Published online before print September 8, 2008, doi: 10.1073/pnas.0803917105
PNAS September 16, 2008 vol. 105 no. 37 13764-13768
Neanderthal brain size at birth provides insights into the evolution of human life history
From Article / Discussion – Much more at PNAS
These findings permit several inferences regarding the evolution of brain growth patterns and of human life history. A neonate brain size of ≈400 ccm is most likely a feature of the last common ancestor of Neanderthals and AMHS, and it might represent the upper physiological and obstetrical limit that can be attained in hominins, irrespective of the course of postnatal brain expansion.
Various studies have proposed that a large neonatal brain size (≈300 ccm) and secondary altriciality were features already present in H. erectus (4, 9, 35) (estimates are summarized in SI Text, Estimates of Homo erectus Neonatal Brain Size). Because fetal brain growth requires substantial maternal energy investment (36), a large neonatal brain size must have represented a significant selective advantage in H. erectus, possibly by providing the primary substrate for complex learning tasks during childhood (4). Likewise, the high early postnatal brain growth rates of Neanderthals and AMHS compared with chimpanzees, which imply a more than twofold increase of ECV during the 1st year of life, might be a feature of their last common ancestor, and there is evidence that high postnatal brain growth rates might already have evolved in H. erectus (4, 9). Overall, therefore, our data support the hypothesis (4, 9) that the origins of “modern” human-like patterns of brain growth and life history must be sought relatively early during the evolution of the genus Homo.
High postnatal brain growth rates have been interpreted as an evolutionary extension of fetal modes of growth into early infancy (36), and this is thought to be the main ontogenetic mechanism to attain an exceptionally high degree of encephalization during adulthood (2). What are the implications of this pattern of brain growth for life history evolution? Recent analyses suggest that the correlation between brain growth patterns, adult brain size, and life history is indirect and results from maternal energetic constraints (2, 5, 7): The additional energetic costs of the fast-growing infant brain are mainly sustained by the mother, such that species investing in large infant brains that grow at high rates to reach large adult sizes require large, late-maturing mothers (2, 5).
In this context, the higher early brain growth rates and larger adult brains of the Neanderthals compared with rAMHS have interesting implications. The pattern of Neanderthal brain growth fits into the general pattern of rate hypermorphosis in this species: Compared with rAMHS, Neanderthals have been shown to attain larger adult cranial sizes and more advanced (peramorphic) shapes within a given period of ontogenetic time (31). Rate hypermorphosis might be a correlate of greater average body size in Neanderthals compared with rAMHS (21, 22). However, it does not imply earlier cessation of brain growth (Fig. 4B), nor does it imply a faster pace of life history (as was suggested in refs. 18 and 19): In light of the maternal energetic constraints hypothesis (2, 5), our results suggest that Neanderthal life history had a similarly slow pace as that of rAMHS, and probably was even somewhat slower.
What are the potential developmental, cognitive, and phyletic implications of these subtle developmental differences between the brains of Neanderthals and rAMHS? In recent humans, the temporal course of endocranial volume expansion is only loosely correlated with the temporal course of brain maturation (37), such that hypotheses regarding differences in cognitive development cannot be substantiated with fossil evidence. Nevertheless, several hypotheses can be proposed to explain how differences in brain growth rates between Neanderthals and AMHS evolved. High brain growth rates in the Neanderthals could represent a derived feature. This hypothesis would be in concert with the notion that Neanderthal morphology is derived in many respects. As an alternative hypothesis, high rates in the Neanderthals might represent an ancestral condition, probably shared with eAMHS as opposed to rAMHS, whose lower brain growth rates would represent a derived condition. Support for this hypothesis comes from the observation that adult brain size of eAMHS was similar in range to that of the Neanderthals (38, 39), such that it is likely that brain growth rates were similar as well.
According to this second hypothesis, the high ancestral rates of brain growth were probably reduced only relatively recently during AMHS evolution. Brain size reduction in AMHS during the late Pleistocene is well documented, and it went in parallel with body size reduction (39). We can only speculate on potential selective constraints driving this evolutionary trend toward rate hypomorphosis. Evidence from recent human populations indicates that size reduction is correlated with faster life histories and higher mortality risks (40). Alternatively, brain size reduction during the Late Pleistocene could be the result of an evolutionary performance optimization. Evidence for substantial cerebral reorganization comes from Late Pleistocene AMHS (Cro-Magnon 1) and Neanderthals (La Chapelle-aux-Saints 1, La Ferrassie 1, and Forbes’ Quarry 1), which had larger cerebral hemispheres relative to cerebellum volume than modern humans (41). It could be argued that growing smaller—but similarly efficient—brains required less energy investment and might ultimately have led to higher net reproduction rates. Such an evolutionary shift might have contributed to the rapid expansion of Upper Paleolithic AMHS populations into Eurasia.
The notion that genes down-regulating rates of early brain growth might have contributed to the fitness of our own species is an intriguing, but testable, hypothesis. Genes involved in the regulation of brain growth that show evidence of recent selective sweeps are of special interest (42, 43), but their known normal variants do not account for variation in brain size (44). Further research is thus necessary to clarify the genetic basis of brain and body size variation in modern humans and its relationship to life history variation.
Overall, integrating neurocranial, dentognathic, and postcranial data on Neanderthal and AMHS development reveals a complex pattern of between-taxon and within-taxon variability of life history-related variables, and indicates that hominin life history evolution was a modular (5), mosaic-like, rather than a linear, process. Inferences on the evolution of hominin life history and cognitive development must be drawn with caution, especially when drawn from isolated aspects of fossil morphology.