Primate Biol., 1, 29–38, 2014 www.primate-biol.net/1/29/2014/ doi:10.5194/pb-1-29-2014 © Author(s) 2014. CC Attribution 3.0 License. Genetic inference of group dynamics and female kin structure in a western lowland gorilla population (Gorilla gorilla gorilla) M. Arandjelovic, J. Head, C. Boesch, M. M. Robbins, and L. Vigilant Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany Correspondence to: M. Arandjelovic ([email protected]) Received: 15 September 2014 – Revised: 20 November 2014 – Accepted: 8 December 2014 – Published: 15 December 2014 Abstract. Dispersal and grouping patterns form the foundations of social interactions in group-living mammals and are the outcomes of a complex interplay between inbreeding avoidance, kin cooperation and competition, predation pressure and food resource distribution. In species where both sexes disperse, the potential for kin- biased associations would seem limited. In one such species, the western lowland gorilla (WLG), short-term data suggest that female kin associations may be present due to directed local dispersal decisions, but monitoring of groups over longer timescales is needed to better elucidate this pattern. Using autosomal genotyping of 419 faecal samples representing 85 unhabituated gorillas collected non-invasively over 5 years in a 132 km2 section of Loango National Park, Gabon, we investigated the dynamics of WLG group composition, social structure and patterns of dispersal. By revealing two group dissolutions, one group formation and the movement of 13 gorillas between groups, this study demonstrates the utility of genetic analysis as a way to track individuals, groups and population dynamics on a larger scale than when monitoring the behaviour of a limited number of habituated groups or through one-time genetic sampling. Furthermore, we find that females are found in groups containing their female kin more often than expected by chance, suggesting that dispersal may not impede female kin associations in WLGs. 1 Introduction Pusey and Packer, 1987; Robbins, 2010; Wrangham, 1979), and these females may disperse to other social units multiple Group living in many mammal species is generally explained times in their lives (Boesch, 2009; Stokes et al., 2003). WLG as an arrangement that maximizes the potential benefits of males also consistently disperse from their natal group and kin cooperation and predator avoidance (Clutton-Brock and become solitary or reside in non-reproductive social units Lukas, 2012; Handley and Perrin, 2007). The potential costs before possibly acquiring females and forming their own of inbreeding and competition, particularly with kin, are usu- reproductive groups. These reproductive groups nearly al- ally invoked to explain the prevalence of sex-biased natal ways contain only a single fully mature adult (silverback) dispersal in mammals (Handley and Perrin, 2007; Thierry, male along with mature females and immatures of both sexes 2008). However, the dispersing sex would seem to lose the (Bradley et al., 2004; Gatti et al., 2004; Robbins et al., 2004). potential for fitness-enhancing interactions with life-long as- However, unlike most harem species, including mountain go- sociates who may also be close kin (Langergraber et al., rillas (Watts, 2000), hamadryas baboons (Swedell and Tes- 2007, 2009; Silk, 2009; Silk et al., 2006). Unlike most faye, 2003), plains zebras (Rubenstein, 1986) and greater mammal species which display predominantly male disper- sac-winged bats (Voigt and Streich, 2003), neither internal sal (Greenwood, 1980), great apes such as eastern gorillas, (“queuing”) nor external group takeovers by adult silver- western lowland gorillas (WLGs, Gorilla gorilla gorilla), backs have been observed in WLGs (Harcourt and Stewart, bonobos and chimpanzees typically exhibit dispersal of fe- 2007). Instead, new groups may form when females join lone males from the natal group at maturity (Greenwood, 1980; silverback males or females transfer to existing groups dur- Published by Copernicus Publications on behalf of the Deutsches Primatenzentrum GmbH (DPZ). 30 M. Arandjelovic et al.: Genetic inference of group dynamics and female kin structure ing intergroup encounters. It has been suggested that WLGs, et al., 2004; Stokes et al., 2003; Tutin, 1996), and these stud- with routine dispersal by both sexes, may be one of the best ies have elucidated some of the apparent contrasts between models for studying early hominid evolution (Koenig and WLGs and mountain gorillas. For example, all-male bachelor Borries, 2012). groups, mixed-sex non-reproductive groups and single-male It is currently thought that female gorillas gain little from breeding groups have all been documented in WLGs, but residing with kin but obtain benefits from dispersing by in contrast to mountain gorillas, multi-male breeding groups avoiding potential inbreeding in their natal community and have not been observed except for a few transient cases (Gatti by having the ability to choose a new male in a new group et al., 2004; Jeffery et al., 2007; Magliocca et al., 1999; Par- (Breuer et al., 2012; Caillaud et al., 2008; Guschanski et al., nell, 2002; Robbins et al., 2004; Stokes et al., 2003; Tutin, 2008; Harcourt and Stewart, 2007). However, genetic anal- 1996). Furthermore, group fissions (the splitting of one group ysis of multiple adjacent WLG groups at one site suggested into two or more) have also not been observed in WLGs, and that, despite routine dispersal by both sexes, female WLGs the only mode of group formation observed has been by the may maintain kin associations post-emigration (Bradley et acquisition of females by lone silverback males (Gatti et al., al., 2007). Furthermore, in mountain gorillas, a WLG sis- 2004; Robbins et al., 2004). Group dissolutions (the cessa- ter taxon displaying non-obligate female and male disper- tion of existence of a group, wherein the group silverback sal, non-dispersing related females are more tolerant of each no longer retains any females and females transfer to several other than of non-relatives (Watts, 1994a, b). On the other different new groups) have been observed at one WLG site at hand, Douadi et al. (2007) suggested that the proportion of a rate approximately 5 times higher than in mountain gorillas related WLG female dyads (including both adults and imma- (Robbins et al., 2004). In general, however, the difficulty of tures) within groups did not differ from the proportion be- simultaneous observational monitoring of multiple groups of tween groups, while another study found few WLG female a long-lived species has limited the direct study of patterns kin dyads in their study population (Inoue et al., 2013). How- of dispersal and group formation in WLGs. ever, the latter two studies relied upon estimation of dyadic Genetic analyses provide an opportunity for understanding relatedness values, which is not considered an accurate way the dispersal choices of individuals in such elusive species. to identify related pairs in a population (Csillery et al., 2006), In this study we use samples collected within a 132 km2 thus leaving the question of female kin associations in WLGs area over a total of 33 months spanning 5 years in Loango unresolved. National Park, Gabon, and employ autosomal microsatellite Because female gorillas only transfer between groups dur- genotyping in conjunction with parentage analysis to deter- ing intergroup encounters or after group dissolution and are mine the composition of groups in the study area. We take never solitary (Harcourt and Stewart, 2007), the timing and advantage of the temporal depth of the sampling to focus distance of single dispersal events are limited. Furthermore, on group dynamics and to estimate the frequency of group because the risk of infanticide would appear to inhibit trans- formations, dissolutions and individual dispersal events. Fi- fer by females with dependent young, opportunities for fe- nally, we use relatedness analyses to test the hypotheses that male dispersal are constrained in comparison to males (Rob- female WLGs are found in proximity to their same-sex kin bins et al., 2013; Robbins, 2010). Nevertheless, females may post-dispersal. move across multiple groups over a lifetime as the result of multiple transfers which are believed to reflect female 2 Methods choice (Breuer, 2010; Jeffery et al., 2007; Robbins et al., 2004). While females typically disperse singly, the trans- 2.1 Study site and sample collection fer of pairs of females has been inferred twice, with two females observed in one group, and shortly thereafter in a As detailed previously, we opportunistically collected a total new group after the death of their group’s silverback (Par- of 396 gorilla faecal samples across a 132 km2 area in the nell, 2002; Stokes et al., 2003). Such transfers subsequent central sector of Loango National Park, Gabon (Head et al., to group dissolution are generally considered involuntary in 2011), between February 2005 and September 2007 (Arand- nature. Based on these considerations and the observation jelovic et al., 2010). We collected an additional 23 samples of higher than expected average relatedness among females from the same area from March to April 2009. We pre- within groups at one site, it is hypothesized in WLGs that fe- served the faeces using the two-step ethanol–silica proce- males may be able to maintain kin relationships despite natal dure (Nsubuga et al., 2004). The gorillas in the research area and secondary dispersal