Large brains have evolved multiple times and in multiple taxa (Jerison, 1973). This is puzzling because a brain disproportionately large for a given body size is metabolically expensive (Aiello & Wheeler, 1995; Isler & van Schaik, 2006, 2009a,b) and takes a substantial time to reach structural and functional maturity (Casey et al., 2005). Long developmental periods result in significant fitness costs for large-brained species, both in terms of increased offspring mortality risk (Sacher & Staffeldt, 1974; Stearns, 2000; Deaner et al., 2003; Barrickman et al., 2008) and delayed age of first reproduction (Deaner et al., 2003; Barrickman et al., 2008). Consequently, natural selection should have favoured the evolution of large brains only if they provide advantages that counterbalance their production and maintenance costs.
Several hypotheses have been proposed to explain the adaptive advantages of larger brains (see Deaner et al., 2003; van Schaik & Deaner, 2003; Dunbar & Shultz, 2007a; Sol, 2009a), most of which assume that enlarged brains carry cognitive advantages. Amongst others, these include monitoring food sources that vary in space and time (Clutton-Brock & Harvey, 1980; Milton, 1988), using hard-to-eat foods (Parker & Gibson, 1977, 1979), exploiting novel foraging opportunities (Lefebvre et al., 1997) and modifying behaviour in response to conspecifics (Jolly, 1966; Humphrey, 1976; Cheney & Seyfarth, 1986; Byrne & Whiten, 1988; Whiten, 2000; Dunbar & Shultz, 2007b). The above hypotheses focus on selective advantages of enlarged brains but do not provide an explicit explanation for how these benefits balance the developmental costs of affording large brains. However, if these benefits reflect general cognitive capacities for constructing behavioural responses to novel socio-ecological challenges, then this should reduce extrinsic mortality and partially compensate the developmental costs with a longer reproductive life (Allman et al., 1993; Allman, 2000; Deaner et al., 2003; Sol et al., 2007; Sol, 2009a,b). This interpretation, the so-called ‘cognitive buffer hypothesis’, thus integrates previous hypotheses, acknowledges that brains carry out multiple functions and provides an explicit explanation of the benefits of brain enlargement (Allman et al., 1993; Allman, 2000; Deaner et al., 2003; Sol, 2009a).
Recently, comparative work on brain evolution has been criticized because diverse findings regarding correlates of brain enlargement have not been integrated (Healy & Rowe, 2007). The lack of consideration of alternative hypotheses for the evolution of enlarged brains is a repeated criticism (Deaner et al., 2000; Reader & Laland, 2002; Dunbar & Shultz, 2007b). The diversity of reported correlates of brain enlargement probably reflects the fact that the brain performs multiple functions: postulating a single cognitive benefit for brain enlargement is unlikely to be successful. There is considerable evidence that species with enlarged brains for their body size show enhanced cognitive capacities, although the mechanisms behind these relationships are obscure and warrant study (reviewed in Healy & Rowe, 2007; Lefebvre & Sol, 2008). For example, multiple studies have demonstrated associations between brain size and components of behavioural flexibility, such as innovation, tool use, tactical deception, social learning, reversal-learning and combined measures of laboratory learning performance, in both birds and primates (Lefebvre et al., 1997, 2004; Reader & Laland, 2002, 2003; Reader, 2003; van Schaik & Deaner, 2003; Byrne & Bates, 2007; Deaner et al., 2007). Evidence is also accumulating that flexibility in behaviour facilitates the production of adaptive responses to a wide array of ecological challenges (reviewed in Sol, 2009a). In birds and mammals, for example, large-brained species are more likely to be successful when introduced by humans in novel environments than are small-brained species (Sol et al., 2005, 2008). Moreover, amongst British birds, species with relatively large brains were less likely to suffer population declines (Shultz et al., 2005). Thus several lines of evidence support the idea that brain volume is associated with diverse measures of behavioural flexibility and with success in novel or changed environments, providing a route to integrate previous findings.
Surprisingly, however, evidence for a critical prediction of the cognitive-buffer hypothesis that brain enlargement translates to increased life expectancy remains mixed. In mammals, the animals with the largest relative brain sizes, some studies have demonstrated a significant relationship between brain size and lifespan (e.g. Hakeem et al., 1996; Deaner et al., 2003; Kaplan et al., 2003; Isler & van Schaik, 2009a,b), but others did not (e.g. Barton, 1999; Ross & Jones, 1999; Judge & Carey, 2000). The disparity of results may arise from differences in the way that previous studies controlled or failed to control for confounding factors and phylogenetic effects. Moreover, previous analyses were generally based on a reduced number of species and were biassed towards primates (reviewed in Barrickman et al., 2008). This focus potentially reduces the interspecific variation observed in brain size and lifespan, which could reduce the possibility of detecting patterns. Understanding the evolution of large brains is only possible if we further validate the brain–lifespan association in many taxa and with approaches that properly deal with phylogenetic and confounding factors (Lefebvre et al., 2004; Sol, 2009a). Here, we ask whether large-brained mammals live longer with a global phylogenetic-based comparative analysis covering 493 mammalian species. We extend on recent similar analyses (Isler & van Schaik, 2009a,b) by taking into account previously unconsidered confounding variables, using datasets covering additional taxa (e.g. marsupials), and directly estimating and accounting for phylogenetic effects (Hansen & Orzack, 2005). We show that the association of larger brains with longer lifespan holds independently of other life history traits, of research effort, and of energetic, environmental, dietary and habitat variables, thus providing unambiguous support for the idea that the costs of delaying reproduction in large-brained species can be partly compensated by a longer reproductive life.