The present analysis of the cellular composition of the orangutan and gorilla cerebellum shows that, in these great apes, this structure conforms to the cellular scaling rules that apply to other primate species, including humans. Further, the number of cells in the cerebellum is a good predictor of cortical and brain mass, which makes it seem likely that the entire brains of these great apes also conform to the scaling rules that apply to other primates. Thus, we infer that the brains of the gorilla and the orangutan are, like the human brain, built according to the same linear cellular scaling rules that apply to other primates. In this case, these cellular scaling rules can be used to estimate the number of neurons and other cells in the major divisions of the brains of now-extinct hominin species. We expect that our estimates of the numbers of neurons that composed the brains of hominin species will be illuminating in upcoming studies of the evolution of cognitive capacity across species, as well as in comparative studies across large-brained taxa such as elephants, dolphins and whales, particularly in light of the proposition that absolute numbers of brain neurons, regardless of brain size, should be a limiting factor for cognition and thus a better predictor of cognitive ability than relative or absolute brain size or encephalization [Herculano-Houzel, 2009
Interestingly, while the cellular scaling rules that apply to primate brains seem to have remained stable in hominin evolution, body size seems to have increased faster than brain size until the divergence of the Cercopithecidae and Pongidae lineages, but appears to have increased only little in the Homo lineage [Montgomery et al., 2010
], to the point where current humans have the same relative brain size found in groups that diverged earlier in primate evolution, such as Cercopithecidae and Cebidae. This is best understood by considering brain and body mass separately: while brain mass tends to have increased in primate species over the last 30 million years, decreasing only in H. floresiensis
[Montgomery et al., 2010
], body mass underwent major increases in the Pongidae and Cercopithecidae lineages.
Such discrepancy between the evolution of brain and body mass is compatible with our previous observation that while the cellular scaling rules identified for a group of 6 primate species also apply to other samples of primates [Gabi et al., 2010
], including humans [Azevedo et al., 2009
], and hence probably to primates as a whole, the allometric rules relating body and brain size are very sensitive to the particular species sampled [Gabi et al., 2010
]. This is also in line with the recent evidence that brain and body mass have been subject to separate selection pressures in primates [Montgomery et al., 2010
] and that these often highly correlated traits can show differences in their patterns of evolution [Finarelli and Flynn, 2009
; Gonzalez-Voyer et al., 2009
]. Thus, brain size variation across species may be neither determined by body size nor together with it, but rather only loosely correlated with body size.
This notion is compatible with the view that body size can evolve either by change in the frequencies of genes that affect both brain and body size, generally during fetal and early postnatal growth, or by change only in the frequencies of genes that affect body size alone, and not brain size, generally in later growth [Riska and Atchley, 1985
]. As a result, body size evolution occurring by changes in late growth will be accompanied by little parallel change in brain size. The correlation between adult brain and body mass therefore can vary between very low and very high, depending on the extent to which adult body mass is determined during early development alone or during later development as well.
Body mass, therefore, should not be considered as a variable determining, or contributing directly to, brain size – even though it is often correlated with brain size. In this sense, the finding of a particularly large adult body size in a species, such as the gorilla, does not imply that its brain should be correspondingly larger. Indeed, Shea [1983
] notes that gorilla and chimpanzee neonates are very similar in size, and that body size divergence between these species has occurred by differences in rates of later postnatal growth, which occurs after the brain has achieved most of its mature size. This later postnatal growth is all the more evident in species with great sexual dimorphism, such as orangutans and gorillas – an issue that we cannot address here. However, the much larger sexual dimorphism of body size compared to brain size [Sherwood et al., 2004
] in great apes also supports the notion that the determination and evolution of brain size can occasionally be dissociated from body size.
In light of the possibility of continued growth of the body after the brain has reached its adult size, we consider that the size of the human body, or of the body of any species, is not an accurate predictor of its brain mass, and should not be used as such, even though the calculation of relative brain mass or encephalization quotient may be useful for examining how brain and body masses relate across species. Along these lines, evolution of brain size should not be evaluated in light of adult body mass, but rather as a simultaneous process that is related to the evolution of adult body mass only to the extent that these 2 variables change together in early development. We propose, therefore, that the evolution of the hominin brain, and of the human brain in particular, involved 2 parallel but not necessarily related phenomena: an increase in brain size and number of neurons, obeying the same cellular scaling rules that apply to other primates, and a moderate increase in body size, compared to gorillas and orangutans, whose body size increased greatly compared to other primates who diverged earlier from the common ancestor.
Based on the results presented here, therefore, we consider that the notion that humans evolved too large a brain for their bodies is inappropriate, given that it is based on predictions made from body mass [Jerison, 1973
; Marino, 1998
]. Rather, we believe that human evolution is best accounted for by considering that, while the brain of all extant species as well as fossil hominins scaled in the same manner as a function of the number of neurons, great apes evolved a large body (diverging from the brain-body relationship that applies to earlier-diverging primates as well as for later-diverging humans) for reasons that may not be directly related to their brain size – a trend in evolution that was not pursued in the Homo
Growing a large body once adult brain size is achieved comes at a cost. While large animals require less energy per unit of body weight, they have considerably larger total metabolic requirements [Schmidt-Nielsen, 1984
; Martin, 1990
; Bonner, 2006
]. Thus, large mammals need to eat more, and they cannot concentrate on rare, hard-to-find or catch foods [Conroy, 1990
]. Indeed, great apes tend to eat more abundant but lower-quality plant foods. In exchange, as in many mammals, a larger size offers clear advantages in protection from predators, and more success in competition with others of the same species, or other species, for food and territory. In addition, a larger size in males typically reflects sexual selection as larger males are favored in male-male competition for mates [Plavcan and van Schaik, 1997a
; Lindenfors and Tullberg, 1998
]. Therefore, the unusually large and late-grown body size of the great apes appears to be a consequence of a focus on feeding on relatively abundant but less nutritious food under conditions of competition for food and territory as well as considerable male-male competition for mates.
Hominin evolution seems to have favored body sizes that do not require much late growth. As a result, modern humans have a body size that conforms to the brain-body relationship that applies to Old-World and New-World monkeys [Herculano-Houzel et al., 2007
], and possibly to chimpanzees as well. While our species is mildly sexually dimorphic in body size, male-male competition does not seem to be highly dependent on body size. Notice that, until the Homo
radiation, the first known hominin species had body masses in the same range as chimpanzees, and brain masses and predicted numbers of brain neurons in the same range as gorillas and orangutans. This suggests that hominin competition for resources was not strongly tied to body size. Rather, the addition of larger numbers of brain neurons, possibly first afforded in H. erectus
by the ability to control the use of fire to cook and thus improve the caloric efficiency of foodstuffs [Wrangham, 2009
] (although extractive foraging and food processing by other means were probably contributing factors as well), may have been a key factor in reproductive success in our lineage.
Given that cognitive abilities of non-human primates are directly correlated with absolute brain size [Deaner et al., 2007
], and hence necessarily to the total number of neurons in the brain, it is interesting to consider that enlarged brain size, consequence of an increased number of neurons in the brain, may itself have contributed to shedding a dependence on body size for successful competition for resources and mates, besides contributing with larger cognitive abilities towards the success of our species [Herculano-Houzel, 2009
]. In this regard, it is tempting to speculate on our prediction that the modern range of number of neurons observed in the human brain [Azevedo et al., 2009
] was already found in H. heidelbergensis
and H. neanderthalensis
, raising the intriguing possibility that they had similar cognitive potential to our species. Compared to their societies, our outstanding accomplishments as individuals, as groups, and as a species, in this scenario, would be witnesses of the beneficial effects of cultural accumulation and transmission over the ages.