Reproductive inequality among males in the genus Pan.

Reproductive inequality, or reproductive skew, drives natural selection, but has been difficult to assess, particularly for males in species with promiscuous mating and slow life histories, such as bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Although bonobos are often portrayed as more egalitarian than chimpanzees, genetic studies have found high male reproductive skew in bonobos. Here, we discuss mechanisms likely to affect male reproductive skew in Pan, then re-examine skew patterns using paternity data from published work and new data from the Kokolopori Bonobo Reserve, Democratic Republic of Congo and Gombe National Park, Tanzania. Using the multinomial index (M), we found considerable overlap in skew between the species, but the highest skew occurred among bonobos. Additionally, for two of three bonobo communities, but no chimpanzee communities, the highest ranking male had greater siring success than predicted by priority-of-access. Thus, an expanded dataset covering a broader demographic range confirms that bonobos have high male reproductive skew. Detailed comparison of data from Pan highlights that reproductive skew models should consider male-male dynamics including the effect of between-group competition on incentives for reproductive concessions, but also female grouping patterns and factors related to male-female dynamics including the expression of female choice. This article is part of the theme issue 'Evolutionary ecology of inequality'.

Mothers stick together: how the death of an infant affects female social relationships in a group of wild bonobos (Pan paniscus).

Sociality is widespread among group-living primates and is beneficial in many ways. Sociality amongst female bonobos (Pan paniscus) has been proposed to have evolved as a female counterstrategy to male infanticide and sexual coercion. In male-philopatric bonobo societies, females mostly form relationships with unrelated females. Among these social relationships, it has been proposed that females with infants (also referred to as mothers) tend to have strong relationships with each other (mother-bonding hypothesis). In this paper, we use the case of an infant death in a group of wild bonobos in the Kokolopori Bonobo Reserve, Democratic Republic of Congo, to test this hypothesis. By using dyadic sociality indices for grooming, proximity, and aggression, we investigated whether the infant death influenced dyadic relationships the mother had with other group members. Before the infant death, grooming index (GI) and proximity index (PI) scores were the highest between the focal mother and another mother. After the death, the relationship of this mother dyad weakened, as indicated by lower GI and PI scores, whereas the relationship of another mother dyad became stronger. Aggression index scores among the mothers were comparable before and after the death, suggesting that changes in mother affiliative relationships were not a by-product of changes in overall interaction frequencies. Also, PI scores increased between the focal mother and three non-mothers after the death. Collectively, the shift in social dynamics between the focal mother and other group members after the infant death partially supported the mother-bonding hypothesis.

Importance of subterranean fungi in the diet of bonobos in Kokolopori.

Nonstaple food is a food resource which sole consumption does not allow the maintenance of regular physiological functions, thus constituting a minor portion of an individual's diet. Many primates consume nonstaple food such as meat, insects, and fungi. Hypotheses on the dietary importance of nonstaple food include its role as fallback food and as source of specific nutrients. We tested these two hypotheses by investigating mycophagy (i.e., the consumption of fungi) in a population of wild bonobos in the Kokolopori Bonobo Reserve, DRC. Specifically, we examined the relationship between fungus consumption and various factors relevant to bonobo feeding ecology (i.e., fruit abundance and the consumption of other food types). Additionally, we measured the deviation from linear travel when bonobos searched for fungi to evaluate the nature of fungus consumption (e.g., opportunistic or targeted). Lastly, we examined the nutritional content of the major fungus species consumed (Hysterangium bonobo) to test whether this food item was potentially consumed as source of specific nutrients. We found that bonobos spent a higher proportion of their time feeding on fungi when fruit abundance was higher, indicating that fungi were not consumed as a fallback food. Moreover, bonobos deviated from linear travel when visiting fungus patches more than observed when visiting fruit patches, suggesting that they actively sought out fungi. Lastly, initial analyses suggest that H. bonobo samples contained high concentration of sodium. Collectively, these results suggest that subterranean fungi appear to be attractive food source to Kokolopori bonobos, and that mycophagy may serve to supplement nutrients, like sodium, in bonobo diet.

Variation in aggression rates and urinary cortisol levels indicates intergroup competition in wild bonobos.

Intergroup competition is a widespread phenomenon across taxa and groups typically compete over access to limited resources, such as food and mates. Such competition may be quantified by changes in individuals' behavioral and physiological status in response to intergroup encounters (IGEs). Bonobos, one of our closest living relatives, are often regarded as xenophilic and exhibit high tolerance towards out-group individuals. This tolerance between groups may still be accompanied by intergroup competition over resources. We hereby compared variation in aggression rates and urinary cortisol levels of bonobos during and outside contexts of IGEs in the Kokolopori Bonobo Reserve and investigated whether food and mate availability influenced males' and females' aggression and cortisol levels, when controlling for dominance rank and the number of individuals present. We found that although females had higher aggression rates and urinary cortisol levels during than outside contexts of IGEs, these increases were not related to food availability or changes in between-group dynamics when maximally tumescent females were present, rather than absent. Furthermore, males showed higher aggression rates and urinary cortisol levels during than outside contexts of IGEs. However, males' responses during IGEs were not related to the presence of maximally tumescent females and food availability. Taken together, while competition intensified during seemingly tolerant IGEs in bonobos, such competition was unrelated to short-term changes in food and mate availability. Despite physical and physiological costs of aggression, bonobos associate with out-group individuals frequently and for extended periods. This suggests potential benefits of bonobo intergroup associations.

Reply to Fischer et al.

We welcome the correspondence from Fischer and colleagues regarding our recent paper on vocal learning in chimpanzee food grunts [1]. Fischer et al. make two challenges to our paper's conclusions, which we address here.

Vocal learning in the functionally referential food grunts of chimpanzees.

One standout feature of human language is our ability to reference external objects and events with socially learned symbols, or words. Exploring the phylogenetic origins of this capacity is therefore key to a comprehensive understanding of the evolution of language. While non-human primates can produce vocalizations that refer to external objects in the environment, it is generally accepted that their acoustic structure is fixed and a product of arousal states. Indeed, it has been argued that the apparent lack of flexible control over the structure of referential vocalizations represents a key discontinuity with language. Here, we demonstrate vocal learning in the acoustic structure of referential food grunts in captive chimpanzees. We found that, following the integration of two groups of adult chimpanzees, the acoustic structure of referential food grunts produced for a specific food converged over 3 years. Acoustic convergence arose independently of preference for the food, and social network analyses indicated this only occurred after strong affiliative relationships were established between the original subgroups. We argue that these data represent the first evidence of non-human animals actively modifying and socially learning the structure of a meaningful referential vocalization from conspecifics. Our findings indicate that primate referential call structure is not simply determined by arousal and that the socially learned nature of referential words in humans likely has ancient evolutionary origins.