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1.  The costs of dominance: testosterone, cortisol and intestinal parasites in wild male chimpanzees 
Background
Male members of primate species that form multi-male groups typically invest considerable effort into attaining and maintaining high dominance rank. Aggressive behaviors are frequently employed to acquire and maintain dominance status, and testosterone has been considered the quintessential physiological moderator of such behaviors. Testosterone can alter both neurological and musculoskeletal functions that may potentiate pre-existing patterns of aggression. However, elevated testosterone levels impose several costs, including increased metabolic rates and immunosuppression. Cortisol also limits immune and reproductive functions.
Methods
To improve understanding of the relationships between dominance rank, hormones and infection status in nonhuman primates, we collected and analyzed 67 fecal samples from 22 wild adult male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. Samples were analyzed for cortisol and testosterone levels as well as intestinal parasite prevalence and richness. 1,700 hours of observation data were used to determine dominance rank of each animal. We hypothesized that dominance rank would be directly associated with fecal testosterone and cortisol levels and intestinal parasite burden.
Results
Fecal testosterone (but not cortisol) levels were directly associated with dominance rank, and both testosterone and cortisol were directly associated with intestinal parasite richness (number of unique species recovered). Dominance rank was directly associated with helminth (but not protozoan) parasite richness, so that high ranking animals had higher testosterone levels and greater helminth burden.
Conclusions
One preliminary interpretation is that the antagonist pleiotropic effects of androgens and glucocorticoids place a cost on attaining and maintaining high dominance rank in this species. Because of the costs associated with elevated steroid levels, dominance status may be an honest signal of survivorship against helminth parasites.
doi:10.1186/1751-0759-4-21
PMCID: PMC3004803  PMID: 21143892
2.  Foci of Endemic Simian Immunodeficiency Virus Infection in Wild-Living Eastern Chimpanzees (Pan troglodytes schweinfurthii) 
Journal of Virology  2003;77(13):7545-7562.
Simian immunodeficiency virus of chimpanzees (SIVcpz) is the immediate precursor to human immunodeficiency virus type 1 (HIV-1), yet remarkably, the distribution and prevalence of SIVcpz in wild ape populations are unknown. Studies of SIVcpz infection rates in wild chimpanzees are complicated by the species' endangered status and by its geographic location in remote areas of sub-Saharan Africa. We have developed sensitive and specific urine and fecal tests for SIVcpz antibody and virion RNA (vRNA) detection and describe herein the first comprehensive prevalence study of SIVcpz infection in five wild Pan troglodytes schweinfurthii communities in east Africa. In Kibale National Park in Uganda, 31 (of 52) members of the Kanyawara community and 39 (of ∼145) members of the Ngogo community were studied; none were found to be positive for SIVcpz infection. In Gombe National Park in Tanzania, 15 (of 20) members of the Mitumba community, 51 (of 55) members of the Kasekela community, and at least 10 (of ∼20) members of the Kalande community were studied. Seven individuals were SIVcpz antibody and/or vRNA positive, and two others had indeterminate antibody results. Based on assay sensitivities and the numbers and types of specimens analyzed, we estimated the prevalence of SIVcpz infection to be 17% in Mitumba (95% confidence interval, 10 to 40%), 5% in Kasekela (95% confidence interval, 4 to 7%), and 30% in Kalande (95% confidence interval, 15 to 60%). For Gombe as a whole, the SIVcpz prevalence was estimated to be 13% (95% confidence interval, 7 to 25%). SIVcpz infection was confirmed in five chimpanzees by PCR amplification of partial pol and gp41/nef sequences which revealed a diverse group of viruses that formed a monophyletic lineage within the SIVcpzPts radiation. Although none of the 70 Kibale chimpanzees tested SIVcpz positive, we estimated the likelihood that a 10% or higher prevalence existed but went undetected because of sampling and assay limitations; this possibility was ruled out with 95% certainty. These results indicate that SIVcpz is unevenly distributed among P. t. schweinfurthii in east Africa, with foci or “hot spots” of SIVcpz endemicity in some communities and rare or absent infection in others. This situation contrasts with that for smaller monkey species, in which infection rates by related SIVs are generally much higher and more uniform among different groups and populations. The basis for the wide variability in SIVcpz infection rates in east African apes and the important question of SIVcpz prevalence in west central African chimpanzees (Pan troglodytes troglodytes) remain to be elucidated.
doi:10.1128/JVI.77.13.7545-7562.2003
PMCID: PMC164799  PMID: 12805455
3.  The Apolipoprotein E (APOE) Gene Appears Functionally Monomorphic in Chimpanzees (Pan troglodytes) 
PLoS ONE  2012;7(10):e47760.
Background
The human apolipoprotein E (APOE) gene is polymorphic, with three primary alleles (E2, E3, E4) that differ at two key non-synonymous sites. These alleles are functionally different in how they bind to lipoproteins, and this genetic variation is associated with phenotypic variation for several medical traits, including cholesterol levels, cardiovascular health, Alzheimer’s disease risk, and longevity. The relative frequencies of these alleles vary across human populations, and the evolution and maintenance of this diversity is much debated. Previous studies comparing human and chimpanzee APOE sequences found that the chimpanzee sequence is most similar to the human E4 allele, although the resulting chimpanzee protein might function like the protein coded for by the human E3 allele. However, these studies have used sequence data from a single chimpanzee and do not consider whether chimpanzees, like humans, show intra-specific and subspecific variation at this locus.
Methodology and Principal Findings
To examine potential intraspecific variation, we sequenced the APOE gene of 32 chimpanzees. This sample included 20 captive individuals representing the western subspecies (P. troglodytes verus) and 12 wild individuals representing the eastern subspecies (P. t. schweinfurthii). Variation in our resulting sequences was limited to one non-coding, intronic SNP, which showed fixed differences between the two subspecies. We also compared APOE sequences for all available ape genera and fossil hominins. The bonobo APOE protein is identical to that of the chimpanzee, and the Denisovan APOE exhibits all four human-specific, non-synonymous changes and appears functionally similar to the human E4 allele.
Conclusions
We found no coding variation within and between chimpanzee populations, suggesting that the maintenance of functionally diverse APOE polymorphisms is a unique feature of human evolution.
doi:10.1371/journal.pone.0047760
PMCID: PMC3480407  PMID: 23112842
4.  Molecular Ecology and Natural History of Simian Foamy Virus Infection in Wild-Living Chimpanzees 
PLoS Pathogens  2008;4(7):e1000097.
Identifying microbial pathogens with zoonotic potential in wild-living primates can be important to human health, as evidenced by human immunodeficiency viruses types 1 and 2 (HIV-1 and HIV-2) and Ebola virus. Simian foamy viruses (SFVs) are ancient retroviruses that infect Old and New World monkeys and apes. Although not known to cause disease, these viruses are of public health interest because they have the potential to infect humans and thus provide a more general indication of zoonotic exposure risks. Surprisingly, no information exists concerning the prevalence, geographic distribution, and genetic diversity of SFVs in wild-living monkeys and apes. Here, we report the first comprehensive survey of SFVcpz infection in free-ranging chimpanzees (Pan troglodytes) using newly developed, fecal-based assays. Chimpanzee fecal samples (n = 724) were collected at 25 field sites throughout equatorial Africa and tested for SFVcpz-specific antibodies (n = 706) or viral nucleic acids (n = 392). SFVcpz infection was documented at all field sites, with prevalence rates ranging from 44% to 100%. In two habituated communities, adult chimpanzees had significantly higher SFVcpz infection rates than infants and juveniles, indicating predominantly horizontal rather than vertical transmission routes. Some chimpanzees were co-infected with simian immunodeficiency virus (SIVcpz); however, there was no evidence that SFVcpz and SIVcpz were epidemiologically linked. SFVcpz nucleic acids were recovered from 177 fecal samples, all of which contained SFVcpz RNA and not DNA. Phylogenetic analysis of partial gag (616 bp), pol-RT (717 bp), and pol-IN (425 bp) sequences identified a diverse group of viruses, which could be subdivided into four distinct SFVcpz lineages according to their chimpanzee subspecies of origin. Within these lineages, there was evidence of frequent superinfection and viral recombination. One chimpanzee was infected by a foamy virus from a Cercopithecus monkey species, indicating cross-species transmission of SFVs in the wild. These data indicate that SFVcpz (i) is widely distributed among all chimpanzee subspecies; (ii) is shed in fecal samples as viral RNA; (iii) is transmitted predominantly by horizontal routes; (iv) is prone to superinfection and recombination; (v) has co-evolved with its natural host; and (vi) represents a sensitive marker of population structure that may be useful for chimpanzee taxonomy and conservation strategies.
Author Summary
Cross-species transmissions of infectious agents from primates to humans have led to major disease outbreaks, with AIDS representing a particularly serious example. It has recently been shown that humans who hunt primates frequently acquire simian foamy virus (SFV) infections. Thus, these viruses have been proposed as an “early warning system” of human exposure to wild primates. In this study, we have tested this concept by developing non-invasive methods to determine the extent to which wild chimpanzees are infected with SFV. We analyzed more than 700 fecal samples from 25 chimpanzee communities across sub-Saharan Africa and obtained viral sequences from a large number of these. SFV was widespread among all chimpanzee subspecies, with infection rates ranging from 44% to 100%. The new viruses formed subspecies-specific lineages consistent with virus/host co-evolution. We also found mosaic sequences due to recombination, indicating that chimpanzees can be infected with multiple viral strains. One chimpanzee harbored an SFV from a monkey species, indicating cross-species transmission in the wild. These data indicate that chimpanzees represent a substantial natural reservoir of SFV. Thus, monitoring humans for these viruses should identify locations where human/chimpanzee encounters are most frequent, and where additional transmissions of chimpanzee pathogens should be anticipated.
doi:10.1371/journal.ppat.1000097
PMCID: PMC2435277  PMID: 18604273

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