Shared community effects and the non-genetic maternal environment shape cortisol levels in wild chimpanzees.

Mechanisms of inheritance remain poorly defined for many fitness-mediating traits, especially in long-lived animals with protracted development. Using 6,123 urinary samples from 170 wild chimpanzees, we examined the contributions of genetics, non-genetic maternal effects, and shared community effects on variation in cortisol levels, an established predictor of survival in long-lived primates. Despite evidence for consistent individual variation in cortisol levels across years, between-group effects were more influential and made an overwhelming contribution to variation in this trait. Focusing on within-group variation, non-genetic maternal effects accounted for 8% of the individual differences in average cortisol levels, significantly more than that attributable to genetic factors, which was indistinguishable from zero. These maternal effects are consistent with a primary role of a shared environment in shaping physiology. For chimpanzees, and perhaps other species with long life histories, community and maternal effects appear more relevant than genetic inheritance in shaping key physiological traits.

Maternal effects on the development of vocal communication in wild chimpanzees.

Early-life experiences, such as maternal care received, influence adult social integration and survival. We examine what changes to social behavior through ontogeny lead to these lifelong effects, particularly whether early-life maternal environment impacts the development of social communication. Chimpanzees experience prolonged social communication development. Focusing on a central communicative trait, the "pant-hoot" contact call used to solicit social engagement, we collected cross-sectional data on wild chimpanzees (52 immatures and 36 mothers). We assessed early-life socioecological impacts on pant-hoot rates across development, specifically: mothers' gregariousness, age, pant-hoot rates and dominance rank, maternal loss, and food availability, controlling for current maternal effects. We found that early-life maternal gregariousness correlated positively with offspring pant-hoot rates, while maternal loss led to reduced pant-hoot rates across development. Males had steeper developmental trajectories in pant-hoot rates than females. We demonstrate the impact of maternal effects on developmental trajectories of a rarely investigated social trait, vocal production.

Early maternal loss leads to short- but not long-term effects on diurnal cortisol slopes in wild chimpanzees.

The biological embedding model (BEM) suggests that fitness costs of maternal loss arise when early-life experience embeds long-term alterations to hypothalamic-pituitary-adrenal (HPA) axis activity. Alternatively, the adaptive calibration model (ACM) regards physiological changes during ontogeny as short-term adaptations. Both models have been tested in humans but rarely in wild, long-lived animals. We assessed whether, as in humans, maternal loss had short- and long-term impacts on orphan wild chimpanzee urinary cortisol levels and diurnal urinary cortisol slopes, both indicative of HPA axis functioning. Immature chimpanzees recently orphaned and/or orphaned early in life had diurnal cortisol slopes reflecting heightened activation of the HPA axis. However, these effects appeared short-term, with no consistent differences between orphan and non-orphan cortisol profiles in mature males, suggesting stronger support for the ACM than the BEM in wild chimpanzees. Compensatory mechanisms, such as adoption, may buffer against certain physiological effects of maternal loss in this species.

Patterns of urinary cortisol levels during ontogeny appear population specific rather than species specific in wild chimpanzees and bonobos.

Compared with most mammals, postnatal development in great apes is protracted, presenting both an extended period of phenotypic plasticity to environmental conditions and the potential for sustained mother-offspring and/or sibling conflict over resources. Comparisons of cortisol levels during ontogeny can reveal physiological plasticity to species or population specific socioecological factors and in turn how these factors might ameliorate or exaggerate mother-offspring and sibling conflict. Here, we examine developmental patterns of cortisol levels in two wild chimpanzee populations (Budongo and Taï), with two and three communities each, and one wild bonobo population (LuiKotale), with two communities. Both species have similar juvenile life histories. Nonetheless, we predicted that key differences in socioecological factors, such as feeding competition, would lead to interspecific variation in mother-offspring and sibling conflict and thus variation in ontogenetic cortisol patterns. We measured urinary cortisol levels in 1394 samples collected from 37 bonobos and 100 chimpanzees aged up to 12 years. The significant differences in age-related variation in cortisol levels appeared population specific rather than species specific. Both bonobos and Taï chimpanzees had comparatively stable and gradually increasing cortisol levels throughout development; Budongo chimpanzees experienced declining cortisol levels before increases in later ontogeny. These age-related population differences in cortisol patterns were not explained by mother-offspring or sibling conflict specifically; instead, the comparatively stable cortisol patterns of bonobos and Taï chimpanzees likely reflect a consistency in experience of competition and the social environment compared with Budongo chimpanzees, where mothers may adopt more variable strategies related to infanticide risk and resource availability. The clear population-level differences within chimpanzees highlight potential intraspecific flexibility in developmental processes in apes, suggesting the flexibility and diversity in rearing strategies seen in humans may have a deep evolutionary history.

A Novel Orthohepadnavirus Identified in a Dead Maxwell's Duiker (Philantomba maxwellii) in Taï National Park, Côte d'Ivoire.

New technologies enable viral discovery in a diversity of hosts, providing insights into viral evolution. We used one such approach, the virome capture sequencing for vertebrate viruses (VirCapSeq-VERT) platform, on 21 samples originating from six dead Maxwell's duikers (Philantomba maxwellii) from Taï National Park, Côte d'Ivoire. We detected the presence of an orthohepadnavirus in one animal and characterized its 3128 bp genome. The highest viral copy numbers were detected in the spleen, followed by the lung, blood, and liver, with the lowest copy numbers in the kidney and heart; the virus was not detected in the jejunum. Viral copy numbers in the blood were in the range known from humans with active chronic infections leading to liver histolytic damage, suggesting this virus could be pathogenic in duikers, though many orthohepadnaviruses appear to be apathogenic in other hosts, precluding a formal test of this hypothesis. The virus was not detected in 29 other dead duiker samples from the Côte d'Ivoire and Central African Republic, suggesting either a spillover event or a low prevalence in these populations. Phylogenetic analysis placed the virus as a divergent member of the mammalian clade of orthohepadnaviruses, though its relationship to other orthohepadnaviruses remains uncertain. This represents the first orthohepadnavirus described in an artiodactyl. We have tentatively named this new member of the genus Orthohepadnavirus (family Hepadnaviridae), Taï Forest hepadnavirus. Further studies are needed to determine whether it, or some close relatives, are present in a broader range of artiodactyls, including livestock.

The Use of Neopterin as a Noninvasive Marker in Monitoring Diseases in Wild Chimpanzees.

Pathogen analysis in wild great apes is both time- and resource-consuming. Therefore, we examined the potential use of urinary neopterin, a sensitive marker of cell-mediated immune system activation, as a disease marker and unspecific screening tool to facilitate informed pathogen analysis in great ape health monitoring. To test this, urinary neopterin was correlated to other disease markers such as sickness behaviors, fever, and urine parameters. Seasonal variation in urinary neopterin levels was investigated as well. The study encompassed noninvasively collected longitudinal data of young wild chimpanzees from the Taï National Park, Côte d´Ivoire. Relationships between disease markers were examined using a linear mixed model and a case study approach. Seasonal variation in urinary neopterin was tested using a linear mixed model. While the linear mixed model found no obvious relationship between urinary neopterin levels and other disease markers, the case study approach revealed a pattern resembling those found in humans. Urinary neopterin levels indicated seasonal immune system activation peaking in times of low ambient temperatures. We suggest the use of urinary neopterin as an unspecific screening tool in great ape health monitoring to identify relevant samples, individuals, and time periods for selective pathogen analysis and zoonotic risk assessment.

Seasonal and inter-annual variation of malaria parasite detection in wild chimpanzees.

BACKGROUND: Cross-sectional surveys of chimpanzee (Pan troglodytes) communities across sub-Saharan Africa show large geographical variation in malaria parasite (Plasmodium spp.) prevalence. The drivers leading to this apparent spatial heterogeneity may also be temporally dynamic but data on prevalence variation over time are missing for wild great apes. This study aims to fill this fundamental gap. METHODS: Some 681 faecal samples were collected from 48 individuals of a group of habituated chimpanzees (Taï National Park, Côte d'Ivoire) across four non-consecutive sampling periods between 2005 and 2015. RESULTS: Overall, 89 samples (13%) were PCR-positive for malaria parasite DNA. The proportion of positive samples ranged from 0 to 43% per month and 4 to 27% per sampling period. Generalized Linear Mixed Models detected significant seasonal and inter-annual variation, with seasonal increases during the wet seasons and apparently stochastic inter-annual variation. Younger individuals were also significantly more likely to test positive. CONCLUSIONS: These results highlight strong temporal fluctuations of malaria parasite detection rates in wild chimpanzees. They suggest that the identification of other drivers of malaria parasite prevalence will require longitudinal approaches and caution against purely cross-sectional studies, which may oversimplify the dynamics of this host-parasite system.

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.

Wild African great apes as natural hosts of malaria parasites: current knowledge and research perspectives.

Humans and African great apes (AGAs) are naturally infected with several species of closely related malaria parasites. The need to understand the origins of human malaria as well as the risk of zoonotic transmissions and emergence of new malaria strains in human populations has markedly encouraged research on great ape Plasmodium parasites. Progress in the use of non-invasive methods has rendered investigations into wild ape populations possible. Present knowledge is mainly focused on parasite diversity and phylogeny, with still large gaps to fill on malaria parasite ecology. Understanding what malaria infection means in terms of great ape health is also an important, but challenging avenue of research and has been subject to relatively few research efforts so far. This paper reviews current knowledge on African great ape malaria and identifies gaps and future research perspectives.