Evolutionary transitions toward pair living in nonhuman primates as stepping stones toward more complex societies

Abstract

Nonhuman primate societies vary tremendously in size and composition, but how and why evolutionary transitions among different states occurred remains highly controversial. In particular, how many times pair living evolved and the social states of the ancestors of pair- and group-living species remains contentious. We examined evolutionary transitions in primate social evolution by using new, independent categorizations of sociality and different phylogenetic hypotheses with a vastly expanded dataset. Using Bayesian phylogenetic comparative methods, we consistently found the strongest support for a model that invokes frequent transitions between solitary ancestors and pair-living descendants, with the latter giving rise to group-living species. This result was robust to systematic variation in social classification, sample size, and phylogeny. Our analyses therefore indicate that pair living was a stepping stone in the evolution of structurally more complex primate societies, a result that bolsters the role of kin selection in social evolution.

Fig. 1. Alternative evolutionary models of social evolution.

Arrows represent permitted transitions between different social organizations for each model. (A) Unstructured models: Under this model, all possible transitions are allowed. ER: All rates are fixed to a single optimized rate parameter; SYM Forward and reverse rates between two states are identical; ARD: Rates are fully independent. (B) Increasing complexity (IC) model: Transitions are only allowed between solitary and pair living, pair living and unimale groups, and unimale groups and multimale organization. (C) Shultz et al. (4): Transitions are allowed from solitary to multimale and from multimale to pair living and to unimale and back. (D) Reversible-jump–derived model (RJ-MCMC): Transitions are permitted from solitary to pair living, from pair living to multimale, and from multimale to unimale. All transitions are reversible. The RJ-MCMC (dashed box) was the preferred model using Bayes factor (see Table 1).

Fig. 2. Transition scheme for RJ-MCMC

Arrows with different weights representing likelihood of transition from one state to the other. Numbers indicate the average number of inferred changes between states across 10,000 mapped trees.

Fig. 3. Primate phylogeny showing ancestral state reconstructions for sociality under the RJ-MCMC–derived model of evolution.

Branches and tips are colored for solitary (black), pair living (red), unimale (orange), and multimale (yellow) using one tree randomly selected from the 10,000 trees in the stochastic mapping process. Pies at each node are derived from ancestral state reconstruction using the function ace (R package ape v.5.0). Ancestral state reconstruction using both stochastic mapping (SIMMAP/ace) and BayesTraits for eight main nodes (1: primate root; 2: Strepsirhini root; 3: Haplorhini root; 4: Anthropoidea root; 5: Platyrrhini root; 6: Catarrhini root; 7: Cercopithecoidea root; 8: Hominoidea root) are reported in the stacked bar graphs on the left.

Fig. 4. Proportion of pairs among primate social units with at least some pairs.

Some species appear to be obligatorily pair living because all of their social units consists of only one pair of adults (black). In other species, more than 50%, but less than 100%, of social units consist of pairs (dark gray). The remaining species are characterized by not only a predominance of groups with three or more adults but also some pairs (light gray). Total sample size is 1081 social units from 38 species.