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Combined analysis of primate and parasite traits reveals new insights on ecological networks

/ Beth Preston / Leave a comment
This blog post is provided by James Herrera, Ph.D., Duke Lemur Center SAVA Conservation Initiative and tells the #StoryBehindthePaper for the paper “Predicting primate-parasite associations using exponentional random graph models”, which was recently published in Journal of Animal Ecology. In their paper they show that large primates in warm climates and sharing the same biogeographic region have more parasites than small species in cool, dry climates. Parasites known from multiple non-primate hosts, especially viruses, protozoa, and helminth worms infect more primates than primate-specific parasites or fungi and bacteria. Advanced social network analyses allowed the first multidimensional analysis of primate-parasite ecological interactions.

After three years of the coronavirus pandemic, we have all become keenly aware of the impacts pathogens have on global systems. Parasites are ubiquitous in nature, including all species that live on or inside another organism – the host – from which they get their resources. Wild animals are often co-infected by multiple parasites at the same time. The chimpanzee, for example, is known to host over 100 parasites; chimps are one of the best studied primates because of their close relationship to people and the relevance of chimp parasites for human health. In contrast, species like the indri, a lemur only found on Madagascar, are only known to host about 10 parasites. Many other primates are so poorly studied, only 1 parasite has ever been recorded.

Chimpanzees (left) are one of the best studied primates for parasite interactions. In contrast, the indri (right) is comparatively poorly known for its parasites. (Photo credits: chimpanzee: Wikimedia Commons; indri: James Herrera)

In a new study published in the Journal of Animal Ecology, we examined which traits of both primates and parasites predict the likelihood of their interactions. Using advanced techniques in social network analysis, called the exponential random graph, we were able to simultaneously test the traits of primates and parasites to determine what predisposes primates to infection and what gives some parasites a unique advantage. For primates, larger species that are found in warmer, wetter climates are more likely to host diverse parasites, compared to smaller species living in drier, cooler climates. Further, species in the same branches of the evolutionary tree and those that live in the same geographic region are more likely to share parasites than more distantly related species found on different continents. Viruses, protozoa, and helminth worms are more likely to infect diverse primates than fungi, arthropods, and bacteria. Parasites that are known to infect non-primate mammals are also more likely to infect diverse primates.

A photo from a microscope slide showing the blood parasite Plasmodium falciparum, one of the pathogens that causes malaria, a devastating disease in people, and also infects 118 other primates. In contrast, there are at least 30 other kinds of Plasmodium that only infect one or a few primates and effects on disease are poorly understood. (Photo credit: Wikimedia Commons)

These new results were made possible by the great advances being made in infectious disease ecology. Over the last two decades, Dr. Charles Nunn at Duke University’s Evolutionary Anthropology and Global Health departments has been working with teams of researchers to compile all published records of primate-parasite interactions. Combing through the literature, almost 600 published sources were obtained to glean which parasites are found in over 200 primates species, with over 2,300 interactions recorded. With the analytical tools in social network science mastered by Duke Sociology professor Dr. James Moody, we were able to systematically test how traits of both hosts and parasites affect the likelihood of their interaction for the first time. While many previous studies used subsets of this database and examined either hosts or parasites in isolation, we were able to make new inferences about the critical links in this unique ecological network.

This work builds on a recent study that showed how extinction of primate hosts could lead to the co-extinction of almost 200 parasite species. While at first this might seem like a good thing, in fact it could have negative impacts on biodiversity as a whole. Many parasites don’t actually cause disease or death in the hosts, and some may even have beneficial properties. We simply don’t know enough about these critical and co-evolved relationships to understand what effects host-parasite coextinctions could have in the long-term.

While it might seem strange to worry about parasite extinctions, they are actually an important part of biodiversity and ecosystem functions. Understanding how primates and parasites interact reveals new insights into coevolutionary theory, and could also contribute to the conservation of underappreciated species richness. While from a public health perspective, we’d like to see some parasites disappear, like corona and ebola viruses, from an evolutionary stance, the sheer diversity of parasites and their intimate relationships with their hosts make them fascinating and crucial components of biodiversity.

Read the paper

Read the full paper here: Herrera, J.P., Moody, J. and Nunn, C.L. (2023), Predicting primate-parasite associations using exponentional random graph models. J Anim Ecol. Accepted Author Manuscript. https://doi.org/10.1111/1365-2656.13883

The baboons of Amboseli

/ Journal of Animal Ecology / 1 Comment

Founded in 1971, the Amboseli Baboon Project is one of the longest-running studies of wild primates in the world. The project centres on the savannah baboon, Papio cynocephalus that lives in the Amboseli basin of southern Kenya and tracks hundreds of known individuals in several social groups over the course of their entire lives.

With over 40 years of data, the project can answer questions about the relationships between social behaviour, relatedness, and population genetic structure in wild populations that would not be possible with only a few years of research. The project also addresses other aspects of baboon biology, such as genetics, hormones, nutrition, hybridization, parasitology, and relations with other species.

Susan Alberts from Duke University co-directs the Amboseli Baboon Research Project with Jeanne Altmann at Princeton University, out now in the current issue of the journal is a new Synthesis paper by Susan on Social influences on survival and reproduction: Insights from a long‐term study of wild baboons.

To complement the publication of this Synthesis paper, Susan shares some of the best photos from her fieldwork in Amboseli and reveals more about the lives of the baboons.

Figure 1. The Amboseli Baboon Research Project represents one of the best-studied wild mammal populations in the world. Conducted in the Amboseli basin of southern Kenya, the research includes full life course data, collected continuously since 1971, on more than six generations of known individuals. Photo credit: Elizabeth A. Archie.
Figure 2. The study subjects are habituated to the presence of human observers and go about their daily lives un-interuputed while they are being observed. Left: Senior Observer J. Kinyua Warutere, who has been with the project since 1995, collecting daily monitoring data. Right: Amboseli often provides excellent observation conditions. Here, the author observes baboons on a short-grass plain. Photo credits: Jeanne Altmann (left), Robert Zimmerman (right).
Figure 3. Baboons are intensely social animals, and social interactions and relationships – both affiliative and antagonistic – are a highly salient component of their environment. On the right, a young infant climbs and plays on an adult male. At least, an adult female sits near here infant. They are surrounded by other members of their social group. Photo credit: Jeanne Altmann, taken Oct 1990, in the project’s 19th year.
Figure 4. Social relationships affect an individual’s access to food and other resources, its access to information, and its vulnerability to predation. Social relationships can also represent protection against other baboons who are threatening or competitive. Probably for these reasons, individuals form social bonds early in life, and these bonds may persist for years. This is especially true for females, who remain throughout life in the social group into which they were born; males tend to move between social groups periodically. Photo credit: Chelsea Weibel.
Figure 5. Left: One adult female grooms another, while the groomer’s yearling infant nurses. Right: An adult female grooms her 16-month old daughter (foreground) while two adolescent females groom just behind them. Social grooming – picking through the fur of a partner to remove dirt, debris, and ectoparasites – is a frequent affiliative behavior in baboon social groups. Photo credits: Elizabeth A. Archie (left), Susan C. Alberts (right).
Figure 6. The number and strength of a female’s social bonds – measured via grooming relationships and other social interactions – have been linked to offspring survival, adult survival, or both, in three different wild baboon populations, including Amboseli. Photo credits: Susan C. Alberts
Figure 7. This female was badly wounded on her flanks, tail, head, and face during a series of intense aggressive conflicts among adult females that preceded a permanent social group fission. While some permanent fissions are peaceful and gradual, the one involving this female occurred over the course of only two weeks, and at least 3 infants are suspected to have died as a result of the aggression, with numerous females wounded. Conspecifics represent not only social resources, but serious social competitors: animals living in social groups must constantly balance the benefits of group living against the costs. Photo credit: A. Catherine Markham.
Figure 8. This infant’s life will be strongly affected by its early experiences: females that experience more adversity early in life have much shorter lifespans. Among females that survive to adulthood, those who experience three or more sources of early adversity die a median of 10 years earlier than ‘silver spoon’ females who experience little or no adversity. The sources of adversity that were studied include losing one’s mother in the first four years of life, having a close-in-age younger sibling, being born in a drought, born to a low-ranking mother, and born to a socially isolated mother. Note: the adult male in the foreground is wearing a radio collar, which the research team uses to help locate study groups and follow males when they move between social groups. Photo credit: Elizabeth A. Archie.
Figure 9. This infant is nursing while being groomed by his mother. Infant baboons are completely dependent upon their mother for the first year of life. Over the 47 years of the Amboseli baboon study, only a handful of infants whose mothers died in their first year of life have survived to adulthood. Even after weaning (at approximately 16 months of age) the loss of the mother has a negative effect on juvenile survival. Photo credit: Chelsea Weibel.
Figure 10. Infant baboons are born able to cling to their mother, and they ride ventrally for the first several months of life as shown by the female infant on the left. During this stage they have a black coat, in contrast to the golden-brown coats of older animals. At 2-3 months of age they learn to ride on the mother’s back as shown on the right. By this age the black natal coat has begun to turn golden-brown, resulting in the patchwork appearance seen in this 4-month old male infant. Photo credits: Susan C. Alberts (left panel), Chelsea Weibel (right panel) .
Figure 11. Muzzle-sniffing, seen here, appears to be an important source of information for infants about what is safe to eat and how various foods are processed; many baboon foods (e.g., grass corms, tree gum, tubers) require digging, opening, extracting, or separating from a substrate, and infants may require considerable time to gain the strength and knowledge to acquire these foods. Photo credit: A. Catherine Markham.
Figure 12. This 3-month old infant will not be harassed or threatened by other baboons when he is in the vicinity of this large, high-ranking male, who is highly tolerant and protective of him. Baboon males differentiate their own offspring from the offspring of other males and provide care to them; paternity analyses are pending for this infant. At the same time, this same male is suspected of killing two other infants in the six weeks prior to this photo being taken; most likely, those infants were not his biological offspring (paternity analyses are pending). Photo credit: Susan C. Alberts.
Figure 13. Adult males can be benevolent figures in an infant baboon’s life, as shown here. The adult male on the left is holding an infant who may or may not be his biological offspring; males can be benevolent or violent towards non-offspring and infants must correctly navigate their complicated social landscape in order to survive. Note the considerable difference in coat color between the male on the left and the female on the right: the Amboseli baboon population is composed mostly of yellow baboons (Papio cynocephalus) but some natural hybridization occurs with nearby populations of olive baboons (P. anubis), which are darker, producing great variation in coat colors in Amboseli. Photo credit: Elizabeth A. Archie.
Figure 14. Left: an adult male protecting a young juvenile (screaming, between his legs) against an older one (crouching in front of the male). Right: an adult male during the act of infanticide. Instead of killing the infant quickly with his teeth, as is often observed, this male ‘kidnapped’ the infant and kept it from its mother until it died of dehydration. Note again the difference in coat color between these two males; the male on the left shows clear evidence of being a hybrid yellow-olive baboon, while the male on the right shows the typical yellow baboon coat color. Photo credits: A. Catherine Markham (left) and Raphael S. Mututua (right).
Figure 15. The permanent field team of the Amboseli Baboon Research Project, responsible for the large majority of the regular monitoring and data collection. Raphael Mututua (center, back row) is the Project Manager and has been working with the Amboseli Baboon Research Project since 1981. Back row from left: Moonyoi ole Parsetau (camp staff), Lenkai ‘Nkii’ ole Rikoyan (camp cook), Jackson Kinyua Warutere (Senior Observer), Raphael Supeet Mututua (Project Manager and Senior Observer), Isaiah Longida ole Siodi (Observer), Serah Sayialel (Senior Observer), Benard Ochieng’ Oyath (Junior Observer). Front row from left: Gideon Marinka (Junior Observer), Lenkai ’Alex’ ole Meloimet (camp staff). Photo credit: Kerri Smith.
Figure 16. The leaders of the Amboseli Baboon Research Project. Far left: Susan Alberts (Duke University) on the left and Jeanne Altmann (Princeton University) on the right observing baboons. Top right: Elizabeth Archie collecting data (University of Notre Dame). Bottom right: Jenny Tung in the project’s ‘lab tent’ processing biological samples (Duke University). Photo credits: Courtney L. Fitzpatrick, Susan C. Alberts.
Figure 17. The author has not only watched many young baboons grow up, she has also watched her own daughters Michele (left) and Teresa (right) grow up during their visits to Amboseli, which were frequent when they were young. Photo credits: Robert Zimmerman.