Stepwise evolution of stable sociality in primates. Nature

Institute of Cognitive and Evolutionary Anthropology, 64 Banbury Road, University of Oxford, Oxford OX2 6PN, UK.
Nature (Impact Factor: 41.46). 11/2011; 479(7372):219-22. DOI: 10.1038/nature10601
Source: PubMed


Although much attention has been focused on explaining and describing the diversity of social grouping patterns among primates, less effort has been devoted to understanding the evolutionary history of social living. This is partly because social behaviours do not fossilize, making it difficult to infer changes over evolutionary time. However, primate social behaviour shows strong evidence for phylogenetic inertia, permitting the use of Bayesian comparative methods to infer changes in social behaviour through time, thereby allowing us to evaluate alternative models of social evolution. Here we present a model of primate social evolution, whereby sociality progresses from solitary foraging individuals directly to large multi-male/multi-female aggregations (approximately 52 million years (Myr) ago), with pair-living (approximately 16 Myr ago) or single-male harem systems (approximately 16 Myr ago) derivative from this second stage. This model fits the data significantly better than the two widely accepted alternatives (an unstructured model implied by the socioecological hypothesis or a model that allows linear stepwise changes in social complexity through time). We also find strong support for the co-evolution of social living with a change from nocturnal to diurnal activity patterns, but not with sex-biased dispersal. This supports suggestions that social living may arise because of increased predation risk associated with diurnal activity. Sociality based on loose aggregation is followed by a second shift to stable or bonded groups. This structuring facilitates the evolution of cooperative behaviours and may provide the scaffold for other distinctive anthropoid traits including coalition formation, cooperative resource defence and large brains.

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    • "Moreover, behavior does not fossilize, and social structure leaves no direct marks in the earth. This is why we must resort to the relationship between phylogenetic proximity and social organization in living primate species (Shultz et al. 2011). The hominin lineage branched off from the primate mainstream some 6.5 million years ago or earlier (Langergraber 2012; Wood 2010). "
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    ABSTRACT: We provide the most up-to-date evidence available in various behavioral fields in support of the hypothesis that the emergence of bipedalism and cooperative breeding in the hominin line—together with environmental developments that made a diet of meat from large animals adaptive as well as cultural innovation in the form of fire and cooking—created a niche for hominins in which there was a high return for coordinated, cooperative scavenging and hunting of large mammals. This was accompanied by an increasing use of wooden spears and lithic points as lethal hunting weapons that transformed human sociopolitical life. The combination of social interdependence and the availability of such weapons in early hominin society undermined the standard social dominance hierarchy of multimale/multifemale primate groups. The successful sociopolitical structure that ultimately replaced the ancestral social dominance hierarchy was an egalitarian political system in which lethal weapons made possible group control of leaders, and group success depended on the ability of leaders to persuade and of followers to contribute to a consensual decision process. The heightened social value of nonauthoritarian leadership entailed enhanced biological fitness for such leadership traits as linguistic facility, ability to form and influence coalitions, and, indeed, hypercognition in general.
    Current Anthropology 04/2015; 56(3):000-000. DOI:10.1086/681217 · 2.93 Impact Factor
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    • "pithecia) and the ruffed lemur (Varecia) also exhibited substantial flexibility. Our results are consistent with previous studies that have also found a phylogenetic component associated with aspects of social organization at the interspecific (Shultz et al. 2011) and intergeneric levels (DiFiore and Rendall 1994). It is important to note that while our predictive analyses " controlled for " phylogeny, phylogenetic signal can be quantified in a trait itself (in this case, social organization flexibility). "
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    ABSTRACT: The importance of behavioral flexibility for understanding primate ecology and evolutionary diversity is becoming increasingly apparent, and yet despite the abundance of long-term studies across diverse sampling localities, we still do not understand the myriad factors responsible for among-site variation in species’ social organization. The goals of our study were to address this question via three main objectives: to quantify social organization flexibility (i.e., across-site intraspecific variation) of well-studied primate species, test the idea that closely related species exhibit similar levels of flexibility, and test hypotheses explaining variation in social organization flexibility among primate species. We obtained data for a total of 175 study sites from 32 primate species representing all major primate clades. We employed phylogenetic principal components analysis to quantify social organization flexibility for each species. We quantified the phylogenetic signal in social organization flexibility and then evaluated the best predictors of flexibility. We found that mean group size was positively related to social organization flexibility. Large social groups may be more flexible because the foraging costs and predation risk associated with adding or subtracting individuals are lower compared to small social groups. There was some support that absolute brain size and the presence of fission–fusion dynamics were also related to high levels of social organization flexibility, suggesting that cognitive ability and/or within-site behavioral flexibility may also lead to increased variation across sites. Our results serve as an early step in understanding the patterns and processes related to social organization flexibility in primates and other social mammals.
    Behavioral Ecology and Sociobiology 07/2014; 68(10). DOI:10.1007/s00265-014-1776-x · 2.35 Impact Factor
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    • "Here, we assess variance in male LRS and reproductive timing for an anthropoid primate, the rhesus macaque (Macaca mulatta) (see Bercovitch 1997; Plavcan 2001). This species forms multimale– multifemale groups (Shultz et al. 2011) in which several immigrant males live year-round with unrelated females. The genetic mating system of this species is unclear. "
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    ABSTRACT: The degree of polygyny is predicted to influence the strength of direct male–male competition, leading to a high variance in male lifetime reproductive success and to reproduction limited to the prime period of adulthood. Here, we explore the variance in male lifetime reproductive success and reproductive time in an anthropoid primate forming multimale–multifemale groups. Males of this species form dominance hierarchies, which are expected to skew reproduction toward few high-ranking males. At the same time, however, females mate with multiple males (polygynandry), which should limit the degree of polygyny. Using 20 years of genetic and demographic data, we calculated lifetime reproductive success for the free-ranging rhesus macaque (Macaca mulatta) population of Cayo Santiago for subjects that died naturally or reached senescence. Our results show that 1) male lifetime reproductive success was significantly skewed (range: 0–47 offspring; males reproducing below average: 62.8%; nonbreeders: 17.4%), 2) variance in male lifetime reproductive success was 5 times larger than in females, and 3) male lifetime reproductive success was more influenced by variation in fecundity (60%) than longevity (25%), suggesting that some direct male–male competition takes place. However, the opportunity for selection (i.e., standardized variance in male lifetime reproductive success) is low compared with that in other large mammal species characterized by a high degree of polygyny. Moreover, male reproductive life extended much beyond the prime period, showing that physical strength was not required to acquire mates. We conclude that rhesus macaques exhibit a moderate degree of polygyny and, therefore, low levels of direct male–male competition for fertile females, despite the fact that males form linear dominance hierarchies.
    Behavioral Ecology 07/2014; 25:878-889. DOI:10.1093/beheco/aru052 · 3.18 Impact Factor
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