Mountain gorilla tug-of-war: Silverbacks have limited control over reproduction in multimale groups

Abstract

To determine who fathers the offspring in wild mountain gorilla groups containing more than one adult male silverback, we genotyped nearly one-fourth (n ‫؍‬ 92) of the mountain gorillas (Gorilla beringei beringei) living in the Virunga Volcanoes region of Africa. Paternity analysis of 48 offspring born into four groups between 1985 and 1999 revealed that, although all infants were sired by within-group males, the socially dominant silverback did not always monopolize reproduction within his group. Instead, the second-ranking male sired an average of 15% of group offspring. This result, in combination with previous findings that secondranking males fare best by not leaving the group but by staying and waiting to assume dominance even if no reproduction is possible while waiting, is not consistent with expectations from a reproductive skew model in which the silverback concedes controllable reproduction to the second-ranking male. Instead, the data suggest a ''tug-of-war'' scenario in which neither the dominant nor the second-ranking male has full control over his relative reproductive share. The two top-ranked males were typically unrelated and this, in combination with the mixed paternity of group offspring, means that multimale gorilla groups do not approximate family groups. Instead, as long-term assemblages of related and unrelated individuals, gorilla groups are similar to chimpanzee groups and so offer interesting possibilities for kinbiased interactions among individuals.genotyping ͉ Gorilla beringei beringei ͉ noninvasive sampling ͉ paternity ͉ reproductive skew

Low paternity skew and the influence of maternal kin in an egalitarian, patrilocal primate

“…Excluding females' adult sons (known from long-term pedigree records) from the set of potential sires of those female's subsequent offspring did not alter these findings (B = 0.013, CI −0.043 to 0.063, P = 0.148). The B index in muriquis is much lower than that found for gorillas (7) and capuchins (8), and the fact that the lower limit of the 95% CI is less than zero indicates that the muriqui's paternity distribution does not deviate significantly from random expectations. The most successful male in the group sired only 18% of the infants sampled (n = 4); this value is far lower than the percentages reported for the most successful (and typically, high-ranking) males in the hierarchical societies of other patrilocal and matrilocal primates ( Table 1).…”

“…Paternity analyses have demonstrated that dominant males typically sire a disproportionate number of offspring, consistent with the priority of access that high rank often confers in competition over limited resources, including fertile females (2,(4)(5)(6)(7). In hierarchical societies, deviations from rank-biased paternity have been attributed to the mitigating effects of inbreeding avoidance (8) and to demographic, reproductive, and socioecological conditions that affect the number of male competitors, the monopolizability of fertile females, and the accessibility and effectiveness of coalition partners (3,(9)(10)(11)(12).…”

The lemur syndrome unresolved: extreme male reproductive skew in sifakas (Propithecus verreauxi), a sexually monomorphic primate with female dominance

“…Given this observed reproductive skew in favor of dominant males, it remains puzzling why subordinate males do not attempt takeovers more often. One possibility is that they are queuing for the alpha position (Kokko and Johnstone 1999;Cant and English 2006), as for example mountain gorillas (Bradley et al 2005) or spotted hyenas (East and Hofer 2001), but adult mortality rates are low, and sifaka life span may reach up to 30 years (Richard et al 2002). The potential success of this tactic can therefore not be evaluated with the available data.…”

“…In a cross-sectional genetic study of gentle lemur (Hapalemur griseus) population, 91% of infants were also sired by a single resident male (Nievergelt et al 2002), whereas dominant males reaped 67% of all paternities in redfronted lemurs (Wimmer and Kappeler 2002), suggesting the existence of similar processes in other lemur taxa. Because the degree of male reproductive skew observed in this sifaka population equals or exceeds that of highly sexually dimorphic anthropoids living in highly polygynous systems, such as mountain gorillas (Bradley et al 2005), orang-utans (Utami et al 2002), mandrills (Charpentier et al 2005), patas monkeys (Ohsawa et al 1993), and red howler monkeys (Pope 1990), mechanisms other than exclusion and physical superiority are primary determinants of reproductive success of male sifaka. Perhaps dominant males are particularly effective at mate guarding at crucial times during the females' estrus (Clutton-Brock and Isvaran 2006) because their testes are clearly not adapted to intense sperm competition when examined from a comparative perspective (Kappeler 1997).…”

“…Most studies to date have focused on reproductive skew among females, not only particularly in insects and birds (Reeve and Keller 2001;Haydock and Koenig 2002) but also in mammals (Cooney and Bennett 2000;Clutton-Brock et al 2001;Gerlach and Bartmann 2002;Gilchrist 2006;Young et al 2006). Male reproductive skew, however, has only been studied in a few mammals (Garnier et al 2001;Engh et al 2002;Alberts et al 2003;Widdig et al 2004;Bradley et al 2005), even though reproductive competition is intimately linked to patterns of parental investment, which predispose male mammals towards higher potential reproductive rates, and, hence, competition over access to fertile females (Williams 1966;Trivers 1974;Clutton-Brock and Parker 1992).…”