Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology
ReviewMetabolic correlates of hominid brain evolution☆
Introduction
From the perspective of comparative physiology and nutrition, what is extraordinary about the large brains of humans is their high metabolic cost. Brain tissue has very high energy demands per unit weight, roughly 16 times greater than those of muscle tissue (Kety, 1957, Holliday, 1986). Yet, despite the fact that humans have much larger brains per body weight than other terrestrial mammals, the total (resting) energy demands for the human body are no more than for any other mammal of the same size (Leonard and Robertson, 1992, Leonard and Robertson, 1994). The consequence of this paradox is that humans allocate a much larger share of their daily energy budget to ‘feed their brains’. Brain metabolism accounts for ∼20–25% of resting energy demands in an adult human body. This is far more than the 8–10% observed in other primate species, and still more than the 3–5% allocated to the brain by other (non-primate) mammals (Leonard and Robertson, 1994).
The question that remains from all of this is how humans have evolved to support the very high nutritional needs of our large brains. To address this question, we will use comparative analyses to examine two major domains through which hominids have adapted to the metabolic demands of greater encephalization: (1) improvements in dietary quality, and (2) changes in body composition. Dietary quality refers to the energetic and/or nutrient density of a diet. Increases in diet quality may result from changes in diet composition (i.e. what you eat) or the ways in which foods are modified (processing, cooking, or genetic manipulation) (see Leonard and Robertson, 1994, Wragham et al., 1999). In terms of body composition, we will specifically consider how changes in the relative proportions of adipose and muscle tissue may help accommodate the metabolic demands of larger brains. We will also consider the developmental aspects of these patterns of body composition. These analyses provide a context for understanding the major selective forces that were likely necessary to support the evolution of large hominid brains.
Section snippets
Primate data: brain size, body size, metabolic rate and diet
Table 1 presents data on body mass (kg), resting metabolic rate (RMR; kcal/day), brain mass (g) and dietary quality for 41 species of primates, including humans. Data on metabolic rates and associated body masses were derived from Leonard and Robertson, 1994, McNab and Wright, 1987, Thompson et al., 1994, Kappeler, 1996. Data on brain weights and body masses were obtained from Bauchot and Stefan, 1969, Stephan et al., 1981, Jerison, 1973. Information on dietary quality was obtained from data
Variation in brain size, body size and diet quality in modern primates
Among primates, as in other mammals, RMR scales to body mass with an exponent of less than 1. As shown in Fig. 1, the relationship between RMR and body mass among primate species is similar to the Kleiber relationship for mammals in general (Kleiber, 1961).
The consequence of this scaling relationship is that small primates have low total energy needs but very high energy demands per unit mass. Conversely, large primates have high total energy needs, but low mass-specific
Discussion
The high energy demands of human brain size appeared to have necessitated both improvements in dietary quality and changes in body composition over the course of hominid evolution. Indeed many of the important changes and evolutionary innovations in human evolutionary history have been about improvements in dietary quality. Such changes were critical to the evolution of our large brains and to the broad expansion of humans throughout the world (Leonard, 2002). With H. erectus, we see
Acknowledgements
We are grateful to Drs. Peter Hochachka and Kathy Myburgh for the opportunity to contribute to this special issue. The comments and suggestions from Dr Susan Antón and two anonymous reviewers helped to substantially improve this paper. This research was supported, in part, by grants to WRL by the Natural Sciences and Engineering Council (NSERC) of Canada (OGP-0116785) and the Wenner-Gren Foundation for Anthropological Research (#295).
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2019, Journal of Theoretical BiologyCitation Excerpt :Our study is based on the hominin phylogenetic tree summarizing the best trees obtained in the dated Bayesian analysis of Dembo et al. (2015, Fig. 1), which is displayed in Fig. 2. We combined data from several articles in order to get the body mass and the cranial capacity of as many species as possible, namely from Kappelman (1996, Table 1), Wood and Collard (1999, Table 3), Leonard et al. (2003, Table 3), Young (2006, Table 1), Schoenemann (2013, Tables 8.1 and 8.2), Grabowski et al. (2015, Table 4), Will et al. (2017, Table 4) and Du et al. (2018, Elec. Supp.). We excluded data associated to ambiguously identified species and to juvenile specimens.
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This paper is part of a collection of inter-disciplinary, peer-reviewed articles under the Theme: “Origin and Diversity of Human Physiological Adaptability” invited by K.H. Myburgh and the late P.W. Hochachka.