: lessons in ecology and evolution. Am. J. Primatol. 80, e22867 (2018).

    PubMed  Google Scholar 

  29. MacArthur, R. H. & Wilson, E. O. The Theory of Island Biogeography (Princeton Univ. Press, 2001).

  30. Whittaker, R. J., Fernández-Palacios, J. M., Matthews, T. J., Borregaard, M. K. & Triantis, K. A. Island biogeography: taking the long view of nature’s laboratories. Science 357, eaam8326 (2017).

    PubMed  Google Scholar 

  31. Costello, E. K., Stagaman, K., Dethlefsen, L., Bohannan, B. J. & Relman, D. A. The application of ecological theory toward an understanding of the human microbiome. Science 336, 1255–1262 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Chisholm, C., Lindo, Z. & Gonzalez, A. Metacommunity diversity depends on connectivity and patch arrangement in heterogeneous habitat networks. Ecography 34, 415–424 (2011).

    Google Scholar 

  33. Forbes, A. E. & Chase, J. M. The role of habitat connectivity and landscape geometry in experimental zooplankton metacommunities. Oikos 96, 433–440 (2002).

    Google Scholar 

  34. Gascuel, F., Laroche, F., Bonnet-Lebrun, A. S. & Rodrigues, A. S. The effects of archipelago spatial structure on island diversity and endemism: predictions from a spatially-structured neutral model. Evolution 70, 2657–2666 (2016).

    PubMed  Google Scholar 

  35. Burns, A. R. et al. Interhost dispersal alters microbiome assembly and can overwhelm host innate immunity in an experimental zebrafish model. Proc. Natl Acad. Sci. USA 114, 11181–11186 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Koskella, B., Hall, L. J. & Metcalf, C. J. E. The microbiome beyond the horizon of ecological and evolutionary theory. Nat. Ecol. Evol. 1, 1606–1615 (2017).

    PubMed  Google Scholar 

  37. Mihaljevic, J. R. Linking metacommunity theory and symbiont evolutionary ecology. Trends Ecol. Evol. 27, 323–329 (2012).

    PubMed  Google Scholar 

  38. Moeller, A. H. et al. Dispersal limitation promotes the diversification of the mammalian gut microbiota. Proc. Natl Acad. Sci. USA 114, 13768–13773 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Miller, E. T., Svanbäck, R. & Bohannan, B. J. Microbiomes as metacommunities: understanding host-associated microbes through metacommunity ecology. Trends Ecol. Evol. 33, 926–935 (2018).

    PubMed  Google Scholar 

  40. Robinson, C. D. et al. Experimental bacterial adaptation to the zebrafish gut reveals a primary role for immigration. PLoS Biol. 16, e2006893 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Altizer, S. et al. Social organization and parasite risk in mammals: integrating theory and empirical studies. Annu. Rev. Ecol. Evol. Syst. 34, 517–547 (2003).

    Google Scholar 

  42. White, L. A., Forester, J. D. & Craft, M. E. Using contact networks to explore mechanisms of parasite transmission in wildlife. Biol. Rev. 92, 389–409 (2017).

    PubMed  Google Scholar 

  43. Schmid-Hempel, P. Parasites and their social hosts. Trends Parasitol. 33, 453–462 (2017).

    PubMed  Google Scholar 

  44. Browne, H. P., Neville, B. A., Forster, S. C. & Lawley, T. D. Transmission of the gut microbiota: spreading of health. Nat. Rev. Microbiol. 15, 531–543 (2017).

    PubMed  PubMed Central  Google Scholar 

  45. Schwarz, R. S., Moran, N. A. & Evans, J. D. Early gut colonizers shape parasite susceptibility and microbiota composition in honey bee workers. Proc. Natl Acad. Sci. USA 113, 9345–9350 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Koch, H. & Schmid-Hempel, P. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc. Natl Acad. Sci. USA 108, 19288–19292 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Martinson, V. G. et al. A simple and distinctive microbiota associated with honey bees and bumble bees. Mol. Ecol. 20, 619–628 (2011).

    PubMed  Google Scholar 

  48. Lombardo, M. P. Access to mutualistic endosymbiotic microbes: an underappreciated benefit of group living. Behav. Ecol. Sociobiol. 62, 479–497 (2008).

    Google Scholar 

  49. Troyer, K. Microbes, herbivory and the evolution of social behavior. J. Theor. Biol. 106, 157–169 (1984).

    Google Scholar 

  50. Tung, J. et al. Social networks predict gut microbiome composition in wild baboons. eLife 4, e05224 (2015).

    PubMed Central  Google Scholar 

  51. 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 

  52. Hamady, M. & Knight, R. Microbial community profiling for human microbiome projects: tools, techniques, and challenges. Genome Res. 19, 1141–1152 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Moeller, A. H. et al. Social behavior shapes the chimpanzee pan-microbiome. Sci. Adv. 2, e1500997 (2016).

    PubMed  PubMed Central  Google Scholar 

  54. Perofsky, A. C., Lewis, R. J., Abondano, L. A., Di Fiore, A. & Meyers, L. A. Hierarchical social networks shape gut microbial composition in wild Verreaux’s sifaka. Proc. R. Soc. B 284, 20172274 (2017).

    PubMed  PubMed Central  Google Scholar 

  55. Amato, K. R. et al. Patterns in gut microbiota similarity associated with degree of sociality among sex classes of a neotropical primate. Microb. Ecol. 74, 250–258 (2017).

    PubMed  Google Scholar 

  56. Amato, K. R. Co-evolution in context: the importance of studying gut microbiomes in wild animals. Microbiome Sci. Med. 1, 10–29 (2013).

    Google Scholar 

  57. Archie, E. A. & Theis, K. R. Animal behaviour meets microbial ecology. Anim. Behav. 82, 425–436 (2011).

    Google Scholar 

  58. Ezenwa, V. O., Gerardo, N. M., Inouye, D. W., Medina, M. & Xavier, J. B. Animal behavior and the microbiome. Science 338, 198–199 (2012).

    CAS  PubMed  Google Scholar 

  59. Raulo, A. et al. Social behaviour and gut microbiota in red‐bellied lemurs (Eulemur rubriventer): in search of the role of immunity in the evolution of sociality. J. Anim. Ecol. 87, 388–399 (2018).

    PubMed  Google Scholar 

  60. Gogarten, J. F. et al. Factors influencing bacterial microbiome composition in a wild non-human primate community in Taï National Park, Côte d’Ivoire. ISME J. 12, 2559–2574 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Lax, S. et al. Longitudinal analysis of microbial interaction between humans and the indoor environment. Science 345, 1048–1052 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Song, S. J. et al. Cohabiting family members share microbiota with one another and with their dogs. eLife 2, e00458 (2013).

    PubMed  PubMed Central  Google Scholar 

  63. Yatsunenko, T. et al. Human gut microbiome viewed across age and geography. Nature 486, 222–227 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Barberán, A. et al. The ecology of microscopic life in household dust. Proc. R. Soc. B 282, 20151139 (2015).

    PubMed Central  Google Scholar 

  65. Fujimura, K. E. et al. House dust exposure mediates gut microbiome Lactobacillus enrichment and airway immune defense against allergens and virus infection. Proc. Natl Acad. Sci. USA 111, 805–810 (2014).

    CAS  PubMed  Google Scholar 

  66. Fierer, N. et al. Forensic identification using skin bacterial communities. Proc. Natl Acad. Sci. USA 107, 6477–6481 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Hoisington, A. J., Brenner, L. A., Kinney, K. A., Postolache, T. T. & Lowry, C. A. The microbiome of the built environment and mental health. Microbiome 3, 60 (2015).

    PubMed  PubMed Central  Google Scholar 

  68. Lax, S. et al. Forensic analysis of the microbiome of phones and shoes. Microbiome 3, 21 (2015).

    PubMed  PubMed Central  Google Scholar 

  69. Lax, S., Nagler, C. R. & Gilbert, J. A. Our interface with the built environment: immunity and the indoor microbiota. Trends Immunol. 36, 121–123 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Kort, R. et al. Shaping the oral microbiota through intimate kissing. Microbiome 2, 41 (2014).

    PubMed  PubMed Central  Google Scholar 

  71. de Waal, F. B. M. Primates—a natural heritage of conflict resolution. Science 289, 586–590 (2000).

    PubMed  Google Scholar 

  72. Gardy, J. L. et al. Whole-genome sequencing and social-network analysis of a tuberculosis outbreak. N. Engl. J. Med. 364, 730–739 (2011).

    CAS  PubMed  Google Scholar 

  73. Dill-McFarland, K. et al. Close social relationships correlate with human gut microbiota composition. Sci. Rep. 9, 703 (2018).

    Google Scholar 

  74. Brito, I. L. & Alm, E. J. Tracking strains in the microbiome: insights from metagenomics and models. Front. Microbiol. 7, 712 (2016).

    PubMed  PubMed Central  Google Scholar 

  75. Nayfach, S., Rodriguez-Mueller, B., Garud, N. & Pollard, K. S. An integrated metagenomics pipeline for strain profiling reveals novel patterns of bacterial transmission and biogeography. Genome Res. 26, 1612–1625 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  76. Asnicar, F. et al. Studying vertical microbiome transmission from mothers to infants by strain-level metagenomic profiling. MSystems 2, e00164–16 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Brito, I. L. et al. Transmission of human-associated microbiota along family and social networks. Nat. Microbiol. 4, 964–971 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Johnson, K. V.-A. Gut microbiome composition and diversity are related to human personality traits. Hum. Microbiome J. 15, 100069 (2020).

    Google Scholar 

  79. Janzen, D. H. Host plants as islands in evolutionary and contemporary time. Am. Nat. 102, 592–595 (1968).

    Google Scholar 

  80. Kuris, A. M., Blaustein, A. R. & Alio, J. J. Hosts as islands. Am. Nat. 116, 570–586 (1980).

    Google Scholar 

  81. Freeland, W. J. Primate social groups as biological islands. Ecology 60, 719–728 (1979).

    Google Scholar 

  82. Trosvik, P. et al. Multilevel social structure and diet shape the gut microbiota of the gelada monkey, the only grazing primate. Microbiome 6, 84 (2018).

    PubMed  PubMed Central  Google Scholar 

  83. Degnan, P. H. et al. Factors associated with the diversification of the gut microbial communities within chimpanzees from Gombe National Park. Proc. Natl Acad. Sci. USA 109, 13034–13039 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Amaral, W. Z. et al. Social influences on Prevotella and the gut microbiome of young monkeys. Psychosom. Med. 79, 888–897 (2017).

    PubMed  PubMed Central  Google Scholar 

  85. Orkin, J. D., Webb, S. E. & Melin, A. D. Small to modest impact of social group on the gut microbiome of wild Costa Rican capuchins in a seasonal forest. Am. J. Primatol. 81, e22985 (2019).

    CAS  PubMed  Google Scholar 

  86. 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).

    CAS  PubMed  Google Scholar 

  87. Goodfellow, C. K. et al. Divergence in gut microbial communities mirrors a social group fission event in a black‐and‐white colobus monkey (Colobus vellerosus). Am. J. Primatol. 81, e22966 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Wikberg, E. C., Christie, D., Sicotte, P. & Ting, N. Interactions between social groups of colobus monkeys (Colobus vellerosus) explain similarities in their gut microbiomes. Anim. Behav. 163, 17–31 (2020).

    Google Scholar 

  89. Springer, A. et al. Patterns of seasonality and group membership characterize the gut microbiota in a longitudinal study of wild Verreaux’s sifakas (Propithecus verreauxi). Ecol. Evol. 7, 5732–5745 (2017).

    PubMed  PubMed Central  Google Scholar 

  90. Antwis, R. E., Lea, J. M., Unwin, B. & Shultz, S. Gut microbiome composition is associated with spatial structuring and social interactions in semi-feral Welsh Mountain ponies. Microbiome 6, 207 (2018).

    PubMed  PubMed Central  Google Scholar 

  91. Grosser, S. et al. Fur seal microbiota are shaped by the social and physical environment, show mother–offspring similarities and are associated with host genetic quality. Mol. Ecol. 28, 2406–2422 (2019).

    CAS  PubMed  Google Scholar 

  92. Leung, M. H., Wilkins, D. & Lee, P. K. Insights into the pan-microbiome: skin microbial communities of Chinese individuals differ from other racial groups. Sci. Rep. 5, 11845 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Altermatt, F. & Holyoak, M. Spatial clustering of habitat structure effects patterns of community composition and diversity. Ecology 93, 1125–1133 (2012).

    PubMed  Google Scholar 

  94. Brown, B. L. & Swan, C. M. Dendritic network structure constrains metacommunity properties in riverine ecosystems. J. Anim. Ecol. 79, 571–580 (2010).

    CAS  PubMed  Google Scholar 

  95. Economo, E. P. & Keitt, T. H. Species diversity in neutral metacommunities: a network approach. Ecol. Lett. 11, 52–62 (2008).

    PubMed  Google Scholar 

  96. Matthews, T. J., Rigal, F., Triantis, K. A. & Whittaker, R. J. A global model of island species–area relationships. Proc. Natl Acad. Sci. USA 116, 12337–12342 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  97. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Relman, D. A. The human microbiome: ecosystem resilience and health. Nutr. Rev. 70, S2–S9 (2012).

    PubMed  Google Scholar 

  99. Coyte, K. Z., Schluter, J. & Foster, K. R. The ecology of the microbiome: networks, competition, and stability. Science 350, 663–666 (2015).

    CAS  PubMed  Google Scholar 

  100. Johnson, K. V.-A. & Burnet, P. W. J. Microbiome: should we diversify from diversity? Gut Microbes 7, 455–458 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Moeller, A. H. et al. SIV-induced instability of the chimpanzee gut microbiome. Cell Host Microbe 14, 340–345 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Kolodny, O. et al. Coordinated change at the colony level in fruit bat fur microbiomes through time. Nat. Ecol. Evol. 3, 116–124 (2019).

    PubMed  Google Scholar 

  103. Clutton-Brock, T. H., Harvey, P. H. & Rudder, B. Sexual dimorphism, socionomic sex ratio and body weight in primates. Nature 269, 797–800 (1977).

    CAS  PubMed  Google Scholar 

  104. Jašarević, E., Morrison, K. E. & Bale, T. L. Sex differences in the gut microbiome–brain axis across the lifespan. Philos. Trans. R. Soc. B 371, 20150122 (2016).

    Google Scholar 

  105. Kundu, P., Blacher, E., Elinav, E. & Pettersson, S. Our gut microbiome: the evolving inner self. Cell 171, 1481–1493 (2017).

    CAS  PubMed  Google Scholar 

  106. Sapolsky, R. M. & Share, L. J. A pacific culture among wild baboons: its emergence and transmission. PLoS Biol. 2, e106 (2004).

    PubMed  PubMed Central  Google Scholar 

  107. Silk, J. B., Altmann, J. & Alberts, S. C. Social relationships among adult female baboons (Papio cynocephalus) I. Variation in the strength of social bonds. Behav. Ecol. Sociobiol. 61, 183–195 (2006).

    Google Scholar 

  108. Silk, J. B., Alberts, S. C. & Altmann, J. Social relationships among adult female baboons (Papio cynocephalus) II. Variation in the quality and stability of social bonds. Behav. Ecol. Sociobiol. 61, 197–204 (2006).

    Google Scholar 

  109. Koren, O. et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 150, 470–480 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Nuriel-Ohayon, M. et al. Progesterone increases Bifidobacterium relative abundance during late pregnancy. Cell Rep. 27, 730–736 (2019).

    CAS  PubMed  Google Scholar 

  111. Newman, M. E. Modularity and community structure in networks. Proc. Natl Acad. Sci. USA 103, 8577–8582 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  112. Ezenwa, V. O. & Williams, A. E. Microbes and animal olfactory communication: where do we go from here? BioEssays 36, 847–854 (2014).

    PubMed  Google Scholar 

  113. Theis, K. R., Schmidt, T. M. & Holekamp, K. E. Evidence for a bacterial mechanism for group-specific social odors among hyenas. Sci. Rep. 2, 615 (2012).

    PubMed  PubMed Central  Google Scholar 

  114. Leclaire, S., Nielsen, J. F. & Drea, C. M. Bacterial communities in meerkat anal scent secretions vary with host sex, age, and group membership. Behav. Ecol. 25, 996–1004 (2014).

    Google Scholar 

  115. Gese, E. M. & Ruff, R. L. Scent-marking by coyotes, Canis latrans: the influence of social and ecological factors. Anim. Behav. 54, 1155–1166 (1997).

    CAS  PubMed  Google Scholar 

  116. Barja, I., Miguel, F. D. & Barcena, F. Faecal marking behaviour of Iberian wolf in different zones of their territory. Folia Zool. 54, 21–29 (2005).

    Google Scholar 

  117. Barja, I. & List, R. Faecal marking behaviour in ringtails (Bassariscus astutus) during the non-breeding period: spatial characteristics of latrines and single faeces. Chemoecology 16, 219–222 (2006).

    Google Scholar 

  118. Brashares, J. S. & Arcese, P. Scent marking in a territorial African antelope: II. The economics of marking with faeces. Anim. Behav. 57, 11–17 (1999).

    CAS  PubMed  Google Scholar 

  119. Ruiz-Aizpurua, L., Planillo, A., Carpio, A. J., Guerrero-Casado, J. & Tortosa, F. S. The use of faecal markers for the delimitation of the European rabbit’s social territories (Oryctolagus cuniculus L.). Acta Ethol. 16, 157–162 (2013).

    Google Scholar 

  120. Marneweck, C., Jürgens, A. & Shrader, A. M. Ritualised dung kicking by white rhino males amplifies olfactory signals but reduces odour duration. J. Chem. Ecol. 44, 875–885 (2018).

    CAS  PubMed  Google Scholar 

  121. Cowl, V. B. & Shultz, S. Large brains and groups associated with high rates of agonism in primates. Behav. Ecol. 28, 803–810 (2017).

    Google Scholar 

  122. Wilson, M. L. et al. Lethal aggression in Pan is better explained by adaptive strategies than human impacts. Nature 513, 414–417 (2014).

    CAS  PubMed  Google Scholar 

  123. Wilson, M. L. & Wrangham, R. W. Intergroup relations in chimpanzees. Annu. Rev. Anthropol. 32, 363–392 (2003).

    Google Scholar 

  124. Wrangham, R. W. & Glowacki, L. Intergroup aggression in chimpanzees and war in nomadic hunter-gatherers. Hum. Nat. 23, 5–29 (2012).

    PubMed  Google Scholar 

  125. Heinsohn, R. Group territoriality in two populations of African lions. Anim. Behav. 53, 1143–1147 (1997).

    CAS  PubMed  Google Scholar 

  126. Mosser, A. & Packer, C. Group territoriality and the benefits of sociality in the African lion, Panthera leo. Anim. Behav. 78, 359–370 (2009).

    Google Scholar 

  127. Cassidy, K. A., MacNulty, D. R., Stahler, D. R., Smith, D. W. & Mech, L. D. Group composition effects on aggressive interpack interactions of gray wolves in Yellowstone National Park. Behav. Ecol. 26, 1352–1360 (2015).

    Google Scholar 

  128. Mullon, C., Keller, L. & Lehmann, L. Social polymorphism is favoured by the co-evolution of dispersal with social behaviour. Nat. Ecol. Evol. 2, 132–140 (2018).

    PubMed  Google Scholar 

  129. Alberts, S. C. & Altmann, J. Balancing costs and opportunities: dispersal in male baboons. Am. Nat. 145, 279–306 (1995).

    Google Scholar 

  130. Greenwood, P. J. Mating systems, philopatry and dispersal in birds and mammals. Anim. Behav. 28, 1140–1162 (1980).

    Google Scholar 

  131. Isbell, L. A. & Van Vuren, D. Differential costs of locational and social dispersal and their consequences for female group-living primates. Behaviour 133, 1–36 (1996).

    Google Scholar 

  132. Pusey, A. E. Sex-biased dispersal and inbreeding avoidance in birds and mammals. Trends Ecol. Evol. 2, 295–299 (1987).

    CAS  PubMed  Google Scholar 

  133. Pusey, A. E. & Packer, C. The evolution of sex-biased dispersal in lions. Behaviour 101, 275–310 (1987).

    Google Scholar 

  134. Cozzi, G., Maag, N., Börger, L., Clutton‐Brock, T. H. & Ozgul, A. Socially informed dispersal in a territorial cooperative breeder. J. Anim. Ecol. 87, 838–849 (2018).

    PubMed  Google Scholar 

  135. Dosmann, A., Bahet, N. & Gordon, D. M. Experimental modulation of external microbiome affects nestmate recognition in harvester ants (Pogonomyrmex barbatus). PeerJ 4, e1566 (2016).

    PubMed  PubMed Central  Google Scholar 

  136. Matsuura, K. Nestmate recognition mediated by intestinal bacteria in a termite, Reticulitermes speratus. Oikos 92, 20–26 (2001).

    Google Scholar 

  137. Bentley‐Condit, V. K., Moore, T. & Smith, E. O. Analysis of infant handling and the effects of female rank among Tana River adult female yellow baboons (Papio cynocephalus cynocephalus) using permutation/randomization tests. Am. J. Primatol. 55, 117–130 (2001).

    PubMed  Google Scholar 

  138. Cremer, S., Armitage, S. A. & Schmid-Hempel, P. Social immunity. Curr. Biol. 17, R693–R702 (2007).

    CAS  PubMed  Google Scholar 

  139. Maestripieri, D. Social structure, infant handling, and mothering styles in group-living Old World monkeys. Int. J. Primatol. 15, 531–553 (1994).

    Google Scholar 

  140. Silk, J. B. Why are infants so attractive to others? The form and function of infant handling in bonnet macaques. Anim. Behav. 57, 1021–1032 (1999).

    CAS  PubMed  Google Scholar 

  141. 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).

    PubMed  PubMed Central  Google Scholar 

  142. Moeller, A. H., Suzuki, T. A., Phifer-Rixey, M. & Nachman, M. W. Transmission modes of the mammalian gut microbiota. Science 362, 453–457 (2018).

    CAS  PubMed  Google Scholar 

  143. Dettmer, A. M., Allen, J. M., Jaggers, R. M. & Bailey, M. T. A descriptive analysis of gut microbiota composition in differentially reared infant rhesus monkeys (Macaca mulatta) across the first 6 months of life. Am. J. Primatol. 81, e22969 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  144. Chu, D. M. et al. Maturation of the infant microbiome community structure and function across multiple body sites and in relation to mode of delivery. Nat. Med. 23, 314–326 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  145. Ferretti, P. et al. Mother-to-infant microbial transmission from different body sites shapes the developing infant gut microbiome. Cell Host Microbe 24, 133–145 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  146. Korpela, K. et al. Selective maternal seeding and environment shape the human gut microbiome. Genome Res. 28, 561–568 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  147. Moeller, A. H. et al. Sympatric chimpanzees and gorillas harbor convergent gut microbial communities. Genome Res. 23, 1715–1720 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  148. David, L. A. et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559–563 (2014).

    CAS  PubMed  Google Scholar 

  149. Farine, D. R., Garroway, C. J. & Sheldon, B. C. Social network analysis of mixed-species flocks: exploring the structure and evolution of interspecific social behaviour. Anim. Behav. 84, 1271–1277 (2012).

    Google Scholar 

  150. Goodale, E. & Kotagama, S. W. Vocal mimicry by a passerine bird attracts other species involved in mixed-species flocks. Anim. Behav. 72, 471–477 (2006).

    Google Scholar 

  151. Krebs, J. R. Social learning and the significance of mixed-species flocks of chickadees (Parus spp.). Can. J. Zool. 51, 1275–1288 (1973).

    Google Scholar 

  152. Pays, O., Ekori, A. & Fritz, H. On the advantages of mixed-species groups: impalas adjust their vigilance when associated with larger prey herbivores. Ethology 120, 1207–1216 (2014).

    Google Scholar 

  153. Stensland, E. V. A., Angerbjörn, A. & Berggren, P. E. R. Mixed species groups in mammals. Mammal. Rev. 33, 205–223 (2003).

    Google Scholar 

  154. Terborgh, J. Mixed flocks and polyspecific associations: costs and benefits of mixed groups to birds and monkeys. Am. J. Primatol. 21, 87–100 (1990).

    PubMed  Google Scholar 

  155. Goodale, E. et al. Mixed company: a framework for understanding the composition and organization of mixed‐species animal groups. Biol. Rev. https://doi.org/10.1111/brv.12591 (2020).

  156. Venkataraman, V. V., Kerby, J. T., Nguyen, N., Ashenafi, Z. T. & Fashing, P. J. Solitary Ethiopian wolves increase predation success on rodents when among grazing gelada monkey herds. J. Mammal. 96, 129–137 (2015).

    Google Scholar 

  157. de Barros Damgaard, P. et al. The first horse herders and the impact of early Bronze Age steppe expansions into Asia. Science 360, eaar7711 (2018).

    PubMed  PubMed Central  Google Scholar 

  158. Loftus, R. T., MacHugh, D. E., Bradley, D. G., Sharp, P. M. & Cunningham, P. Evidence for two independent domestications of cattle. Proc. Natl Acad. Sci. USA 91, 2757–2761 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  159. Almathen, F. et al. Ancient and modern DNA reveal dynamics of domestication and cross-continental dispersal of the dromedary. Proc. Natl Acad. Sci. USA 113, 6707–6712 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  160. Larson, G. et al. Worldwide phylogeography of wild boar reveals multiple centers of pig domestication. Science 307, 1618–1621 (2005).

    CAS  PubMed  Google Scholar 

  161. Chessa, B. et al. Revealing the history of sheep domestication using retrovirus integrations. Science 324, 532–536 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  162. Pollinger, J. P. et al. Genome-wide SNP and haplotype analyses reveal a rich history underlying dog domestication. Nature 464, 898–902 (2010).

    PubMed  PubMed Central  Google Scholar 

  163. Ellis, R. J. et al. Comparison of the distal gut microbiota from people and animals in Africa. PLoS ONE 8, e54783 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  164. Hunt, K. M. et al. Characterization of the diversity and temporal stability of bacterial communities in human milk. PLoS ONE 6, e21313 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  165. Reese, A. T. et al. Parallel signatures of mammalian domestication and human industrialization in the gut microbiota. Preprint at bioRxiv https://doi.org/10.1101/611483 (2019).

  166. Caruso, R., Ono, M., Bunker, M. E., Núñez, G. & Inohara, N. Dynamic and asymmetric changes of the microbial communities after cohousing in laboratory mice. Cell Rep. 27, 3401–3412 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  167. Hilbert, T. et al. Vendor effects on murine gut microbiota influence experimental abdominal sepsis. J. Surg. Res. 211, 126–136 (2017).

    PubMed  Google Scholar 

  168. McIntosh, C. M., Chen, L., Shaiber, A., Eren, A. M. & Alegre, M. L. Gut microbes contribute to variation in solid organ transplant outcomes in mice. Microbiome 6, 96 (2018).

    PubMed  PubMed Central  Google Scholar 

  169. Rasmussen, T. S. et al. Mouse vendor influence on the bacterial and viral gut composition exceeds the effect of diet. Viruses 11, 435 (2019).

    CAS  PubMed Central  Google Scholar 

  170. Hufeldt, M. R., Nielsen, D. S., Vogensen, F. K., Midtvedt, T. & Hansen, A. K. Variation in the gut microbiota of laboratory mice is related to both genetic and environmental factors. Comp. Med. 60, 336–347 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  171. Ivanov, I. I. et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139, 485–498 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  172. Velazquez, E. M. et al. Endogenous Enterobacteriaceae underlie variation in susceptibility to Salmonella infection. Nat. Microbiol. 4, 1057–1064 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  173. Villarino, N. F. et al. Composition of the gut microbiota modulates the severity of malaria. Proc. Natl Acad. Sci. USA 113, 2235–2240 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  174. Robertson, S. J. et al. Comparison of co-housing and littermate methods for microbiota standardization in mouse models. Cell Rep. 27, 1910–1919 (2019).

    CAS  PubMed  Google Scholar 

  175. Laukens, D., Brinkman, B. M., Raes, J., De Vos, M. & Vandenabeele, P. Heterogeneity of the gut microbiome in mice: guidelines for optimizing experimental design. FEMS Microbiol. Rev. 40, 117–132 (2015).

    PubMed  PubMed Central  Google Scholar 

  176. Campbell, J. H. et al. Host genetic and environmental effects on mouse intestinal microbiota. ISME J. 6, 2033–2044 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  177. Hildebrand, F. et al. Inflammation-associated enterotypes, host genotype, cage and inter-individual effects drive gut microbiota variation in common laboratory mice. Genome Biol. 14, R4 (2013).

    PubMed  PubMed Central  Google Scholar 

  178. Ng, K. M. et al. Recovery of the gut microbiota after antibiotics depends on host diet and environmental reservoirs. Cell Host Microbe 26, 650–665 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  179. Reese, A. T. et al. Antibiotic-induced changes in the microbiota disrupt redox dynamics in the gut. eLife 7, e35987 (2018).

    PubMed  PubMed Central  Google Scholar 

  180. Ridaura, V. K. et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science 341, 1241214 (2013).

    PubMed  Google Scholar 

  181. Bel, S. et al. Reprogrammed and transmissible intestinal microbiota confer diminished susceptibility to induced colitis in TMF−/− mice. Proc. Natl Acad. Sci. USA 111, 4964–4969 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  182. Ussar, S. et al. Interactions between gut microbiota, host genetics and diet modulate the predisposition to obesity and metabolic syndrome. Cell Metabol. 22, 516–530 (2015).

    CAS  Google Scholar 

  183. McCafferty, J. et al. Stochastic changes over time and not founder effects drive cage effects in microbial community assembly in a mouse model. ISME J. 7, 2116–2125 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  184. Benson, A. K. et al. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proc. Natl Acad. Sci. USA 107, 18933–18938 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  185. Grieneisen, L. E. et al. Genes, geology and germs: gut microbiota across a primate hybrid zone are explained by site soil properties, not host species. Proc. R. Soc. B 286, 20190431 (2019).

    PubMed  PubMed Central  Google Scholar 

  186. Knowles, S. C. L., Eccles, R. M. & Baltrūnaitė, L. Species identity dominates over environment in shaping the microbiota of small mammals. Ecol. Lett. 22, 826–837 (2019).

    CAS  PubMed  Google Scholar 

  187. Suzuki, T. A. et al. Host genetic determinants of the gut microbiota of wild mice. Mol. Ecol. 28, 3197–3207 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  188. Turnbaugh, P. J. et al. A core gut microbiome in obese and lean twins. Nature 457, 480–484 (2009).

    CAS  PubMed  Google Scholar 

  189. Zoetendal, E. G., Akkermans, A. D., Akkermans-van Vliet, W. M., de Visser, J. A. G. & de Vos, W. M. The host genotype affects the bacterial community in the human gastrointestinal tract. Microb. Ecol. Health Dis. 13, 129–134 (2001).

    Google Scholar 

  190. Fields, C. T., Chassaing, B., Paul, M. J., Gewirtz, A. T. & de Vries, G. J. Vasopressin deletion is associated with sex-specific shifts in the gut microbiome. Gut Microbes 9, 13–25 (2018).

    CAS  PubMed  Google Scholar 

  191. Khachatryan, Z. A. et al. Predominant role of host genetics in controlling the composition of gut microbiota. PLoS ONE 3, e3064 (2008).

    PubMed  PubMed Central  Google Scholar 

  192. Salzman, N. H. et al. Enteric defensins are essential regulators of intestinal microbial ecology. Nat. Immmunol. 11, 76–82 (2010).

    CAS  Google Scholar 

  193. Spor, A., Koren, O. & Ley, R. Unravelling the effects of the environment and host genotype on the gut microbiome. Nat. Rev. Microbiol. 9, 279–290 (2011).

    CAS  PubMed  Google Scholar 

  194. Goodrich, J. K. et al. Genetic determinants of the gut microbiome in UK twins. Cell Host Microbe 19, 731–743 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  195. Turpin, W. et al. Association of host genome with intestinal microbial composition in a large healthy cohort. Nat. Genet. 48, 1413–1417 (2016).

    CAS  PubMed  Google Scholar 

  196. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  197. Shykoff, J. A. & Schmid-Hempel, P. Genetic relatedness and eusociality: parasite-mediated selection on the genetic composition of groups. Behav. Ecol. Sociobiol. 28, 371–376 (1991).

    Google Scholar 

  198. Shykoff, J. A. & Schmid-Hempel, P. Parasites and the advantage of genetic variability within social insect colonies. Proc. R. Soc. B 243, 55–58 (1991).

    Google Scholar 

  199. Perofsky, A. C., Lewis, R. J. & Meyers, L. A. Terrestriality and bacterial transfer: a comparative study of gut microbiomes in sympatric Malagasy mammals. ISME J. 13, 50–63 (2019).

    PubMed  Google Scholar 

  200. Clutton‐Brock, T. H. & Harvey, P. H. Primate ecology and social organization. J. Zool. 183, 1–39 (1977).

    Google Scholar 

  201. Janson, C. H. & Goldsmith, M. L. Predicting group size in primates: foraging costs and predation risks. Behav. Ecol. 6, 326–336 (1995).

    Google Scholar 

  202. Ayres, J. M. & Clutton-Brock, T. H. River boundaries and species range size in Amazonian primates. Am. Nat. 140, 531–537 (1992).

    CAS  PubMed  Google Scholar 

  203. King, S. L. et al. Bottlenose dolphins retain individual vocal labels in multi-level alliances. Curr. Biol. 28, 1993–1999.e3 (2018).

    CAS  PubMed  Google Scholar 

  204. Lusseau, D. & Newman, M. E. Identifying the role that animals play in their social networks. Proc. R. Soc. B 271, S477–S481 (2004).

    PubMed  PubMed Central  Google Scholar 

  205. Rendell, L. & Whitehead, H. Culture in whales and dolphins. Behav. Brain Sci. 24, 309–324 (2001).

    CAS  PubMed  Google Scholar 

  206. Baird, R. W. & Dill, L. M. Ecological and social determinants of group size in transient killer whales. Behav. Ecol. 7, 408–416 (1996).

    Google Scholar 

  207. Brent, L. J. et al. Ecological knowledge, leadership, and the evolution of menopause in killer whales. Curr. Biol. 25, 746–750 (2015).

    CAS  PubMed  Google Scholar 

  208. Fox, K. C., Muthukrishna, M. & Shultz, S. The social and cultural roots of whale and dolphin brains. Nat. Ecol. Evol. 1, 1699–1705 (2017).

    PubMed  Google Scholar 

  209. Guinet, C. Intentional stranding apprenticeship and social play in killer whales (Orcinus orca). Can. J. Zool. 69, 2712–2716 (1991).

    Google Scholar 

  210. Hoelzel, A. R. et al. Evolution of population structure in a highly social top predator, the killer whale. Mol. Biol. Evol. 24, 1407–1415 (2007).

    CAS  PubMed  Google Scholar 

  211. Apprill, A. et al. Humpback whale populations share a core skin bacterial community: towards a health index for marine mammals? PLoS ONE 9, e90785 (2014).

    PubMed  PubMed Central  Google Scholar 

  212. Bik, E. M. et al. Marine mammals harbor unique microbiotas shaped by and yet distinct from the sea. Nat. Commun. 7, 10516 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  213. Dudek, N. K. et al. Novel microbial diversity and functional potential in the marine mammal oral microbiome. Curr. Biol. 27, 3752–3762 (2017).

    CAS  PubMed  Google Scholar 

  214. Sanders, J. G. et al. Baleen whales host a unique gut microbiome with similarities to both carnivores and herbivores. Nat. Commun. 6, 8285 (2015).

    CAS  PubMed  Google Scholar 

  215. Orkin, J. D. et al. Seasonality of the gut microbiota of free-ranging white-faced capuchins in a tropical dry forest. ISME J. 13, 183–196 (2019).

    CAS  PubMed  Google Scholar 

  216. Li, H. et al. Pika population density is associated with the composition and diversity of gut microbiota. Front. Microbiol. 7, 758 (2016).

    PubMed  PubMed Central  Google Scholar 

  217. Escallón, C., Belden, L. K. & Moore, I. T. The cloacal microbiome changes with the breeding season in a wild bird. Integt. Organismal Biol. 1, oby009 (2019).

    Google Scholar 

  218. Kimura, M. Evolutionary rate at the molecular level. Nature 217, 624–626 (1968).

    CAS  PubMed  Google Scholar 

  219. Borthagaray, A. I., Berazategui, M. & Arim, M. Disentangling the effects of local and regional processes on biodiversity patterns through taxon‐contingent metacommunity network analysis. Oikos 124, 1383–1390 (2015).

    Google Scholar 

  220. Milani, C. et al. Tracing mother–infant transmission of bacteriophages by means of a novel analytical tool for shotgun metagenomic datasets: METAnnotatorX. Microbiome 6, 145 (2018).

    PubMed  PubMed Central  Google Scholar 

  221. Rheinbaben, F. V., Schünemann, S., Gross, T. & Wolff, M. H. Transmission of viruses via contact in a household setting: experiments using bacteriophage φX174 as a model virus. J. Hosp. Infect. 46, 61–66 (2000).

    CAS  PubMed  Google Scholar 

  222. Seed, K. D. et al. Evolutionary consequences of intra-patient phage predation on microbial populations. eLife 3, e03497 (2014).

    PubMed  PubMed Central  Google Scholar 

  223. Mirzaei, M. K. et al. Bacteriophages isolated from stunted children can regulate gut bacterial communities in an age-specific manner. Cell Host Microbe 27, 199–212 (2020).

    Google Scholar 

Download references

Acknowledgements

We thank C. Allen-Blevins, V. Bentley-Condit, J. Diaz, C. Diggins, K. Eappen, A. Reese, E. Venable and F. Young for helpful discussion and feedback on earlier drafts of this manuscript. A.S., S.H. and R.I.M.D. declare no research funding. K.V.-A.J.’s research has been supported by the Biotechnology and Biological Sciences Research Council (BB/J014427/1). A.H.M.’s research has been supported by the College of Agriculture and Life Sciences at Cornell University and by a Miller Research Fellowship from the Miller Institute for Basic Research in Science at the University of California, Berkeley. E.A.A.’s research has been supported by funds from the National Science Foundation (DEB 1840223 and IOS 1053461). L.D.S.’s research has been supported by the William F. Milton Fund, Harvard Dean’s Competitive Fund for Promising Scholarship, and a Graduate Research Fellowship from the National Science Foundation. R.N.C.’s research has been supported by the National Science Foundation (BCS-1919892), National Institutes of Health (R01AG049395), William F. Milton Fund, and the Harvard Dean’s Competitive Fund for Promising Scholarship. T.H.C.-B.’s research has been supported by the European Research Council (742808). P.W.J.B.’s research has been supported by the Biotechnology and Biological Sciences Council Industrial Partnership Award (BB/I006311/1), and research funds from Clasado Biosciences Ltd.

Author information

Authors and Affiliations

Authors

Contributions

A.S. developed the general concept and wrote the first draft of the manuscript. K.V.-A.J. substantially edited the content at all stages. S.H. and A.H.M. contributed text and hypotheses to the manuscript throughout its preparation. E.A.A., L.D.S., R.N.C., T.H.C.-B., R.I.M.D. and P.W.J.B. contributed revisions, ideas, text and examples. S.H. drafted the figures, with A.S., K.V.-A.J., A.H.M., E.A.A. and R.N.C. providing input. All authors approved the final manuscript for submission.

Corresponding author

Correspondence to Amar Sarkar.

Ethics declarations

Competing interests

Some of P.W.J.B.’s microbiome-related research has been supported by Clasado Biosciences Ltd. The remaining authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sarkar, A., Harty, S., Johnson, K.VA. et al. Microbial transmission in animal social networks and the social microbiome. Nat Ecol Evol 4, 1020–1035 (2020). https://doi.org/10.1038/s41559-020-1220-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-020-1220-8

Further reading

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing