Proactive prosociality

The first and perhaps most important consequence of cooperative breeding is that it leads to higher levels of proactive prosociality at the group level. To test this, we used the group service paradigm, in which an individual can provide food to other group members without receiving any food itself, and applied it to 24 groups of 15 species of nonhuman primates (Burkart et al. Reference Burkart, Allon, Amici, Fichtel, Finkenwirth, Heschl, Huber, Isler, Kosonen, Martins, Meulman, Richiger, Rueth, Spillmann, Wiesendanger and van Schaik2014). The results (Fig. 1A) show that the extent of allomaternal care directed at immatures is the best predictor of experimentally assessed proactive prosociality within a group, far better in fact than any other factor proposed so far, including brain size, social tolerance, cooperative hunting, or the presence of strong social bonds. Most importantly, humans perfectly fit the nonhuman primate regression, suggesting that we do not need a special explanation for our proactive prosociality.

Figure 1. The relationship between allomaternal care and (A) proactive prosociality and (B) social tolerance. Humans fit the general primate trend and do not represent an outlier.

Social transmission

Cooperatively breeding primates, the callitrichid monkeys, consistently show enhanced performance in social learning tasks (Burkart & van Schaik Reference Burkart and van Schaik2010; Snowdon Reference Snowdon2001) compared to their independently breeding sister taxa, most likely due to their high social tolerance (Coussi-Korbel & Fragaszy Reference Coussi-Korbel and Fragaszy1995), which, like proactive prosociality, demonstrably increases with increasing levels of allomaternal care across primates (Fig. 1B). Indeed, callitrichid monkeys not only show high levels of social learning, but also the best evidence for teaching among nonhuman primates comes from callitrichids (Dell'Mour et al. Reference Dell'Mour, Range and Huber2009; Humle & Snowdon Reference Humle and Snowdon2008; Rapaport Reference Rapaport2011), and not from the intelligent, yet independently breeding great apes (Boesch Reference Boesch1991; Humle et al. Reference Humle, Snowdon and Matsuzawa2009; Lonsdorf Reference Lonsdorf2006). Among non-primates, teaching is similarly over-represented in cooperatively breeding species (Byrne & Rapaport Reference Byrne and Rapaport2011; Kline Reference Kline2015).

Communication and language

Callitrichids also show remarkably complex vocal communication (Rukstalis et al. Reference Rukstalis, Fite and French2003; Zuberbühler Reference Zuberbühler, Tallerman and Gibson2012), with large vocal repertoires and unusual levels of vocal learning, both as immatures (including babbling) and as adults, as well as vocal control (Roy et al. Reference Roy, Miller, Gottsch and Wang2011; Snowdon Reference Snowdon and Helekar2013). Intriguingly, and reflecting their prosocial attitude, cooperatively breeding monkeys regularly use food-offering calls (Vitale et al. Reference Vitale, Zanzoni, Queyras and Chiarotti2003) and cooperative vocal communication (Takahashi et al. Reference Takahashi, Narayanan and Ghazanfar2013), in that they take turns in extended sequences of call exchanges that are based on conversation rules strikingly similar to those used by humans (Stivers et al. Reference Stivers, Enfield, Brown, Englert, Hayashi, Heinemann, Hoymann, Rossario, de Ruiter, Yoon and Levinson2009). Notably, apes altogether lack communicative turn taking. Information donation (in the form of functionally referential food calls, teaching, or vocal cooperation; Takahashi et al. Reference Takahashi, Narayanan and Ghazanfar2013) is thus over-represented in cooperatively breeding primates compared to independently breeding ones. It is the basis for language, which explains why apes, who possess most basic cognitive requirements for language but largely lack this prosocial motivation (Tomasello Reference Tomasello2007), never evolved language.

These broad evolutionary trends can explain why human psychology became different from that of the other great apes: Alone among great apes, our ancestors started to rear their offspring cooperatively. Extensive allomaternal care is a better explanation than the other source of human cooperation, male bonding and the resulting cooperative hunting and indirect reciprocity in food sharing, because in other male-bonded or cooperatively hunting species, we do not see similar prosocial tendencies, unless they also are cooperative breeders (Burkart et al. Reference Burkart, Hrdy and Van Schaik2009; Burkart & van Schaik Reference Burkart and van Schaik2010).

In sum, comparative evidence supports the idea that cooperative breeding installed in our ancestors the psychological predispositions that functioned as the pre-adaptive substrate upon which CGS could eventually be built: the design for group function (language – see target article, sect. 6.1) and mechanisms maintaining intergroup variation (social learning – sect. 2; prosociality – sect. 6.3). This argument enhances the plausibility of CGS in the Holocene transition. First, without this foundation, CGS has a circularity problem. High-fidelity, low-cost signaling had to evolve first in order to allow gene-culture coevolutionary processes to install a more prosocial psychology, which in turn would have paved the way for high-fidelity, low-cost signaling and eventually language. Second, the adoption of cooperative breeding offers a plausible explanation for why our ancestors, but none of the other great apes, took this extraordinary trajectory. Thus, regardless of whether CGS is needed to explain the Holocene transition to large-scale societies, cooperative breeding is necessary to explain its operation in the first place.