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 influencesmore »
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Free, publicly-accessible full text available February 15, 2023
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Current methods used to quantify brain size and compartmental scaling relationships in studies of social insect brain evolution involve manual annotations of images from histological samples, confocal microscopy or other sources. This process is susceptible to human bias and error and requires time-consuming effort by expert annotators. Standardized brain atlases, constructed through 3D registration and automatic segmentation, surmount these issues while increasing throughput to robustly sample diverse morphological and behavioral phenotypes. Here we design and evaluate three strategies to construct statistical brain atlases, or templates, using ants as a model taxon. The first technique creates a template by registering multiple brains of the same species. Brain regions are manually annotated on the template, and the labels are transformed back to each individual brain to obtain an automatic annotation, or to any other brain aligned with the template. The second strategy also creates a template from multiple brain images but obtains labels as a consensus from multiple manual annotations of individual brains comprising the template. The third technique is based on a template comprising brains from multiple species and the consensus of their labels. We used volume similarity as a metric to evaluate the automatic segmentation produced by each method againstmore »Free, publicly-accessible full text available February 17, 2023
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Abstract 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 ratiosmore »
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Human brain size nearly quadrupled in the six million years since Homo last shared a common ancestor with chimpanzees, but human brains are thought to have decreased in volume since the end of the last Ice Age. The timing and reason for this decrease is enigmatic. Here we use change-point analysis to estimate the timing of changes in the rate of hominin brain evolution. We find that hominin brains experienced positive rate changes at 2.1 and 1.5 million years ago, coincident with the early evolution of Homo and technological innovations evident in the archeological record. But we also find that human brain size reduction was surprisingly recent, occurring in the last 3,000 years. Our dating does not support hypotheses concerning brain size reduction as a by-product of body size reduction, a result of a shift to an agricultural diet, or a consequence of self-domestication. We suggest our analysis supports the hypothesis that the recent decrease in brain size may instead result from the externalization of knowledge and advantages of group-level decision-making due in part to the advent of social systems of distributed cognition and the storage and sharing of information. Humans live in social groups in which multiple brains contributemore »