Gowdy & Krall (G&K) make a strong argument that agriculture was a major evolutionary step toward ultrasociality in human social organization. We agree that, with the introduction of collective management of food production, new emergent properties appeared that are similar in overall function to those seen in eusocial species of ants and termites. We disagree, however, with the authors' view that ultrasociality would have abruptly appeared with the advent of farming. Sophisticated civilizations and technology, which emerged over a relatively short period of human evolutionary history, would have required a foundation of highly cooperative pre-existing social structures to develop. We argue that the target article lacks depth about the phylogenetic origins of human sociality and culture, including the cognitive mechanisms required to learn agricultural processes, neural plasticity during development that allows for the learning process to occur, and the existence of organized warfare and social hierarchies prior to the advent of agriculture.

Even though they share many of the defining features, humans employ a different set of social and cognitive mechanisms than insects do to generate and maintain agriculture. Habitual planting, cultivation, and harvesting in human farming systems are dependent on tool use, which necessitates abilities such as the cognitive manipulation of objects and symbols, observational trial and error learning, linguistic instruction, semantic knowledge, intentional modelling and imitation, and procedural memory (Guilmet Reference Guilmet1977; Mahaney Reference Mahaney2014). The evolution of tool use itself is the product of millions of years of evolution, and requires sophisticated problem solving skills as well as the ability to flexibly read social cues in cooperative-communicative contexts to successfully pass down technological knowledge to future generations (Hare Reference Hare2007). For agricultural practices to spread horizontally across populations and vertically down generations, humans had to teach each other how to implement new technologies, which would have involved pre-existing neural mechanisms, such as a mirror neuron system and the capacity for true language. While the emergence of language remains debated, with some theorists promoting a gradualist view and others an integration view, its origins still dramatically predate the appearance of agriculture, with language appearance estimates between 750,000 years ago to 100,000 years ago (Berwick et al. Reference Berwick, Friederici, Chomsky and Bolhuis2013; Boeckx & Benítez-Burraco Reference Boeckx and Benítez-Burraco2014; Corballis Reference Corballis2014; Nóbrega & Miyagawa Reference Nóbrega and Miyagawa2015). Without these neural systems and cognitive capacities, agriculture could not have appeared so suddenly.

Possibly the strongest evidence that humans transitioned to a unique stage of social evolution during phylogenetic development, prior to the existence of agriculture, is the biological mark that the stage has left on ontogeny. Humans have an extended period of altricial development and dependency on others, compared to other animals and primates, which requires sustained nurturing, time, and resources from parents, grandparents, and non-related adults (Hrdy Reference Hrdy, Carter, Anhert, Grossmann, Hrdy, Lamb, Porges and Sachser2005). As well, infants display altruistic behaviors and will expend energy to assist non-kin strangers with no reward (Warneken & Tomasello Reference Warneken and Tomasello2006). Even though one-year-olds can make distinctions between the recipients of their prosocial actions (Hay & Cook Reference Hay, Cook, Brownell and Kopp2007), young children will display indiscriminate sharing with non-related others and will do so prior to the emergence of contingent and indirect reciprocity, indicating strong intrinsic influences on prosocial behavior (Dahlman et al. Reference Dahlman, Ljungqvist and Johannesson2007; House et al. Reference House, Silk, Henrich, Barrett, Scelza, Boyette, Hewlett, McElreath and Laurence2013; Kenward & Dahl Reference Kenward and Dahl2011; Sebastián-Enesco et al. Reference Sebastián-Enesco, Hernández-Lloreda and Colmenares2013; Warneken & Tomasello Reference Warneken and Tomasello2013).

Additionally, G&K's claim that social hierarchies and warfare were products of agriculture may not be completely accurate. Dominance hierarchies, created by alpha status individuals through unequal fighting ability and/or inheritance, have deep evolutionary roots in many group-living animal species, including chimps, who display strong social inequality. Similar structures are also seen in modern hunter-gatherer societies (Drummond Reference Drummond2006; Holekamp & Smale Reference Holekamp and Smale1991; Smith et al. Reference Smith, Hill, Marlowe, Nolin, Wiessner, Gurven, Bowles, Borgerhoff Mulder, Hertz and Bell2010). Regarding organized warfare, Fry and Soderberg (Reference Fry and Söderberg2013) found that deaths occurring by warfare did occur in modern-day hunter-gatherer societies, and that disputes over resources were uncommon. Moreover, evidence exists that warfare predates the Neolithic period and very likely emerged during the Paleolithic (Choi & Bowles Reference Choi and Bowles2007; Thorpe Reference Thorpe2003).

Human agricultural systems must have been based on at least one previous evolutionary step to ultrasociality, from aggregate loosely tied groups based primarily on kinship to cooperative social networks based on culture and symbolism. Humans' exponential population growth, and successful migration and survival across different ecosystems, in addition to the advent of culture, also occurred prior to the advent of agriculture and would have represented a major evolutionary transition in social organization beyond kin-selection and what is seen in other primates (Nowak & Highfield Reference Nowak and Highfield2011; Warneken & Tomasello Reference Warneken and Tomasello2009; Wilson et al. Reference Wilson, Van Vugt and O'Gorman2008). The requirements for social and cultural learning, such as shared intentionality, symbolic representation, empathy, imitation, and theory of mind, would have required a substantial phylogenic period of prosocial interaction for the genetic and neurophysiological changes to become established within the human species (Henrich Reference Henrich2004; Tomasello et al. Reference Tomasello, Carpenter, Call, Behne and Moll2005). The advent of agriculture would have facilitated a new evolutionary transition in human social organization, and would be responsible for new social behaviors and structures such as written language (Basu & Waymire Reference Basu and Waymire2006); however, these innovations would have to be predicated on pre-existing social behaviors and structures such as spoken language.

G&K provide a strong case for agriculture catalyzing ultrasociality in humans, but we cannot restrict the causes to agriculture alone without considering the preceding socio-cognitive machinery in early humans. Overall, discussions of a major evolutionary transition into ultrasociality and agriculture must address the adaptive mechanisms and transitions that allowed such adaptability to occur in humans.