Primate phageomes are structured by superhost phylogeny and environment.

Humans harbor diverse communities of microorganisms, the majority of which are bacteria in the gastrointestinal tract. These gut bacterial communities in turn host diverse bacteriophage (hereafter phage) communities that have a major impact on their structure, function, and, ultimately, human health. However, the evolutionary and ecological origins of these human-associated phage communities are poorly understood. To address this question, we examined fecal phageomes of 23 wild nonhuman primate taxa, including multiple representatives of all the major primate radiations. We find relatives of the majority of human-associated phages in wild primates. Primate taxa have distinct phageome compositions that exhibit a clear phylosymbiotic signal, and phage-superhost codivergence is often detected for individual phages. Within species, neighboring social groups harbor compositionally and evolutionarily distinct phageomes, which are structured by superhost social behavior. Captive nonhuman primate phageome composition is intermediate between that of their wild counterparts and humans. Phage phylogenies reveal replacement of wild great ape-associated phages with human-associated ones in captivity and, surprisingly, show no signal for the persistence of wild-associated phages in captivity. Together, our results suggest that potentially labile primate-phage associations have persisted across millions of years of evolution. Across primates, these phylosymbiotic and sometimes codiverging phage communities are shaped by transmission between groupmates through grooming and are dramatically modified when primates are moved into captivity.

Persistent anthrax as a major driver of wildlife mortality in a tropical rainforest.

Anthrax is a globally important animal disease and zoonosis. Despite this, our current knowledge of anthrax ecology is largely limited to arid ecosystems, where outbreaks are most commonly reported. Here we show that the dynamics of an anthrax-causing agent, Bacillus cereus biovar anthracis, in a tropical rainforest have severe consequences for local wildlife communities. Using data and samples collected over three decades, we show that rainforest anthrax is a persistent and widespread cause of death for a broad range of mammalian hosts. We predict that this pathogen will accelerate the decline and possibly result in the extirpation of local chimpanzee (Pan troglodytes verus) populations. We present the epidemiology of a cryptic pathogen and show that its presence has important implications for conservation.

Fifty+ years of primate research illustrates complex drivers of abundance and increasing primate numbers.

Many primate populations are threatened by human actions and a central tool used for their protection is establishing protected areas. However, even if populations in such areas are protected from hunting and deforestation, they still may be threatened by factors such as climate change and its cascading impacts on habitat quality and disease dynamics. Here we provide a long-term and geographically wide-spread population assessment of the five common diurnal primates of Kibale National Park, Uganda. Over 7 year-long or longer census efforts that spanned 52 years, our team walked 1466 km, and recorded 480 monkey groups. Populations were generally relatively stable with a few exceptions, for which no apparent causative factors could be identified. This stability is unexpected as many ecological changes documented over the last 34+ years (e.g., decreasing food abundance and quality) were predicted to have negative impacts. Populations of some species declined at some sites but increased at others. This highlights the need for large, protected areas so that declines in particular areas are countered by gains in others. Kibale has large areas of regenerating forest and this most recent survey revealed that after 20+ years, forest regeneration in many of these areas appears sufficient to sustain sizeable primate populations, except for blue monkeys that have not colonized these areas. Indeed, the average primate abundance in the regenerating forest was only 8.1% lower than in neighboring old-growth forest. Thus, park-wide primate abundance has likely increased, despite many pressures on the park having risen; however, some areas in the park remain to be assessed. Our study suggests that the restoration, patrolling, and community outreach efforts of the Uganda Wildlife Authority and their partners have contributed significantly to protecting the park and its animals.

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.

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.

Primates Can Be a Rallying Symbol to Promote Tropical Forest Restoration.

With 60% of all primate species now threatened with extinction and many species only persisting in small populations in forest fragments, conservation action is urgently needed. But what type of action? Here we argue that restoration of primate habitat will be an essential component of strategies aimed at conserving primates and preventing the extinctions that may occur before the end of the century and propose that primates can act as flagship species for restoration efforts. To do this we gathered a team of academics from around the world with experience in restoration so that we could provide examples of why primate restoration ecology is needed, outline how primates can act as flagship species for restoration efforts of tropical forest, review what little is known about how primate populations respond to restoration efforts, and make specific recommendations of the next steps needed to make restoration of primate populations successful. We set four priorities: (1) academics must effectively communicate both the value of primates and the need for restoration; (2) more research is needed on how primates contribute to forest restoration; (3) more effort must be put into Masters and PhD level training for tropical country nationals; and finally (4) more emphasis is needed to monitor the responses of regenerating forest and primate populations where restoration efforts are initiated. We are optimistic that populations of many threatened species can recover, and extinctions can be prevented, but only if concerted large-scale efforts are made soon and if these efforts include primate habitat restoration.

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

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.

Reconstruction of ancestral 16S rRNA reveals mutation bias in the evolution of optimal growth temperature in the Thermotogae phylum.

Optimal growth temperature is a complex trait involving many cellular components, and its physiology is not yet fully understood. Evolution of continuous characters, such as optimal growth temperature, is often modeled as a one-dimensional random walk, but such a model may be an oversimplification given the complex processes underlying the evolution of continuous characters. Recent articles have used ancestral sequence reconstruction to infer the optimal growth temperature of ancient organisms from the guanine and cytosine content of the stem regions of ribosomal RNA, allowing inferences about the evolution of optimal growth temperature. Here, we investigate the optimal growth temperature of the bacterial phylum Thermotogae. Ancestral sequence reconstruction using a nonhomogeneous model was used to reconstruct the stem guanine and cytosine content of 16S rRNA sequences. We compare this sequence reconstruction method with other ancestral character reconstruction methods, and show that sequence reconstruction generates smaller confidence intervals and different ancestral values than other reconstruction methods. Unbiased random walk simulation indicates that the lower temperature members of the Thermotogales have been under directional selection; however, when a simulation is performed that takes possible mutations into account, it is the high temperature lineages that are, in fact, under directional selection. We find that the evolution of Thermotogales optimal growth temperatures is best fit by a biased random walk model. These findings suggest that it may be easier to evolve from a high optimal growth temperature to a lower one than vice versa.

Seasonal mortality patterns in primates: implications for the interpretation of dental microwear.

The microscopic traces of use wear on teeth have been extensively studied to provide information that will assist in elucidating the dietary habits of extinct hominin species. It has been amply documented that dental microwear provides information pertaining to diet for living animals, where there is a strong and consistent association between dental microwear patterns and different types of foods that are chewed. The details of occlusal surface wear patterns are capable of distinguishing among diets when the constituent food items differ in their fracture properties. For example, the microwear traces left on the teeth of mammals that crush hard, brittle foods such as nuts are generally dominated by pits, whereas traces left on the teeth of mammals that shear tough items such as leaves tend to be characterized by scratches. These microwear features result from and thus record actual chewing events. As such, microwear patterns are expected to be variably ephemeral, as individual features are worn away and replaced or overprinted by others as the tooth wears down in subsequent bouts of mastication. Indeed, it has been demonstrated, both in the laboratory and the wild, that short-term dietary variation can result in the turnover of microwear. Because occlusal microwear potentially reflects an individual's diet for a short time (days, weeks, or months, depending on the nature of the foods being masticated), tooth surfaces sampled at different times will display differences that relate to temporal (for example, seasonal) differences in diet.

Microsatellite DNA suggests that group size affects sex-biased dispersal patterns in red colobus monkeys.

Dispersal is a major life history trait of social organisms influencing the behavioral and genetic structure of their groups. Unfortunately, primate dispersal is difficult to quantify, because of the rarity of these events and our inability to ascertain if individuals dispersed or died when they disappear. Socioecological models have been partially developed to understand the ecological causes of different dispersal systems and their social consequences. However, these models have yielded confusing results when applied to folivores. The folivorous red colobus monkey (Procolobus rufomitratus) in Kibale National Park, Uganda is thought to exhibit female-biased dispersal, although both sexes have been observed to disperse and there remains considerable debate over the selective pressures favoring the transfers of males and females and the causes of variation in the proportion of each sex to leave the natal group. We circumvent this problem by using microsatellite DNA data to investigate the prediction that female dispersal will be more frequent in larger groups as compared to smaller ones. The rationale for this prediction is that red colobus exhibit increased within-group competition in bigger groups, which should favor higher female dispersal rates and ultimately lower female relatedness. Genetic data from two unequally sized neighboring groups of red colobus demonstrate increased female relatedness within the smaller group, suggesting females are less likely to disperse when there is less within-group competition. We suggest that the dispersal system is mediated to some degree by scramble competition and group size. Since red colobus group sizes have increased throughout Kibale by over 50% in the last decade, these changes may have major implications for the genetic structure and ultimately the population viability of this endangered primate.

Artificially raised roost temperatures lead to larger body sizes in wild bats.

Climate warming has major consequences for animal populations, as ambient temperature profoundly influences all organisms' physiology, behavior, or both.1 Body size in many organisms has been found to change with increased ambient temperatures due to influences on metabolism and/or access to resources.2,3,4,5,6 Changes in body size, in turn, can affect the dynamics and persistence of populations.7 Notably, in some species, body size has increased over the last decades in response to warmer temperatures.3,8 This has primarily been attributed to higher food availability,3 but might also result from metabolic savings in warmer environments.9,10 Bechstein's bats (Myotis bechsteinii) grow to larger body sizes in warmer summers,11 which affects their demography as larger females reproduce earlier at the expense of a shorter life expectancy.12,13 However, it remains unclear whether larger body sizes in warmer summers were due to thermoregulatory benefits or due to increased food availability. To disentangle these effects, we artificially heated communal day roosts of wild maternity colonies over four reproductive seasons. We used generalized mixed models to analyze these experimental results along with 25 years of long-term data comprising a total of 741 juveniles. We found that individuals raised in heated roosts grew significantly larger than those raised in unheated conditions. This suggests that metabolic savings in warmer conditions lead to increased body size, potentially resulting in the decoupling of body growth from prey availability. Our study highlights a direct mechanism by which climate change may alter fitness-relevant traits, with potentially dire consequences for population persistence.

Primate population dynamics in Ngogo, Kibale National Park, Uganda, over nearly five decades.

Many anthropogenic-driven changes, such as hunting, have clear and immediate negative impacts on wild primate populations, but others, like climate change, may take generations to become evident. Thus, informed conservation plans will require decades of population monitoring. Here, we expand the duration of monitoring of the diurnal primates at Ngogo in Kibale National Park, Uganda, from 32.9 to 47 years. Over the 3531 censuses that covered 15,340 km, we encountered 2767 primate groups. Correlation analyses using blocks of 25 census walks indicate that encounters with groups of black and white colobus, blue monkeys, and baboons neither increased nor decreased significantly over time, while encounters with groups of redtail monkeys and chimpanzees marginally increased. Encounters with mangabeys and L'Hoesti monkeys increased significantly, while red colobus encounters dramatically decreased. Detailed studies of specific groups at Ngogo document changes in abundances that were not always well represented in the censuses because these groups expanded into areas away from the transect, such as nearby regenerating forest. For example, the chimpanzee population increased steadily over the last 2 + decades but this increase is not revealed by our census data because the chimpanzees expanded, mainly to the west of the transect. This highlights that extrapolating population trends to large areas based on censuses at single locations should be done with extreme caution, as forests change over time and space, and primates adapt to these changes in several ways.

Vertebrate environmental DNA from leaf swabs.

Terrestrial vertebrates are threatened by anthropogenic activities around the world. The rapid biodiversity loss that ensues is most intense in the tropics and affects ecosystem functions, such as seed dispersal, or may facilitate pathogen transmission1. Monitoring vertebrate distributions is essential for understanding changes in biodiversity and ecosystems and also for adaptive management strategies. Environmental DNA (eDNA) approaches have the potential to play a key role in such efforts. Here, we explore whether eDNA swabbed from terrestrial vegetation in a tropical biodiversity hotspot is a useful tool for vertebrate biomonitoring. By swabbing leaves, we collected eDNA from 24 swabs at three locations in Kibale National Park, Uganda and used two metabarcoding systems to catalog the vertebrate taxa in the samples. We detected 52 wild vertebrate genera, including 26 avian and 24 mammalian genera; 30 of these assignments could be refined to the species level. We detected an average of 7.6 genera per swab. This approach, with its inexpensive and simple collection and DNA extraction, opens the door for inexpensive large-scale vertebrate biomonitoring.

Estrogenic plant consumption predicts red colobus monkey (Procolobus rufomitratus) hormonal state and behavior.

Numerous studies have examined the effects of anthropogenic endocrine disrupting compounds; however, very little is known about the effects of naturally occurring plant-produced estrogenic compounds (i.e., phytoestrogens) on vertebrates. To examine the seasonal pattern of phytoestrogen consumption and its relationship to hormone levels (407 fecal samples analyzed for estradiol and cortisol) and social behavior (aggression, mating, and grooming) in a primate, we conducted an 11-month field study of red colobus (Procolobus rufomitratus) in Kibale National Park, Uganda. The percent of diet from estrogenic plants averaged 10.7% (n=45 weeks; range: 0.7-32.4%). Red colobus fed more heavily on estrogenic Millettia dura young leaves during weeks of higher rainfall, and the consumption of this estrogenic item was positively correlated to both their fecal estradiol and cortisol levels. Social behaviors were related to estradiol and cortisol levels, as well as the consumption of estrogenic plants and rainfall. The more the red colobus consumed estrogenic plants the higher their rates of aggression and copulation and the lower their time spent grooming. Our results suggest that the consumption of estrogenic plants has important implications for primate health and fitness through interactions with the endocrine system and changes in hormone levels and social behaviors.

Protozoan parasites in group-living primates: testing the biological island hypothesis.

A series of articles by W.J. Freeland published in the 1970s proposed that social organization and behavioral processes were heavily influenced by parasitic infections, which led to a number of intriguing hypotheses concerning how natural selection might act on social factors because of the benefits of avoiding parasite infections. For example, Freeland [1979] showed that all individuals within a given group harbored identical gastrointestinal protozoan faunas, which led him to postulate that social groups were akin to "biological islands" and suggest how this isolation could select specific types of ranging and dispersal patterns. Here, we reexamine the biological island hypothesis by quantifying the protozoan faunas of the same primate species examined by Freeland in the same location; our results do not support this hypothesis. In contrast, we quantified two general changes in protozoan parasite community of primates in the study area of Kibale National Park, Uganda, over the nearly 35 years between sample collections: (1) the colobines found free of parasites in the early 1970s are now infected with numerous intestinal protozoan parasites and (2) groups are no longer biological islands in terms of their protozoan parasites. Whatever the ultimate explanation for these changes, our findings have implications for studies proposing selective forces shaping primate behavior and social organization.

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.

The Movement of Pathogen Carrying Flies at the Human-Wildlife Interface.

Flies form high-density associations with human settlements and groups of nonhuman primates and are implicated in transmitting pathogens. We investigate the movement of nonhuman primate-associated flies across landscapes surrounding Kibale National Park, Uganda, using a mark-recapture experiment. Flies were marked in nine nonhuman primate groups at the forest edge ([Formula: see text] = 929 flies per group), and we then attempted to recapture them in more anthropized areas (50 m, 200 m and 500 m from where marked; 2-21 days after marking). Flies marked in nonhuman primate groups were recaptured in human areas (19/28,615 recaptured). Metabarcoding of the flies in nonhuman primate groups revealed the DNA of multiple eukaryotic primate parasites. Taken together, these results demonstrate the potential of flies to serve as vectors between nonhuman primates, livestock and humans at this biodiverse interface.

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.

Archival influenza virus genomes from Europe reveal genomic variability during the 1918 pandemic.

The 1918 influenza pandemic was the deadliest respiratory pandemic of the 20th century and determined the genomic make-up of subsequent human influenza A viruses (IAV). Here, we analyze both the first 1918 IAV genomes from Europe and the first from samples prior to the autumn peak. 1918 IAV genomic diversity is consistent with a combination of local transmission and long-distance dispersal events. Comparison of genomes before and during the pandemic peak shows variation at two sites in the nucleoprotein gene associated with resistance to host antiviral response, pointing at a possible adaptation of 1918 IAV to humans. Finally, local molecular clock modeling suggests a pure pandemic descent of seasonal H1N1 IAV as an alternative to the hypothesis of origination through an intrasubtype reassortment.

Molecular archeology of human viruses.

The evolution of human-virus associations is usually reconstructed from contemporary patterns of genomic diversity. An intriguing, though still rarely implemented, alternative is to search for the genetic material of viruses in archeological and medical archive specimens to document evolution as it happened. In this chapter, we present lessons from ancient DNA research and incorporate insights from virology to explore the potential range of applications and likely limitations of archeovirological approaches. We also highlight the numerous questions archeovirology will hopefully allow us to tackle in the near future, and the main expected roadblocks to these avenues of research.