One of the great enduring mysteries in disease ecology is the timing of the AIDS pandemic. AIDS emerged as a clinical entity in the late 1970s, but HIV-1, the retrovirus that causes pandemic AIDS, entered the human population from wild primates many decades earlier, probably near the turn of the 20th century. Where was HIV during this long interval? We propose a novel ecological model for the delayed emergence of AIDS. Conceptually, in a metapopulation consisting of multiple, loosely interconnected sub-populations, a pathogen could persist at low levels indefinitely through a dynamic balance between localized transmission, localized extinction, and long-distance migration between sub-populations. This situation might accurately describe a network of villages in which population sizes are small and rates of migration are low, as would have been the case in Sub-Saharan Africa over a century ago. We will test our model in a highly relevant non-human primate system. In 2009, we documented three simian retroviruses co-circulating in a metapopulation of wild red colobus monkeys (Procolobus rufomitratus) in Kibale National Park, Uganda, where we have conducted research for over two decades. We will collect detailed data on social interactions, demography, health, and infection from animals in a core social group. We will also study a series of 20 red colobus sub-populations, each inhabiting a separate, isolated forest fragment. We will determine the historic connectivity of these sub-populations using a time series of remotely sensed images of forest cover going back to 1955, as well as using population genetic analyses of hypervariable nuclear DNA markers. We will assess the infection status of each animal over time and use viral molecular data to reconstruct transmission pathways. Our transmission models will define the necessary conditions for a retrovirus to persist, but they will not be sufficient to explain why a retrovirus might emerge. This is because human social factors ultimately create the conditions that allow zoonotic diseases to be transmitted from animal reservoirs and to spread. We will therefore conduct an integrated analysis of the root eco-social drivers of human-primate contact and zoonotic transmission in this system. We will study social networks to understand how social resources structure key activities relevant to human-primate contact and zoonotic transmission risk, and we will explore knowledge, beliefs, and perceptions of human-primate contact and disease transmission for a broad sample of the population. We will reconcile perceived risk with actual risk through a linked human health survey and diagnostic testing for zoonotic primate retroviruses. The ultimate product of our research will a data-driven set of transmission models to explain the long-term persistence of retroviruses within a metapopulation of hosts, as well as a linked analysis of how human social factors contribute to zoonotic infection risk in a relevant Sub-Saharan African population. Our study will elucidate not only the origins of HIV/AIDS, but also how early-stage zoonoses in general progress from "smoldering" subclinical infections to full-fledged pandemics.

Public Health Relevance

AIDS emerged as a pandemic long after HIV entered the human population from African primates, but the reasons for this delayed emergence are unknown. This project will examine the transmission of simian retroviruses in Ugandan monkeys in order to understand how primate behavior and ecology allow the long-term persistence and eventual emergence of these important pathogens. Through linked studies of local people, the project will identify how human social factors contribute to the cross-species transmission of simian retroviruses, thus providing critical information for preventing the future emergence of primate-borne diseases.

National Institute of Health (NIH)
National Institute of Allergy and Infectious Diseases (NIAID)
Research Project (R01)
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Special Emphasis Panel (ZRG1-BDCN-T (80))
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Sharma, Opendra K
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University of Wisconsin Madison
Schools of Veterinary Medicine
United States
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Paige, Sarah B; Malavé, Carly; Mbabazi, Edith et al. (2015) Uncovering zoonoses awareness in an emerging disease 'hotspot'. Soc Sci Med 129:78-86
Ghai, Ria R; Chapman, Colin A; Omeja, Patrick A et al. (2014) Nodule worm infection in humans and wild primates in Uganda: cryptic species in a newly identified region of human transmission. PLoS Negl Trop Dis 8:e2641
Bailey, Adam L; Lauck, Michael; Weiler, Andrea et al. (2014) High genetic diversity and adaptive potential of two simian hemorrhagic fever viruses in a wild primate population. PLoS One 9:e90714
Sibley, Samuel D; Lauck, Michael; Bailey, Adam L et al. (2014) Discovery and characterization of distinct simian pegiviruses in three wild African Old World monkey species. PLoS One 9:e98569
Paige, Sarah B; Frost, Simon D W; Gibson, Mhairi A et al. (2014) Beyond bushmeat: animal contact, injury, and zoonotic disease risk in Western Uganda. Ecohealth 11:534-43
Miyamoto, Michael M; Allen, Julie M; Gogarten, Jan F et al. (2013) Microsatellite DNA suggests that group size affects sex-biased dispersal patterns in red colobus monkeys. Am J Primatol 75:478-90
Thurber, Mary I; Ghai, Ria R; Hyeroba, David et al. (2013) Co-infection and cross-species transmission of divergent Hepatocystis lineages in a wild African primate community. Int J Parasitol 43:613-9
Lauck, Michael; Sibley, Samuel D; Lara, James et al. (2013) A novel hepacivirus with an unusually long and intrinsically disordered NS5A protein in a wild Old World primate. J Virol 87:8971-81
Chapman, Colin A; Bonnell, Tyler R; Sengupta, Raja et al. (2013) Is Markhamia lutea's abundance determined by animal foraging? For Ecol Manage 308:
Salyer, Stephanie J; Gillespie, Thomas R; Rwego, Innocent B et al. (2012) Epidemiology and molecular relationships of Cryptosporidium spp. in people, primates, and livestock from Western Uganda. PLoS Negl Trop Dis 6:e1597