Evolutionary Anthropology 23:65–75 (2014) ARTICLE How Humans Evolved Large Brains: Comparative Evidence KARIN ISLER* AND CAREL P. VAN SCHAIK The human brain is about three times as large as that of our closest living rela- (see Dunbar and Shultz6). Each spe- tives, the great apes. Overall brain size is a good predictor of cognitive perform- cies does not just occupy an ecologi- ance in a variety of tests in primates.1,2 Therefore, hypotheses explaining the cal niche, it also constructs that evolution of this remarkable difference have attracted much interest. In this niche by influencing the external review, we give an overview of the current evidence from comparative studies conditions.7 An increase in brain size testing these hypotheses. If cognitive benefits are diverse and ubiquitous, it is may change the conditions, and possible that most of the variation in relative brain size among extant primates when such evolutionary feedback is explained by variation in the ability to avoid the fitness costs of increased loops occur, cause and effect become brain size (allocation trade-offs and increased minimum energy needs). This is impossible to disentangle. As we look indeed what we find, suggesting that an energetic perspective helps to comple- at the current endpoints of a long ment approaches to explain variation in brain size that postulate cognitive bene- evolutionary history, such a model fits. The expensive brain framework also provides a coherent scenario for how cannot and should not look for these factors may have shaped early hominin brain expansion. causal pathways, but only for pat- terns of correlated evolution. As a result, although the cost and benefit During most of the past 30 years, lutionary changes in the size of a approaches obviously complement there were two major approaches to structure rarely need to be con- each other, their combination in a explain the evolution of larger brains cerned about the energetic costs of predictive model is not trivial, since relative to the overall trend with its production or maintenance, one many correlates of brain size can be body size. Although analyses of evo- approach has stressed that because interpreted either way. For example, of the high metabolic costs of brain a high-quality diet may indicate tissue,3 brains can increase in size increased digestive efficiency and only if the additional energy costs thus be an independent external 4 Karin Isler studies brain size evolution in can somehow be met. Another determinant that is relevant for mammals and birds using a phylogenetic approach, while recognizing these understanding brain size variation comparative approach. She has pub- from an energetic perspective but, on lished a series of papers on energetic costs, focused on the enhanced cog- correlates of brain size evolution and is nitive abilities in the ecological or the other hand, it may also reflect a currently investigating cognitive and social domain of larger brains and cognitive benefit of an enhanced abil- physiological strategies to buffer lean periods. Email: [email protected] on the fitness benefits this brings to ity to find or gain access to high- their owners by increasing survival quality food items. Therefore, most Carel van Schaik is interested in the 5 studies so far have concentrated on social, cognitive and cultural evolution of or reproductive output. Because primates, focusing specifically on selection can only favor an increase one or the other approach and, until explaining traits that are unusually devel- in the size of a structure relative to recently, most focused on benefits.8 oped in humans. He currently focuses on comparative studies of cooperative its ancestral state if the net balance Here, we place the emphasis on breeding and cooperative hunting to of fitness costs and benefits is posi- reviewing the empirical evidence for identify convergent developments in the tive (Fig. 1), it is clear that the two energetic correlates of brain size evo- hominin lineage. approaches necessarily complement lution. We discuss each potential cor- each other. relate separately and then test The first aim of this review is to whether a combination of various Key words: energetics; comparative phylogenetic integrate cost and benefit approaches factors explains more of the existing analysis; hominin evolution in a predictive model to explain the variation in primate brain size than existing variation in brain size by does any single factor. VC 2014 Wiley Periodicals, Inc. taking a broad comparative perspec- Our second aim is to apply DOI: 10.1002/evan.21403 tive, considering primates and other these insights to human evolution. Published online in Wiley Online Library (wileyonlinelibrary.com). mammals, and birds where necessary Starting from a statistical model for 66 Isler and Van Schaik ARTICLE Although the Social Brain Hypoth- esis explains much of the variation of relative brain (and especially neo- cortex) size in cercopithecoid prima- tes, it does not account for some striking grade shifts.16 For instance, lemurs appear to experience similar social challenges, but are clearly less encephalized than monkeys.17 There- fore, we will pursue the idea that some grade shifts arise because of problems in generating sufficient energy or a large enough survival benefit for selection to have favored increased brain size. ECOLOGY AND GENERAL FLEXIBILITY A relatively large brain may prefer- Figure 1. A simple model of the energetic costs and fitness benefit effects of an evolu- entially evolve in those species or lin- tionary increase in brain size. While energetic costs may decrease fitness, the benefits of eages that rely on a variety of enhanced cognitive performance increase fitness. Both must be considered to assess the net effect of an increase in brain size on fitness. cognitive skills to obtain food or avoid predators or parasites. The causal link is straightforward: more skilled individuals acquire more or nonhuman primates that includes The best known benefits-oriented better food and are better at avoid- both benefits and costs, we include explanation of brain size evolution ing starvation, predation, or infec- humans to see whether the charac- argues that the social environment is tions, thus surviving longer and teristics of our species fit the general likely to provide the context in which producing more surviving off- primate pattern. At the end, by look- behavioral flexibility is most benefi- spring.18 This idea is supported by ing at fossil and archeological evi- cial.15 Thus, the Social Brain correlations between survival rates, dence for the order of appearance of Hypothesis proposed that living in invasion success, or longevity, on these human-specific traits, we pres- large groups is feasible only if the one hand, and brain size or innova- ent the most parsimonious historical animals are able to monitor and tion rates on the other hand.19,20 scenario, given current comparative remember social relationships. This However, if survival is increased, evidence. idea thus links increased brain size life-history theory predicts that other to the evolution of large and complex aspects of life history will follow social groups in primates.15 In non- suit.21 The evidence of prolonged BENEFIT APPROACHES primates, this group-size prediction development periods in larger- Several behavioral characteristics was supported for some lineages but brained species9,22 may thus simply have been suggested as the specific not others.10 Therefore, the hypothe- be an inevitable consequence of pro- selective agent that enabled a sis was slightly modified to argue longed life span. Attempts to deter- decrease in mortality and, ultimately, that in birds or mammals other than mine which of the life-history an extension of the maximum primates the most complex form of variables is most closely linked to observed life span in relatively large- social relationship is the pair bond, brain size and thus the most likely brained species. The hypotheses can which explains the positive correla- driver of the correlations between broadly be divided into those focus- tion between the occurrence of pair brain and life history in evolution ing on either social or ecological ben- bonds and brain size in artiodactyls are therefore rather futile. All life- efits of enhanced cognitive abilities and carnivores,10 as well as birds.11 history traits covary; therefore, the (reviewed for example in Deaner, Because primates have friendships results of multivariate regression Barton, and van Schaik9). Social that function like the pair bonds in analyses are mostly determined by skills comprise social strategizing or other lineages, the primate pattern the different amounts of error varia- pair-bonding,5,10,11 whereas ecologi- also fits this new explanation. tion within each variable. The vari- cal skills involve spatial orientation to The Social Brain Hypothesis also able measured with the highest find food patches or remember their explains why, over evolutionary time, accuracy will turn out to explain location, dietary flexibility, food proc- those lineages that had social bonds most of the variation in brain size, essing, tool use, extractive forag- or pair bonds showed steep increases while others are dropped from the ing,12,13 or predator recognition and over time, whereas those that did model. Consequently, studies of dif- avoidance.14 not failed to do so.8 ferent datasets or using slightly ARTICLE Comparative Evidence 67 different methodology may yield because brain tissue is among the specific characteristics of ecology divergent results.23 most energetically expensive tissues and life style. Socioecological factors Specialized skills such as food cach- of the body3 and its energy con- affect a species’ potential to follow ing, tool use, or manual dexterity have sumption rate varies only slightly one or the other of these pathways so far not been related to overall brain between various brain regions or to pay for an evolutionary increase size, but to cerebellum size, the degree during different activities.29 Thus, in brain size.