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How do social and demographic processes control epidemic dynamics?

Subject Area Ecology and Biodiversity of Animals and Ecosystems, Organismic Interactions
Epidemiology and Medical Biometry/Statistics
Theoretical Chemistry: Molecules, Materials, Surfaces
Term from 2014 to 2018
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 263713275
 
Final Report Year 2018

Final Report Abstract

Fundamental processes and key transmission mechanisms underlying disease dynamics in free-ranging populations are little known. Important, yet neglected issues are the effects of individual behaviour and social rank on disease dynamics in hierarchically and spatially structured populations and the molecular, immunological and demographic factors that mediate long-term host-pathogen evolutionary dynamics within ecosystems. Our study system is canine distemper virus (CDV) in spotted hyenas as the host in the Serengeti ecosystem. CDV is an important carnivore disease which is related to measles virus in humans. It has caused significant mortality in Serengeti wild carnivores, including spotted hyenas. By combining long-term data on CDV prevalence and the molecular characteristics of the prevailing strains with more than 26 years of detailed individual demographic and social data on the host, we had a unique opportunity to study demographic and disease dynamics in concert. We proposed to use the whole palette of ecological modelling to explore the wealth of our long-term field data set: from descriptive, statistical analyses of contact rates in a social animal and disease courses via mathematical models to individual-based spatially-explicit simulation models. First, we centered around separating the influence of variation in virus exposure and resource allocation to immune processes on CDV infection probability. With our multi-event capturemark-recapture modeling approach extended to SIR disease states, it was possible to test for an effect of social status on both the likelihood of pathogen exposure and contracting the disease. We demonstrated fitness costs of infection for juveniles, particularly for those with low social status, and showed that patterns of infection can be driven by different mechanisms among juveniles and adults. Second, we developed a stage-structured matrix population model to determine the demographic responses of the spotted hyena to the virulent epidemic of canine distemper virus (CDV) in the Serengeti ecosystem in 1993/1994. Using detailed longitudinal data from 625 known hyenas, we demonstrated that although the population was relatively resistant to the novel CDV genotype present, recovery was slow. Interestingly, high-ranking females had a substantially higher reproductive value, buffering the impact of the epidemic as well as accelerating the population’s recovery. Third, we developed a conceptual model using an individual-based spatially implicit model to explore the question to which extent the contact network structure, specifically the case where ‘kids are kept at home’ and do not come into contact with subadult or adult members of other social groups, buffers against long-term impacts of infectious diseases by forming an immunity barrier around susceptible offspring. We found, more specifically, that the immunity barrier increased the probability of epidemic fadeout in highly social species living in large group size. We conclude that communal nurseries in social animals could potentially be an adaptation against infectious diseases, a hypothesis that has so far never been suggested. Our project results provided new insights on disease dynamics in mixed local networks of individuals, especially on the impact of maternal social status and spatial distribution on disease dynamics, which is a key contribution to epidemiological theory.

Publications

  • (2017). Canine distemper virus in the Serengeti ecosystem: molecular adaptation to different carnivore species. Molecular Ecology, 26(7): 2111–2130
    Nikolin V.M., Olarte‐Castillo X.A., Osterrieder N., Hofer H., Dubovi E., Mazzoni C.M., Brunner E., Goller K.V., Fyumagwa R.D., Moehlman P.D., Thierer D & M.L. East
    (See online at https://doi.org/10.1111/mec.13902)
  • (2018). Robustness of eco-epidemiological capture-recapture parameter estimates to variation in infection state uncertainty. Frontiers in Vetereinary Science, Vol. 5. 2018, 197.
    Benhaiem S., Marescot L., Hofer H., East M.L., Lebreton J.-D., Kramer-Schadt S. & Gimenez O.
    (See online at https://doi.org/10.3389/fvets.2018.00197)
  • (2018). Slow recovery from a disease epidemic in the spotted hyena, a keystone social carnivore. Communications Biology, Vol. 1. 2018, 201.
    Benhaiem S., Marescot L., East M.L., Kramer-Schadt S., Gimenez O., Lebreton J.D. & Hofer H.
    (See online at https://doi.org/10.1038/s42003-018-0197-1)
  • (2018). Social status mediates the fitness costs of infection with canine distemper virus in Serengeti spotted hyenas. Functional Ecology 2018:1-14
    Marescot L., Benhaiem S., Gimenez O., Hofer H., Lebreton J.D., Olarte-Castillo X.A., Kramer- Schadt S. & M.L. East
    (See online at https://doi.org/10.1111/1365-2435.13059)
  • (2021). Keeping the kids at home can limit the persistence of contagious pathogens in social animals. Journal of Animal Ecology, Vol. 90. 2021, Issue 11, pp. 2523-2535.
    Marescot L., Franz M., Benhaiem S., Hofer H., Scherer C., East M.L. & Kramer-Schadt S.
    (See online at https://doi.org/10.1111/1365-2656.13555)
 
 

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