Opposites attract: MHC-associated mate choice in a polygynous primate.

We investigated reproduction in a semi-free-ranging population of a polygynous primate, the mandrill, in relation to genetic relatedness and male genetic characteristics, using neutral microsatellite and major histocompatibility complex (MHC) genotyping. We compared genetic dissimilarity to the mother and genetic characteristics of the sire with all other potential sires present at the conception of each offspring (193 offspring for microsatellite genetics, 180 for MHC). The probability that a given male sired increased as pedigree relatedness with the mother decreased, and overall genetic dissimilarity and MHC dissimilarity with the mother increased. Reproductive success also increased with male microsatellite heterozygosity and MHC diversity. These effects were apparent despite the strong influence of dominance rank on male reproductive success. The closed nature of our study population is comparable to human populations for which MHC-associated mate choice has been reported, suggesting that such mate choice may be especially important in relatively isolated populations with little migration to introduce genetic variation.

Life history correlates of inbreeding depression in mandrills (Mandrillus sphinx).

Inbreeding depression reflects the negative consequences of increased homozygosity at genes that affect fitness. We investigate inbreeding depression in a semi-free-ranging colony of mandrills (Mandrillus sphinx), using high-quality pedigree data, comprising five maternal generations and 20 years of morphological and demographic data. We examine the relationship between inbreeding coefficients and four fitness correlates: two growth parameters (mass and height for age) and longevity in both sexes, and age at first conception in females. Inbreeding was correlated with both growth parameters, but only in females, with inbred females being smaller than noninbred females. Inbreeding was also correlated significantly with age at first conception, with inbred females giving birth earlier in life than noninbred females. We suggest that sex-biased maternal investment may explain this sex-differential response to inbreeding, although the lack of a significant association between inbreeding and growth in males may also be due to the provisioned nature of the colony. The surprising relationship between age at first conception and inbreeding may be related to smaller adult size in inbred females, or to their being less able to escape from male sexual coercion.

Genetic diversity and reproductive success in mandrills (Mandrillus sphinx).

Recent studies of wild animal populations have shown that estimators of neutral genetic diversity, such as mean heterozygosity, are often correlated with various fitness traits, such as survival, disease susceptibility, or reproductive success. We used two estimators of genetic diversity to explore the relationship between heterozygosity and reproductive success in male and female mandrills (Mandrillus sphinx) living in a semifree ranging setting in Gabon. Because social rank is known to influence reproductive success in both sexes, we also examined the correlation between genetic diversity and social rank in females, and acquisition of alpha status in males, as well as length of alpha male tenure. We found that heterozygous individuals showed greater reproductive success, with both females and males producing more offspring. However, heterozygosity influenced reproductive success only in dominant males, not in subordinates. Neither the acquisition of alpha status in males, nor social rank in females, was significantly correlated with heterozygosity, although more heterozygous alpha males showed longer tenure than homozygous ones. We also tested whether the benefits of greater genetic diversity were due mainly to a genome-wide effect of inbreeding depression or to heterosis at one or a few loci. Multilocus effects best explained the correlation between heterozygosity and reproductive success and tenure, indicating the occurrence of inbreeding depression in this mandrill colony.

Identification of hepatitis B virus genome in faecal sample from wild living chimpanzee (Pan troglodytes troglodytes) in Gabon.

Non-invasive faecal sampling in the equatorial forest in Gabon allowed the first identification of the hepatitis B virus (HBV-Ch(RC170)) genome in samples collected from wild chimpanzees (Pan troglodytes troglodytes). The HBV-Ch(RCl70)sequence clustered with 100% bootstrap support with previous viral sequences obtained from Pan troglodytes subspecies. This is the first evidence of HBV infection in wild apes and confirms that the HBV-like strains thus far characterized in captive apes are directly related to those circulating in the wild.

Two distinct STLV-1 subtypes infecting Mandrillus sphinx follow the geographic distribution of their hosts.

The mandrill (Mandrillus sphinx) has been shown to be infected with an STLV-1 closely related to HTLV-1. Two distinct STLV-1 subtypes (D and F) infect wild mandrills with high overall prevalence (27.0%) but are different with respect to their phylogenetic relationship and parallel to the mandrills' geographic range. The clustering of these new STLV-1mnd sequences with HTLV-1 subtype D and F suggests first, past simian-to-human transmissions in Central Africa and second, that species barriers are easier to cross over than geographic barriers.

Occurrence of hepatitis viruses in wild-born non-human primates: a 3 year (1998-2001) epidemiological survey in Gabon.

Hepatitis B and C infections are endemic in human population in central Africa, particularly in Gabon. The aim of this study was to determine the prevalence of hepatitis B virus (HBV) and eventual occurrence of hepatitis C virus (HBC)-related strains in a variety of wild-born non-human primates living in Gabon and Congo. Plasma samples were screened for HBV and HCV markers. A non-invasive method of DNA extraction from faeces followed by specific HBV-DNA amplification was developed to study this infection in wild troops of chimpanzees and gorillas. No HCV infection in non-human primates, wild-born or captive, was detected among 596 samples tested. No HBV infection could be detected in samples tested and obtained from Cercopithecidae. In contrast, 14.7 and 42.2% of wild-born chimpanzees in Gabon and Congo were infected with HBV or had evidence of past HBV infection. At Centre International de Recherches Médicales (CIRMF) Primate Centre, 32.1% of chimpanzees and gorillas were HBV positive or had evidence of past infection. In the cases with past infection, 5.9% wild-born and 8.3% at CIRMF harboured HBV-DNA despite the presence of neutralizing HbsAb. Together with previous findings, we confirm the high HBV prevalence not only in humans but also in chimpanzees and gorillas in Gabon and Congo.

Molecular evidence for deep phylogenetic divergence in Mandrillus sphinx.

Mandrills (Mandrillus sphinx) are forest primates indigenous to western central Africa. Phylogenetic analysis of 267 base pairs (bp) of the cytochrome b gene from 53 mandrills of known and 17 of unknown provenance revealed two phylogeographical groups, with haplotypes differentiated by 2.6% comprising seven synonymous transitions. The distribution of the haplotypes suggests that the Ogooué River, Gabon, which bisects their range, separates mandrill populations in Cameroon and northern Gabon from those in southern Gabon. The haplotype distribution is also concordant with that of two known mandrill simian immunodeficiency viruses, suggesting that these two mandrill phylogroups have followed different evolutionary trajectories since separation.

A preliminary study on the social relationships in a semi-free ranging colony of sun-tailed monkeys (Cercopithecus solatus), a species recently discovered in Gabon.

In 1984, a species of guenon endemic to Gabon was discovered: the sun-tailed monkey (Cercopithecus solatus). This species is difficult to locate and observe in the wild, and hence to date has been little studied. The Centre International de Recherches Medicales de Franceville (CIRMF), Gabon, houses the world's only breeding colony of C. solatus, on which eco-ethological investigations can be carried out in a semi-free ranging environment. The data reported here present the first results of observations on the social relationships of this colony and support the scant field observations available on this species, showing a basic social unit of one adult male and several females with their offspring. The resident male systematically repulses any second adult male in proximity to the group. A clear hierarchy exists among the females, with mature female offspring eventually acquiring a rank just below that of their mother.

Growth and ontogeny of sexual size dimorphism in the mandrill (Mandrillus sphinx).

We present body mass (N = 419) and crown-rump length (CRL, N = 210) measurements from 38 male and 49 female mandrills born into a semifree-ranging colony in order to describe growth from birth to adulthood, and to investigate maternal influences upon growth. Adult male mandrills are 3.4 times the body mass, and 1.3 times the CRL, of adult females. Body mass dimorphism arises from a combination of sex differences in length of the growth period (females attain adult body mass at 7 years, males at 10 years) and growth rate. Both sexes undergo a subadult growth spurt in body mass, and this is much more dramatic in males (peak velocity 551 g/months +/- 89 SEM at 84-96 months). CRL dimorphism arises from bimaturism (females attain adult CRL at 6 years, males after 10 years), and neither sex shows a particular subadult growth spurt in CRL. Sexual size dimorphism thus represents important time and metabolic costs to males, who mature physically approximately 3-4 years after females. Considerable interindividual variation occurs in the size-for-age of both sexes, which is related to maternal variables. Older mothers have heavier offspring than do younger mothers, and higher-ranking mothers have heavier offspring than do lower ranking mothers. Mass advantages conferred upon offspring during lactation by older and higher-ranking mothers tend to persist postweaning in both sexes. Thus maternal factors affect reproductive success in both sexes, influencing the age at which offspring mature and begin their reproductive career.

Wild Mandrillus sphinx are carriers of two types of lentivirus.

Mandrillus sphinx, a large primate living in Cameroon and Gabon and belonging to the Papionini tribe, was reported to be infected by a simian immunodeficiency virus (SIV) (SIVmndGB1) as early as 1988. Here, we have identified a second, highly divergent SIVmnd (designated SIVmnd-2). Genomic organization differs between the two viral types; SIVmnd-2 has the additional vpx gene, like other SIVs naturally infecting the Papionini tribe (SIVsm and SIVrcm) and in contrast to the other SIVmnd type (here designated SIVmnd-1), which is more closely related to SIVs infecting l'hoest (Cercopithecus lhoesti lhoesti) and sun-tailed (Cercopithecus lhoesti solatus) monkeys. Importantly, our epidemiological studies indicate a high prevalence of both types of SIVmnd; all 10 sexually mature wild-living monkeys and 3 out of 17 wild-born juveniles tested were infected. The geographic distribution of SIVmnd seems to be distinct for the two types: SIVmnd-1 viruses were exclusively identified in mandrills from central and southern Gabon, whereas SIVmnd-2 viruses were identified in monkeys from northern and western Gabon, as well as in Cameroon. SIVmnd-2 full-length sequence analysis, together with analysis of partial sequences from SIVmnd-1 and SIVmnd-2 from wild-born or wild-living mandrills, shows that the gag and pol regions of SIVmnd-2 are closest to those of SIVrcm, isolated from red-capped mangabeys (Cercocebus torquatus), while the env gene is closest to that of SIVmnd-1. pol and env sequence analyses of SIV from a related Papionini species, the drill (Mandrillus leucophaeus), shows a closer relationship of SIVdrl to SIVmnd-2 than to SIVmnd-1. Epidemiological surveys of human immunodeficiency virus revealed a case in Cameroon of a human infected by a virus serologically related to SIVmnd, raising the possibility that mandrills represent a viral reservoir for humans similar to sooty mangabeys in Western Africa and chimpanzees in Central Africa.

Corticotropin-releasing hormone in chimpanzee and gorilla pregnancies.

In humans, the length of gestation and the onset of parturition have been linked to the exponential production of placental CRH and a late gestational decline in maternal plasma CRH-binding protein (CRH-BP). CRH has been shown to have direct effects on the myometrium and on the fetal adrenal, where it stimulates production of the estrogen precursor dihydroepiandrosterone sulfate. In vitro placental CRH production is stimulated by cortisol and inhibited by progesterone. To determine whether this mechanism might operate in other apes, we sampled eight chimpanzees and two gorillas through their pregnancies for CRH, CRH-BP, cortisol, estradiol, progesterone, and alpha-fetoprotein. We show that both chimpanzee and gorilla maternal plasma CRH concentrations rise exponentially as observed in the human. The gorillas exhibited a human-like antepartum fall in CRH-BP, whereas CRH-BP in the chimpanzee remained stable. Pregnancy-associated changes in cortisol, estradiol, progesterone, and alpha-fetoprotein were qualitatively similar to those observed in humans. Maternal plasma cortisol correlated with plasma CRH in both gorillas (r = 0.60; P < 0.05) and chimpanzees (r = 0.36; P < 0.02). Further, there was a strong correlation between plasma estradiol and the log of plasma CRH in the gorilla (r = 0.93; P < 0.0001) and in the chimpanzee (r = 0.72; P < 0.001), which is consistent with the hypothesis that placental CRH determines the placental production of estradiol by stimulating the production of fetal adrenal dehydroepiandrosterone sulfate. Plasma CRH and progesterone were positively correlated providing no in vivo support for progesterone inhibition of CRH release.

Ebola hemorrhagic fever outbreaks in Gabon, 1994-1997: epidemiologic and health control issues.

From the end of 1994 to the beginning of 1995, 49 patients with hemorrhagic symptoms were hospitalized in the Makokou General Hospital in northeastern Gabon. Yellow fever (YF) virus was first diagnosed in serum by use of polymerase chain reaction followed by blotting, and a vaccination campaign was immediately instituted. The epidemic, known as the fall 1994 epidemic, ended 6 weeks later. However, some aspects of this epidemic were atypical of YF infection, so a retrospective check for other etiologic agents was undertaken. Ebola (EBO) virus was found to be present concomitantly with YF virus in the epidemic. Two other epidemics (spring and fall 1996) occurred in the same province. GP and L genes of EBO virus isolates from all three epidemics were partially sequenced, which showed a difference of <0.1% in the base pairs. Sequencing also showed that all isolates were very similar to subtype Zaire EBO virus isolates from the Democratic Republic of the Congo.

Protein deficiency in a colony of western lowland gorillas (Gorilla g. gorilla)

A syndrome of alopecia and weight loss in a colony of 10 western lowland gorillas (Gorilla gorilla gorilla) in Gabon during a 3-yr period was apparently due to a dietary protein deficiency, with nine individuals affected to some extent. The most severely afflicted was a 4-yr-old female who eventually died as a result of acute gastroenteritis caused by Shigella flexneri. Clinical signs included chronic alopecia, hair discoloration, failure to thrive, and weight loss, and their severity was directly correlated with the degree of hypoalbuminemia (12 g/L in the most extreme case) and normocytic normochromic anemia. Preliminary clinical tests and autopsy results suggested a dietary protein or amino acid deficiency as the cause of the hypoalbuminemia, and further analyses of serum amino acid and protein levels were consistent with a diagnosis of dietary protein deficiency. Supplementation of the colony diet with a protein preparation for humans produced a rapid amelioration of signs and improvement in body and coat condition, a normalization of serum albumin and total protein levels, and disappearance of the anemia in all affected animals except a 12-yr-old male, who responded well to treatment with anabolic steroids. The natural diet of western lowland gorillas is surprisingly high in protein, and the dietary protein requirement of captive gorillas may be increased as a result of the absence of commensal gastrointestinal ciliates.

Phylogenetic analysis of SIV and STLV type I in mandrills (Mandrillus sphinx): indications that intracolony transmissions are predominantly the result of male-to-male aggressive contacts.

Natural SIVmnd and STLVmnd infections of mandrills in a colony at the Centre International de Recherches Médicales de Franceville (CIRMF) in Gabon were investigated by genetic analysis to determine the extent of intracolony transmission. SIVmnd pol sequence analysis indicates that the six strains present in the colony belong to the SIVmnd lentivirus subgroup previously defined according to the only available prototype sequence (SIVmndGB1), which originated from the same colony. The intraanimal nucleotide diversity (1.1-3.1%) was similar in range to that reported in individuals infected by other HIV/SIVs. The interanimal diversity (0.5-4.3%) was not significantly different from that observed in each individual mandrill, indicating an epidemiological link among the SIVmnd isolates of distinct animals within the colony. Phylogenetic analysis of these isolates, together with seroepidemiological and behavior surveillance within the colony, indicates a predominant male-to-male transmission of SIVmnd that probably occurred during bouts of interanimal aggression. Moreover, our results suggest one case of vertical transmission of SIVmnd from a naturally infected founder female to one of her six offspring. The first genetic analysis of STLV isolates from mandrills is also reported here. Partial tax/rex sequences were used to evaluate the diversity between seven STLVmnd isolates and their phylogenetic relationships with other known strains of human and nonhuman primate T cell leukemia virus, types I and II (PTLV-I/II). They all belong to the PTLV-I subtype, but two genetically distinct STLVmnd groups were evidenced within the mandrill colony. The phylogenetic analyses of the STLVmnd isolates, together with seroepidemiological and behavior surveillance of the mandrills, indicate that intracolony transmissions of STLVmnd are also predominantly the result of male-to-male aggressive contacts.

Characterization of chimpanzee TCRV gene polymorphism: how old are human TCRV alleles?

The functional relevance of the majority of human T-cell receptor A and B variable region gene polymorphisms is controversial. Studies of human and nonhuman primate major histocompatibility complex (MHC) class I and II polymorphisms show that allelic lineages predate human speciation and indicate that selection favors the long-term maintenance of these advantageous mutations. We investigated at the DNA level whether 15 human TCRA and B polymorphisms exist in contemporary chimpanzee populations. Polymorphisms consisted of variable region replacements, a recombination signal sequence base change, and silent mutations. With one exception, none of these human TCR polymorphisms were observed in contemporary chimpanzees. Investigation of the same polymorphisms in a range of other nonhuman primates showed little evidence of the existence of human polymorphism prespeciation. Chimpanzee TCRAV and BV regions were however polymorphic for variation so far not observed in human groups. Levels of mitochondrial and nuclear DNA sequence variation in contemporary chimpanzees suggest that population bottlenecks have not been a feature of chimpanzee evolution and it is therefore probable that most human TCR polymorphisms have evolved in the estimated five million years since the speciation of human and chimpanzees. Thus, over the evolutionary time period studied, ancient TCRA and B polymorphisms have not been maintained by selection to the same degree as postulated for MHC polymorphisms.

Occurrence and frequency of transmission of naturally occurring simian retroviral infections (SIV, STLV, and SRV) at the CIRMF Primate Center, Gabon.

Among the primates held at the CIRMF Primate Center, Gabon, no serological sign of SIV infection could be demonstrated in 68 cynomolgus monkeys, 60 chimpanzees, nine gorillas, and 12 sun-tailed monkeys, while seven of 102 mandrills and six of 24 vervets were infected with SIV. Six mandrills, seven vervets and ten cynomolgus monkeys exhibited a full HTLV type 1 Western blot profile. The sera of two gorillas and one chimpanzee presented with a positive but not typical HTLV Western blot profile. The sera of the gorillas lacked p24 antibodies, and the chimpanzee had a Western blot profile evocative of HTLV-II. All attempts to amplify viruses from these animals by PCR were unsuccessful. Two other chimpanzees and seven gorillas presented with indeterminate HTLV Western blot profiles. In the mandrill colony, only male animals were STLV seropositive and no sexual transmission to females was observed. SIV infection was also more frequent in male than female mandrills and sexual transmission appeared to be a rare event. No SRV infection was observed in macaques.

The effect of increased salt intake on blood pressure of chimpanzees.

A colony of 26 chimpanzees given a fruit and vegetable diet of very low Na and high K intake were maintained in long-standing, socially stable small groups for three years. Half of them had salt added progressively to their diet during 20 months. This addition of salt within the human dietetic range caused a highly significant rise in systolic, mean and diastolic blood pressure. The change reversed completely by six months after cessation of salt. The effect of salt differed between chimpanzees, some having a large blood pressure rise and others small or no rise. These results in the species phylogenetically closest to humans bear directly on causation of human hypertension, particularly in relation to migration of preliterate people, with low Na diet, to a Western urban lifestyle with increased salt intake. The hedonic liking for salt and avid ingestion was apt during human prehistory involving hunter-gatherer-scavenger existence in the interior of continents with a scarcity of salt, but is maladaptive in urban technological life with salt cheap and freely available.