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Metabolism, a metric of the energy cost of behavior, plays a significant role in social evolution. Body size and metabolic scaling are coupled, and a socioecological pattern of increased body size is associated with dietary change and the formation of larger and more complex groups. These consequences of the adaptive radiation of animal societies beg questions concerning energy expenses, a substantial portion of which may involve the metabolic rates of brains that process social information. Brain size scales with body size, but little is understood about brain metabolic scaling. Social insects such as ants show wide variation in worker body size and morphology that correlates with brain size, structure, and worker task performance, which is dependent on sensory inputs and information-processing ability to generate behavior. Elevated production and maintenance costs in workers may impose energetic constraints on body size and brain size that are reflected in patterns of metabolic scaling. Models of brain evolution do not clearly predict patterns of brain metabolic scaling, nor do they specify its relationship to task performance and worker ergonomic efficiency, two key elements of social evolution in ants. Brain metabolic rate is rarely recorded and, therefore, the conditions under which brain metabolism influences the evolution of brain size are unclear. We propose that studies of morphological evolution, colony social organization, and worker ergonomic efficiency should be integrated with analyses of species-specific patterns of brain metabolic scaling to advance our understanding of brain evolution in ants.

Larger animals studied during ontogeny, across populations, or across species, usually have lower mass-specific metabolic rates than smaller animals (hypometric scaling). This pattern is usually observed regardless of physiological state (e.g., basal, resting, field, and maximally active). The scaling of metabolism is usually highly correlated with the scaling of many life-history traits, behaviors, physiological variables, and cellular/molecular properties, making determination of the causation of this pattern challenging. For across-species comparisons of resting and locomoting animals (but less so for across populations or during ontogeny), the mechanisms at the physiological and cellular level are becoming clear. Lower mass-specific metabolic rates of larger species at rest are due to (a) lower contents of expensive tissues (brains, liver, and kidneys), and (b) slower ion leak across membranes at least partially due to membrane composition, with lower ion pump ATPase activities. Lower mass-specific costs of larger species during locomotion are due to lower costs for lower-frequency muscle activity, with slower myosin and Ca++ ATPase activities, and likely more elastic energy storage. The evolutionary explanation(s) for hypometric scaling remain(s) highly controversial. One subset of evolutionary hypotheses relies on constraints on larger animals due to changes in geometry with size; for example, lower surface-to-volume ratios of exchange surfaces may constrain nutrient or heat exchange, or lower cross-sectional areas of muscles and tendons relative to body mass ratios would make larger animals more fragile without compensation. Another subset of hypotheses suggests that hypometric scaling arises from biotic interactions and correlated selection, with larger animals experiencing less selection for mass-specific growth or neurolocomotor performance. An additional third type of explanation comes from population genetics. Larger animals with their lower effective population sizes and subsequent less effective selection relative to drift may have more deleterious mutations, reducing maximal performance and metabolic rates. Resolving the evolutionary explanation for the hypometric scaling of metabolism and associated variables is a major challenge for organismal and evolutionary biology. To aid progress, we identify some variation in terminology use that has impeded cross-field conversations on scaling. We also suggest that promising directions for the field to move forward include (1) studies examining the linkages between ontogenetic, population-level, and cross-species allometries; (2) studies linking scaling to ecological or phylogenetic context; (3) studies that consider multiple, possibly interacting hypotheses; and (4) obtaining better field data for metabolic rates and the life history correlates of metabolic rate such as lifespan, growth rate, and reproduction.