Cole, M.F., Barnes, P., Monroe, I., Rukundo, J., Emery Thompson, M., & Rosati, A.G. (2024). Age-related physiological dysregulation progresses slowly in semi-free-ranging chimpanzees. Evolution, Medicine, and Public Health, 12: 129–142. [PDF] [Supplementary] [Publisher’s version]
Abstract
Background and objectives: Lifestyle has widespread effects on human health and aging. Prior results from chimpanzees, one of human’s closest evolutionary relatives, indicates that these lifestyle effects may also be shared with other species, as semi-free-ranging chimpanzees fed a naturalistic diet show healthier values in several specific health biomarkers, compared with their sedentary, captive counterparts. Here, we examined how lifestyle factors associated with different environments affect rates of physiological aging in closely related chimpanzees (Pan troglodytes). Methodology: We compared physiological dysregulation, an index of biological aging, in semi-free-ranging chimpanzees in an African sanctuary versus captive chimpanzees in US laboratories. If the rate of aging is accelerated by high-calorie diet and sedentism, we predicted greater age-related dysregulation in the laboratory populations. Conversely, if costs of a wild lifestyle accelerate aging, then semi-free-ranging chimpanzees at the sanctuary, whose environment better approximates the wild, should show greater age-related dysregulation. We further tested whether dysregulation differed based on sex or body system, as in humans. Results: We found that semi-free-ranging chimpanzees showed lower overall dysregulation, as well as lower age-related change in dysregulation, than laboratory chimpanzees. Males experienced lower dysregulation than females in both contexts, and the two populations exhibited distinct aging patterns based on body system. Conclusions and implications: Our results support the conclusion that naturalistic living conditions result in healthier aging in chimpanzees. These data provide support for the proposal that lifestyle effects on human health and aging are conserved from deeper in our evolutionary history.
Hernández-Pacheco, R., Steiner, U.K., Rosati, A.G., Tuljapurka, S. (2023). Advancing methods for the biodemography of aging within social contexts. Neuroscience and BioBehavioral Reviews, 153: 105400.
Several social dimensions including social integration, status, early-life adversity, and their interactions across the life course can predict health, reproduction, and mortality in humans. Accordingly, the social environment plays a fundamental role in the emergence of phenotypes driving the evolution of aging. Recent work placing human social gradients on a biological continuum with other species provides a useful evolutionary context for aging questions, but there is still a need for a unified evolutionary framework linking health and aging within social contexts. Here, we summarize current challenges to understand the role of the social environment in human life courses. Next, we review recent advances in comparative biodemography and propose a biodemographic perspective to address socially driven health phenotype distributions and their evolutionary consequences using a nonhuman primate population. This new comparative approach uses evolutionary demography to address the joint dynamics of populations, social dimensions, phenotypes, and life history parameters. The long-term goal is to advance our understanding of the link between individual social environments, population-level outcomes, and the evolution of aging.
Rosati, A.G., Sabbi, K.H., Bryer, M.A.H., Barnes, P., Rukundo, J., Mukungu, T., Sekulya, P., Ampeire, I., Aligumisiriza, H., Kyama, S., Masereka, J., Nabukeera, W., Okello, A., Waiga, B., Atwijuze, S., Camargo Peña, N., Cantwell, A., Felsche, E., Flores-Mendoza, K., Mohamed, S., Monroe, I., Mulhinch, M., O’Gorman, K., Salamango, J., Shamah, R., Otali, E., Wrangham, R.W., & Machanda, Z.P. (2023). Observational approaches to chimpanzee behavior in an African sanctuary: implications for research, welfare, and capacity-building. American Journal of Primatology, 85: e23534.
Research in African ape sanctuaries has emerged as an important context for our understanding of comparative cognition and behavior. While much of this work has focused on experimental studies of cognition, these animals semi-free-range in forest habitats and therefore can also provide important information about the behavior of primates in socioecologically-relevant naturalistic contexts. In this “New Approaches” article, we describe a project where we implemented a synthetic program of observational data collection at Ngamba Island Chimpanzee Sanctuary in Uganda, directly modeled after long-term data collection protocols at the Kibale Chimpanzee Project in Uganda, a wild chimpanzee field site. The foundation for this project was a strong partnership between sanctuary staff, field site staff, and external researchers. We describe how we developed a data-collection protocol through discussion and collaboration among these groups, and trained sanctuary caregivers to collect novel observational data using these protocols. We use these data as a case study to examine: (1) how behavioral observations in sanctuaries can inform primate welfare and care practices, such as by understanding aggression within the group; (2) how matched observational protocols across sites can inform our understanding of primate behavior across different contexts, including sex differences in social relationships; and (3) how more robust collaborations between foreign researchers and local partners can support capacity-building in primate range countries, along with mentoring and training students more broadly.
Dunay, E., Rukundo, J., Atencia, R., Cole, M.F., Cantwell, A., Emery Thompson, M., Rosati, A.G., Goldberg, T.L. (2023). Viruses in saliva from sanctuary chimpanzees (Pan troglodytes) in Republic of Congo and Uganda. PLoS One, 18: e0288007.
Pathogen surveillance for great ape health monitoring has typically been performed on non-invasive samples, primarily feces, in wild apes and blood in sanctuary-housed apes. However, many important primate pathogens, including known zoonoses, are shed in saliva and transmitted via oral fluids. Using metagenomic methods, we identified viruses in saliva samples from 46 wild-born, sanctuary-housed chimpanzees at two African sanctuaries in Republic of Congo and Uganda. In total, we identified 20 viruses. All but one, an unclassified CRESS DNA virus, are classified in five families: Circoviridae, Herpesviridae, Papillomaviridae, Picobirnaviridae, and Retroviridae. Overall, viral prevalence ranged from 4.2% to 87.5%. Many of these viruses are ubiquitous in primates and known to replicate in the oral cavity (simian foamy viruses, Retroviridae; a cytomegalovirus and lymphocryptovirus; Herpesviridae; and alpha and gamma papillomaviruses, Papillomaviridae). None of the viruses identified have been shown to cause disease in chimpanzees or, to our knowledge, in humans. These data suggest that the risk of zoonotic viral disease from chimpanzee oral fluids in sanctuaries may be lower than commonly assumed.
Dunay, E., Owens, L.A., Dunn, C.D., Rukundo, J., Atencia, R., Cole, M.F., Cantwell, A., Emery Thompson, M., Rosati, A.G., & Goldberg, T.L. (2023). Viruses in sanctuary chimpanzees across Africa. American Journal of Primatology, 85: e23452
Infectious disease is a major concern for both wild and captive primate populations. Primate sanctuaries in Africa provide critical protection to thousands of wild‐born, orphan primates confiscated from the bushmeat and pet trades. However, uncertainty about the infectious agents these individuals potentially harbor has important implications for their individual care and long‐term conservation strategies. We used metagenomic next‐generation sequencing to identify viruses in blood samples from chimpanzees (Pan troglodytes) in three sanctuaries in West, Central, and East Africa. Our goal was to evaluate whether viruses of human origin or other “atypical” or unknown viruses might infect these chimpanzees. We identified viruses from eight families: Anelloviridae, Flaviviridae, Genomoviridae, Hepadnaviridae, Parvoviridae, Picobirnaviridae, Picornaviridae, and Rhabdoviridae. The majority (15/26) of viruses identified were members of the family Anelloviridae and represent the genera Alphatorquevirus (torque teno viruses) and Betatorquevirus (torque teno mini viruses), which are common in chimpanzees and apathogenic. Of the remaining 11 viruses, 9 were typical constituents of the chimpanzee virome that have been identified in previous studies and are also thought to be apathogenic. One virus, a novel tibrovirus (Rhabdoviridae: Tibrovirus) is related to Bas‐Congo virus, which was originally thought to be a human pathogen but is currently thought to be apathogenic, incidental, and vector‐borne. The only virus associated with disease was rhinovirus C (Picornaviridae: Enterovirus) infecting one chimpanzee subsequent to an outbreak of respiratory illness at that sanctuary. Our results suggest that the blood‐borne virome of African sanctuary chimpanzees does not differ appreciably from that of their wild counterparts, and that persistent infection with exogenous viruses may be less common than often assumed.
Cole, M.F., Cantwell, A., Rukundo, J. Ajarova, L., Fernandez-Navarro, S., Atencia, R. & Rosati, A.G. (2020). Healthy cardiovascular biomarkers across the lifespan in wild-born chimpanzees (Pan troglodytes).Philosophical Transactions of the Royal Society B, 375: 20190609.
Chimpanzees (Pan troglodytes) are a crucial model for understanding the evolution of human health and longevity. Cardiovascular disease is a major source of mortality during aging in humans and therefore a key issue for comparative research. Current data indicates that compared to humans, chimpanzees have proatherogenic blood lipid profiles, an important risk factor for cardiovascular disease in humans. However, most work to date on chimpanzee lipids come from laboratory-living populations where lifestyles diverge from a wild context. Here we examined cardiovascular profiles in chimpanzees living in African sanctuaries, who semi-free-range in large forested enclosures, consume a naturalistic diet, and generally experience conditions more similar to a wild chimpanzee lifestyle. We measured blood lipids, body weight, and body fat in 75 sanctuary chimpanzees and compared them to publicly-available data from laboratory-living chimpanzees from the Primate Aging Database. We found that semi-free-ranging chimpanzees exhibited lower body weight and lower levels of lipids that are risk factors for human cardiovascular disease, and that some of these disparities increased with age. Our findings support the hypothesis that lifestyle can shape health indices in chimpanzees, similar to effects observed across human populations, and contribute to an emerging understanding of human cardiovascular health in evolutionary context.
Emery Thompson, M., Rosati, A.G., Snyder-Mackler, N. (2020). Insights from evolutionarily-relevant models for human ageing. Philosophical Transactions of the Royal Society B, 375: 20190605.
As the world confronts the health challenges of an aging population, there has been dramatically increased interest in the science of aging. This research has overwhelmingly focused on age-related disease, particularly in industrialized human populations and short-lived laboratory animal models. However, it has become clear that humans and long-lived primates age differently than many typical model organisms, and that many of the diseases causing death and disability in the developed world are greatly exacerbated by modern lifestyles. As such, research on how the human aging process evolved is vital to understanding the origins of prolonged human lifespan and factors increasing vulnerability to degenerative disease. In this issue, we highlight emerging comparative research on primates, highlighting the physical, physiological, behavioural, and cognitive processes of aging. This work comprises data and theory on non-human primates, as well as underrepresented data on humans living in small-scale societies, which help elucidate how environment shapes senescence. Component papers address (1) the critical processes that comprise senescence in long-lived primates; (2) the social, ecological, or individual characteristics that predict variation in the pace of aging; and (3) the complicated relationship between aging trajectories and disease outcomes. Collectively, this work provides essential comparative, evolutionary data on aging and demonstrates its unique potential to inform our understanding of the human aging process.
Stokes, R., Tully, G., & Rosati, A. G. (2018). Pan African Sanctuary Alliance: securing a future for the African great apes. International Zoo Yearbook, 52, 1-9.
The Pan African Sanctuary Alliance (PASA) is the unified voice of primate rescue and rehabilitation pro- jects in Africa, and includes 23 member organizations in 13 countries. PASA improves animal welfare by regularly evaluating these sanctuaries to ensure that they operate at a high standard of care, building the capacity of sanctuary staff and providing crisis support to mitigate emergencies. Moreover, PASA works with its member organizations to raise awareness globally about wildlife issues and to conduct other large-scale conservation projects. In these endeavours, PASA ben- efits greatly from the local experience and connections of its member organizations. Finally, nearly all PASA- member sanctuaries host researchers, thereby contribut- ing to our knowledge of the great apes and other Afri- can primates. Much of PASA’s work is made possible by support from zoos around the world. A brief precis of the current work carried out by PASA and its mem- ber organizations is given, along with descriptions of conservation programmes that are planned for the future.
The Pan African Sanctuary Alliance (PASA), the largest association of wildlife centers in Africa, includes 22 organizations that collectively house more than 3,000 rescued primates (Table 1; Figure 1). Prior to PASA’s formation, these organizations had similar goals and were facing similar challenges, but typically did not communicate with one another. In 2000, conservationists and primatologists arranged a meeting in Uganda to bring these groups together for the first time. The directors of the organizations agreed there was a need for improved ongoing communication and, as a result, PASA was formed.
Rosati, A. G., Herrmann, E., Kaminski, J., Krupenye, C., Melis, A. P., Schroepfer, K., Tan, J., et al. (2013). Assessing the psychological health of captive and wild apes: A response to Ferdowsian et al. (2011). Journal of Comparative Psychology, 127, 329–336.
As many studies of cognition and behavior involve captive animals, assessing any psychological impact of captive conditions is an important goal for comparative researchers. Ferdowsian and colleagues (2011) sought to address whether captive chimpanzees show elevated signs of psychopathology relative to wild apes. They modified a checklist of diagnostic criteria for major depression and posttraumatic stress disorder in humans, and applied these criteria to various captive and wild chimpanzee populations. We argue that measures derived from human diagnostic criteria are not a powerful tool for assessing the psychological health of nonverbal animals. In addition, we highlight certain methodological drawbacks of the specific approach used by Ferdowsian and colleagues (2011). We propose that research should (1) focus on objective behavioral criteria that account for species-typical behaviors and can be reliably identified across populations; (2) account for population differences in rearing history when comparing how current environment impacts psychological health in animals; and (3) focus on how changes in current human practices can improve the well-being of both captive and wild animals.
Schroepfer, K. K., Rosati, A. G., Chartrand, T., & Hare, B. (2011). Use of “entertainment” chimpanzees in commercials distorts public perception regarding their conservation status. PLoS One, 6 e26048.
Chimpanzees (Pan troglodytes) are often used in movies, commercials and print advertisements with the intention of eliciting a humorous response from audiences. The portrayal of chimpanzees in unnatural, human-like situations may have a negative effect on the public’s understanding of their endangered status in the wild while making them appear as suitable pets. Alternatively, media content that elicits a positive emotional response toward chimpanzees may increase the public’s commitment to chimpanzee conservation. To test these competing hypotheses, participants (n = 165) watched a series of commercials in an experiment framed as a marketing study. Imbedded within the same series of commercials was one of three chimpanzee videos. Participants either watched 1) a chimpanzee conservation commercial, 2) commercials containing ‘‘entertainment’’ chimpanzees or 3) control footage of the natural behavior of wild chimpanzees. Results from a post- viewing questionnaire reveal that participants who watched the conservation message understood that chimpanzees were endangered and unsuitable as pets at higher levels than those viewing the control footage. Meanwhile participants watching commercials with entertainment chimpanzees showed a decrease in understanding relative to those watching the control footage. In addition, when participants were given the opportunity to donate part of their earnings from the experiment to a conservation charity, donations were least frequent in the group watching commercials with entertainment chimpanzees. Control questions show that participants did not detect the purpose of the study. These results firmly support the hypothesis that use of entertainment chimpanzees in the popular media negatively distorts the public’s perception and hinders chimpanzee conservation efforts.