The mass of the human brain: is it a spandrel?

10 The mass of the human brain: is it a spandrel? P aul R . Ma ng e r , J as on Hemi ngway, Muha mma d A . S p oc t er and An d r e w G a l l ag h e r Abstract The current chapter examines allometric exponents as they apply to the evolution of the size, or mass, of the modern human brain relative to the mass of the body. The mass of the brain is considered as a single level of organisation of the nervous system and is treated separately to other levels of organisation. A comprehensive dataset is used to examine the relationship between brain and body mass in primates and hominids. This analysis allows us to postulate that the evolution of the size of the human brain can, for the most part, be accounted for by scaling with body size. There appears to be a minimum of two potential adaptive events that have led to alterations in the scaling laws that help explain the actual mass of the human brain. These two events occur at the origin of primates and the origin of the hominid lineage. These scaling laws appear to obviate much of the need for adaptationist explanations in terms of the evolution of the mass of the human brain. Introduction A trend in one specially favoured character…may result in trends in various correlated characters. In other words, a particular trend may be nothing but the byproduct of a trend in a different character, such as body size. (Ernst Mayr, 2002: 240, our italics) The human brain, at an average mass of approximately 1355 g (e.g. Ruff et al., 1997; Wood and Collard, 1999), is potentially the most complex biological structure to have evolved. This brain is composed of 100 billion African Genesis: Perspectives on Hominin Evolution, eds. Sally C. Reynolds and Andrew Gallagher. Published by Cambridge University Press. © Cambridge University Press 2012. 181 9781107019959c10_p181-204.indd 181 11/14/2011 7:44:10 PM 182 Paul R. Manger et al. neurons, each neuron being connected to between 1000 and 10 000 other neurons, up to 5000 billion glial cells and approximately 20 billion neurons in the human cerebral cortex, with a total of 60 trillion synapses (Blinkov and Glezer, 1968). Yet this structure, as with everything to do with the anatomy, biochemistry, physiology and behaviour of Homo sapiens, has evolved over time. This process may be the result of a number of factors, including: (a) natural selection responding to potential adaptations; (b) phylogenetic contingencies and constraints; and (c) structural laws of form (Gould, 2002). Of all the features of modern humans it is the brain and the cognitive power of this organ that distinguishes Homo sapiens most clearly from the rest of the Kingdom Animalia. Few studies to date have examined in suficient detail the internal architecture and structure of the human brain to allow extensive theorising or analysis of changes at the various levels of organisation within the brain in an evolutionary setting (i.e. not enough data is available to analyse suficiently all potential evolutionary explanations relating to the genesis of the form of the various levels of organisation of the human brain). In contrast, signiicant effort has been directed towards establishing the changes in the mass of the brain during the evolution of the Family Hominidae (e.g. Ruff et al., 1997; Henneberg, 1998; Wood and Collard, 1999; amongst many others), as cranial capacity is one parameter that can be determined with a reasonable degree of accuracy from the fossil record (although the exact data is often debated). The brain of Homo sapiens is not the largest brain in existence, this is found in some of the larger cetaceans (Manger, 2006), but the human brain is the largest brain relative to body mass of all animals (e.g. Jerison, 1973). This large relative brain mass has been proposed to be, most prominently by Jerison but also by many others, the major factor in the biological determination of human intelligence. While mass is a readily quantiiable character, has too much emphasis been placed on mass and relative mass in the determination of the capabilities of any individual brain? A recent analysis of the evolution of the cetacean brain suggests that mass and/or relative mass alone may not be the most reliable indicator of intelligence (Manger, 2006). Rather, all levels of organisation of the brain must be examined and explained in order to understand the complexity of information processing of any given brain – the brain is undoubtedly hierarchically organised (Manger, 2005). Despite this, mass is a speciic feature of organisation of the brain and mass does play a major role in overall functioning, as many other features of the brain at various levels of organisation are related to overall mass (e.g. Finlay and Darlington, 1995). Thus how the mass of the human brain evolved is an important focal point of study. The potential effect of mass on other features of brain organisation at various levels is encapsulated by Gould: 9781107019959c10_p181-204.indd 182 11/14/2011 7:44:10 PM The mass of the human brain: is it a spandrel? 183 The spandrels of the human brain must greatly outnumber the immediately adaptive reasons for increase in size… (Gould, 2002: 87, our italics) The present contribution examines the evolution of the mass of the human brain as a single level of neural organisation, and as indicated in the title, puts forward the possibility that the mass of the brain is a spandrel, thus extending even Gould’s (2002) evolutionary explanations of human brain mass evolution. While allometric relationships are well known for brain and body mass amongst mammals, these have not been the central focus of explanation of total brain mass in hominid evolution, with adaptationist explanations, and more recently gene mutational studies, dominating this debate. In contrast, we explore the allometric relationships in the present analysis. We irst examine the allometric data available for brain and body mass in mammalian, primate and hominid evolution. We then discuss the potential ‘chicken and egg’ conundrum that may result from a strong allometric relationship between brain and body mass (speciically stated, did a larger brain mass evolve as a correlation to a selection for larger body mass, or did selection for a larger brain mass lead to an increase in body mass?). We hypothesise that body mass was most likely selected for in hominid evolution, leaving us with the conclusion that the mass of the human brain “may be nothing but the by-product of a trend in a different character” (Mayr, 2002). Structural laws of form and human brain mass Generalized mammalian brain and body mass scaling When examining mammals in a general framework, a distinct, highly predictable and strongly statistically signiicant scaling of body mass to brain mass is found. This relationship has been known since the early 1800s (Dubois, 1897), but was brought to the fore by the publication of Jerison’s 1973 monograph. The relationship between mammalian body mass (Mb) and brain mass (Mbr) is seen as a negative allometric scaling that can be described by the equation (from Manger, 2006): Mbr = 0.069Mb0.718 (r2 = 0.950; P = 2.4 × 10–178) The above equation is derived from a regression plot for all mammals (those with known brain and body masses), but excludes the primates, hominids, cetaceans and pinnipeds due to the fact that these groups exhibit a form of scaling between brain and body mass that differs to the remainder of mammals 9781107019959c10_p181-204.indd 183 11/14/2011 7:44:10 PM 184 Paul R. Manger et al. (Manger, 2006). Using this function we can see that for every doubling in body mass of a mammal, the mass of the brain will increase 1.65 times (20.718). Thus, as mammals get larger the brain will get larger, but the percentage of the entire body mass that is brain mass will decrease, both occurring in a highly predictable fashion (95% of the variability in brain mass can be accounted for by variability in body mass). What, in terms of evolution in brain mass, can be concluded from this statistical analysis? We can conclude that increases in body mass and brain mass in mammals are so strongly interconnected that they should not be treated separately a priori. This scaling law of form can be considered a class-level allometric phylogenetic constraint upon brain mass evolution in mammals. If one were to imagine a colossal mammal, say ive times the body mass of the modern African elephant (Loxodonta africana), one could predict with a relatively high degree of certainty, the mass of the brain this mega-mammal would have. We can also conclude that if a group of mammals exhibits a brain–body mass allometric scaling that differs from, or falls outside of the range of, this generalised scaling law of form for mammals that something different has occurred in the evolution of this group of mammals (see analysis of primates and hominids below). It is this basic allometric phylogenetic constraint that serves as the strongest predictor of the evolution of brain mass amongst the mammals, and it is against this basis that any speciic differences in groups of mammals, or individual species, must be compared (see for example the analysis of cetaceans by Manger, 2006). Primate brain and body mass scaling Primates, as an order, have larger brains than would be expected for their body mass when compared to the generalised mammalian pattern of scaling (e.g. Martin, 1981, 1983; Manger, 2006). Interestingly, the components of the brain, in terms of subdivisions such as neocortex, diencephalon, cerebellum etc., are very close to what one would predict for a mammal with a brain of the mass found in primates (e.g. Finlay and Darlington, 1995). This means that the larger brain mass in primates is not due to selective expansion of one particular structure, for example the neocortex (as often asserted in the literature as neocorticalisation), but is due to an overall allometric increase in the mass of all components of the brain, summing to an increase in total brain mass relative to body mass. We undertook an analysis of non-hominin simian primates (Figure 10.1) and found that the relationship between brain and body mass was highly signiicant and can be described by the equation: 9781107019959c10_p181-204.indd 184 11/14/2011 7:44:10 PM The mass of the human brain: is it a spandrel? 185 (a) Brain mass (g)/cranial capacity (cc) 10 000 Non-hominin simian primates Fossil hominins Modern Homo sapiens 1 000 100 Fossil hominins 1.4232 Cc = 0.0002Mb (r2 = 0.846, P = 1.29 × 10–5) 10 Non-hominin simian primates Mbr = 0.2153Mb0.6858 (r2 = 0.938, P = 2.25 × 10–71) 1 10 100 1000 10 000 1 000 000 100 000 Body mass (g) (b) 9 Non-hominin simian primates Non-hominin hominoids Fossil hominins Modern Homo sapiens logn brain mass/cranial capacity 8 7 6 5 4 3 2 1 5 6 7 8 9 10 11 12 logn body mass Figure 10.1. A: plot of the raw data used in the current analysis depicting body mass plotted against brain mass or cranial capacity. B: more restricted plot of the raw data with 95th percentile ellipses drawn around the different groups. Mbr = 0.2153Mb0.6858 (r2 = 0.938; P = 2.25 ×10–71) This equation suggests several points of interest. First, for every doubling in the body mass of the non-hominin simian primates the brain increases in mass by 1.61 times (20.6858, a negative allometry) which closely parallels that of the 9781107019959c10_p181-204.indd 185 11/14/2011 7:44:11 PM 186 Paul R. Manger et al. general mammalian trend (see above); thus, the manner in which brains and bodies scale in the mammals and the non-hominin simian primates is similar. This indicates that whatever processes are controlling the relationship of brain mass to body mass are likely to be similar in the non-hominin simian primates and mammals in general. Second, the high correlation coeficient tells us that 93.8% of the variability in brain mass in the non-hominin simian primates can be accounted for by variations in body mass. Thus, this relationship is highly predictable for this primate subgroup, as seen in mammals in general. Lastly, the y intercept, at 0.2153 is larger than that seen for mammals in general (0.069), indicating that the brain mass of this group is generally larger in relation to body mass than that found for mammals in general. All primates (including prosimians) exhibit brains that are larger than would be expected for mammals of their body mass, with encephalisation quotients (EQ) ranging from around 1.25 through to that for humans, which falls between 7 and 8 – the average EQ for mammals is 1 (Manger, 2006). We subdivided this group, into non-hominoid simian primates and non-hominin hominoids, and determined the 95% conidence intervals for these two groups (Figure 10.1). Only two species of the latter group (Gorilla gorilla and Pongo pygmaeus) could be distinguished from the non-hominoid simian primates as the data for these two species fell outside of the 95% conidence intervals. These two species exhibited larger body masses than would be expected for a non-hominoid simian primate and this may be the result of secondary somatic growth, or evolutionary adaptation for increased somatic mass in these two species. Despite this data the remaining eight species of non-hominin hominoids fell within the 95% conidence intervals of the non-hominoid simian primates. From this we can conclude that it is highly likely that no speciic change in the allometric relationship between these two groups has occurred and can thus be treated together. This is an important distinction to make, as it indicates that there are no features of the brain–body mass relationship evident in the closest extant relatives of modern humans that indicate variation from the pattern seen across a large cohort of the order primates in the direction of the hominin lineage. Thus, we may conclude that it is likely that no features of the mass of the brain relative to the body in non-hominin primates is indicative of the well documented changes seen in the hominin lineage. Fossil hominin brain and body mass scaling We analysed the manner in which brains and bodies scaled in the fossil hominin species (extinct genera Australopithecus and Homo, including fossil H. sapiens) using as many records as we could ind in the literature (see Tables 10.1 9781107019959c10_p181-204.indd 186 11/14/2011 7:44:11 PM The mass of the human brain: is it a spandrel? 187 and 10.2). We have treated these species as one group, as they all exhibit habitual bipedalism as a locomotory feature that distinguishes them from the remaining primates. Alternative scenarios may indeed subdivide this group in relation to the differing locomotory repertoires, but for the purposes of the present analysis we do not deal with these other possibilities. As absolute brain mass cannot be measured in these species, we used the published estimates of cranial capacity as a substitute for brain mass. While this is a good indicator of changes in the mass of the brain over time, there is one major disadvantage, this being that the brain occupies only between 80 to 85% of the endocranial cavity in modern humans (Tobias, 1994). Thus, the proxies of brain mass that we have used in the analysis of these species may overestimate fossil brain masses, but at present are the best indicators of total brain mass in the fossil hominin species. A second drawback is that estimates of body mass are also used, with all the inherent dificulties involved (Spocter and Manger, 2007). However, with these potential problems and grouping limitations in mind, the analysis indicates an interesting trend in the relationship between the endocranial capacity and the estimates of body mass (Figure 10.1). We found that the relationship between endocranial capacity (Cc) and body mass (Mb) estimates was highly signiicant and can be described by the equation: Cc = 0.0002Mb1.4232 (r2 = 0.846; P = 1.29 × 10–5) Several points of interest emerge from this analysis. The irst point is that the relationship is highly signiicant, and the derived equation indicates that 84.6% of the variability in endocranial capacity can be accounted for by variation in body mass estimates in the fossil hominins. Second, the slope of the derived equation indicates that this relationship forms a positive allometry; thus for every doubling in body mass estimate in the fossil hominins, the endocranial capacity increases by 2.68 times (21.4232). This positive allometry is signiicantly different from that found for the non-hominin simian primates (P = 0.0058, using the mean squares within and between slopes), indicating that the manner in which the brain and body scales in the two groups is very different. If we examine the 95% conidence intervals generated for the various groups used in the current analysis (Figure 10.1), we see that all of the fossil hominins lie outside of the range of the non-hominoid simian primates. Second, we see that only two of the smallest fossil hominins lie with the 95% conidence intervals of the non-hominin hominoids (Australopithecus afarensis and A. africanus). Thus, on statistical grounds, the brain and body mass of the fossil hominins is completely different to that of the non-hominoid simian primates. While the two smallest fossil hominins lie within the 95% conidence intervals of the non-hominin hominoids, they are on the very outer limits of this interval, and the remaining fossil hominins are clearly segregated. Thus, for the 9781107019959c10_p181-204.indd 187 11/14/2011 7:44:11 PM 188 Paul R. Manger et al. Table 10.1. Published body mass estimates for Miocene, Pliocene and Pleistocene hominins. (Data taken from: Aiello and Dean, 1990; McHenry, 1992; Ruff et al., 1997; Abbate et al., 1998; Asfaw et al., 1999, 2002; Senut et al., 2001; Zollikofer et al., 2005; Rightmire et al., 2006) Specimen Element Sex Taxon Age (million years) Mass BAR 1002’00 ? Orrorin tugenensis 6.000 35.96 M 55.00 3.800 47.50 3.600 50.10 3.600 41.40 A.L. 333–7 Distal tibia M 3.600 42.60 A.L. 33w-56 Distal femur M 3.600 40.30 A.L. 333x-26 Proximal tibia M 3.600 48.20 A.L. 333–42 Proximal tibia M 3.600 45.00 A.L. 333–6 Distal tibia F 3.600 33.50 A.L. 288–1 Proximal femur Distal femur F 3.200 28.00 3.200 28.20 F 3.200 27.20 2.300 30.00 Sts 392 Proximal tibia Proximal femur Femoral head 2.300 32.70 StW 25 Femoral head F 2.300 34.40 StW 102 Talus F 2.300 30.60 StW 347 Talus F 2.300 27.60 StW 358 Distal tibia F 2.300 23.40 TM 1513 Distal femur F 2.300 32.60 Sts 34 Distal femur M 2.300 38.50 StW 311 Femoral head M Australopithecus anamensis Australopithecus afarensis Australopithecus afarensis Australopithecus afarensis Australopithecus afarensis Australopithecus afarensis Australopithecus afarensis Australopithecus afarensis Australopithecus afarensis Australopithecus afarensis Australopithecus afarensis Australopithecus afarensis Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus 4.300 A.L. 333–4 Proximal femur Proximal ibia Proximal femur Proximal femur Distal femur 2.300 40.70 KNM-KP 29285 MAK-VP-1/1 A.L. 333–3 A.L. 129–1a A.L. 129–1b Sts 14 9781107019959c10_p181-204.indd 188 M M M F F F 11/14/2011 7:44:11 PM The mass of the human brain: is it a spandrel? 189 Table 10.1. (cont.) Age (million years) Mass Specimen Element Sex Taxon StW 389 Distal tibia M 2.300 38.00 StW 99 Proximal Femur Femoral head M 2.300 45.40 2.300 49.25 F M 1.800 1.800 33.80 37.40 M Paranthropus robustus 1.800 42.90 KNM-ER 1500 KNM-ER 1464 KNM-ER 3735 Talus Proximal femur Proximal femur Partial skeleton Talus Partial skeleton Australopithecus africanus Australopithecus africanus Australopithecus africanus Paranthropus robustus Paranthropus robustus F M M 1.800 1.800 1.800 34.00 48.60 37.00 OH 8 Talus F 1.800 31.00 OH 35 Distal tibia F 1.800 31.90 M M ? Paranthropus boisei Paranthropus boisei Homo habilis sensu stricto Homo habilis sensu stricto Homo habilis sensu stricto Homo sp. indet Homo sp. indet Homo sp. indet 1.950 1.800 1.800 62.00 57.20 51.80 ? ? Homo sp. indet Homo erectus 1.800 1.800 49.70 52.80 M Homo erectus 1.800 59.00 M Homo erectus 1.800 59.00 F Homo erectus 1.800 49.90 F F Homo erectus Homo erectus 1.800 1.800 54.00 51.00 M ? ? Homo erectus Homo erectus Homo erectus 0.400 0.440 0.500 79.20 58.30 53.40 ? ? F ? ? ? M Homo erectus Homo erectus Homo erectus Homo heidelbergensis Homo heidelbergensis Homo heidelbergensis Homo heidelbergensis 0.500 0.600 0.120 0.300 0.300 0.300 0.300 62.10 54.50 54.10 73.80 48.90 62.40 73.60 StW 431 TM 1517 SK 82 SK 97 KNM-ER 3228 KNM-ER 1481 KNM-ER 813 Femoral head Femoral head Femoral diaphysis KNM-ER 1472 Femoral head KNM-ER 737 Femoral diaphysis KNM-ER 736 Femoral diaphysis KNM-ER 1808 Femoral diaphysis KNM-ER 803 Femoral diaphysis OH 28 Acetabulum OH 34 Tibial diaphysis Arago 44 Femoral head Zhoukoudian FeIV Femoral head Gesher-BenotFemoral head Ya’acov KNM-BK 66 Femoral head Ain Maarouf1 Femoral head Ngandong B Femoral head Broken Hill 689 Femoral head Broken Hill 690 Femoral head Broken Hill 691 Femoral head Broken Hill 719 Femoral head 9781107019959c10_p181-204.indd 189 M 11/14/2011 7:44:12 PM 190 Paul R. Manger et al. Table 10.1. (cont.) Specimen Element Sex Taxon Age (million years) Mass Broken Hill 907 Boxgrove 1 Amud 1 La Chapelleaux-Saints La Ferrassie 1 La Ferrassie 2 Fond-de-Foret 1 Kebara 2 Kiik-Koba 1 Lezetxiki 1 Neandertal 1 La Quina 5 Regourdou 1 Saint-Cesaire 1 Spy 1 Spy 2 Shanidar 1 Shanidar 3 Shanidar 5 Krapina 207 Krapina 208 Krapina 209 Krapina 213 Krapina 214 Grotte du Prince Shanidar 2 Shanidar 4 Shanidar 6 Tabun C1 Qafzeh 3 Qafzeh 7 Qafzeh 8 Qafzeh 9 Skhul 4 Skhul 5 Skhul 6 Skhul 7 Skhul 7a Skhul 9 Baousse de Torre 2 Caviglione 1 Cro-Magnon 1 Cro-Magnon 4293 Cro-Magnon 4297 Cro-Magnon 4315 Cro-Magnon 4317 Femoral head Femoral head Femoral head Femoral head ? M M M Homo heidelbergensis Homo heidelbergensis Homo neanderthalensis Homo neanderthalensis 0.300 0.500 0.045 0.052 80.60 86.70 70.30 77.30 Femoral head Femoral head Femoral head Femoral head Femoral head Proximal tibia Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral Head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head M F M M M ? M ? ? M F M M M M M F F M F F M M F F F M M F M M M M F M M M M ? ? M ? Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens 0.072 0.072 0.050 0.060 0.050 0.075 0.050 0.050 0.075 0.036 0.050 0.050 0.050 0.050 0.050 0.130 0.130 0.130 0.130 0.130 0.100 0.100 0.100 0.100 0.150 0.090 0.090 0.090 0.090 0.090 0.090 0.090 0.090 0.090 0.090 0.025 0.025 0.030 0.030 0.030 0.030 0.030 85.00 67.00 83.90 75.60 78.10 73.90 78.90 71.20 72.10 78.90 67.50 83.60 80.50 79.90 68.50 57.10 68.40 63.70 80.60 62.60 74.80 75.20 72.00 59.40 63.20 57.30 67.60 77.40 63.20 70.30 67.60 71.30 65.30 54.70 71.30 75.40 65.20 67.60 67.00 73.10 70.80 59.60 9781107019959c10_p181-204.indd 190 11/14/2011 7:44:12 PM The mass of the human brain: is it a spandrel? 191 Table 10.1. (cont.) Specimen Element Sex Taxon Age (million years) Mass Cro-Magnon 4321 Cro-Magnon 4322 Cro-Magnon 4330 Dolni Vestonice 3 Dolni Vestonice 13 Dolni Vestonice 14 Dolni Vestonice 16 Grotte des Enfants 4 Grotte des Enfants 5 Mladec 24 Mladec 22 Mladec 21 Paglicci 25 Pataud 4 Pataud 5 Paviland Pavlov 1 Predmosti 1 Predmosti 3 Predmosti 4 Predmosti 9 Predmosti 10 Predmosti 14 La Rochette 1 Stetten 1 Nazlet Khater 1 Arene Candide 1-IP Barma Grande 2 Barma Grande 3 Barma Grande 4 Bichon 1 Bruniquel 2 Cap Blanc 1 Chancelade 1 Arene Candide 1a Arene Candide 1 Arene Candide 2 Arene Candide 4 Arene Candide 5 Arene Candide 10 Arene Candide 12 Arene Candide 13 Arene Candide 14 Farincourt 1 Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head ? ? ? F M M M M Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens 0.030 0.030 0.030 0.026 0.026 0.027 0.026 0.028 59.20 70.50 65.30 54.80 68.00 72.00 71.00 83.80 Femoral head F Homo sapiens 0.028 52.80 Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head ? ? M F ? ? M M F M F F F M ? ? M M Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens 0.035 0.035 0.035 0.024 0.021 0.021 0.026 0.026 0.027 0.027 0.027 0.027 0.027 0.027 0.030 0.032 0.032 0.019 76.80 76.50 62.70 60.60 63.00 60.90 72.90 79.00 55.40 70.80 65.10 57.70 70.60 65.90 64.70 65.90 52.20 66.40 Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head M F M M F F M ? M M M M M M F F F Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens 0.019 0.019 0.019 0.012 0.012 0.012 0.012 0.011 0.011 0.011 0.011 0.011 0.011 0.011 0.011 0.011 0.010 80.70 58.50 66.40 58.40 60.10 57.80 64.50 75.40 56.30 67.70 71.60 68.70 68.70 68.30 51.00 53.40 54.20 9781107019959c10_p181-204.indd 191 11/14/2011 7:44:13 PM 192 Paul R. Manger et al. Table 10.1. (cont.) Specimen Element Sex Taxon Age (million years) Mass Continenza 1 Grotte des Enfants 3 Laugerie Basse 54298a Laugerie Basse 54298b Laugerie Basse 9 Laugerie Basse 54298c La Madeleine 1 Neussing 2 Oberkassel 1 Oberkassel 2 Parabita 1 Parabita 2 Le Placard 15 Le Placard 16 Romito 3 Romito 4 Saint Germainla-Riviere 1 San Teodoro 1 San Teodoro 3 San Teodoro 4 Veryier 1 Nahal Ein Gev 1 Kubbaniya 1 Ohalo 2 Minatogawa 1 Minatogawa 2 Minatogawa 3 Minatogawa 4 Ein Gev 1 Neve David 1 Jebel Sahaba 117–1 Jebel Sahaba 117–4 Jebel Sahaba 117–5 Jebel Sahaba 117–6 Jebel Sahaba 117–7 Jebel Sahaba 117–10 Femoral head Femoral head M M Homo sapiens Homo sapiens 0.010 0.010 68.10 51.50 Femoral head ? Homo sapiens 0.012 81.70 Femoral head ? Homo sapiens 0.012 63.60 Femoral head Femoral head ? ? Homo sapiens Homo sapiens 0.012 0.012 60.10 67.20 Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head ? M M F M F ? ? M F F Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens 0.012 0.018 0.012 0.012 0.010 0.010 0.013 0.013 0.011 0.011 0.015 66.70 70.80 72.40 56.80 73.30 69.70 58.60 66.50 72.70 60.40 61.50 Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head F ? F M F M M M F F F F ? ? Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens 0.011 0.011 0.011 0.010 0.021 0.020 0.019 0.018 0.018 0.018 0.018 0.016 0.013 0.013 64.60 61.90 68.20 56.20 51.70 69.60 73.50 60.30 45.90 50.20 47.40 54.30 61.50 66.50 Femoral head F Homo sapiens 0.013 57.60 Femoral head M Homo sapiens 0.013 65.20 Femoral head F Homo sapiens 0.013 65.30 Femoral head F Homo sapiens 0.013 54.50 Femoral head F Homo sapiens 0.013 63.10 9781107019959c10_p181-204.indd 192 11/14/2011 7:44:13 PM The mass of the human brain: is it a spandrel? 193 Table 10.1. (cont.) Specimen Element Sex Taxon Age (million years) Mass Jebel Sahaba 117–11 Jebel Sahaba 117–15 Jebel Sahaba 117–17 Jebel Sahaba 117–18 Jebel Sahaba 117–19 Jebel Sahaba 117–20 Jebel Sahaba 117–21 Jebel Sahaba 117–22 Jebel Sahaba 117–26 Jebel Sahaba 117–28 Jebel Sahaba 117–29 Jebel Sahaba 117–33 Jebel Sahaba 117–39 Jebel Sahaba 117–38 Jebel Sahaba 117–40 Jebel Sahaba 117–42 Jebel Sahaba 117–102 Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Femoral head M Homo sapiens 0.013 62.10 Femoral head F Homo sapiens 0.013 50.30 Femoral head M Homo sapiens 0.013 62.20 Femoral head M Homo sapiens 0.013 70.80 Femoral head M Homo sapiens 0.013 61.70 Femoral head M Homo sapiens 0.013 60.80 Femoral head M Homo sapiens 0.013 59.30 Femoral head F Homo sapiens 0.013 60.10 Femoral head F Homo sapiens 0.013 53.60 Femoral head F Homo sapiens 0.013 54.50 Femoral head M Homo sapiens 0.013 73.10 Femoral head F Homo sapiens 0.013 61.00 Femoral head M Homo sapiens 0.013 65.70 Femoral head M Homo sapiens 0.013 65.90 Femoral head M Homo sapiens 0.013 65.00 Femoral head M Homo sapiens 0.013 67.80 Femoral head M Homo sapiens 0.013 63.90 Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head F F F M F F M M F M M F M Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 52.00 52.00 48.30 63.50 51.40 52.20 66.40 61.00 49.20 67.80 62.90 48.10 60.20 9781107019959c10_p181-204.indd 193 11/14/2011 7:44:13 PM 194 Paul R. Manger et al. Table 10.1. (cont.) Specimen Element Sex Taxon Age (million years) Mass Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head Femoral head M M F F M F F F F F M M M M M F Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 51.00 55.20 43.20 43.20 65.50 53.90 54.30 52.50 54.90 52.70 61.00 58.40 57.10 54.30 59.70 57.90 most part, the fossil hominins are reliably segregated from the non-hominin hominoids. This latter segregation must be tempered slightly by the potential overestimate of brain mass using endocranial volume in the fossil hominins – the exact estimate may change somewhat but the overall pattern identiied in this analysis is unlikely to change. Thus, we propose the following conclusions: (1) fossil hominins show a pattern of brain mass to body mass scaling that is different from other simian primates; (2) this pattern exhibits a positive allometry, indicating that brain mass will increase at a faster rate than body mass when there are increases in body mass; (3) the fossil hominins, including fossil H. sapiens, form a distinct grouping within the primates when examining the brain–body mass relationship; and (4) a unique evolutionary event leading to a phenotypically unusual positive allometry of the brain to body relationship in the primates occurred at the genesis of the hominin clade. The modern human brain body mass On average, Homo sapiens has the largest brain mass relative to body mass of all known animal species (Jerison, 1973) and this distinguishes modern humans from our closest extant counterparts, and from our closest extinct relatives. Despite this, our statistical analysis indicates that this gap based on 9781107019959c10_p181-204.indd 194 11/14/2011 7:44:14 PM The mass of the human brain: is it a spandrel? 195 Table 10.2. Published cranial capacities for Miocene, Pliocene and Pleistocene hominins. (Data taken from: Aiello and Dean, 1990; McHenry, 1992; Ruff et al., 1997; Abbate et al., 1998; Asfaw et al., 1999, 2002; Senut et al., 2001; Zollikofer et al., 2005; Rightmire et al., 2006) Specimen Sex Taxon Age (million years) Cranial capacity (cm3) TM 266–01–60–1 A.L. 333–45 A.L. 162–28 A.L. 444–2 ARA-VP-12/130 KNM-WT 17000 MLD 1 MLD 37/38 Sts 5 Sts 19/58 Sts 60 Sts 71 StW 505 KNM-ER 406 KNM-ER 732 KNM-ER 13750 KNM-ER 407 OH 5 SK 1585 OH 7 OH 13 OH 16 OH 24 KNM-ER 1805 KNM-ER 1813 KNM-ER 1470 D2700 D2280 D2282 KNM-ER 3733 KNM-ER 3883 OH 9 UA 31 BOU-VP-2/66 Gongwangling 1 Sangiran 2 Sangiran 10 Sangiran 12 Sangiran 17 Zhoukoudian D1 Zhoukoudian E1 Zhoukoudian H3 Zhoukoudian L1 Zhoukoudian L2 ? M F M M M M ? M ? ? ? M M F ? ? M M ? ? ? ? ? ? M F M M M M M M M ? ? ? M M M ? M M ? Sahelanthropus tchadensis Australopithecus afarensis Australopithecus afarensis Australopithecus afarensis Australopithecus garhi Paranthropus aethiopicus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Australopithecus africanus Paranthropus boisei Paranthropus boisei Paranthropus boisei Paranthropus boisei Paranthropus boisei Paranthropus robustus Homo habilis Homo habilis Homo habilis Homo habilis Homo habilis Homo habilis Homo rudolfensis Homo georgicus Homo georgicus Homo georgicus Homo erectus Homo erectus Homo erectus Homo erectus Homo erectus Homo erectus Homo erectus Homo erectus Homo erectus Homo erectus Homo erectus Homo erectus Homo erectus Homo erectus Homo erectus 6.000 3.400 3.400 2.900 2.600 2.500 2.600 2.600 2.250 2.250 2.250 2.250 2.250 1.800 1.800 1.800 1.800 1.810 1.810 1.810 1.810 1.810 1.810 1.810 1.810 1.810 1.700 1.700 1.700 1.780 1.580 1.200 1.000 1.000 1.150 1.000 0.800 0.800 0.800 0.440 0.440 0.440 0.440 0.440 365.00 500.00 400.00 500.00 400.00 410.00 500.00 435.00 485.00 436.00 428.00 428.00 585.00 510.00 500.00 475.00 506.00 530.00 530.00 674.00 673.00 638.00 594.00 582.00 509.00 752.00 600.00 775.00 655.00 804.00 848.00 1067.00 775.00 995.00 780.00 813.00 700.00 1059.00 1004.00 1030.00 915.00 1140.00 1225.00 1015.00 9781107019959c10_p181-204.indd 195 11/14/2011 7:44:14 PM 196 Paul R. Manger et al. Table 10.2. (cont.) Specimen Sex Taxon Age (million years) Cranial capacity (cm3) Zhoukoudian L3 Sambungmacan 1 Hexian 1 Ngandong 1 Ngandong 5 Ngandong 6 Ngandong 9 Ngandong 10 Ngandong 11 Saldanha 1 Swanscombe 1 Arago 21 Steinheim 1 Petralona 1 Ndutu 1 Atapuerca 4 Atapuerca 5 Atapuerca 6 Broken Hill 1 Dali 1 Ehringsdorf 9 Jinnu Shan 1 Narmada 1 Singa 1 Laetoli 18 Omo-Kibish 2 Krapina 3 Saccopastore 1 Tabun C1 Amud 1 La Chapelle-auxSaints La Ferrassie 1 Forbes’ Quarry Ganovce 1 Guattari 1 Le Moustier 1 La Quina 5 La Quina 18 Spy 1 Spy 2 Shanidar 1 Shanidar 5 Teshik-Tash 1 Qafzeh 6 Qafzeh 9 Qafzeh 11 ? M ? ? M F M M F M M M F M M M M M M M M F M M M M F F F M M Homo erectus Homo erectus Homo erectus Homo erectus Homo erectus Homo erectus Homo erectus Homo erectus Homo erectus Homo heidelbergensis Homo heidelbergensis Homo heidelbergensis Homo heidelbergensis Homo heidelbergensis Homo heidelbergensis Homo heidelbergensis Homo heidelbergensis Homo heidelbergensis Homo heidelbergensis Homo heidelbergensis Homo heidelbergensis Archaic Homo Archaic Homo Archaic Homo Archaic Homo Archaic Homo Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis 0.440 0.400 0.200 0.200 0.200 0.200 0.200 0.200 0.200 0.500 0.400 0.400 0.300 0.300 0.400 0.300 0.300 0.300 0.300 0.300 0.200 0.200 0.300 0.150 0.130 0.130 0.130 0.100 0.150 0.045 0.052 1030.00 1035.00 1025.00 1172.00 1251.00 1013.00 1135.00 1231.00 1090.00 1225.00 1325.00 1166.00 950.00 1230.00 1100.00 1390.00 1125.00 1140.00 1280.00 1120.00 1450.00 1300.00 1260.00 1550.00 1367.00 1435.00 1200.00 1258.00 1271.00 1750.00 1626.00 M F F M M F F F M M M M M M F Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo neanderthalensis Homo sapiens Homo sapiens Homo sapiens 0.072 0.050 0.050 0.057 0.040 0.050 0.050 0.050 0.050 0.050 0.050 0.050 0.090 0.090 0.090 1681.00 1200.00 1320.00 1550.00 1600.00 1350.00 1310.00 1305.00 1553.00 1600.00 1550.00 1578.00 1535.00 1531.00 1280.00 9781107019959c10_p181-204.indd 196 11/14/2011 7:44:15 PM The mass of the human brain: is it a spandrel? 197 Table 10.2. (cont.) Specimen Sex Skhul 4 M Skhul 5 M Skhul 9 M Cro-Magnon 1 M Dolni Vestonice 3 F Grotte des Enfants 4 M Grotte des Enfants 5 F Grotte des Enfants 6 M Mladec 1 M Mladec 5 M Paderbourne M Pataud 1 F Pavlov 1 M Predmosti 3 M Predmosti 4 M Predmosti 9 M Predmosti 10 F Nazlet Khater 1 M Minatogawa 1 M Minatogawa 2 F Minatogawa 4 F Zhoukoudian Up. M Cave 1 Zhoukoudian Up. F Cave 2 Zhoukoudian Up. F Cave 3 Arene Candide 1-IP M Arene Candide 1 F Arene Candide 2 F Arene Candide 4 M Arene Candide 5 M Barma Grande 2 M Bruniquel 2 M Cap Blanc 1 F Chancelade 1 M Oberkassel 1 M Oberkassel 2 F Saint Germain-la-Riviere 1F San Teodoro 1 F San Teodoro 2 M San Teodoro 3 M San Teodoro 5 F Veryier 1 M Pecos F Pecos F 9781107019959c10_p181-204.indd 197 Taxon Age (million years) Cranial capacity (cm3) Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens 0.090 0.090 0.090 0.030 0.026 0.028 0.028 0.028 0.035 0.035 0.027 0.021 0.026 0.027 0.027 0.027 0.027 0.033 0.018 0.018 0.018 0.018 1554.00 1518.00 1587.00 1600.00 1322.00 1775.00 1375.00 1580.00 1620.00 1500.00 1531.00 1380.00 1522.00 1608.00 1518.00 1555.00 1452.00 1420.00 1390.00 1170.00 1090.00 1500.00 Homo sapiens 0.018 1380.00 Homo sapiens 0.018 1290.00 Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens 0.018 0.011 0.011 0.011 0.011 0.019 0.012 0.012 0.012 0.012 0.012 0.015 1490.00 1414.00 1424.00 1520.00 1661.00 1880.00 1555.00 1434.00 1700.00 1500.00 1370.00 1354.00 Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens 0.011 0.011 0.011 0.011 0.010 0.001 0.001 1565.00 1569.00 1560.00 1484.00 1430.00 1300.00 1030.00 11/14/2011 7:44:15 PM 198 Paul R. Manger et al. Table 10.2 (cont.) Specimen Sex Taxon Age (million years) Cranial capacity (cm3) Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos Pecos F M F F M M F M M F M M M F F M F F F F F M M M M M F Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens Homo sapiens 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 0.001 1275.00 1300.00 1120.00 1380.00 1380.00 1270.00 1100.00 1465.00 1320.00 1285.00 1350.00 1440.00 1410.00 1350.00 1190.00 1300.00 1390.00 1350.00 1140.00 1155.00 1178.00 1340.00 1500.00 1550.00 1400.00 1350.00 1325.00 averages may not be as huge a chasm as previously thought. The normal adult human brain can vary in mass from around 850 g through to 1900 g, with body mass varying from 40 to 140 kg. We plotted the data on brain and body mass from a range of individuals of modern humans and compared these with the data from the fossil hominins (Figure 10.1). One interesting aspect of the plots with the 95% conidence intervals depicted is that for the most part, the brain and body masses of modern humans are statistically indistinguishable from the range predicted statistically for the fossil hominins, and in fact the averaged data we have for the largest fossil hominins (H. sapiens, H. neanderthalensis and H. heidelbergensis) fall well within the 95% conidence intervals for modern humans, with H. erectus lying just outside these intervals. Only the smallest or the very largest modern humans were found to have combined brain and body masses that fell outside the 95% conidence intervals of the fossil hominins. 9781107019959c10_p181-204.indd 198 11/14/2011 7:44:15 PM The mass of the human brain: is it a spandrel? 199 Moreover, the data point for fossil H. sapiens (which includes individuals up to 90 ka before present) lies almost directly in the centre of the 95% conidence interval ellipse for the modern H. sapiens. Given that we have used species averages for both endocranial capacity and body mass estimates in our analysis of the fossil hominins (with their inherent drawbacks), it is still very striking that modern humans are not completely segregated. Modern humans fall outside of the range found for extant non-hominin hominoids. What we can conclude from this comparison, is that the relationship between brain mass and body mass in modern humans is not different from that seen for the fossil hominins – an important point that we will come back to later. Two potential evolutionary events in brain mass evolution The current analysis points to two important events in the evolution of human brain mass that must be considered in more detail. At this point it is important to emphasise that we are discussing species averages – i.e. we are not discussing in detail the great amount of variation that should be found in most species and that we have highlighted in part for modern humans. Moreover, we are not discussing variation, or residuals, around the regressions that indicate the variability that species averages exhibit. Both of these factors are important points, but in terms of the current chapter are peripheral to our central argument. Variation within a species is clearly the material upon which natural selection can select positively to give rise to change, or indeed select negatively to preclude change. The residuals of individual species, whether it is the brain– body mass ratio or any other biological feature, are the material of species speciicity, and by examining residuals one may be able to understand the life history or phenotype of that particular species. However, in this one must also be cognisant of the fact that the residuals may be constituted of the innate error of the regression model on which they are based. What we are attempting to outline in the present analysis is the manner in which the actual average mass of the human brain may have evolved. To this end, we irst discuss the advent of scaling of the primate brain, then look more speciically at the scaling of the hominin brain. The genesis of the primate brain–body scaling The analysis done in the present study for primates, and in many previous studies (e.g. Jerison, 1973; Manger, 2006) indicate that all primates, including prosimians, have larger brains than would be expected for their body mass for 9781107019959c10_p181-204.indd 199 11/14/2011 7:44:15 PM 200 Paul R. Manger et al. a mammal. These studies have also indicated that the non-hominin primates show a strong scaling law of form linking body mass and brain mass. This scaling law of form tells us, with a high and predictable reliability, with which changes in body mass there will be accompanying changes in brain mass. What is also interesting is that the manner in which primate brains and bodies scale runs parallel to that seen for mammals in general, indicating a similar mechanism governing the changes – the only difference being that the brain will be around twice the mass expected for a mammal of similar body mass. Thus, we have an order-speciic phylogenetically constrained scaling law of form in the non-hominin primates regulating the mass of the brain relative to the mass of the body. From this it is possible to extrapolate that this scaling law of form regulating the relative mass of the brain and body was founded at the genesis of the primate order. A possible scenario is the uncoupling of the scaling law between these two variables in the very earliest primates, and after a period of intense, but non-lethal mutational changes in the genotype, the law regulating these two variables was recoupled in a manner not dissimilar to that found in other mammals. It is presently unknowable if there were a small population through which a mutational change of this scaling law of form was rapidly spread, whether it was positively selected for through a speciic environmental selection pressure, or whether a different mechanism was responsible. The exact mechanism is peripheral to the arguments of this essay – the fact that it occurred and persisted in all subsequent primate descendants is the key point. The genesis of hominin brain–body scaling Given the fact that primates have larger brains for their body mass than other mammals and that this is consistent for all primate species, how might the difference in the hominins have arisen? It is important to reiterate here that there is a strong and highly predictable structural law of form that appears to be regulating the relationship between brain and body mass in the hominins. This relationship is evidenced as a positive allometry, meaning that changes in the mass of the brain will occur at a faster rate than changes in the mass of the body. It is possible that the scaling law of form that couples the mass of the brain to the mass of the body in primates may have been uncoupled very early in hominin evolution. Once the hominin lineage stabilised, this scaling law may have recoupled, but in a manner different to that found in the primates, producing the observed positive allometry. It is quite possible that the genetic changes associated with bipedality in the hominins may have had a pleiotropic effect on the genes involved in the regulation of the brain and body mass relationship. 9781107019959c10_p181-204.indd 200 11/14/2011 7:44:15 PM The mass of the human brain: is it a spandrel? 201 The earliest hominins were not large creatures, with body masses in the range of 25 to 50 kg; thus, they would not have had changes in the mass of the brain relative to those in primates that would require major changes in their ecological niche. As the body mass of the hominins increased, we see concomitant increases in the mass of the brain. At irst, this is not so marked in the australopithecines, where body mass may have only increased by a few kilograms relative to the earliest hominids such as Orrorin tugenesis (recovered from Kenya, Senut et al., 2001). Later in hominin evolution there was a marked increase in body mass and an even more marked increase in brain mass, occurring simultaneously in early Homo, where body mass increased by between 15 to 20 kg and cranial capacity by 100 to 200 ml. The greater proportional increase in cranial capacity could be attributed to the positive allometry in the brain–body mass scaling relationship. The remaining evolution of the Homo lineage shows increases in body mass, with allometrically rapid increases in cranial capacity until modern times. We are thus left with the conclusion that the positive allometric relationship between brain and body mass in the hominin lineage is likely to be the reason that the brain of modern Homo sapiens is the mass we can readily observe. This combined with the initial allometrically constrained increase in the brain–body mass relationship of primates provides a substantial evolutionary explanation as to why the modern human brain is far larger that would be expected for our body mass in comparison to other mammals. Conclusion Given that it is possible that the majority of the evolution of the mass of the modern human brain can be explained by allometric laws of scaling, there are still several areas that cannot yet be addressed with our current state of knowledge. The irst is the reason why the scaling laws changed during the early evolution of primates, endowing the primates with larger brains for their body mass than would be expected for mammals. The second is the manner in which the scaling laws changed at the origin of the hominin lineage. We feel it is likely to be related to pleiotropic effects of the genes responsible for bipedalism, but further experimentation is required to determine if this may be true. Third, there is very little information available on the evolution of the microstructure of the human brain. Features such as the complexity of the single neuron (Elston et al., 2006), the number of areas in the cerebral cortex (Manger, 2005), the molecular functionality of intra- and extracellular components of receptor complexes, and so on – all need to be studied in detail across extant primates to determine where modern humans 9781107019959c10_p181-204.indd 201 11/14/2011 7:44:16 PM 202 Paul R. Manger et al. differ and how these difference might have evolved, what effect they will have on the function of the brain, and whether these changes are related to overall mass of the brain (Gould may have called these ‘spandrels upon spandrels’). Another factor that must be understood is whether, with the allometric scalings that are known, there was selection for increased body mass, or increased brain mass in hominin evolution. At this point we may create a chicken-andegg argument – was increased brain mass selected for resulting in increased body mass, or vice versa? The African elephant (Loxodonta africana) has a brain that weighs approximately 6 kg, and a body that is very large; however, it has an encephalisation quotient (EQ) of approximately 1.12, or just slightly larger (1.12 times) than that expected for a mammal of its mass. In explaining the mass of the elephant brain, should we postulate that this mammal required a large brain and the selection pressures providing the impetus for a large brain resulted in a de facto large body? On the other end of the mass scale, if we examine the Proboscis bat (Rhynchonycteris nasa) that has a body mass of 3.8 g and a brain mass of 0.118 g, giving an EQ of 0.9 (slightly smaller than expected for a mammal of its body mass), do we propose that selection pressures requiring a small brain and a concomitantly small body produced this phenotype? In both cases, it is more parsimonious to propose that pressures selecting for the differing body masses produced the mass of the brain – but along the trajectory determined by the mammalian class level allometric scaling law of form. Given the phylogenetic occurrence of allometric scaling between brain and body mass across all vertebrates, and the clear relationship between environmental factors and body mass across all vertebrates (e.g. Pearson, 2000), should we single out the hominin lineage as a special case? This of course has been done when seeking adaptationist rationale for the evolution of the brain mass of modern humans. If, however, we take the more parsimonious approach and argue that the mass of the human brain evolved as a by-product of increasing body mass in hominins, we then must conclude that human brain mass is in fact a spandrel – a functionally useful one to be sure, probably not something to be selected against, but the by-product of a change in the scaling relationship of brain and body mass that occurred at the genesis of the hominin lineage. Further studies into the evolution of hominin body mass and the relationship of this to environmental or other factors will potentially shed more light on the evolution of human brain (Pearson, 2000). References Abbate, E., Albianelli, A., Azzaroli, A. et al. (1998). A one-million-year old Homo cranium from the Danakil (Afar) Depression of Eritrea. Nature, 393: 458–60. 9781107019959c10_p181-204.indd 202 11/14/2011 7:44:16 PM The mass of the human brain: is it a spandrel? 203 Aiello, L. C. and Dean, M. C. (1990). 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