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.

  • Article
  • Published:

Coordinated change at the colony level in fruit bat fur microbiomes through time

Nature Ecology & Evolution volume 3, pages 116–124 (2019)Cite this article

Subjects

Abstract

The host-associated microbiome affects individual health and behaviour, and may be influenced by local environmental conditions. However, little is known about microbiomes’ temporal dynamics in free-living species compared with their dynamics in humans and model organisms, especially in body sites other than the gut. Here, we investigate longitudinal changes in the fur microbiome of captive and free-living Egyptian fruit bats. We find that, in contrast to patterns described in humans and other mammals, the prominent dynamics is of change over time at the level of the colony as a whole. On average, a pair of fur microbiome samples from different individuals in the same colony collected on the same date are more similar to one another than a pair of samples from the same individual collected at different time points. This pattern suggests that the whole colony may be the appropriate biological unit for understanding some of the roles of the host microbiome in social bats’ ecology and evolution. This pattern of synchronized colony changes over time is also reflected in the profile of volatile compounds in the bats’ fur, but differs from the more individualized pattern found in the bats’ gut microbiome.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Microbial composition of fur and gut samples.
Fig. 2: The prominent pattern in the fur microbiome is that of colony-level change over time.
Fig. 3: Similarity of pairs of samples in the captive colony, from the same individual or from the same date.
Fig. 4: In the gut, sex and individual identity are the primary factors that determine microbiome composition.
Fig. 5: Colony and individual-level patterns in profiles of volatile compounds.

Similar content being viewed by others

Data availability

All data used in this study has been uploaded to SRA at NCBI, and can be found under Bioproject PRJNA494618 (biosample accession numbers: SAMN10226814–SAMN10227267 and SAMN10174956–SAMN10175066).

References

  1. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Sharon, G. et al. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc. Natl Acad. Sci. USA 107, 20051–20056 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Hooper, L. V., Littman, D. R. & Macpherson, A. J. Interactions between the microbiota and the immune system. Science 336, 1268–1273 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Bravo, J. A. et al. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc. Natl Acad. Sci. USA 108, 16050–16055 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. O’Mahony, S. M., Clarke, G., Borre, Y. E., Dinan, T. G. & Cryan, J. F. Serotonin, tryptophan metabolism and the brain–gut–microbiome axis. Behav. Brain Res. 277, 32–48 (2015).

    Article  PubMed  CAS  Google Scholar 

  7. Forsythe, P., Bienenstock, J. & Kunze, W. A. in Microbial Endocrinology: The Microbiota–Gut–Brain Axis in Health and Disease 115–133 (Springer, New York, 2014).

  8. Foster, J. A. & Neufeld, K.-A. M. Gut–brain axis: how the microbiome influences anxiety and depression. Trends Neurosci. 36, 305–312 (2013).

    Article  CAS  PubMed  Google Scholar 

  9. Troyer, K. Behavioral acquisition of the hindgut fermentation system by hatchling Iguana iguana. Behav. Ecol. Sociobiol. 14, 189–193 (1984).

    Article  Google Scholar 

  10. Muegge, B. D. et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science 332, 970–974 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Ley, R. E. et al. Evolution of mammals and their gut microbes. Science 320, 1647–1651 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  13. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  15. 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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  17. Albone, E. S., Gosden, P. E., Ware, G. C., Macdonald, D. W. & Hough, N. G. Bacterial action and chemical signalling in the red fox (Vulpes vulpes) and other mammals. In Flavor Chemistry of Animal Foods 78–91 (ACS Symposium Series Volume 67, ACS Publications, 1978).

  18. Albone, E. S., Eglinton, G., Walker, J. M. & Ware, G. C. The anal sac secretion of the red fox (Vulpes vulpes); its chemistry and microbiology. A comparison with the anal sac secretion of the lion (Panthera leo). Life Sci. 14, 387–400 (1974).

    Article  CAS  PubMed  Google Scholar 

  19. 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).

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Caporaso, J. G. et al. Moving pictures of the human microbiome. Genome. Biol. 12, R50 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  22. Faith, J. J. et al. The long-term stability of the human gut microbiota. Science 341, 1237439 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Flores, G. E. et al. Temporal variability is a personalized feature of the human microbiome. Genome Biol. 15, 531 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Costello, E. K. et al. Bacterial community variation in human body habitats across space and time. Science 326, 1694–1697 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. The Human Microbiome Project Consortium Structure, function and diversity of the healthy human microbiome. Nature 486, 207–214 (2012).

  26. Oh, J. et al. Temporal stability of the human skin microbiome. Cell 165, 854–866 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Grice, E. A. & Segre, J. A. The skin microbiome. Nat. Rev. Microbiol. 9, 244–253 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Grice, E. A. et al. Topographical and temporal diversity of the human skin microbiome. Science 324, 1190–1192 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  31. Voigt, C. C., Caspers, B. & Speck, S. Bats, bacteria, and bat smell: sex-specific diversity of microbes in a sexually selected scent organ. J. Mammal. 86, 745–749 (2005).

    Article  Google Scholar 

  32. Voigt, C. C. & von Helversen, O. Storage and display of odour by male Saccopteryx bilineata (Chiroptera, Emballonuridae). Behav. Ecol. Sociobiol. 47, 29–40 (1999).

    Article  Google Scholar 

  33. Theis, K. R. et al. Symbiotic bacteria appear to mediate hyena social odors. Proc. Natl Acad. Sci. USA 110, 19832–19837 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Theis, K. R., Venkataraman, A., Wagner, A. P., Holekamp, K. E. & Schmidt, T. M. in Chemical Signals in Vertebrates 13 87–103 (Springer, Cham, 2016).

  35. Harten, L. et al. Persistent producer–scrounger relationships in bats. Sci. Adv. 4, e1603293 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  36. Clayton, J. B. et al. Captivity humanizes the primate microbiome. Proc. Natl Acad. Sci. USA 113, 10376–10381 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Nelson, T. M., Rogers, T. L., Carlini, A. R. & Brown, M. V. Diet and phylogeny shape the gut microbiota of Antarctic seals: a comparison of wild and captive animals. Environ. Microbiol. 15, 1132–1145 (2013).

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  39. Kohl, K. D., Skopec, M. M. & Dearing, M. D. Captivity results in disparate loss of gut microbial diversity in closely related hosts.Conserv. Physiol. 2, cou009 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  40. Kohl, K. D. & Dearing, M. D. Wild‐caught rodents retain a majority of their natural gut microbiota upon entrance into captivity. Environ. Microbiol. Rep. 6, 191–195 (2014).

    Article  PubMed  Google Scholar 

  41. Lloyd-Price, J. et al. Strains, functions and dynamics in the expanded Human Microbiome Project. Nature 550, 61–66 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Ayorinde, F., Wheeler, J. W., Wemmer, C. & Murtaugh, J. Volatile components of the occipital gland secretion of the bactrian camel (Camelus bactrianus). J. Chem. Ecol. 8, 177–183 (1982).

    Article  CAS  PubMed  Google Scholar 

  43. Mattina, M. J. I., Pignatello, J. J. & Swihart, R. K. Identification of volatile components of bobcat (Lynx rufus) urine. J. Chem. Ecol. 17, 451–462 (1991).

    Article  CAS  PubMed  Google Scholar 

  44. Martín, J., Barja, I. & López, P. Chemical scent constituents in feces of wild Iberian wolves (Canis lupus signatus). Biochem. Syst. Ecol. 38, 1096–1102 (2010).

    Article  CAS  Google Scholar 

  45. Simpson, J. T., Weldon, P. J. & Sharp, T. R. Identification of major lipids from the scent gland secretions of Dumeril’s ground boa (Acrantophis dumerili Jan) by gas chromatography-mass spectrometry. Z. Naturforsch C 43, 914–917 (1988).

    Article  CAS  PubMed  Google Scholar 

  46. Soini, H. A. et al. Investigation of scents on cheeks and foreheads of large felines in connection to the facial marking behavior. J. Chem. Ecol. 38, 145–156 (2012).

    Article  CAS  PubMed  Google Scholar 

  47. Apps, P., Mmualefe, L. & McNutt, J. W. Identification of volatiles from the secretions and excretions of African wild dogs (Lycaon pictus). J. Chem. Ecol. 38, 1450–1461 (2012).

    Article  CAS  PubMed  Google Scholar 

  48. Khannoon, E. R. R. Secretions of pre-anal glands of house-dwelling geckos (Family: Gekkonidae) contain monoglycerides and 1,3-alkanediol. A comparative chemical ecology study. Biochem. Syst. Ecol. 44, 341–346 (2012).

    Article  CAS  Google Scholar 

  49. Kim, H. B. et al. Longitudinal investigation of the age-related bacterial diversity in the feces of commercial pigs. Vet. Microbiol. 153, 124–133 (2011).

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Mueller, N. T., Bakacs, E., Combellick, J., Grigoryan, Z. & Dominguez-Bello, M. G. The infant microbiome development: mom matters. Trends Mol. Med. 21, 109–117 (2015).

    Article  PubMed  Google Scholar 

  52. Lemieux-Labonté, V., Tromas, N., Shapiro, B. J. & Lapointe, F.-J. Environment and host species shape the skin microbiome of captive neotropical bats. PeerJ 4, e2430 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  53. Avena, C. V. et al. Deconstructing the bat skin microbiome: influences of the host and the environment. Front. Microbiol. 7, 1753 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  54. Winter, A. S. et al. Skin and fur bacterial diversity and community structure on American southwestern bats: effects of habitat, geography and bat traits. PeerJ 5, e3944 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  55. Hicks, A. L. et al. Gut microbiomes of wild great apes fluctuate seasonally in response to diet. Nat. Commun. 9, 1786 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. 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 (2017).

    Article  PubMed  Google Scholar 

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

    Article  PubMed Central  Google Scholar 

  59. Smith, I. & Wang, L.-F. Bats and their virome: an important source of emerging viruses capable of infecting humans. Curr. Opin. Virol. 3, 84–91 (2013).

    Article  PubMed  Google Scholar 

  60. Luis, A. D. et al. A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special?. Proc. R. Soc. B 280, 20122753 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  61. Hayman, D. T. S. et al. Ecology of zoonotic infectious diseases in bats: current knowledge and future directions. Zoonoses Public Health 60, 2–21 (2013).

    Article  CAS  PubMed  Google Scholar 

  62. Calisher, C. H., Childs, J. E., Field, H. E., Holmes, K. V. & Schountz, T.Bats: important reservoir hosts of emerging viruses.Clin. Microbiol. Rev. 19, 531–545 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  63. Dietrich, M., Kearney, T., Seamark, E. C. J. & Markotter, W.The excreted microbiota of bats: evidence of niche specialisation based on multiple body habitats.FEMS Microbiol. Lett. 364, fnw284 (2017).

    Article  PubMed  CAS  Google Scholar 

  64. Hoyt, J. R. et al. Bacteria isolated from bats inhibit the growth of Pseudogymnoascus destructans, the causative agent of white-nose syndrome. PLoS ONE 10, e0121329 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. Vanderwolf, K. J., Malloch, D. & McAlpine, D. F.Fungi on white-nose infected bats (Myotis spp.) in Eastern Canada show no decline in diversity associated with Pseudogymnoascus destructans (Ascomycota: Pseudeurotiaceae). Int. J. Speleol. 45, 43–50 (2016).

    Article  Google Scholar 

  66. Blehert, D. S. et al. Bat white-nose syndrome: an emerging fungal pathogen? Science 323, 227 (2009).

    Article  CAS  PubMed  Google Scholar 

  67. Leopardi, S., Blake, D. & Puechmaille, S. J. White-nose syndrome fungus introduced from Europe to North America. Curr. Biol. 25, R217–R219 (2015).

    Article  CAS  PubMed  Google Scholar 

  68. Zilber‐Rosenberg, I. & Rosenberg, E. Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol. Rev. 32, 723–735 (2008).

    Article  PubMed  CAS  Google Scholar 

  69. Theis, K. R. et al. Getting the hologenome concept right: an eco-evolutionary framework for hosts and their microbiomes. mSystems 1, e00028-16 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  70. Dinsdale, E. A. et al. Functional metagenomic profiling of nine biomes. Nature 452, 629–632 (2008).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Doolittle, W. F. & Inkpen, S. A. Processes and patterns of interaction as units of selection: an introduction to ITSNTS thinking. Proc. Natl Acad. Sci. USA 115, 4006–4014 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Moran, N. A. & Sloan, D. B. The hologenome concept: helpful or hollow? PLoS Biol. 13, e1002311 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Dugatkin, L. A. & Reeve, H. K. Behavioral ecology and levels of selection: dissolving the group selection controversy. Adv. Study Behav. 23, 101–133 (1994).

    Article  Google Scholar 

  75. Gould, S. J. & Lloyd, E. A. Individuality and adaptation across levels of selection: how shall we name and generalize the unit of Darwinism? Proc. Natl Acad. Sci. USA 96, 11904–11909 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Tedman, R. A. & Hall, L. S. The morphology of the gastrointestinal tract and food transit time in the fruit bats Pteropus alecto and P. poliocephalus (Megachiroptera). Aust. J. Zool. 33, 625–640 (1985).

    Article  Google Scholar 

  77. Utzurrum, R. C. B. & Heideman, P. D. Differential ingestion of viable vs nonviable Ficus seeds by fruit bats. Biotropica 23, 311–312 (1991).

    Article  Google Scholar 

  78. Zhang, J., Kobert, K., Flouri, T. & Stamatakis, A. PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30, 614–620 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  79. Caporaso, J. G. et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335–336 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Rognes, T., Flouri, T., Nichols, B., Quince, C. & Mahé, F. VSEARCH: a versatile open source tool for metagenomics. PeerJ 4, e2409v1 (2016).

    Article  Google Scholar 

  81. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank A. Letten, P.-J. Ke, M. Donald, N. Dudek, W. Van Treuen, L. Costello, M. Maor, T. Simon and E. Ebel for technical help and insightful comments. O.K. is supported by the John Templeton Foundation and Stanford Center for Computational, Evolutionary, and Human Genomics. This research was partially supported by the European Research Council (ERC–GPSBAT).

Author information

Author notes

  1. These authors contributed equally: Oren Kolodny, Maya Weinberg.

Authors and Affiliations

  1. Department of Biology, Stanford University, Stanford, CA, USA

    Oren Kolodny & Marcus W. Feldman

  2. Department of Ecology, Evolution and Behavior, The Hebrew University of Jerusalem, Jerusalem, Israel

    Oren Kolodny

  3. School of Zoology, Tel Aviv University, Tel Aviv, Israel

    Maya Weinberg, Lee Harten, Abraham Hefetz & Yossi Yovel

  4. School of Molecular Cell Biology and Biotechnology, Tel Aviv University, Tel Aviv, Israel

    Leah Reshef & Uri Gophna

  5. Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel

    Yossi Yovel

Authors
  1. Oren Kolodny
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maya Weinberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Leah Reshef
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lee Harten
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Abraham Hefetz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Uri Gophna
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marcus W. Feldman
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yossi Yovel
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

O.K., M.W., L.R. and Y.Y. planned the study, analysed the data and wrote the manuscript. M.W., L.R. and L.H. collected and processed the samples. All co-authors commented on the study design, data analysis and manuscript.

Corresponding authors

Correspondence to Oren Kolodny, Maya Weinberg or Yossi Yovel.

Ethics declarations

Competing interests

The 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.

Supplementary information

Supplementary Information

Supplementary Information Sections 1–8

Reporting Summary

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kolodny, O., Weinberg, M., Reshef, L. et al. Coordinated change at the colony level in fruit bat fur microbiomes through time. Nat Ecol Evol 3, 116–124 (2019). https://doi.org/10.1038/s41559-018-0731-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-018-0731-z

This article is cited by

Search

Advanced search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

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