Christopher Opie

Stepwise evolution of stable sociality in primates

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.

Male infanticide leads to social monogamy in primates.

Although common in birds, social monogamy, or pair-living, is rare among mammals because internal gestation and lactation in mammals makes it advantageous for males to seek additional mating opportunities. A number of hypotheses have been proposed to explain the evolution of social monogamy among mammals: as a male mate-guarding strategy, because of the benefits of biparental care, or as a defense against infanticidal males. However, comparative analyses have been unable to resolve the root causes of monogamy. Primates are unusual among mammals because monogamy has evolved independently in all of the major clades. Here we combine trait data across 230 primate species with a Bayesian likelihood framework to test for correlated evolution between monogamy and a range of traits to evaluate the competing hypotheses. We find evidence of correlated evolution between social monogamy and both female ranging patterns and biparental care, but the most compelling explanation for the appearance of monogamy is male infanticide. It is only the presence of infanticide that reliably increases the probability of a shift to social monogamy, whereas monogamy allows the secondary adoption of paternal care and is associated with a shift to discrete ranges. The origin of social monogamy in primates is best explained by long lactation periods caused by altriciality, making primate infants particularly vulnerable to infanticidal males. We show that biparental care shortens relative lactation length, thereby reducing infanticide risk and increasing reproductive rates. These phylogenetic analyses support a key role for infanticide in the social evolution of primates, and potentially, humans.

Phylogenetic reconstruction of Bantu kinship challenges Main Sequence Theory of human social evolution.

Significance The agricultural revolution had a dramatic effect on all aspects of human society, but piecing together how humans lived as they spread farming practices worldwide remains difficult. In particular, the fundamental structures of human society, namely the way that property is inherited and the rules governing postmarriage residence, do not leave a clear trace in the archaeological record and, therefore, have been largely intractable. However, the recent availability of phylogenetic language trees coupled with new Bayesian statistical techniques makes it possible to reconstruct the ancestral state of Bantu kinship and reveals that inheritance and residence rules coevolved as farming spread throughout sub-Saharan Africa. Our results question current theory suggesting that residence rules are the primary driver of all other human social structures. Kinship provides the fundamental structure of human society: descent determines the inheritance pattern between generations, whereas residence rules govern the location a couple moves to after they marry. In turn, descent and residence patterns determine other key relationships such as alliance, trade, and marriage partners. Hunter-gatherer kinship patterns are viewed as flexible, whereas agricultural societies are thought to have developed much more stable kinship patterns as they expanded during the Holocene. Among the Bantu farmers of sub-Saharan Africa, the ancestral kinship patterns present at the beginning of the expansion are hotly contested, with some arguing for matrilineal and matrilocal patterns, whereas others maintain that any kind of lineality or sex-biased dispersal only emerged much later. Here, we use Bayesian phylogenetic methods to uncover the history of Bantu kinship patterns and trace the interplay between descent and residence systems. The results suggest a number of switches in both descent and residence patterns as Bantu farming spread, but that the first Bantu populations were patrilocal with patrilineal descent. Across the phylogeny, a change in descent triggered a switch away from patrifocal kinship, whereas a change in residence triggered a switch back from matrifocal kinship. These results challenge “Main Sequence Theory,” which maintains that changes in residence rules precede change in other social structures. We also indicate the trajectory of kinship change, shedding new light on how this fundamental structure of society developed as farming spread across the globe during the Neolithic.

Reply to Lukas and Clutton-Brock: Infanticide still drives primate monogamy

For many years, it has been variously suggested that the evolution of monogamy in primates was due to paternal care, dispersed female ranging, or infanticide. It was therefore of little surprise to us that we should find that these traits are strongly associated with mating systems in primates (1). The crucial question, however, is whether these traits are potential drivers of, or secondary responses to, the appearance of monogamy. We found that it was only infanticide that reliably preceded monogamy and could therefore be implicated in its evolution. In contrast, dispersed female ranges and paternal care followed the adoption of monogamy, suggesting they are consequences and not causes of monogamy.

The evolutionary history of primate mating systems

Unlike bones, behavior does not fossilize, so it is hard to infer the evolutionary history of social traits. However, we have shown elsewhere that Bayesian phylogenetic methods allow the investigation of ancestral states and models of evolution of social grouping behaviour in primates. Here, we extend this analysis to another significant aspect of primate social life, which may be subject to different evolutionary pressures—mating systems. We show that mating systems evolved from a polygynandrous state at the root of the phylogeny to the two derived states of harem-polygyny and monogamy. Unlike social organization, where there were no transitions from uni-male groups to pairs, here we found positive transition rates from both polygynous mating states into monogamy. There were no transitions out of monogamy to another mating state. Both derived mating systems evolved late in primate evolution. Nocturnal primates remained solitary foragers while their mating systems evolved from polygynandry to harem-polygyny and monogamy. However, among diurnal primates the derived mating states evolved at the same time as the derived states of social organization.

Postcopulatory sexual selection influences baculum evolution in primates and carnivores.

The extreme morphological variability of the baculum across mammals is thought to be the result of sexual selection (particularly, high levels of postcopulatory selection). However, the evolutionary trajectory of the mammalian baculum is little studied and evidence for the adaptive function of the baculum has so far been elusive. Here, we use Markov chain Monte Carlo methods implemented in a Bayesian phylogenetic framework to reconstruct baculum evolution across the mammalian class and investigate the rate of baculum length evolution within the primate order. We then test the effects of testes mass (postcopulatory sexual selection), polygamy, seasonal breeding and intromission duration on the baculum in primates and carnivores. The ancestral mammal did not have a baculum, but both ancestral primates and carnivores did. No relationship was found between testes mass and baculum length in either primates or carnivores. Intromission duration correlated with baculum presence over the course of primate evolution, and prolonged intromission predicts significantly longer bacula in extant primates and carnivores. Both polygamous and seasonal breeding systems predict significantly longer bacula in primates. These results suggest the baculum plays an important role in facilitating reproductive strategies in populations with high levels of postcopulatory sexual selection.

Reply to Dixson: Infanticide triggers primate monogamy

We thank Alan Dixson (1) for his interest in our paper (2). Unfortunately, he seems to have misread it. First, contrary to Dixson’s claim, we did not conflate callitrichid “monogamy” with obligate monogamy in other primates, like gibbons and the small cebids. We note that these were conflated in Lukas and Clutton-Brock’s (3) recent report on the evolution of monogamy but not in our paper. Dixson may have confused the two papers [in their commentary on the papers, de Waal and Gavrilets (4) make the same mistake]. Instead, we classified callitrichids as having a variable mating system [as most field workers now acknowledge: see also Dunbar (5)].