Roles for non-human primate-associated phage diversity in improving medicine and public health

Mammals harbor trillions of microorganisms and understanding the ecological and evolutionary processes structuring these ecosystems may provide insights relevant to public health and medicine. Comparative studies with our closest living relatives, non-human primates, have provided first insights into their rich bacteriophage communities. Here, I discuss how this phage diversity can be useful for combatting antibiotic-resistant infections and understanding disease emergence risk. For example, some primate-associated phages show a pattern suggesting a long-term co-divergence with their primate superhosts—co-diverging phages may be more likely to exhibit a narrow host range and thus less useful for phage therapy. Captive primates lose their natural phageome, which is replaced by human-associated phages making phages an exciting tool for studying rates of microorganism transmission at human–wildlife interfaces. This commentary tackles avenues for selecting phages for therapeutic interventions based on their ecological and evolutionary history, while discussing frameworks to allow primate-associated phages to be incorporated into the arsenal of clinicians.Peer Reviewe

A 40-year evaluation of drivers of African rainforest change

Background: Tropical forests are repositories of much of the world’s biodiversity and are critical for mitigation of climate change. Yet, the drivers of forest dynamics are poorly understood. This is in large part due to the lack of long-term data on forest change and changes in drivers. Methodology: We quantify changes in tree abundance, diversity, and stand structure along transects first enumerated in 1978 and resampled 2019 in Kibale National Park, Uganda. We tested five predictions. First, based on the purported role of seed dispersal and herbivory and our quantification of changes in the abundance of frugivores and herbivores, we tested two predictions of how faunal change could have influenced forest composition. Second, based on an evaluation of life history strategies, we tested two predictions concerning how the forest could have changed following disturbance that happened prior to written history. Finally, based on a 50-year climate record, we evaluate the possible influence of climate change on forest dynamics. Results: More trees were present on the assessed transects in 2019 (508) than in 1978 (436), species richness remained similar, but diversity declined as the number of dominant species increased. Rainfall increased by only 3 mm over the 50 years but this had not significant effect on forest changes measured here. Annual average monthly maximum temperature increased significantly by 1.05 °C over 50 years. The abundance of frugivorous and folivorous primates and elephants increased over the 50 years of monitoring. Neither the prediction that an increase in abundance of seed dispersing frugivores increases the abundance of their preferred fruiting tree species, nor that as an increase in folivore abundance causes a decline in their preferred species were supported. As predicted, light-demanding species decreased in abundance while shade-tolerant species increased as expected from Kibale being disturbed prior to historical records. Finally, while temperature increased over the 50 years, we found no means to predict a priori how individual species would respond. Conclusions: Our study revealed subtle changes in the tree community over 40 years, sizable increases in primate numbers, a substantial increase in the elephant population and an increase in local temperature. Yet, a clear picture of what set of interactions impact the change in the tree community remains elusive. Our data on tree life-history strategies and frugivore/herbivore foraging preferences suggest that trees species are under opposing pressures

What is the predictive power of the colobine protein-to-fiber model and its conservation value?

Predicting variation in animal abundance across time and space has proven very difficult; however, a model exists to predict the biomass of small folivorous primates that has considerable correlative support. This model suggests that the protein-to-fiber ratio of leaves in a habitat can predict folivore biomass. Here we present an experimental test of this protein-to-fiber model to assess if the number of infant monkeys per female and group size can be predicted based on the leaf chemistry of a habitat. We expected regenerating forest in Kibale National Park, Uganda to have leaves with higher concentrations of crude protein and lower concentrations of fiber than old-growth forest trees, and consequently, we expected a greater number of infants per female in the folivorous red colobus (Procolobus rufomitratus) with access to this area. As predicted, regenerating forests did have trees with leaves with high concentrations of protein and low concentrations of fiber, but there was no corresponding change in the demographic structure of red colobus groups. We also tested whether energy was a potential determinant of these parameters, but found no evidence for its importance. Our findings support recent studies that are critical of the protein-to-fiber model, which lead us to question the model’s generality, particularly for conservation and management

Consistency of Social Interactions in Sooty Mangabeys and Chimpanzees

Predictability of social interactions can be an important measure for the social complexity of an animal group. Predictability is partially dependent on how consistent interaction patterns are over time: does the behavior on 1 day explain the behavior on another? We developed a consistency measure that serves two functions: detecting which interaction types in a dataset are so inconsistent that including them in further analyses risks introducing unexplained error; and comparatively quantifying differences in consistency within and between animal groups. We applied the consistency measure to simulated data and field data for one group of sooty mangabeys (Cercocebus atys atys) and to groups of Western chimpanzees (Pan troglodytes verus) in the Taï National Park, Côte d'Ivoire, to test its properties and compare consistency across groups. The consistency measures successfully identified interaction types whose low internal consistency would likely create analytical problems. Species-level differences in consistency were less pronounced than differences within groups: in all groups, aggression and dominance interactions were the most consistent, followed by grooming; spatial proximity at different levels was much less consistent than directed interactions. Our consistency measure can facilitate decision making of researchers wondering whether to include interaction types in their analyses or social networks and allows us to compare interaction types within and between species regarding their predictability.Peer Reviewe

The future of sub-Saharan Africa’s biodiversity in the face of climate and societal change

Many of the world’s most biodiverse regions are found in the poorest and second most populous continent of Africa; a continent facing exceptional challenges. Africa is projected to quadruple its population by 2100 and experience increasingly severe climate change and environmental conflict—all of which will ravage biodiversity. Here we assess conservation threats facing Africa and consider how these threats will be affected by human population growth, economic expansion, and climate change. We then evaluate the current capacity and infrastructure available to conserve the continent’s biodiversity. We consider four key questions essential for the future of African conservation: (1) how to build societal support for conservation efforts within Africa; (2) how to build Africa’s education, research, and management capacity; (3) how to finance conservation efforts; and (4) is conservation through development the appropriate approach for Africa? While the challenges are great, ways forward are clear, and we present ideas on how progress can be made. Given Africa’s current modest capacity to address its biodiversity crisis, additional international funding is required, but estimates of the cost of conserving Africa’s biodiversity are within reach. The will to act must build on the sympathy for conservation that is evident in Africa, but this will require building the education capacity within the continent. Considering Africa’s rapidly growing population and the associated huge economic needs, options other than conservation through development need to be more effectively explored. Despite the gravity of the situation, we believe that concerted effort in the coming decades can successfully curb the loss of biodiversity in Africa.National Research Foundation (ZA, Grant 98404)Wilson Cente

Evidence against Zika virus infection of pets and peri-domestic animals in Latin America and Africa

Decades after its discovery in East Africa, Zika virus (ZIKV) emerged in Brazil in 2013 and infected millions of people during intense urban transmission. Whether vertebrates other than humans are involved in ZIKV transmission cycles remained unclear. Here, we investigate the role of different animals as ZIKV reservoirs by testing 1723 sera of pets, peri-domestic animals and African non-human primates (NHP) sampled during 2013–2018 in Brazil and 2006–2016 in Côte d'Ivoire. Exhaustive neutralization testing substantiated co-circulation of multiple flaviviruses and failed to confirm ZIKV infection in pets or peri-domestic animals in Côte d'Ivoire (n=259) and Brazil (n=1416). In contrast, ZIKV seroprevalence was 22.2% (2/9, 95% CI, 2.8–60.1) in West African chimpanzees (Pan troglodytes verus) and 11.1% (1/9, 95% CI, 0.3–48.3) in king colobus (Colobus polycomos). Our results indicate that while NHP may represent ZIKV reservoirs in Africa, pets or peri-domestic animals likely do not play a role in ZIKV transmission cycles.Peer Reviewe

Yaws Disease Caused by Treponema pallidum subspecies pertenue in Wild Chimpanzee, Guinea, 2019

Yaws-like lesions are widely reported in wild African great apes, yet the causative agent has not been confirmed in affected animals. We describe yaws-like lesions in a wild chimpanzee in Guinea for which we demonstrate infection with Treponema pallidum subsp. pertenue. Assessing the conservation implications of this pathogen requires further research

The cost of living in larger primate groups includes higher fly densities

Flies are implicated in carrying and mechanically transmitting many primate pathogens. We investigated how fly associations vary across six monkey species (Cercopithecus ascanius, Cercopithecus mitis, Colobus guereza, Lophocebus albigena, Papio anubis, and Piliocolobus tephrosceles) and whether monkey group size impacts fly densities. Fly densities were generally higher inside groups than outside them, and considering data from these primate species together revealed that larger groups harbored more flies. Within species, this pattern was strongest for colobine monkeys, and we speculate this might be due to their smaller home ranges, suggesting that movement patterns may influence fly–primate associations. Fly associations increase with group sizes and may thus represent a cost to sociality

Quantifying within-group variation in sociality—covariation among metrics and patterns across primate groups and species

It has long been recognized that the patterning of social interactions within a group can give rise to a social structure that holds very different places for different individuals. Such within-group variation in sociality correlates with fitness proxies in fish, birds, and mammals. Broader integration of this research has been hampered by the lack of agreement on how to integrate information from a plethora of dyadic interactions into individual-level metrics. As a step towards standardization, we collected comparative data on affinitive and affiliative interactions from multiple groups each of five species of primates to assess whether the same aspects of sociality are measured by different metrics and indices. We calculated 16 different sociality metrics used in previous research and thought to represent three different sociality concepts. We assessed covariation of metrics within groups and then summarized covariation patterns across all 15 study groups, which varied in size from 5 to 41 adults. With some methodological and conceptual caveats, we found that the number of weak ties individuals formed within their groups represented a dimension of sociality that was largely independent from the overall number of ties as well as from the number and strength of the strong ties they formed. Metrics quantifying indirect connectedness exhibited strong covariation with strong tie metrics and thus failed to capture a third aspect of sociality. Future research linking affiliation and affinity to fitness or other individual level outcomes should quantify inter-individual variation in three aspects: the overall number of ties, the number of weak ties, and the number or strength of strong ties individuals form, after taking into account effects of social network density. Significance statement: In recent years, long-term studies of individually known animals have revealed strong correlations between individual social bonds and social integration, on the one hand, and reproductive success and survival on the other hand, suggesting strong natural selection on affiliative and affinitive behavior within groups. It proved difficult to generalize from these studies because they all measured sociality in slightly different ways. Analyzing covariation between 16 previously used metrics identified only three rather independent dimensions of variation. Thus, different studies have tapped into the same biological phenomenon. How individuals are weakly connected within their group needs further attention.Peer Reviewe

Fly-derived DNA and camera traps are complementary tools for assessing mammalian biodiversity

Background Metabarcoding of vertebrate DNA found in invertebrates (iDNA) represents a potentially powerful tool for monitoring biodiversity. Preliminary evidence suggests fly iDNA biodiversity assessments compare favorably with established approaches such as camera trapping or line transects. Aims and Methods To assess whether fly-derived iDNA is consistently useful for biodiversity monitoring across a diversity of ecosystems, we compared metabarcoding of the mitochondrial 16S gene of fly pool-derived iDNA (range = 49–105 flies/site, N = 784 flies) with camera traps (range = 198–1,654 videos of mammals identified to the species level/site) at eight sites, representing different habitat types in five countries across tropical Africa. Results We detected a similar number of mammal species using fly-derived iDNA (range = 8–15 species/site) and camera traps (range = 8–27 species/site). However, the two approaches detected mostly different species (range = 6%–43% of species detected/site were detected with both methods), with fly-derived iDNA detecting on average smaller-bodied species than camera traps. Despite addressing different phylogenetic components of local mammalian communities, both methods resulted in similar beta-diversity estimates across sites and habitats. Conclusion These results support a growing body of evidence that fly-derived iDNA is a cost- and time-efficient tool that complements camera trapping in assessing mammalian biodiversity. Fly-derived iDNA may facilitate biomonitoring in terrestrial ecosystems at broad spatial and temporal scales, in much the same way as water eDNA has improved biomonitoring across aquatic ecosystems.Peer Reviewe