Tropical rainforest flies carrying pathogens form stable associations with social nonhuman primates

Abstract

Living in groups provides benefits but also incurs costs such as attracting disease vectors. For example, synanthropic flies associate with human settlements, and higher fly densities increase pathogen transmission. We investigated whether such associations also exist in highly mobile nonhuman primate (NHP) Groups. We studied flies in a group of wild sooty mangabeys (Cercocebus atys atys) and three communities of wild chimpanzees (Pan troglodytes verus) in Taï National Park, Côte d'Ivoire. We observed markedly higher fly densities within both mangabey and chimpanzee groups. Using a mark–recapture experiment, we showed that flies stayed with the sooty mangabey group for up to 12 days and for up to 1.3 km. We also tested mangabey‐associated flies for pathogens infecting mangabeys in this ecosystem, Bacillus cereus biovar anthracis (Bcbva), causing sylvatic anthrax, and Treponema pallidum pertenue, causing yaws. Flies contained treponemal (6/103) and Bcbva (7/103) DNA. We cultured Bcbva from all PCR‐positive flies, confirming bacterial viability and suggesting that this bacterium might be transmitted and disseminated by flies. Whole genome sequences of Bcbva isolates revealed a diversity of Bcbva, probably derived from several sources. We conclude that flies actively track mangabeys and carry infectious bacterial pathogens; these associations represent an understudied cost of sociality and potentially expose many social animals to a diversity of pathogens.

Shoo fly don't bother me: Flies track social primates and carry viable anthrax

“…This suggests that perhaps the significance of filth flies in pathogen transmission has been underestimated. Gogarten et al () utilize molecular approaches to detect DNA from two pathogens, TPE, and Bacillus cereus biovar anthracis ( Bc bv a ), the causative agent of sylvatic anthrax on captured filth flies. While this method does not definitively incriminate the captured fly species as mechanical vectors, their approach in culturing Bc bv a to determine its viability on flies is laudable and demonstrates the possibility of sylvatic anthrax being transmitted by flies.…”

“…By exploiting the natural history of fly relationships with their surrounding ecosystem, molecular ecologists and entomologists can use flies as sentinels to address ecological and evolutionary knowledge gaps. (b) Gogarten et al () marked and tracked flies and found that a small number of marked flies stayed with primate social groups for up to 12 days and 1 km. This method is demonstrated here by flies with blue markings remaining near mangabey groups (blue circle) and flies with red markings remaining near chimpanzee groups (red circle).…”

“…By following two nonhuman primate species and conducting mark‐recapture experiments on captured flies, Gogarten et al () found that filth flies associate with primate social groups and reveal compelling trends to suggest that flies remain with “host” social groups as they move (Figure b). One critical factor to consider, however, is the mechanism which drives these associations.…”

“…To identify fly species, Gogarten et al () used DNA from captured flies; however, often this was not beyond the family level. The significance of morphological identification and taxonomy in this work can not be underestimated, because many species have specialized associations with “hosts” or may have a preference for specific waste material such as faecal‐matter or carrion that would each contain a unique sets of pathogens.…”

“…To capture filth flies, Gogarten et al () used a synthetic bait that mimicked the odor of rotting carcasses and another bait comprised of warmed mangabey faecal material to attract a diverse group of flies (specifically those that prefer carrion vs. faeces). In this study, researchers found that they were able to detect mangabey DNA from nearly all flies from the faeces traps and relatively fewer flies caught with the synthetic carrion traps.…”