Life history costs and benefits of encephalization: a comparative test using data from long-term studies of primates in the wild

Abstract

The correlation between brain size and life history has been investigated in many previous studies, and several viable explanations have been proposed. However, the results of these studies are often at odds, causing uncertainties about whether these two character complexes underwent correlated evolution. These disparities could arise from the mixture of wild and captive values in the datasets, potentially obscuring real relationships and from differences in the methods of controlling for phylogenetic nonindependence of species values. This paper seeks to resolve these difficulties by (1) proposing an overarching hypothesis that encompasses many of the previously proposed hypotheses; (2) testing the predictions of this hypothesis using rigorously compiled data and utilizing multiple methods of analysis. Our hypothesis is that the adaptive benefit of increased encephalization is an increase in reproductive lifespan or efficiency, which must be sufficient to outweigh the costs due to growing and maturing the larger brain. These costs and benefits are directly reflected in the length of life history stages. We tested this hypothesis on a wide range of primate species. Our results demonstrate that encephalization is significantly correlated with prolongation of all stages of developmental life history except the lactational period, and is significantly correlated with an extension of the reproductive lifespan. These results support the contention that the link between brain size and life history is caused by a balance between the costs of growing a brain and the survival benefits the brain provides, and specifically the slowing of life history during human evolution is caused by increased encephalization. 1Life history costs and benefits of encephalization: a comparative test using data from long-term studies of primates in the wild Nancy L. Barrickman AbstractThe correlation between brain size and life history has been investigated in many previous studies, and several viable explanations have been proposed. However, the results of these studies are often at odds, causing uncertainties about whether these two character complexes underwent correlated evolution. These disparities could arise from the mixture of wild and captive values in the datasets, potentially obscuring real relationships and from differences in the methods of controlling for phylogenetic nonindependence of species values. This paper seeks to resolve these difficulties by (1) proposing an overarching hypothesis that encompasses many of the previously proposed hypotheses; (2) testing the predictions of this hypothesis using rigorously compiled data and utilizing multiple methods of analysis. Our hypothesis is that the adaptive benefit of increased encephalization is an increase in reproductive lifespan or efficiency, which must be sufficient to outweigh the costs due to growing and maturing the larger brain. These costs and benefits are directly reflected in the length of life history stages. We tested this hypothesis on a wide range of pr...

The Expensive Brain: A framework for explaining evolutionary changes in brain size

“…If results differ between raw and independent contrasts analyses, we adhere to the following rationale for interpretation (see also Barrickman et al 2008): If a grade shift is detected that influences raw data regressions, IC results are given preference. Otherwise, if IC results do not confirm significant relationships found in raw data analysis, we tested whether omission of those contrasts with absolute studentized residuals larger than three yield more consistent results (Jones and Purvis 1997).…”

Explaining brain size variation: from social to cultural brain

“…Concerning the second pathway, among the various possibilities (cf. [70]), only the tradeoff between brain size and 'production' (the combination of growth and reproduction) is empirically supported [64,70,71]. Reflecting this tradeoff, larger-brained mammals mostly have slower development [70,72].…”

Increased juvenile predation is not associated with evolved differences in adult brain size in Trinidadian killifish (Rivulus hartii)

“…There are clear fitness benefits associated with a larger brain as brain size is positively correlated with increased intelligence, cognition, learning capability, population persistence, and decreased susceptibility to predation (Sol & Lefebvre, 2000; Tebbich & Bshary, 2004; Shultz & Dunbar, 2006a; Sol, Szekely, Liker, & Lefebvre, 2007; Sol, Bacher, Reader, & Lefebvre, 2008; Overington, Morand‐Ferron, Boogert, & Lefebvre, 2009; Barrickman, Bastian, Isler, & van Schaik, 2008; Amiel, Tingley, & Shine, 2011; Reader, Hager, & Laland, 2011; Kotrschal et al., 2013b; MacLean et al., 2014; Kotrschal et al., 2015a; Kotrschal, Corral‐Lopez, Amcoff, & Kolm, 2015b; Benson‐Amram, Dantzer, Stricker, Swanson, & Holekamp, 2016; but also see Drake, 2007). Key hypotheses, such as the expensive tissue hypothesis (i.e., expensive metabolic cost of brain tissue) (Aiello & Wheeler, 1995; Isler & van Schaik, 2009) and energy trade‐off hypothesis (increased encephalization leads to trade‐offs with other functions) (Isler & van Schaik, 2006a,b, 2009; Navarrete, van Schaik, & Isler, 2011; Tsuboi et al., 2015), recognize that brain tissue is costly and that fitness trade‐offs likely underlie increased encephalization (Aiello & Wheeler, 1995).…”