How lemur social networks shape microbial transmission

This post is by UT Austin graduate student Amanda Perofsky.

Amanda Perofsky holding a sedated Verraux’s sifaka in 2012. The Sifaka Research Project at Ankoatsifaka Research Station captures animals periodically to mark them with collars, monitor health, and collect genetic material.

Primates exhibit diverse ecological and behavioral patterns, ranging from solitary foragers to several hundred individuals, as in the multi-level societies of hamadryas baboons [1]. Many wild primates live in social groups that range from stable to highly fluid, and this has important implications for the transmission of viruses, bacteria, and parasites between individuals. Several studies have demonstrated that host contact patterns alter the course of disease spread in wildlife populations [e.g., 2–6]. However, the effects of social contacts on commensal and mutualistic microorganisms, such as the mammalian gut microbiome, are just beginning to be appreciated [e.g., 3–5].

As a PhD student in Dr. Lauren Ancel Meyers’ research group at UT-Austin, my research aims to better understand the impact of primate social behavior on susceptibility to intestinal bacteria, and to identify factors that shape the gut microbiomes of individuals, social groups, and populations. In particular, I study Verreaux’s sifaka (Propithecus verreauxi), an endangered lemur species, in close collaboration with Dr. Rebecca Lewis, a primatologist in the Department of Anthropology at UT. Verreaux’s sifaka, like all lemurs, are unique to Madagascar, an island country off the southeastern coast of Africa. Dr. Lewis has studied sifaka behavior for over twenty years and directs the Ankoatsifaka Research Station located in Kirindy Mitea National Park in southwestern Madagascar. To distinguish between individuals, Dr. Lewis has fitted the sifaka at her field site with nylon collars and tags. One adult female in each social group has a radio collar, which enables researchers to locate specific groups in the forest using a radio transmitter.

A sifaka social group sunbathing in Kirindy Mitea National Park, Madagascar.

Sifaka live in small, tight-knit social groups that feed, sleep, rest, and travel together. Physical contact that promotes bacteria transmission may occur when sifaka groom each other, co-feed in trees, and huddle together. Within a social group, some pairs spend more time grooming each other than others [10]. Because sifaka (like all lemurs) groom with their mouths and toothcombs, do close grooming partners exchange intestinal bacteria more frequently compared to sifaka that rarely interact? Additionally, some individuals groom everyone in their social group, whereas others have only one or two close relationships. Are these highly social sifaka exposed to a greater diversity of microbes?

An unmarked sifaka grooms an adult female with infant nursing.

To answer these questions, I examine both sifaka social network structure and bacterial communities in sifaka fecal samples. Based on the behavioral data recorded by Dr. Lewis and her field assistants, I construct social network models that represent potential microbe-transmitting social contacts that occur within and between social groups. Social network models provide an intuitive framework for visualizing a population as a set of individuals (or, “nodes”) connected by “edges” [11] that, in this context, represent pathways for bacteria transmission.

In 2012, I traveled to Madagascar to collect fecal samples from each sifaka in the Ankoatsifaka study population and will be returning this summer to collect more samples. Each morning, we use a radio transmitter to locate the social group we’ll be following for the day. Collecting the fecal samples can be exasperating at times, and I couldn’t have accomplished my 2012 field season without the generous help of my collaborator, Elvis Rakatomalala, a Malagasy PhD student at the University of Antananarivo. Even with two people, it can be difficult to follow a large social group when the lemurs are jumping away in every direction and defecating all at the same time in different places. The fecal pellets scatter as they hit branches and leaves on the way down to the ground. We then crawl on our hands and knees through scratchy thorns, looking for pellets the size of Tic Tacs in the leaf litter. Once we locate a sample, we record the GPS point, the date, and the sifaka’s identity, and then put the pellets in a tube with liquid that preserves the DNA. The rest of the research— DNA extraction, bacteria sequencing, and data analysis— takes place back at UT.

After describing my fieldwork as difficult at times, why would I travel across the world to collect lemur fecal samples? Although collecting lemur fecal samples isn’t always easy, I love working outside surrounded by the forest,, and it’s fascinating to observe animals that can’t be found anywhere else in the world. Being in the field and collecting the samples myself gives me a deeper intuition for sifaka social behavior and its potential epidemiological consequences, providing insights that wouldn’t occur to me if I were at my desk in Austin.

  1. Griffin, R. H. & Nunn, C. L. 2011 Community structure and the spread of infectious disease in primate social networks. Evolutionary Ecology 26, 779–800.
  2. Böhm, M., Palphramand, K. L., Newton-Cross, G., Hutchings, M. R. & White, P. C. L. 2008 Dynamic interactions among badgers: implications for sociality and disease transmission. Journal of Animal Ecology 77, 735–745.
  3. Hamede, R. K., Bashford, J., McCallum, H. & Jones, M. 2009 Contact networks in a wild Tasmanian devil (Sarcophilus harrisii) population: using social network analysis to reveal seasonal variability in social behaviour and its implications for transmission of devil facial tumour disease. Ecology letters 12, 1147–57.
  4. Clay, C. A., Lehmer, E. M., Previtali, A., St Jeor, S. & Dearing, M. D. 2009 Contact heterogeneity in deer mice: implications for Sin Nombre virus transmission. Proceedings of the Royal Society B-Biological Sciences 276, 1305–1312.
  5. Craft, M. E., Volz, E., Packer, C. & Meyers, L. A. 2011 Disease transmission in territorial populations: the small-world network of Serengeti lions. Journal of the Royal Society Interface 8, 776–86.
  6. Rushmore, J., Caillaud, D., Matamba, L., Stumpf, R. M., Borgatti, S. P. & Altizer, S. 2013 Social network analysis of wild chimpanzees provides insights for predicting infectious disease risk. The Journal of Animal Ecology , 976–986.
  7. Tung, J., Barreiro, L. B., Burns, M. B., Grenier, J.-C., Lynch, J., Grieneisen, L. E., Altmann, J., Alberts, S. C., Blekhman, R. & Archie, E. A. 2015 Social networks predict gut microbiome composition in wild baboons. eLife 4.
  8. Moeller, A., Foerster, S., Wilson, M., Pusey, A., Hahn, B. & Ochman, H. 2016 Social behavior shapes the chimpanzee pan-microbiome. Science Advances.
  9. Bull, C. M., Godfrey, S. S. & Gordon, D. M. 2012 Social networks and the spread of Salmonella in a sleepy lizard population. Molecular Ecology 21, 4386–4392.
  10. Lewis, R. J. 2010 Grooming patterns in Verreaux’s sifaka. American Journal of Primatology 72, 254–261.
  11. Newman, M. 2010 Networks: An Introduction. Oxford University Press.


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