Ratio of central nervous system to body metabolism in vertebrates: its constancy and functional basis

Mink, Jonathan W.; Blumenschine, Robert J.; Adams, David B.

doi:10.1152/ajpregu.1981.241.3.r203

Cited by 403 publications

(413 citation statements)

References 27 publications

(33 reference statements)

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“…The brain is one of the most energetically expensive organs in the vertebrate body; therefore, the large amount of energy required to maintain brain tissue should impose serious constraints on brain size evolution [37]. In fact, humans expend a much larger share of their resting energy budget on brain metabolism than other primates or nonprimate mammals.…”

Section: Energy Constraints For the Enlarging Brainmentioning

confidence: 99%

The evolutionary roles of nutrition selection and dietary quality in the human brain size and encephalization

Burini

Leonard

2018

Nutrire

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Background: Humans and other primates have evolved particular morphological and biological traits (e.g., larger brains, slower growth, longer-lived offspring) that distinguish them from most other mammals. The evolution of many distinctive human characteristics, such as our large brain sizes, reduced gut sizes, and high activity budgets, suggest major energetic and dietary shifts. Main body: Over the course of the last three million years, hominin brain sizes tripled. It is often taken for granted that the benefit of a larger brain is an increase in "intelligence" that makes us stand out among other mammals, including our nearest relatives, the primates. In the case of humans, brain expansion was associated with changes in diet, foraging, and energy metabolism. The first marked expansion occurred with the appearance of the genus Homo. Improved diet quality, allomaternal subsidies, cognitive buffering [by earlier weaning and longer juvenile periods], reduced costs for locomotion and by cooperative behavior, and reduced allocation to production, all operated simultaneously, thus enabling the extraordinary brain enlargement in our lineage. Conclusion: It appears that major expansion of brain size in the human lineage is the product of synergistically interacting dietary/nutritional and social forces. Although dietary change was not being the sole force responsible for the evolution of large brain size, the exploitation of high-quality foods likely fueled the energetic costs of larger brains and necessitated more complex behaviors that would have selected for greater brain size.

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Section: Energy Constraints For the Enlarging Brainmentioning

confidence: 99%

The evolutionary roles of nutrition selection and dietary quality in the human brain size and encephalization

Burini

Leonard

2018

Nutrire

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“…It has long been known that vertebrates exhibit extensive variation in brain size (Bauchot, Bauchot, Platel, & Ridet, 1977; Crile & Quiring, 1940; Jarvis et al., 2005; Mink, Blumenschine, & Adams, 1981; Striedter, 2005; Taylor & van Schaik, 2007). 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).…”

Section: Introductionmentioning

confidence: 99%

“…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). Research has indeed shown that increased allocation to brain tissue leads to declines in other components of fitness (Kaufman, Hladik, & Pasquet, 2003; Kotrschal et al., 2013a; Mink et al., 1981; Navarrete et al., 2011; Raichle & Gusnard, 2002; Tsuboi et al., 2015). The observed costs and benefits of brain size, as well as the connections between brain size and fitness, foreshadow that variation in ecological factors have the potential to exert selection and influence observed patterns of brain size variation (Gittleman, 1994).…”

Section: Introductionmentioning

confidence: 99%

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

Beston

Broyles

Walsh

2017

Ecology and Evolution

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Vertebrates exhibit extensive variation in brain size. The long‐standing assumption is that this variation is driven by ecologically mediated selection. Recent work has shown that an increase in predator‐induced mortality is associated with evolved increases and decreases in brain size. Thus, the manner in which predators induce shifts in brain size remains unclear. Increased predation early in life is a key driver of many adult traits, including life‐history and behavioral traits. Such results foreshadow a connection between age‐specific mortality and selection on adult brain size. Trinidadian killifish, Rivulus hartii, are found in sites with and without guppies, Poecilia reticulata. The densities of Rivulus drop dramatically in sites with guppies because guppies prey upon juvenile Rivulus. Previous work has shown that guppy predation is associated with the evolution of adult life‐history traits in Rivulus. In this study, we compared second‐generation laboratory‐born Rivulus from sites with and without guppies for differences in brain size and associated trade‐offs between brain size and other components of fitness. Despite the large amount of existing research on the importance of early‐life events on the evolution of adult traits, and the role of predation on both behavior and brain size, we did not find an association between the presence of guppies and evolutionary shifts in Rivulus brain size. Such results argue that increased rates of juvenile mortality may not alter selection on adult brain size.

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“…Large brains are metabolically costly. Thus, humans allocate approximately 20% of their total energy to the brain, compared with 11-13% for apes and 2-8% for other mammalian species (2). This increased metabolic demand has been associated with elevated expression of genes involved in neuronal functions and energy metabolism (3,4).…”

mentioning

confidence: 99%

Rapid metabolic evolution in human prefrontal cortex

Giavalisco

Liu

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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Human evolution is characterized by the rapid expansion of brain size and drastic increase in cognitive capabilities. It has long been suggested that these changes were accompanied by modifications of brain metabolism. Indeed, human-specific changes on gene expression or amino acid sequence were reported for a number of metabolic genes, but actual metabolite measurements in humans and apes have remained scarce. Here, we investigate concentrations of more than 100 metabolites in the prefrontal and cerebellar cortex in 49 humans, 11 chimpanzees, and 45 rhesus macaques of different ages using gas chromatography-mass spectrometry (GC-MS). We show that the brain metabolome undergoes substantial changes, both ontogenetically and evolutionarily: 88% of detected metabolites show significant concentration changes with age, whereas 77% of these metabolic changes differ significantly among species. Although overall metabolic divergence reflects phylogenetic relationships among species, we found a fourfold acceleration of metabolic changes in prefrontal cortex compared with cerebellum in the human lineage. These human-specific metabolic changes are paralleled by changes in expression patterns of the corresponding enzymes, and affect pathways involved in synaptic transmission, memory, and learning.H uman evolution is characterized by rapid expansion of brain size and increase in cognitive capabilities, leading to the emergence of unique and complex cognitive skills. These changes have long been associated with changes in brain metabolism, in particular with respect to increased energy demand (1). Large brains are metabolically costly. Thus, humans allocate approximately 20% of their total energy to the brain, compared with 11-13% for apes and 2-8% for other mammalian species (2). This increased metabolic demand has been associated with elevated expression of genes involved in neuronal functions and energy metabolism (3, 4). These changes may have been evolutionary advantageous, as indicated by signatures of positive selection reported for the amino acid changes, which occur in the mitochondrial electron-transport chain proteins, in anthropoid primates and humans, as well as elevated expression of the energy metabolism pathways in the human brain (5, 6). On the histological level, human brains show the largest density of glia cells relative to neurons in the prefrontal cortex, which provides an indirect indication of increased neuronal metabolic demand (7).Changes in brain metabolism are also implicated in neuropsychiatric disorders, such as schizophrenia, which affect some of the human-specific cognitive abilities (8, 9). Furthermore, direct measurements of 21 metabolites in the prefrontal cortex of adult human controls compared with human schizophrenia patients, chimpanzees, and rhesus macaques, carried out using proton NMR spectroscopy have shown significant overlap between human-specific evolutionary changes and metabolic differences between controls and schizophrenia patients (10). Notably, this study has identified not ...

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Ratio of central nervous system to body metabolism in vertebrates: its constancy and functional basis

Cited by 403 publications

References 27 publications

The evolutionary roles of nutrition selection and dietary quality in the human brain size and encephalization

The evolutionary roles of nutrition selection and dietary quality in the human brain size and encephalization

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

Rapid metabolic evolution in human prefrontal cortex

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