Comparative analyses of evolutionary rates reveal different pathways to encephalization in bats, carnivorans, and primates

Abstract

Variation in relative brain size is commonly interpreted as the result of selection on neuronal capacity. However, this approach ignores that relative brain size is also linked to another highly adaptive variable: body size. Considering that one-way tradeoff mechanisms are unlikely to provide satisfactory evolutionary explanations, we introduce an analytical framework that describes and quantifies all possible evolutionary scenarios between two traits. To investigate the effects of body mass changes on the interpretation of relative brain size evolution, we analyze three mammalian orders that are expected to be subject to different selective pressures on body size due to differences in locomotor adaptation: bats (powered flight), primates (primarily arboreal), and carnivorans (primarily terrestrial). We quantify rates of brain and body mass changes along individual branches of phylogenetic trees using an adaptive peak model of evolution. We find that the magnitude and variance of the level of integration of brain and body mass rates, and the subsequent relative influence of either brain or body size evolution on the brain–body relationship, differ significantly between orders and subgroups within orders. Importantly, we find that variation in brain–body relationships was driven primarily by variability in body mass. Our approach allows a more detailed interpretation of correlated trait evolution and variation in the underlying evolutionary pathways. Results demonstrate that a principal focus on interpreting relative brain size evolution as selection on neuronal capacity confounds the effects of body mass changes, thereby hiding important aspects that may contribute to explaining animal diversity.