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Metabolic Correlates of Hominid Brain Evolution૾

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Metabolic Correlates of Hominid Brain Evolution૾ Comparative Biochemistry and Physiology Part A 136 (2003) 5–15 Review Metabolic correlates of hominid brain evolution૾ William R. Leonard*, Marcia L. Robertson, J. Josh Snodgrass, Christopher W. Kuzawa Laboratory for Human Biology Research, Department of Anthropology, Northwestern University, 1810 Hinman Avenue, Evanston, IL 60208, USA Received 25 July 2002; received in revised form 22 April 2003; accepted 23 April 2003 Abstract Large brain sizes in humans have important metabolic consequences as humans expend a relatively larger proportion of their resting energy budget on brain metabolism than other primates or non-primate mammals. The high costs of large human brains are supported, in part, by diets that are relatively rich in energy and other nutrients. Among living primates, the relative proportion of metabolic energy allocated to the brain is positively correlated with dietary quality. Humans fall at the positive end of this relationship, having both a very high quality diet and a large brain size. Greater encephalization also appears to have consequences for aspects of body composition. Comparative primate data indicate that humans are ‘under-muscled’, having relatively lower levels of skeletal muscle than other primate species of similar size. Conversely, levels of body fatness are relatively high in humans, particularly in infancy. These greater levels of body fatness and reduced levels of muscle mass allow human infants to accommodate the growth of their large brains in two important ways: (1) by having a ready supply of stored energy to ‘feed the brain’, when intake is limited and (2) by reducing the total energy costs of the rest of the body. Paleontological evidence indicates that the rapid brain evolution observed with the emergence of Homo erectus at approximately 1.8 million years ago was likely associated with important changes in diet and body composition. ᮊ 2003 Elsevier Science Inc. All rights reserved. Keywords: Encephalization; Resting metabolism; Diet quality; Body composition; Adiposity; Homo erectus 1. Introduction brains per body weight than other terrestrial mam- mals, the total (resting) energy demands for the From the perspective of comparative physiology human body are no more than for any other and nutrition, what is extraordinary about the large mammal of the same size (Leonard and Robertson, brains of humans is their high metabolic cost. 1992, 1994). The consequence of this paradox is Brain tissue has very high energy demands per that humans allocate a much larger share of their unit weight, roughly 16 times greater than those daily energy budget to ‘feed their brains’. Brain ( ) of muscle tissue Kety, 1957; Holliday, 1986 . Yet, metabolism accounts for ;20–25% of resting despite the fact that humans have much larger energy demands in an adult human body. This is far more than the 8–10% observed in other primate ૾ This paper is part of a collection of inter-disciplinary, peer-reviewed articles under the Theme: ‘‘Origin and Diversity species, and still more than the 3–5% allocated to of Human Physiological Adaptability’’ invited by K.H. the brain by other (non-primate) mammals (Leon- Myburgh and the late P.W. Hochachka. ard and Robertson, 1994). q q *Corresponding author. Tel.: 1-8474914839; fax: 1- The question that remains from all of this is 8474671778. E-mail address: [email protected] how humans have evolved to support the very (W.R. Leonard). high nutritional needs of our large brains. To 1095-6433/03/$ - see front matter ᮊ 2003 Elsevier Science Inc. All rights reserved. doi:10.1016/S1095-6433(03)00132-6 6 W.R. Leonard et al. / Comparative Biochemistry and Physiology Part A 136 (2003) 5–15 address this question, we will use comparative where sspercent of diet derived from structural analyses to examine two major domains through plant parts (e.g. leaves, stems, and bark), rs which hominids have adapted to the metabolic percent of diet derived from reproductive plant demands of greater encephalization: (1) improve- parts (e.g. fruits, flowers, nectar, and resin) and ments in dietary quality, and (2) changes in body aspercent of diet derived from animal parts composition. Dietary quality refers to the energetic (including both vertebrates and invertebrates). The andyor nutrient density of a diet. Increases in diet DQ ranges from a minimum of 100 (100% foliage) quality may result from changes in diet composi- to a maximum of 350 (100% animal material). tion (i.e. what you eat) or the ways in which foods are modified (processing, cooking, or genetic 2.2. Comparative body composition: skeletal mus- manipulation)(see Leonard and Robertson, 1994; cle mass, infant body fatness Wragham et al., 1999). In terms of body compo- sition, we will specifically consider how changes Table 2 presents information on skeletal muscle in the relative proportions of adipose and muscle mass and body weight compiled for 15 primates tissue may help accommodate the metabolic (including humans). The non-human primate data demands of larger brains. We will also consider were derived from Grand (1977) and Zihlman the developmental aspects of these patterns of (1984). The human data were obtained from Wang body composition. These analyses provide a con- et al. (2001). In addition, limited data on percent text for understanding the major selective forces body fatness at birth for 15 mammalian species that were likely necessary to support the evolution (including humans) were derived from Kuzawa of large hominid brains. (1998)(see Fig. 6). 2. Sample and methods 2.3. Fossil hominid data 2.1. Primate data: brain size, body size, metabolic Table 3 presents data on geological ages (mil- rate and diet lions of years ago), brain size (cm3), estimated ( ) ( ) male and female body weights kg , and posterior Table 1 presents data on body mass kg , resting ( 2) ( ) ( ) tooth surface areas mm for selected fossil hom- metabolic rate RMR; kcalyday , brain mass g inid species. All data presented in Table 3 were and dietary quality for 41 species of primates, derived from McHenry and Coffing (2000) other including humans. Data on metabolic rates and than the information on Homo erectus. For early associated body masses were derived from Leonard H. erectus brain size was calculated from data and Robertson (1994), McNab and Wright (1987), ( ) ( ) ( ) presented by McHenry 1994b for the African Thompson et al. 1994 and Kappeler 1996 . specimens, Anton´ and Swisher (2001) for Indo- Data on brain weights and body masses were ( ) ( ) nesian specimens, and Gabunia et al. 2000, 2001 obtained from Bauchot and Stefan 1969 , Stephan for Georgian (Dmanisi) remains. All data for late et al. (1981) and Jerison (1973). Information on H. erectus were taken from McHenry (1994a). dietary quality was obtained from data presented ( ) by Leonard and Robertson 1994 , Sailer et al. 3. Results (1985), Richard (1985) and Rowe (1996). The human data point is an average based on dietary 3.1. Variation in brain size, body size and diet data from 5 human foraging populations: the quality in modern primates !Kung, Ache, Hiwi, Ituri Pygmies and Inuit (from ) ( ) Leonard and Robertson, 1994 . Diet quality DQ Among primates, as in other mammals, RMR was assessed using an index developed by Sailer ( ) scales to body mass with an exponent of less than et al. 1985 that considers the relative energy and 1. As shown in Fig. 1, the relationship between nutrient density of dietary items. The DQ index is RMR and body mass among primate species is a weighted average of the proportions of foliage, similar to the Kleiber relationship for mammals in reproductive plant material, and animal material. general (Kleiber, 1961). DQ is calculated as: s 0.81 ( s ) DQssq2(r)q3.5(a) RMR 55Wt r 0.97 W.R. Leonard et al. / Comparative Biochemistry and Physiology Part A 136 (2003) 5–15 7 Table 1 Metabolic rate (RMR; kcalyday), body mass (kg), brain mass (g) and diet quality (DQ) for 41 primate species Species Metabolic data Brain data RMR (kcalyd) Body mass (kg) Brain mass (g) Body mass (kg) DQ Suborder strepsirhini Arctocebus calabarensis 15.2 0.206 7.2 0.323 327.5 Cheirogaleus medius 22.7 0.300 3.1 0.177 Eulemur fulvus 42.0 2.397 25.2 2.397 129 Euoticus elegantulus 25.1 0.260 7.2 0.274 230 Galago moholi 13.9 0.155 Galago senegalensis 18.1 0.215 4.8 0.186 278 Galagoides demidoff 6.3 0.058 3.4 0.081 305 Lemur catta 45.1 2.678 25.6 2.678 166 Lepilemur ruficaudatus 27.6 0.682 7.6 0.682 149 Loris tardigradus 14.8 0.284 6.6 0.322 327.5 Microcebus murinus 4.9 0.054 1.8 0.054 Nycticebus coucang 32.4 1.380 12.5 0.800 Otolemur crassicaudatus 47.6 0.950 10.3 0.850 195 Otolemur garnettii 47.8 1.028 275 Perodicticus potto 41.3 1.000 14 1.150 190 Propithecus verreauxi 86.8 3.080 26.7 3.480 200 Varecia variegata 69.9 3.512 34.2 3.512 Suborder haplorhini Alouatta palliata 231.9 4.670 51 6.400 136 Aotus trivirgatus 52.4 1.020 16 0.850 177.5 Callithrix geoffroyi 27.0 0.225 7.6 0.280 235 Callithrix jacchus 22.8 0.356 7.6 0.280 235 Cebuella pygmaea 10.1 0.105 4.5 0.140 249.5 Cercopithecus mitis 407.7 8.500 76 6.500 201.5 Cercocebus torquatus 196.2 4.000 104 7.900 234 Colobus guereza 357.9 10.450 73 7.000 126 Erythrocebus patas 186.9 3.000 118 8.000 Homo sapiens 1400.0 53.500 1295 53.500 263 Hylobates lar 123.4 1.900 102 6.000 181 Leontopithecus rosalia 51.1 0.718 Macaca fascicularis 400.9 7.100 74 5.500 200 Macaca fuscata 485.4 9.580 84 5.900 223 Macaca mulatta 231.9 5.380 110 8.000 159 Pan troglodytes 581.9 18.300 420 46.000 178 Papio anubis 342.9 9.500 205 26.000 207 Papio cynacephalus 668.9 14.300 195 19.000 184 Papio papio 297.3 6.230 190 18.000 Papio ursinus 589.3 16.620 190 18.000 189.5 Pongo pygmaeus 569.1 16.200 370 55.000 172.5 Saguinus geoffroyi 50.5 0.500 10 3.800 263 Saimiri sciureus 68.8 0.850 22 6.800 323 Tarsius syrichta 8.9 0.113 350 Sources: Bauchot and Stefan (1969), Stephan et al.
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