Paternity and kin structure among neighbouring groups in wild bonobos at Wamba

Although both bonobos and chimpanzees are male-philopatric species, outcomes of male–male reproductive competition seem to be more closely associated with mating success in chimpanzees. This suggests that the extent of male reproductive skew is lower in bonobos. In addition, between- group male–male reproductive competition is more lethal in chimpanzees. This suggests that between-group differentiation in male kinship is lower in bonobos. We analysed the paternity of 17 offspring in two bonobo groups and estimated the relatedness of individuals among three neighbouring groups by using DNA extracted from non-invasive samples at Wamba, in the Democratic Republic of the Congo. The alpha males sired at least nine of 17 offspring. This supports a previous finding that the male reproductive skew is higher in bonobos than that in chimpanzees. Average relatedness among males within groups was significantly higher than that among males across groups, whereas there was no significant difference among females between within and across groups. These results are consistent with male philopatry, highly skewed reproductive success of males and female dispersal. Higher average relatedness among males within groups suggest that the differences in hostility towards males of different groups between bonobos and chimpanzees may be explained by factors other than kinship.

Genetic analysis of migration pattern of female bonobos (Pan paniscus) among three neighboring groups

Relationships between females of different groups in female philopatric species are typically antagonistic, whereas those in female dispersing species can be more moderate. Such nonantagonistic relationships among females of neighboring groups may allow immigrant females to minimize dispersal costs by migrating into those groups, whereas the frequency of female migration among neighboring groups is little understood in female dispersing species. Bonobos are a species in which females disperse and often show affinitive interactions between groups during inter-group encounters. We examined the frequency of female migration into neighboring groups in bonobos using genetic and demographic data. The estimated frequency of female migration into any neighboring group was 53%. Our results suggest that female bonobos do not disperse far from their natal groups, which may be because they usually transfer between groups during intergroup encounters.

Males with a mother living in their group have higher paternity success in bonobos but not chimpanzees

In many group-living mammals, mothers may increase the reproductive success of their daughters even after they are nutritionally independent and fully grown. However, whether such maternal effects exist for adult sons is largely unknown. Here we show that males have higher paternity success when their mother is living in the group at the time of the offspring’s conception in bonobos (N = 39 paternities from 4 groups) but not in chimpanzees (N = 263 paternities from 7 groups). These results are consistent with previous research showing a stronger role of mothers (and females more generally) in bonobo than chimpanzee societies.

Comparisons of between-group differentiation in male kinship between bonobos and chimpanzees

Bonobos and chimpanzees share many characteristics of social systems including male philopatry, whereas one major difference between the two species is the nature of intergroup relationship. Intergroup male aggressions are much more intensive in chimpanzees than in bonobos. Such behavioural differences may facilitate more frequent between-group male gene flow and greater between-group differentiation in male kinship in bonobos than in chimpanzees. Here we compared extent of between-group differentiation in male kinship between bonobos and chimpanzees. Contrary to expectation, intergroup male kinship was similarly or more differentiated in bonobos than in chimpanzees. Our results suggest that the major differences in intergroup male aggressions between the two species may be explained by other factors beside kinship.

Bonobos’ saliva remaining on the pith of terrestrial herbaceous vegetation can serve as non-invasive wild genetic resources

Evaluating the genetic diversity of natural populations of endangered species is important for conservation. Although the genetic analysis of wildlife usually requires collecting DNA non-invasively, the variety of non-invasive DNA sampling methods is limited for each species. We present a method to obtain DNA of an endangered species, the bonobo (Pan paniscus), in which the pith of the terrestrial herbaceous vegetation (THV) that they consumed was newly utilized. We investigated the (1) frequency of encountering remnant saliva on three types of THV pith; (2) concentrations of DNA in the saliva samples by the real-time quantitative PCR; and (3) rates of positive PCR, accurate genotyping, and allelic drop out by analyzing two autosomal microsatellite loci (D7s817 and D9s910). The number of remnant saliva samples was recorded by following the bonobo groups on a daily basis. The frequency of encountering DNA samples was higher in saliva samples than in fecal samples. More than half of the saliva samples remaining on two types of THV pith provided sufficient concentrations of bonobo DNA (> 200 pg/μl). Rates of positive PCR and accurate genotyping were high, and allelic drop out rate was low when the amount of template DNA was above 200 pg per reaction. Our results suggest that the remnants of bonobo saliva on the pith of THV are a potential resource for obtaining DNA, and better than other kinds of samples from the perspective of the abundant sampling opportunities.

Sex-Specific Effects of Juvenile Offspring on their Mothers’ Social Relationships with Other Females in Japanese Macaques (Macaca fuscata) on Shodoshima Island

Females of female-philopatric species form lifelong affiliative relationships with one another. Given that adult daughters can provide benefits to mothers in the future, mothers may invest more in juvenile daughters than juvenile sons. A potential implication of this sex difference in investment is that mothers of juvenile daughters have reduced capacity to form affiliative relationships with other adult females. We tested whether the strength of female–female affiliative relationships varies depending on the sex of their juvenile offspring in free-ranging Japanese macaques (Macaca fuscata). We analyzed affiliative interactions (spatial proximity and social grooming) of 14 adult females to assess the strength of affiliative relationships between them over a 3-month period. We found that affiliative relationships between females with juvenile daughters were weaker than those between females without juvenile daughters. In contrast, the presence of juvenile sons did not significantly influence the strength of affiliative relationships between females. Mothers associated more with juvenile daughters than with juvenile sons, suggesting that mothers invested more in associating with juvenile daughters than with juvenile sons. Our data confirmed that females form strong affiliative relationships with kin, as is typical for this species. The results imply that females invest more effort in offspring with whom they can maintain affiliative relationships after maturing, which may reduce their level of affiliative relationships with non-kin. Further studies over longer time periods are required to determine whether the reduction in non-kin affiliative relationships is temporary or permanent.

Fake twins? Two cases of intensive allomaternal care by female Japanese macaques before and after their own partum

Allomaternal care is widely observed among primate species. Although diverse allomothering behavioral repertoire and types of caretakers have been reported, it remains unclear what social or physiological conditions may trigger such care in each individual. For a better understanding of mechanisms that give rise to allomaternal care in primates, more observational reports are needed with information on social or physiological conditions of caretakers. Here I report two cases of intensive allomaternal care in two different populations of Japanese macaques (Macaca fuscata). The two adult females provided intensive allomaternal care including carrying, grooming, and nursing towards others’ infants. Their allomaternal care began 20 or 29 days prior to their own partum and lasted for 84 days at the most. This study firstly showed that nursing forms part of the allomothering behavioral repertoire, and allomaternal caretakers can be individuals that are prior to the time of their own partum in Japanese macaques. Their intensive allomaternal care may stem from their good nutritional conditions, increased concentrations of several hormones, or disappearance of the newborn infants’ biological mothers.

Do dominant monkeys gain more warmth? Number of physical contacts and spatial positions in huddles for male Japanese macaques in relation to dominance rank

Animals show various forms of behavioral thermoregulation to minimize cold stress. Given that higher dominance rank is often associated with increased fitness in group-living animals, higher-ranking individuals may also benefit from better access to thermally optimal spatial positions within huddles. This study examined the association between dominance rank and the potential thermoregulatory benefits of huddling behavior in Japanese macaques (Macaca fuscata) inhabiting Shodoshima Island, which form exceptionally large huddles. I photographed monkey huddles, and analyzed the number of individuals that males were in contact with and males’ spatial positons in huddles. Higher-ranking males were significantly more likely to be in contact with larger numbers of individuals in huddles. Higher-ranking males occupied non-peripheral positions in huddles more often than lower-ranking males, which put them in contact with larger numbers of individuals. These results suggest that high dominance rank may confer potential thermal advantages on male Japanese macaques. The mechanism for this is likely that the highest-ranking male often intrude in already-formed huddles, although such behaviors of males were not quantitatively assessed. This study contributes to a better understanding of the mechanisms of cold adaptation in relation to dominance rank in group-living animals.