Cultural group selection (CGS) does indeed, as the target article argues, play an important role in explaining human cooperation. However, social selection offers a powerful explanation of extreme human prosociality that contradicts Richerson et al.'s second thesis that only CGS “can easily account for the institutionalized cooperation that characterizes human societies” (sect. 7, para. 2).

The authors document transmissible substantial variations between cultural groups that account for the growth and persistence of some human groups at the expense of other groups. Examples from religious groups confirm the theory. The Shakers had 6,000 members in the mid-19th century but the norm of celibacy shrank the group by outmigration and lack of reproduction, so only one small community remains. In contrast, the Catholic Church's prohibition of birth control fosters group growth.

CGS not only occurs, but also it can act on between-group variations in cooperativeness to help explain human prosociality. Groups with norms enforcing cooperation tend to expand and displace other groups, although, as the target article notes, complexities arise because of the costs of cooperating, the costs of punishing defectors, and movement of individuals and norms between groups. Nonetheless, CGS offers a plausible explanation for cooperation within groups, and tendencies for conflict between groups. Once established, cultural norms for in-group cooperation create forces of natural selection that give advantages to individuals with tendencies to learn and conform to those norms, as well as to their groups, in a recursive cycle that gives rise to capacities for complex culture.

CGS is not, however, the only plausible explanation for extreme human prosociality, and it does little to explain how the process gets going. Social selection can explain extreme human prosocial traits that CGS cannot. This is not Herbert Simon's social selection or that of Joan Roughgarden; it is the idea, first explored in depth in a pair of papers by Mary Jane West-Eberhard, that describe how self-interested social choices create strong selection forces that may account for extreme prosociality and other traits that are otherwise difficult to explain (West-Eberhard Reference West-Eberhard1979; Reference West-Eberhard1983; cf. Nesse Reference Nesse, Verplaetse, Schrijver, Vanneste and Braeckman2009). She defines social selection in relation to its exemplar and subtype, sexual selection:

Peahen preferences for peacocks with flamboyant tails give a fitness advantage to males with extreme traits, and to females who prefer males with extreme traits. Positive feedback between selection for the trait and the preference increases the prevalence of alleles that increase mating success until the fitness costs to health and survival outweigh their mating benefits.

West-Eberhard's core insight was that social selection occurs for competition over resources other than matings. A recent review noted, “It would have made as much sense for Darwin (and everybody since) to distinguish between selection by choice versus competition rather than on sexual versus non-sexual selection” (Lyon & Montgomerie Reference Lyon and Montgomerie2012, p. 5). Social selection for competition opens up a whole world of important explanations, but partner choice is more important for explaining cooperation. Despite formal models (Frank Reference Frank, Fox and Wolf2006; Tanaka Reference Tanaka1996; Wolf et al. Reference Wolf, Brodie and Moore1999) and detailed descriptions with examples from many species (Flinn & Alexander Reference Flinn, Alexander, Gangestad and Simpson2007; Lyon & Montgomerie Reference Lyon and Montgomerie2012; Tobias et al. Reference Tobias, Montgomerie and Lyon2012), social selection has been neglected as an explanation for human prosociality.

As many have noted, most social exchanges are mutualisms or are readily explained by kin selection or reciprocity. However, some extreme human prosocial traits still need explanation. CGS has a hard time explaining the pervasiveness and intensity of guilt, motivations for reparations, extreme sensitivity to what others think, concern for other's welfare, pity, commitment, empathy, philanthropy, and pride in generosity. Such traits are, however, expected outcomes from social selection that gives advantages to those preferred as relationship partners or group members.

People prefer partners and group members who have plentiful resources that they generously and reliably share (albeit selectively) with their partners. Thus, to be preferred as a partner requires striving to get resources and a reputation for sharing them. The fitness benefits are not as direct as increased matings, but they are more pervasive. Day by day, reputations and relationships grow and fade as the result of actions small and large. The most desirable relationship partners pair with each other, and this selective association gives them a selective advantage. As West and colleagues note in a critique of trait group selection models, “An alternative is to state as simply as possible what they are – models of nonrandom assortment of altruistic genes” (West et al. Reference West, Griffin and Gardner2007, p. 11).

The benefits experienced by prosocial individuals, and the benefits of preferring such individuals as partners or group members, shape social traits as extreme and costly as a peacock's tail. This requires no kin selection, reciprocity, group selection, or CGS, although all of those phenomena are also involved in selecting for prosocial traits.

Social selection has been modeled in economic terms as partner choice that shapes advertisements for generosity (Noë et al. Reference Noë, van Hooff and Hammerstein2001) that can become more honest and costly than intended. However, effort invested in carefully assessing partners and making oneself a preferred partner is only the start. Models describing whether to stay or walk away from an existing relationship illustrate how walking away can be inexpensive or even beneficial for the punisher but devastating to the person punished, efficiently enforcing social norms (Aktipis Reference Aktipis2004). Shunning and solitary confinement are cruel for good evolutionary reasons.

Careful selection of partners and group members offers little advantage in a species unless differentiated relationships offer a net advantage, some more than others. After a tipping point was reached, however, investments in careful partner choice and traits that make one a preferred partner could coevolve in a possibly runaway process that may have been crucial in making culture possible (Nesse Reference Nesse, Schaller, Heine, Norenzayan, Yamagishi and Kameda2010). Social selection may explain how self-interested social choices could have created selection forces by which humans domesticated themselves.