Comparative expression analysis of the phosphocreatine circuit in extant primates: Implications for human brain evolution

Pfefferle, Adam D.; Warner, Lisa; Wang, Catrina W.; Nielsen, William; Babbitt, Courtney C.; Fédrigo, Olivier; Wray, Gregory A.

doi:10.1016/j.jhevol.2010.10.004

Cited by 26 publications

(19 citation statements)

References 62 publications

(116 reference statements)

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“…This pattem is consistent with the previous findings in mammals (Jones & MacLamon, 2004;Navarrete et al, 2011) and fish (Warren & Iglesias, 2012). However, most studies testing the expensive-tissue hypothesis have shown that an increase of brain mass has been accompanied by a reduction in gut length across taxa (primates: Aiello & Wheeler, 1995;Aiello, Bates & Joffe, 2001;Pfefferle et al, 2011;fish: Kaufman et al, 2003;cattle: Mau, Südekum & Kaiser, 2009;guppies: Kotrschal et al, 2013). Diet quality as a proxy for gut dimensions may affect brain size evolution (MacLamon, Chivers & Martin, 1986;Isler & Van Schaik, 2006b).…”

Section: Discussionsupporting

confidence: 90%

Evidence for neither the compensation hypothesis nor the expensive-tissue hypothesis in Carassius auratus

2014

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In many taxa, the left and right testes often differ in size. The compensation hypothesis states that an increase in size of one tesüs can compensate for a reduced function in the other testis. Moreover, the expensive-tissue hypothesis predicts that an increase in investment of a metabolically costly tissue is offset by decreasing investment in the other metaboUcally costly tissues. Here we tested these two hypotheses in Carassius auratus, by analysing difference between left and right testes mass, and between brain mass and both gut length and gonad mass (testes mass in males and clutch mass in females). We found no difference between left and right testis mass and no correlations between relative testis size and body measurements. These findings suggest that the left testis cannot serve a compensatory role. Nonetheless, contrary to the predictions of the expensive-tissue hypothesis, brain mass was positively correlated with both gut length and gonad mass within each sex. This positive correlation between brain mass and other organs (gut, gonad and clutch tissues) suggests that organisms may compensate for substantial variation in investment in tissues without sacrificing other expensive tissues.

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Section: Discussionsupporting

confidence: 90%

Evidence for neither the compensation hypothesis nor the expensive-tissue hypothesis in Carassius auratus

2014

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“…We do not discard the influence of other modifications in human or nonhuman primate evolution, such as changes in the distribution of glucose between brain and skeletal muscle (47,48) or an overall decrease in basal metabolic rate (49), which might themselves be adaptations to limited energetic availability. Our findings are also compatible with the general essence of the "maternal energy hypothesis," according to which the maternal supply of energy to the fetus may be limiting to brain expansion (23), although the specific link proposed by that hypothesis is between the mother's basal metabolic rate (rather than simply energy availability, as proposed here) and the brain size of her offspring.…”

Section: Discussionmentioning

confidence: 99%

Metabolic constraint imposes tradeoff between body size and number of brain neurons in human evolution

Fonseca-Azevedo

Herculano‐Houzel

2012

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

161

120

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Despite a general trend for larger mammals to have larger brains, humans are the primates with the largest brain and number of neurons, but not the largest body mass. Why are great apes, the largest primates, not also those endowed with the largest brains? Recently, we showed that the energetic cost of the brain is a linear function of its numbers of neurons. Here we show that metabolic limitations that result from the number of hours available for feeding and the low caloric yield of raw foods impose a tradeoff between body size and number of brain neurons, which explains the small brain size of great apes compared with their large body size. This limitation was probably overcome in Homo erectus with the shift to a cooked diet. Absent the requirement to spend most available hours of the day feeding, the combination of newly freed time and a large number of brain neurons affordable on a cooked diet may thus have been a major positive driving force to the rapid increased in brain size in human evolution.encephalization | expensive tissue hypothesis | brain metabolism T he human brain is a linearly scaled-up primate brain in its relationship between brain size and number of neurons (1), having evolved while being subjected to the same cellular scaling rules that apply to primates as a whole (2, 3), including great apes (4). With the largest brain among primates, humans thus have the largest number of neurons among these and possibly all mammals (5), a number that we estimate to be close to three times larger than in gorillas and orangutans, owners of the next largest brains among extant primates (4). We are not outstanding primates, on the contrary, in body size: gorillas can grow to be three times larger than humans. This discrepancy between body and brain size led to the predominant view that encephalization (that is, a larger brain size than expected for body size) is the main characteristic that sets humans apart from other primates and mammals as a whole (6). Although a relatively large brain compared with body size is expected to bring cognitive advantages (6), and despite the well-documented evidence for an increase in brain size during human evolution (7), there is still no consensus on what mechanisms or reasons led to brain enlargement in the Homo lineage.Why are the largest primates not those endowed with the largest brains as well? Rather than evidence that humans are an exception among primates, we consider this disparity to be a clue that, in primate evolution, developing a very large body and a very large brain have been mutually excluding strategies, probably because of metabolic reasons (4, 8). The brain is the third most energy-expensive organ in the human body, ranking in total organ metabolic cost below only skeletal muscle and liver (9). Accordingly, several studies have suggested that the main constraints to increasing primate brain size in evolution are metabolic in nature (10-18). The human brain, in particular, has come to cost ∼20% of the total body resting metabolic rate, even though it ...

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“…Homo erectus, for instance, was clearly more predatory and a larger consumer of animal products than earlier species (Shipman & Walker, 1989). Therefore, a prominent role of meat in the bioenergetic transformations needed to support the development of the human brain has been suggested, acting via increases in the dopaminergic activity (Previc, 2009) and nicotinamide adenine dinucleotide levels (Williams & Dunbar, 2013), and via the fuelling of the cerebral phosphocreatine circuits (Pfefferle et al, 2011).…”

Section: Meat For Brainsmentioning

confidence: 99%

Meat traditions. The co-evolution of humans and meat

2015

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Comparative expression analysis of the phosphocreatine circuit in extant primates: Implications for human brain evolution

Cited by 26 publications

References 62 publications

Evidence for neither the compensation hypothesis nor the expensive-tissue hypothesis in Carassius auratus

Evidence for neither the compensation hypothesis nor the expensive-tissue hypothesis in Carassius auratus

Metabolic constraint imposes tradeoff between body size and number of brain neurons in human evolution

Meat traditions. The co-evolution of humans and meat

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