Stress, social behaviour, and secondary sexual traits in a male primate.

We examined variation in glucocorticoid levels in the mandrill, a brightly coloured primate species, to identify major social influences on stress hormones, and investigate relationships among glucocorticoid levels, testosterone and secondary sexual ornamentation. We collected a total of 317 fecal samples for 16 adult male mandrills over 13 months, including mating and non-mating periods and periods of both dominance rank stability and instability, and compared fecal glucocorticoid levels with dominance rank, rank stability, presence of receptive females, gastro-intestinal parasite infection, fecal testosterone and facial red coloration. Glucocorticoid levels did not vary systematically with dominance rank, but increased when the dominance hierarchy was unstable, and increased in the presence of receptive females. The relationship between dominance rank and glucocorticoid levels changed direction according to the stability of the dominance hierarchy: glucocorticoid levels were higher in subordinate males under stable conditions, but under conditions of instability higher ranking males had higher glucocorticoid levels. The influence of dominance rank also interacted with the presence of receptive females: glucocorticoids were higher in dominant males than in subordinates, but only during mating periods, suggesting that dominant males are more stressed than subordinates during such periods. These findings support previous studies showing that the relationship between glucocorticoids and dominance rank in male baboons is dependent on the social environment. We also found that males with higher glucocorticoids suffered a higher diversity of gastrointestinal parasite infection, in line with evidence that glucocorticoids suppress the immune system in other species. However, we found no support for the stress-mediated immunocompetence handicap hypothesis for the evolution of condition-dependent ornaments: glucocorticoid and testosterone levels were positively related, rather than the negative relationship predicted by the hypothesis, and we found no relationship between red colour and glucocorticoid levels, suggesting that glucocorticoids do not play a role in translating social conditions or physical health into ornament expression in this species.

The role of Pleistocene refugia and rivers in shaping gorilla genetic diversity in central Africa.

The role of Pleistocene forest refugia and rivers in the evolutionary diversification of tropical biota has been the subject of considerable debate. A range-wide analysis of gorilla mitochondrial and nuclear variation was used to test the potential role of both refugia and rivers in shaping genetic diversity in current populations. Results reveal strong patterns of regional differentiation that are consistent with refugial hypotheses for central Africa. Four major mitochondrial haplogroups are evident with the greatest divergence between eastern (A, B) and western (C, D) gorillas. Coalescent simulations reject a model of recent east-west separation during the last glacial maximum but are consistent with a divergence time within the Pleistocene. Microsatellite data also support a similar regional pattern of population genetic structure. Signatures of demographic expansion were detected in eastern lowland (B) and Gabon/Congo (D3) mitochondrial haplogroups and are consistent with a history of postglacial expansion from formerly isolated refugia. Although most mitochondrial haplogroups are regionally defined, limited admixture is evident between neighboring haplogroups. Mantel tests reveal a significant isolation-by-distance effect among western lowland gorilla populations. However, mitochondrial genetic distances also correlate with the distance required to circumnavigate intervening rivers, indicating a possible role for rivers in partitioning gorilla genetic diversity. Comparative data are needed to evaluate the importance of both mechanisms of vicariance in other African rainforest taxa.

Colonization processes and the maintenance of genetic diversity: insights from a pioneer rainforest tree, Aucoumea klaineana.

Despite recurrent episodes of range expansion and contraction, forest trees often harbour high genetic diversity. Studies of temperate forest trees suggest that prolonged juvenile phase and high pollen flow are the main factors limiting founder effects. Here, we studied the local colonization process of a pioneer rainforest tree in central Africa, Aucoumea klaineana. We identified 87% of parents among trees up to 20-25 years old and could thus compare direct parentage structure data with classical population genetics estimators. In this species, genetic diversity was maintained during colonization. The absence of founder effects was explained by (i) local random mating and (ii) local recruitment, as we showed that 75% of the trees in the close neighbourhood participated in the recruitment of new saplings. Long-distance pollen flow contributed little to genetic diversity: pollen and seed dispersal was mainly within stand (128 and 118 m, respectively). Spatial genetic structure was explained by aggregated seed dispersal rather than by mother-offspring proximity as assumed in classical isolation-by-distance models. Hence, A. klaineana presents a genetic diversity pattern typical of forest trees but does not follow the classical rules by which this diversity is generally achieved. We suggest that while high local genetic variability is of general importance to forest tree survival, the proximate mechanisms by which it is achieved may follow very different scenarios.

Small-scale spatial genetic structure in the Central African rainforest tree species Aucoumea klaineana: a stepwise approach to infer the impact of limited gene dispersal, population history and habitat fragmentation.

Under the isolation-by-distance model, the strength of spatial genetic structure (SGS) depends on seed and pollen dispersal and genetic drift, which in turn depends on local demographic structure. SGS can also be influenced by historical events such as admixture of differentiated gene pools. We analysed the fine-scale SGS in six populations of a pioneer tree species endemic to Central Africa, Aucoumea klaineana. To infer the impacts of limited gene dispersal, population history and habitat fragmentation on isolation by distance, we followed a stepwise approach consisting of a Bayesian clustering method to detect differentiated gene pools followed by the analysis of kinship-distance curves. Interestingly, despite considerable variation in density, the five populations situated under continuous forest cover displayed very similar extent of SGS. This is likely due to an increase in dispersal distance with decreased tree density. Admixture between two gene pools was detected in one of these five populations creating a distinctive pattern of SGS. In the last population sampled in open habitat, the genetic diversity was in the same range as in the other populations despite a recent habitat fragmentation. This result may due to the increase of gene dispersal compensating the effect of the disturbance as suggested by the reduced extent of SGS estimated in this population. Thus, in A. klaineana, the balance between drift and dispersal may facilitate the maintenance of genetic diversity. Finally, from the strength of the SGS and population density, an indirect estimate of gene dispersal distances was obtained for one site: the quadratic mean parent-offspring distance, sigma(g), ranged between 210 m and 570 m.

Social correlates of testosterone and ornamentation in male mandrills.

We investigated relationships between fecal androgen concentrations, facial coloration and behaviour in semi-free-ranging male mandrills. We found that fecal androgen levels were significantly positively related to dominance rank, independent of rank stability and the mating period, suggesting that male mandrills live in a permanently aggressive context in which they must actively maintain their dominance status. Facial red coloration was also significantly related to both fecal androgen levels and rank, with high ranking males having both higher androgen levels and redder faces, although dominant males did not always have the highest androgen levels or the reddest faces. Predictive relationships between androgen levels, coloration and rank were short-term. Androgen concentrations and facial redness both increased in the presence of receptive females, as did the former during periods of rank instability. We conclude that male facial redness is likely to represent an honest signal (to other males) of current androgen status, competitive ability and willingness to engage in fights and that females may also use this to assess male condition. Further, our findings provide support for the "challenge hypothesis" as originally proposed for birds by Wingfield.

Factors affecting fecal glucocorticoid levels in semi-free-ranging female mandrills (Mandrillus sphinx).

Subordinate female cercopithecine primates often experience decreased reproductive success in comparison with high-ranking females, with a later age at sexual maturity and first reproduction and/or longer interbirth intervals. One explanation that has traditionally been advanced to explain this is high levels of chronic social stress in subordinates, resulting from agonistic and aggressive interactions and leading to higher basal levels of glucocorticoids. We assessed the relationships among fecal cortisol levels and reproductive condition, dominance rank, degree of social support, and fertility in female mandrills (Mandrillus sphinx) living in a semi-free-ranging colony in Franceville, Gabon. Lower-ranking females in this colony have a reproductive disadvantage relative to higher-ranking females, and we were interested in determining whether this relationship between dominance rank and reproductive success is mediated through stress hormones. We analyzed 340 fecal samples from 19 females, collected over a 14-month period. We found that pregnant females experienced higher fecal cortisol levels than cycling or lactating females. This is similar to results for other primate species and is likely owing to increased metabolic demands and interactions between the hypothalamus-pituitary-adrenal axis, estrogen, and placental production of corticotrophin releasing hormones during pregnancy. There was no influence of dominance rank on fecal cortisol levels, suggesting that subordinate females do not suffer chronic stress. This may be because female mandrills have a stable social hierarchy, with low levels of aggression and high social support. However, we found no relationship between matriline size, as a measure of social support, and fecal cortisol levels. Subordinates may be able to avoid aggression from dominants in the large enclosure or may react only transiently to specific aggressive events, rather than continuously expecting them. Finally, we found no relationship between fecal cortisol levels and fertility. There was no difference in fecal cortisol levels between conceptive and nonconceptive cycles, and no significant relationship between fecal cortisol level and either the length of postpartum amenorrhea or the number of cycles before conception. This suggests that the influence of dominance rank on female reproductive success in this population is not mediated through chronic stress in subordinate females, and that alternative explanations of the relationship between social rank and reproduction should be sought.

Complex phylogeographic history of central African forest elephants and its implications for taxonomy.

BACKGROUND: Previous phylogenetic analyses of African elephants have included limited numbers of forest elephant samples. A large-scale assessment of mitochondrial DNA diversity in forest elephant populations here reveals a more complex evolutionary history in African elephants as a whole than two-taxon models assume. RESULTS: We analysed hypervariable region 1 of the mitochondrial control region for 71 new central African forest elephants and the mitochondrial cytochrome b gene from 28 new samples and compare these sequences to other African elephant data. We find that central African forest elephant populations fall into at least two lineages and that west African elephants (both forest and savannah) share their mitochondrial history almost exclusively with central African forest elephants. We also find that central African forest populations show lower genetic diversity than those in savannahs, and infer a recent population expansion. CONCLUSION: Our data do not support the separation of African elephants into two evolutionary lineages. The demographic history of African elephants seems more complex, with a combination of multiple refugial mitochondrial lineages and recurrent hybridization among them rendering a simple forest/savannah elephant split inapplicable to modern African elephant populations.

Signal content of red facial coloration in female mandrills (Mandrillus sphinx).

Studies of secondary sexual ornamentation and its maintenance by sexual selection tend to focus on males; however, females may also possess showy ornaments. For example, female mandrills possess facial coloration that ranges from black to bright pink. We used fortnightly photographs of 52 semi-free-ranging females aged above 3years over 19 months to evaluate whether colour conveys information concerning female competitive ability, reproductive quality, age or reproductive status. Colour was not related to female rank or quality (body mass index, age at first birth or mean inter-birth interval); however, colour did increase significantly with age and primiparous females were darker than multiparous females. Colour may therefore signal reproductive quality, as younger females are less fertile and produce smaller offspring. Colour was brighter during the follicular phase than during the luteal phase, suggesting that it may signal fertility. Colour also varied across gestation and peaked at four and eight weeks post-parturition, suggesting that it may signal approaching parturition and lactation. Future studies should examine the relationship between colour and the menstrual cycle in more detail, the hormonal basis of female colour, and determine experimentally whether mandrills of both sexes attend to differences in colour between and within females.

Ten days in the life of a mandrill horde in the Lopé Reserve, Gabon.

Mandrills have long been known to form large aggregations in the wild, but it has proved difficult to obtain detailed information on the socioecology of these groups. An unusually large (>600) horde of mandrills was followed for ten days during the 1995 dry season in Central Gabon, and data were collected on group composition and ecology while the mandrills were in an area of forest-savanna mosaic habitat in the north of the Lopé Reserve. Three separate counts of most of the group showed that fully coloured "fatted" adult males were present throughout the horde at a mean ratio to other individuals of 1:21. Paler "non-fatted" adult and sub-adult males were also distributed throughout. Mandrill diet over the ten days consisted mainly of insects, seeds from forest trees, and leaves or stems of understory herbaceous plants. Feeding was extremely selective, with most food items consumed in a much higher proportion than would be predicted from their relative availability. Ranging data also showed that the mandrills foraged preferentially in certain forest types within the forest-savanna mosaic, namely in Marantaceae and Rocky Forest. It is suggested that one reason why mandrills pass through gallery forests and forest-savanna mosaic in the dry season in the Lopé Reserve is because they find fruit there from preferred species, which are no longer fruiting in the main forest block, thus allowing them to maintain the fruit component of their diet at a time of fruit shortage. © 1996 Wiley-Liss, Inc.

Canine tooth size and fitness in male mandrills (Mandrillus sphinx).

Sexual selection theory explains the evolution of exaggerated male morphologies and weaponry, but the fitness consequences of developmental and age-related changes in these features remain poorly understood. This long-term study of mandrill monkeys (Mandrillus sphinx) demonstrates how age-related changes in canine tooth weaponry and adult canine size correlate closely with male lifetime reproductive success. Combining long-term demographic and morphometric data reveals that male fitness covaries simply and directly with canine ontogeny, adult maximum size, and wear. However, fitness is largely independent of other somatometrics. Male mandrills sire offspring almost exclusively when their canines exceed approximately 30 mm, or two-thirds of average adult value (45 mm). Moreover, sires have larger canines than nonsires. The tooth diminishes through wear as animals age, corresponding with, and perhaps influencing, reproductive senescence. These factors combine to constrain male reproductive opportunities to a brief timespan, defined by the period of maximum canine length. Sexually-selected weaponry, especially when it is nonrenewable like the primate canine tooth, is intimately tied to the male life course. Our analyses of this extremely dimorphic species indicate that sexual selection is closely intertwined with growth, development, and aging, pointing to new directions for sexual selection theory. Moreover, the primate canine tooth has potential as a simple mammalian system for testing genetically-based models of aging. Finally, the tooth may record details of life histories in fossil primates, especially when sexual selection has played a role in the evolution of dimorphism.

Distinguishing gorilla mitochondrial sequences from nuclear integrations and PCR recombinants: guidelines for their diagnosis in complex sequence databases.

Nuclear integrations of mitochondrial DNA (Numts) are widespread in many taxa and if left undetected can confound phylogeny interpretation and bias estimates of mitochondrial DNA (mtDNA) diversity. This is particularly true in gorillas, where recent studies suggest multiple integrations of the first hypervariable (HV1) domain of the mitochondrial control region. Problems can also arise through the inadvertent incorporation of artifacts produced by in vitro recombination between sequence types during polymerase chain reaction amplification. This issue has attracted little attention yet could potentially exacerbate errors in databases already contaminated by Numts. Using a set of existing diagnostic tools, this study set out to systematically inventory Numts and PCR recombinants in a gorilla HV1 sequence database and address the degree to which existing public databases are contaminated. Phylogenetic analysis revealed three distinct gorilla HV1 Numt groups (I, II, and III) that could be readily differentiated from mtDNA sequences by Numt-specific diagnostic sites and sequence-based motifs. Several instances of genuine recombination were also identified by a suite of detection methods. The location of putative breakpoints was identified by eye and by likelihood analysis. Findings from this study reveal widespread nuclear contamination of gorilla HV1 GenBank databases and underline the importance of recognizing not only Numts but also PCR recombinant artifacts as potential sources of data contamination. Guidelines for the routine identification of Numts and in vitro recombinants are presented and should prove useful in the detection of similar artifacts in other species mtDNA databases.

High levels of diversity characterize mandrill (Mandrillus sphinx) Mhc-DRB sequences.

The major histocompatibility complex (MHC) is highly polymorphic in most primate species studied thus far. The rhesus macaque (Macaca mulatta) has been studied extensively and the Mhc-DRB region demonstrates variability similar to humans. The extent of MHC diversity is relatively unknown for other Old World monkeys (OWM), especially among genera other than Macaca. A molecular survey of the Mhc-DRB region in mandrills (Mandrillus sphinx) revealed extensive variability, suggesting that other OWMs may also possess high levels of Mhc-DRB polymorphism. In the present study, 33 Mhc-DRB loci were identified from only 13 animals. Eleven were wild-born and presumed to be unrelated and two were captive-born twins. Two to seven different sequences were identified for each individual, suggesting that some mandrills may have as many as four Mhc-DRB loci on a single haplotype. From these sequences, representatives of at least six Mhc-DRB loci or lineages were identified. As observed in other primates, some new lineages may have arisen through the process of gene conversion. These findings indicate that mandrills have Mhc-DRB diversity not unlike rhesus macaques and humans.

Life history in male mandrills (Mandrillus sphinx): physical development, dominance rank, and group association.

We assess life history from birth to death in male mandrills (Mandrillus sphinx) living in a semifree-ranging colony in Gabon, using data collected for 82 males that attained at least the age of puberty, including 33 that reached adulthood and 25 that died, yielding data for their entire lifespan. We describe patterns of mortality and injuries, dominance rank, group association, growth and stature, and secondary sexual character expression across the male lifespan. We examine relationships among these variables and investigate potential influences on male life history, including differences in the social environment (maternal rank and group demography) and early development, with the aim of identifying characteristics of successful males. Sons of higher-ranking females were more likely to survive to adulthood than sons of low-ranking females. Adolescent males varied consistently in the rate at which they developed, and this variation was related to a male's own dominance rank. Males with fewer peers and sons of higher-ranking and heavier mothers also matured faster. However, maternal variables were not significantly related to dominance rank during adolescence, the age at which males attained adult dominance rank, or whether a male became alpha male. Among adult males, behavior and morphological development were related to a male's own dominance rank, and sons of high-ranking females were larger than sons of low-ranking females. Alpha males were always the most social, and the most brightly colored males, but were not necessarily the largest males present. Finally, alpha male tenure was related to group demography, with larger numbers of rival adult males and maturing adolescent males reducing the time a male spent as alpha male. Tenure did not appear to be related to characteristics of the alpha male himself.

Violent coalitionary attack by female mandrills against an injured alpha male.

Female contact aggression against males is relatively rare in species in which the adult males are larger than the females, but it has the potential to influence group structure, male group membership, tenure, and dominance rank. We report an incident in which female mandrills living in a semi-free-ranging group in Franceville, Gabon, attacked a male that was apparently incapacitated after a fight with another male and was unable to escape. The attack involved the alpha male and did not occur in a sexual or infanticidal context. Other adult and adolescent males observed the attack, but when one adult male attempted to participate he was chased away by the females. This observation adds to reports of female coalitions excluding unwanted males from primate groups, or even killing them. The fact that this can also occur in mandrills suggests that females have a degree of control over male group membership, despite the large degree of sexual dimorphism in this species, and highlights the importance of coalitions in primate social organization.

Social and seasonal influences on the reproductive cycle in female mandrills (Mandrillus sphinx).

We present 12 years of perineal swelling data for a semifree-ranging colony of mandrills (Mandrillus sphinx), and evaluate the influence of rank, parity, and seasonality on reproductive parameters. Female sexual swellings showed a seasonal pattern, with August the median month of ovulation. Overlapping periovulatory periods did not decrease the likelihood of conception. Females showed their first genital swelling at age 3.6 years (n = 28; range, 3.2-4.6 years), and higher-ranking females experienced their first swelling earlier than low-ranking females. Median postpartum amenorrhea (PPA) duration was 208 days (n = 92; range, 74-538 days). PPA was longer in primiparous females than in multiparous females, but PPA duration was unrelated to female rank. Median follicular phase duration was 24 days for the first cycle after parturition (n = 84; range, 12-40 days), shortening to 17 days in subsequent cycles (n = 55; range, 6-39 days). The follicular phase was longer in nulliparous females than in parous females, but was unrelated to female rank. Median cycle length (from one sexual swelling breakdown to the next) was 38 days (n = 57; range, 18-108 days). Eighty-seven percent of conceptions occurred within two cycles, and half of the nulliparous females conceived during their first swelling cycle. Lower-ranking females were more likely to require more cycles to conceive than higher-ranking females. The cycling phase was significantly longer in nulliparous females than in parous females, and was also significantly longer in lower-ranking females than in higher-ranking females. We discuss the influence of provisioning on female reproductive parameters, the influence of parity and rank on the different phases of the interbirth interval, and the evolution of long and variable follicular phases in mandrills.

Sequences and timing of dental eruption in semi-free-ranging mandrills (Mandrillus sphinx).

The chronology of tooth emergence is often used to examine the growth and development of individuals and to compare life histories across species. Emergence patterns are also used to age animals and to infer life history influences for extinct species. However, comparative studies of primates are hindered by a lack of dental development data for many species. Here we describe the sequences and timing of tooth emergence for a large sample of semi-free-ranging mandrills (Mandrillus sphinx) and compare this with other life history variables for this species. Deciduous dentition emerged in the sequence i1 i2 c p3 p4. The augmented sequence (including information about variability in emergence sequence) was i1 i2 [c p3] p4 for the female maxilla and the male mandible, and i1 i2 c p3 p4 for the female mandible and the male maxilla. Deciduous dentition was complete by 5.0 months in females and 6.4 months in males. The permanent dentition began to emerge at 26 months, and complete adult dentition had emerged by 68 months for males and 85 months for females. Sex differences occurred in the augmented eruption sequences: females M1 I1 I2 [M2 C] P3 P4 M3, males M1 I1 [I2 M2] [P4 = P3 = C] M3. The order of tooth eruption and the occurrence of sequence polymorphisms were very similar to those observed for baboons and macaques. Comparison with life history variables showed that mandrills have complete deciduous dentition at weaning, females possess both adult incisors and M1 when they first reproduce, but still have deciduous canines and premolars, and that both sexes have full adult dentition before they attain their full adult stature and mass.

Changes in social interactions during adolescence in male mandrills (Mandrillus sphinx).

The adolescent period in male mandrills extends from the time the testicles descend (at the age of 3-4 years) to the time adult characteristics develop (at the age of 10 years), and is thus one of the longest adolescent periods in cercopithecines. In this short cross-sectional study of 11 male mandrills (4.7-9.1 years old), we analyzed social behavioral patterns to investigate partner preference and changes in types of interactions throughout puberty. The mandrills were separated into two clusters on the basis of all of the social interactions scored, as well as the age and sex of the protagonist. During early to mid puberty, immature individuals interacted preferentially with other male adolescents and juveniles. Playing was an important activity, and some affiliative interactions with juveniles were observed. Older adolescents interacted more with adult males and females. These older adolescents were predominantly aggressive toward other adolescents, females, and juveniles, and showed little or no affiliative or playful behaviors. These results indicate a shift in social partners: older males interacted more frequently with adult males, and their behavior involved more aggression and less submission compared to younger adolescents, which showed predominantly submissive and playful behavior. These changes are consistent with preparation for dispersal and future intermale competition.

Mitochondrial DNA phylogeography of western lowland gorillas (Gorilla gorilla gorilla).

The geographical distribution of genetic variation within western lowland gorillas (Gorilla gorilla gorilla) was examined to clarify the population genetic structure and recent evolutionary history of this group. DNA was amplified from shed hair collected from sites across the range of the three traditionally recognized gorilla subspecies: western lowland (G. g. gorilla), eastern lowland (G. g. graueri) and mountain (G. g. beringei) gorillas. Nucleotide sequence variation was examined in the first hypervariable domain of the mitochondrial control region and was much higher in western lowland gorillas than in either of the other two subspecies. In addition to recapitulating the major evolutionary split between eastern and western lowland gorillas, phylogenetic analysis indicates a phylogeographical division within western lowland gorillas, one haplogroup comprising gorilla populations from eastern Nigeria through to southeast Cameroon and a second comprising all other western lowland gorillas. Within this second haplogroup, haplotypes appear to be partitioned geographically into three subgroups: (i) Equatorial Guinea, (ii) Central African Republic, and (iii) Gabon and adjacent Congo. There is also evidence of limited haplotype admixture in northeastern Gabon and southeast Cameroon. The phylogeographical patterns are broadly consistent with those predicted by current Pleistocene refuge hypotheses for the region and suggest that historical events have played an important role in shaping the population structure of this subspecies.