http://informahealthcare.com/ahb ISSN: 0301-4460 (print), 1464-5033 (electronic) Ann Hum Biol, 2014; 41(4): 368–380 ! 2014 Informa UK Ltd. DOI: 10.3109/03014460.2014.923938 REVIEW Humans are not cooperative breeders but practice biocultural reproduction Barry Bogin 1 , Jared Bragg 2 , and Christopher Kuzawa 2 1 School of Sport, Exercise & Health Sciences, Loughborough University, Loughborough, UK and 2 Department of Anthropology, Northwestern University, Evanston, IL, USA Abstract Context: Alloparental care and feeding of young is often called ‘‘cooperative breeding’’ and humans are increasingly described as being a cooperative breeding species. Objective: To critically evaluate whether the human offspring care system is best grouped with that of other cooperative breeders. Methods: (1) Review of the human system of offspring care in the light of definitions of cooperative, communal and social breeding; (2) re-analysis of human lifetime reproductive effort. Results: Human reproduction and offspring care are distinct from other species because alloparental behaviour is defined culturally rather than by genetic kinship alone. This system allows local flexibility in provisioning strategies and ensures that care and resources often flow between unrelated individuals. This review proposes the term ‘‘biocultural reproduction’’ to describe this unique human reproductive system. In a re-analysis of human life history data, it is estimated that the intense alloparenting typical of human societies lowers the lifetime reproductive effort of individual women by 14–29% compared to expectations based upon other mammals. Conclusion: Humans are not cooperative breeders as classically defined; one effect of the unique strategy of human biocultural reproduction is a lowering of human lifetime reproductive effort, which could help explain lifespan extension. Keywords Alloparenting, human life history, childhood, lifetime reproductive effort, longevity History Received March 2014 Accepted 9 May 2014 Published online 16 June 2014 Introduction Compared with most species of primates, especially the apes, humans have an unusual style of producing and raising offspring that is often described as cooperative breeding (Burkart et al., 2009; Hrdy, 1999, 2009). This special issue of the Annals of Human Biology focuses on ‘‘Human Biology of the Past’’ and the evolution of the human biocultural style of reproduction is a central feature of the topic. Here we review evidence and provide new analyses showing that, although sharing many features with cooperative breeders, the human strategy of reproduction and child rearing is distinct from that of most cooperative breeders. We argue that the human species practices biocultural reproduction. Biocultural reproduction describes a suite of biological and sociocultural adaptations, including: (1) cognitive capacities for non- genetically based marriage and kinship behaviour that provide demographically and ecologically flexible, but culturally universal, alloparental care for offspring, (2) a life history phase of childhood, characterized by the absence of nursing but considerable ongoing nutritional dependence, creating extended opportunities and needs for the provision of care by individuals other than the parents, (3) early weaning, leading to an increased rate of reproduction and (4) decreased lifetime reproductive effort, which likely contributed to decreased mortality and lifespan extension. Cooperative breeding vs human cooperation in reproduction We begin by making our case for the introduction of the neologism biocultural reproduction, as distinct from recent work that groups the type of highly social childcare practiced in human social groups as cooperative breeding (Burkart et al., 2009; Hrdy, 1999, 2009; Meehan et al., 2014). To be ‘‘cooperative’’ in breeding is often defined to mean that individuals of a species live in groups and that members of the group help to feed, care for or protect offspring that they did not bear (Burkart et al., 2009). Individuals providing these services are called alloparents. Another commonly cited criterion is that the provisioning, care and protection that alloparents provide must come at some cost to the alloparents. That cost may be measured in assisting others to gain access to food or in terms of reducing the alloparents’ opportunities to reproduce (Lukas & Clutton-Brock, 2012; Solomon & French, 1997). Cooperative breeding species are not common in the Order Primates and, indeed, marmosets and tamarins of South America are the only widely-recognized species of coopera- tive breeding non-human primates (Fite et al., 2005; Correspondence: Barry Bogin, School of Sport, Exercise & Health Sciences, Loughborough University, Loughborough, UK. Tel: 44 (0)1509 228819. E-mail: b.a.bogin@lboro.ac.uk Ann Hum Biol Downloaded from informahealthcare.com by Loughborough University on 06/16/14 For personal use only.