Gottfried Hohmann

Amplification of hypervariable simple sequence repeats (microsatellites) from excremental DNA of wild living bonobos (Pan paniscus)

We show that nuclear DNA extracted from faeces of free living bonobos (Pan paniscus) can be used to amplify hypervariable simple sequence repeats, which can be used for paternity analysis and kinship studies. Of 130 DNA extractions of samples from 33 different animals, about two‐thirds yielded PCR products at the first attempt. For several samples only a second extraction resulted in positive amplifications. Consistency tests revealed that in some cases only one of the two alleles was amplified. Presumably this is due to a very limited amount of bonobo DNA in the sample and we suggest therefore that a sample found to be homozygous at a given locus should be typed repeatedly for verification.

Intracommunity relationships, dispersal pattern and paternity success in a wild living community of Bonobos (Pan paniscus) determined from DNA analysis of faecal samples

Differences in social relationships among community members are often explained by differences in genetic relationships. The current techniques of DNA analysis allow explicit testing of such a hypothesis. Here, we have analysed the genetic relationships for a community of wild bonobos (Pan paniscus) using nuclear and mitochondrial DNA markers extracted from faecal samples. Bonobos show an opportunistic and promiscuous mating behaviour, even with mates from outside the community. Nonetheless, we find that most infants were sired by resident males and that two dominant males together attained the highest paternity success. Intriguingly, the latter males are the sons of high-ranking females, suggesting an important influence of mothers on the paternity success of their sons. The molecular data support previous inferences on female dispersal and male philopatry. We find a total of five different mitochondrial haplotypes among 15 adult females, suggesting a frequent migration of females. Moreover, for most adult and subadult males in the group we find a matching mother, while this is not the case for most females, indicating that these leave the community during adolescence. Our study demonstrates that faecal samples can be a useful source for the determination of kinship in a whole community.

Use and function of genital contacts among female bonobos

Female bonobos, Pan paniscus, show a mounting behaviour that differs physically from that in other primate species. They embrace each other ventroventrally and rub their genital swellings against each other. We investigated five hypotheses on the function of ventroventral mounting (genital contacts) that derive from previous studies of both primate and nonprimate species: (1) reconciliation; (2) mate attraction; (3) tension regulation; (4) expression of social status; and (5) social bonding. We collected data in six field seasons (1993-1998) from members of a habituated, unprovisioned community of wild bonobos at Lomako, Democratic Republic of Congo. No single hypothesis could account for the use of genital contacts, which appeared to be multifunctional. We found support for hypotheses 1 and 3. Rates of postconflict genital contacts exceeded preconflict rates suggesting that the display is used in the context of reconciliation. Rates of genital contacts were high when food could be monopolized and tension was high. However, genital contacts also occurred independently of agonistic encounters. Our study shows rank-related asymmetries in initiation and performance of genital contacts supporting the social status hypothesis: low-ranking females solicited genital contacts more often than high-ranking females while the latter were more often mounter than mountee. Although subordinates took more initiative to achieve genital contact, dominants mostly responded to the solicitation (ventral presentation) with mounting, indicating that the performance benefits both individuals. We suggest that genital contacts can be used to investigate both quality and dynamics of dyadic social relationships among female bonobos. Copyright 2000 The Association for the Study of Animal Behaviour.

Rivers influence the population genetic structure of bonobos (Pan paniscus)

Bonobos are large, highly mobile primates living in the relatively undisturbed, contiguous forest south of the Congo River. Accordingly, gene flow among populations is assumed to be extensive, but may be impeded by large, impassable rivers. We examined mitochondrial DNA control region sequence variation in individuals from five distinct localities separated by rivers in order to estimate relative levels of genetic diversity and assess the extent and pattern of population genetic structure in the bonobo. Diversity estimates for the bonobo exceed those for humans, but are less than those found for the chimpanzee. All regions sampled are significantly differentiated from one another, according to genetic distances estimated as pairwise FSTs, with the greatest differentiation existing between region East and each of the two Northern populations (N and NE) and the least differentiation between regions Central and South. The distribution of nucleotide diversity shows a clear signal of population structure, with some 30% of the variance occurring among geographical regions. However, a geographical patterning of the population structure is not obvious. Namely, mitochondrial haplotypes were shared among all regions excepting the most eastern locality and the phylogenetic analysis revealed a tree in which haplotypes were intermixed with little regard to geographical origin, with the notable exception of the close relationships among the haplotypes found in the east. Nonetheless, genetic distances correlated with geographical distances when the intervening distances were measured around rivers presenting effective current–day barriers, but not when straight‐line distances were used, suggesting that rivers are indeed a hindrance to gene flow in this species.

Culture in Bonobos? Between-species and within-species variation in behavior

Long-term studies on wild chimpanzees (Pan troglodytes) conducted over the past four decades have revealed extensive behavioral variation within and between local populations (McGrew 1983, Nishida et al. 1983, McGrew 1992, Boesch et al. 1994, Wrangham, de Waal, and McGrew 1994, McGrew et al. 1997, Whiten et al. 1999, McGrew et al. 2001). Because chimpanzees live in different habitats across the African continent, they have to cope with a variety of environmental conditions, and therefore the extent of behavioral variation among them is not unexpected. In response to seasonal drought, populations in West and Central Africa have developed special techniques for obtaining water (Hunt and McGrew 2002, Lanjouw 2002). Chimpanzees in dry habitats with low tree density are reported to use nests repeatedly while those living in dense forest habitats rarely use the same nest twice (Fruth and Hohmann 1996). Similarly, the frequency of combining several small trees to construct a single nest varies between populations, probably as a function of forest structure (Fruth and Hohmann 1994). Variation in the extent and quality of insectivory across populations often reflects differences in the availability of prey species (McGrew 1992). Chimpanzees at different sites use different strategies to hunt red colobus monkeys (Colobus badius), and some of this variation can be related to the behavior of the prey species, density of forest cover, and, perhaps, food competition between predator and prey (Boesch 1994, Stanford 1998).

Mothers matter! Maternal support, dominance status and mating success in male bonobos (Pan paniscus)

Variation in male mating success is often related to rank differences. Males who are unable to monopolize oestrous females alone may engage in coalitions, thus enhancing their mating success. While studies on chimpanzees and dolphins suggest that coalitions are independent of kinship, information from female philopatric species shows the importance of kin support, especially from mothers, on the reproductive success of females. Therefore, one might expect a similar effect on sons in male philopatric species. We evaluate mating success determinants in male bonobos using data from nine male individuals from a wild population. Results reveal a steep, linear male dominance hierarchy and a positive correlation between dominance status and mating success. In addition to rank, the presence of mothers enhances the mating success of sons and reduces the proportion of matings by the highest ranking male. Mothers and sons have high association rates and mothers provide agonistic aid to sons in conflicts with other males. As bonobos are male-philopatric and adult females occupy high dominance status, maternal support extends into adulthood and females have the leverage to intervene in male conflicts. The absence of female support to unrelated males suggests that mothers gain indirect fitness benefits by supporting their sons.

Y‐chromosome analysis confirms highly sex‐biased dispersal and suggests a low male effective population size in bonobos (Pan paniscus)

Dispersal is a rare event that is difficult to observe in slowly maturing, long‐lived wild animal species such as the bonobo. In this study we used sex‐linked (mitochondrial DNA sequence and Y‐chromosome microsatellite) markers from the same set of individuals to estimate the magnitude of difference in effective dispersal between the sexes and to investigate the long‐term demographic history of bonobos. We sampled 34 males from four distinct geographical areas across the bonobo distribution range. As predicted for a female‐dispersing species, we found much higher levels of differentiation among local bonobo populations based upon Y‐chromosomal than mtDNA genetic variation. Specifically, almost all of the Y‐chromosomal variation distinguished populations, while nearly all of the mtDNA variation was shared between populations. Furthermore, genetic distance correlated with geographical distance for mtDNA but not for the Y chromosome. Female bonobos have a much higher migration rate and/or effective population size as compared to males, and the estimate for the mitochondrial TMRCA (time to most recent common ancestor) was approximately 10 times greater than the estimate for the Y chromosome (410 000 vs. 40 000–45 000). For humans the difference is merely a factor of two, suggesting a more stable demographic history in bonobos in comparison to humans.

Nest building behavior in the great apes: the great leap forward?

INTRODUCTION Over decades apes have served as either referential or conceptual models in attempts to reconstruct the path of human evolution (Ghiglieri, 1987; Wrangham, 1987). In the search for behavioral traits shared by all members of the great apes, few have turned out to be conservative, that is, common features seen in all extant hominoids, and by inference present in our common ancestor. Of these shared traits, skilled object manipulation has been of great interest in comparative analyses as a basic criterion for hominization. Tool use and tool production, however, vary tremendously not only among the four species but also within a single species. Thus the trait in common is not tool use itself, but the general ability for environmental problem solving (McGrew, 1992). Nest building is part of this ability. It is probably the most pervasive form of material skill in apes. Whether or not this trait should be considered as tool use is much disputed (Goodall, 1968; Alcock, 1972; Beck, 1980; Galdikas, 1982). Nest building is called ‘bed building’ by some investigators (Itani, 1979; Hiraiwa-Hasegawa, 1986). It is a daily habit of weaned great apes to build a place in which to rest. The technique employed depends on the site and on the available materials. Orangutans, chimpanzees and bonobos start their arboreal constructions by preparing a foundation of solid sidebranches or forks, bending, breaking and inter-weaving sidebranches crosswise.

Social bonds and genetic ties: Kinship association and affiliation in a community of bonobos (Pan paniscus)

Studies of captive populations of bonobos suggest that females are more gregarious than males. This seems to contradict assumed sex-differences in kinship deriving from a species-typical dispersal pattern of female exogamy and male philopatry. Here we present data on spatial associations and affiliative relations among members of one wild community (Eyengo) for which genetic relationships were identified by analysing mitochondrial and nuclear DNA. Our data from Lomako confirm the existence of spatial associations among resident females. In addition, they reveal strong social bonds between males and females. While most female-female associations did not last longer than one field season, long-term associations occurred predominantly between mixed-sex dyads and involved both close kin and unrelated individuals. Differences in social grooming appeared to be related to patterns of spatial association rather than to kinship. It is suggested that under natural conditions social organisation of bonobos is characterised by strong inter-sexual bonds. Males may benefit from bonding with females by increased reproductive success via rank acquisition. For females benefits may derive from inclusive fitness and reduced food competition. Preliminary evidence suggests that females also may benefit from protection by resident males against male intruders.

Dynamics in social organization of bonobos (Pan paniscus)

INTRODUCTION In the last 20 years, chimpanzee ( Pan troglodytes ) and bonobo ( Pan paniscus ) research has produced contrasting pictures of these two sister species. Chimpanzee society has been characterized as male dominated and structured by a linear hierarchy amongst males, with more egalitarian relations amongst females. Male dominance rank is often based on alliances with other males and exerted by intense aggression (Riss & Goodall 1977; Goodall 1986; McGrew 1996; Watts 1998). Parous females, except when they are in oestrus, tend to avoid travelling with males in order to prevent aggression and to improve their foraging efficiency (Williams et al ., Chapter 14; Wrangham, Chapter 15). Consequently, parties are relatively small and often male biased (Nishida 1979; Wrangham 1986; Wrangham et al . 1992; Boesch & Boesch-Achermann 2000). In comparison, bonobo society is characterized by egalitarian relations between the sexes (Furuichi 1997) and females may collaborate to defend food sources against males (Idani 1991; Parish 1994; Hohmann & Fruth 1996;Vervaecke et al ., 2000). Males establish dominance relationships with each other but aggression amongst males and between the sexes is less intense than in chimpanzees, and conflicts are often settled in a non-agonistic way (Furuichi & Ihobe 1994; de Waal 1995). Compared to chimpanzees, bonobo parties are large and biased towards females. Recently, the behavioural contrasts between the two Pan species have been questioned (Stanford 1998) for various reasons. These include scarcity of information from wild bonobos, and the failure to compare data from wild chimpanzees with what is known from studies of captive bonobos. The goal of this chapter is to address these issues by providing new data on the social organization of wild bonobos.