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

Abstract

Patterns of kinship among individuals in different groups have been rarely examined in animals. Two closest living relatives of humans, 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 relationship is basically antagonistic and males sometimes kill individuals of other groups in chimpanzees, whereas it is much more moderate in bonobos and copulations between individuals of different groups are often observed during intergroup encounters. 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 differences between average relatedness among males within groups and that among males of neighbouring groups, and between-group male genetic distance between bonobos and chimpanzees. Contrary to expectation, the differences between average relatedness among males within groups and that among males of neighbouring groups were significantly greater in bonobos than in chimpanzees. There were no significant differences in autosomal and Y-chromosomal between-group male genetic distance between the two species. Our results showed that intergroup male kinship is similarly or more differentiated in bonobos than in chimpanzees. Kinship is one of key factors to affect affinity among animals 1. It has been clarified that reciprocity and cooperation in animals have been attributed to kin selection, a process whereby individuals cooperate with relatives and gain indirect fitness benefits through the reproduction of kin 2. Researchers have clarified that kin selection can occur within social groups of each species. However, patterns of kinship among individuals in different groups have been rarely examined in especially large mammalian species (e.g. chimpanzee 3 , western lowland gorilla 4), since it is tough to examine them in the wild. For a better understanding of the influences of kinship on social interactions in animals, patterns of kinship among individuals in different groups should be investigated with references about patterns of social interactions among them. Comparisons between bonobos and chimpanzees are effective in examining the relationships between intergroup interactions and kinship among individuals in different groups. These two species share many characteristics of their social system including male philopatry, multi-male/multi-female group composition, and fission-fusion dynamics 5-7. Despite these similarities, the nature of intergroup relationship largely differs between the two species. Intergroup relationship in chimpanzees is basically antagonistic and male chimpanzees sometimes make lethal coalitionary attacks and kill males of different groups 8-11. Contrary to chimpanzees, bonobos show much more moderate intergroup relationships. Although intergroup male-male relationships are antagonistic, male bonobos rarely show lethal...

Better together? How intergroup associations affect energy balance and feeding behavior in wild bonobos

“…This hypothesis is supported by our previous finding that bonobos were less likely to terminate associations when ranging in less familiar areas of their home range (Lucchesi et al 2020). On the social level, the fact that communities were less likely to terminate associations when the number of maximally tumescent females in the party was high indicates the possibility of reproductive advantages to these associations (but see Ishizuka et al 2018Ishizuka et al , 2020.…”

“…In many species, members of different groups associate with the purpose to increase the number of social (African elephants, L. africana: Wittemyer et al 2005) and mating (Hanuman langurs, S. entellus: Launhardt et al 2001;Verreaux's sifaka, P. verreauxi: Lawler 2007) partners or to evaluate the possibility of transfer from their natal group (meerkats, S. suricatta: Drewe et al 2009). In bonobos, non-energetic benefits of associations may include extra-community paternities (but see Ishizuka et al 2018;Ishizuka et al 2020), facilitation of the transfer of young nulliparous females or even males to other communities (Hohmann 2001;Sakamaki et al 2015;Toda et al 2018), and maintenance of social bonds among females of adjacent communities (Sakamaki et al 2018). For instance, copulation between members of different communities is common during associations (Furuichi 2011;Lucchesi et al 2020), and in previous research we have shown that communities are more likely to remain in association when the number of maximally tumescent females is high.…”

“…For instance, copulation between members of different communities is common during associations (Furuichi 2011;Lucchesi et al 2020), and in previous research we have shown that communities are more likely to remain in association when the number of maximally tumescent females is high. However, the rarity of extra-community paternities in bonobos suggests that intercommunity copulations infrequently lead to the siring of offspring outside an individual's own social group (Ishizuka et al 2018(Ishizuka et al , 2020. Socio-sexual behavior is a hallmark trait of bonobos' behavioral repertoire.…”

Pedigree reconstruction and distant pairwise relatedness estimation from genome sequence data: A demonstration in a population of rhesus macaques (Macaca mulatta)

“…Investigating and understanding behavioural interactions among individuals, patterns of mate selection (Vigilant et al, 2001), dispersal and intergroup migration (Cheney & Seyfarth, 1983; Langergraber et al, 2014; Van Cise et al, 2017), group fission and critical aspects of natural selection such as variation in interbirth intervals or infant survivorship (Silk et al, 2003) requires information about the relationships among the actors in the continual drama of mammalian social behaviour and life history. Unfortunately, documenting kinship among individuals in natural populations of animals, especially among long‐lived mammals such as primates, cetaceans, elephants and other large‐bodied species, has traditionally required many years (often decades) of continuous observation of recognizable individuals (Alberts & Altmann, 2012; Ishizuka et al, 2020; McComb et al, 2001). Even then, paternity is often uncertain without some form of genetic testing.…”

“…In addition, investigations of smaller animals with shorter generation times but that are migratory or are otherwise difficult to repeatedly observe or identify can also present challenges for the assessment of kinship among study individuals. Research in various aspects of the ethology, social organization, ecology, demography and population genetics of natural populations benefits directly from methods to identify or confirm relationships among individuals that do not require long‐term observation of habituated populations (Foroughirad et al, 2019; Ishizuka et al, 2020; Langergraber et al, 2014; Snyder‐Mackler et al, 2016; Stadele et al, 2016; Van Cise et al, 2017). In addition, biomedical research using captive populations of nonhuman primates or other species can benefit from the capacity to determine parentage or other relationships among individuals whenever reliable pedigree information is not available (Kanthaswamy et al, 2006; Rogers et al, 2006; Vinson et al, 2013).…”