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How and Why Humans Grow Thin Skulls: Experimental Evidence for Systemic Cortical Robusticity

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How and Why Humans Grow Thin Skulls: Experimental Evidence for Systemic Cortical Robusticity AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 101:217-236 (1996) How and Why Humans Grow Thin Skulls: Experimental Evidence for Systemic Cortical Robusticity DANIEL E. LIEBERMAN Department of Anthropology, Rutgers Uniuersity, Douglas Campns, New Brunswick, New Jersey 08903-0270 KEY WORDS Skull, Neurocranium, Cortical bone, Robusticity, Homo, Pigs, Armadillos ABSTRACT To what extent is cranial vault thickness (CVT) a character that is strongly linked to the genome, or to what extent does it reflect the activity of an individual prior to skeletal maturity? Experimental data from pigs and armadillos indicate that CVT increases more rapidly in exercised juveniles than in genetically similar controls, despite the low levels of strain generated by chewing or locomotion in the neurocranium. CVT increases in these individuals appear to be a consequence of systemic cortical bone growth induced by exercise. In addition, an analysis of the variability in vault thick- ness in the genus Homo demonstrates that, until the Holocene, there has been only a slight, general decrease in vault thickness over time with no consistent significant differences between archaic and early anatomically modern humans from the Late Pleistocene. Although there may be some genetic component to variation in CVT, exercise-related, non-genetically heri- table stimuli appear to account for most of the variance between individuals. The thick cranial vaults of most hunter-gatherers and early agriculturalists suggests that they may have experienced higher levels of sustained exercise relative to body mass than the majority of recent, post-industrial humans. 0 1996 Wiley-Liss, Inc. Nature is not greatly concerned over the precise Neanderthals. Cranial vault thickness thickness of the cranium. (CVT) is frequently used as a character to Todd (1924:255) make inferences about the phylogenetic rela- tionships among recent taxa of Homo (e.g., Why modern humans have generally thin- Stringer, 1984, 1987; Thorne and Wolpoff, ner bones and, in particular, thinner skulls 1981; Groves, 1989; Frayer et al., 1993), and than archaic humans has long been a subject to make inferences about the behavioral dif- of speculation for clinical and hominid ferences between modern and archaic hu- palaeontological research. The degree of cor- mans (e.g., Coon, 1962; Brace, 1979). tical robusticity throughout the skeleton CVT is an interesting character to exam- and, more specifically, in the cranial vault ine in depth because the vault grows some- is often considered a major morphological what differently than long bones that have distinction between anatomically modern traditionally been the focus of most research Homo sapiens and earlier taxa ofHomo (e.g., on cortical robusticity. Unlike bones that Wolpoff, 1980; Stringer, 1988). Weidenreich form within a cartilagenous framework, the (1943), for example, noted that the mean pa- bones of the neurocranium-the parietals rietal thickness at bregma of modern Euro- peans, 5.5 mm, is 60% thinner than that of the Sinanthropus pekinensis fossils from Zhoukoudian and 40% thinner than that of Received August 29, 1995; accepted April 29, 1996. 0 1996 WILEY-LISS, INC 2 18 D.E. LIEBERMAN and the squamous portions of the occipital, vaults are a possible adaptation for pro- frontal and temporal-all develop intra- tecting the skull from injury, suggesting that membranously from the membranes that “the technological innovations of the Late surround the inside and outside, respec- Stone Age, including the use of efficient long- tively, of the vault. Early in development, distance hunting weapons such as bows with osteoblasts in these membranes rapidly de- poisoned arrows reduced the necessity for posit highly vascularized woven bone within large size and skeletal robustness in hunting numerous ossification centers (Ohtsuki, populations.” According to this hypothesis, 1977).As growth slows after birth, both the the recent decline in vault thickness most inner membrane, the endocranium, and the likely reflects a relaxation of selection pres- outer membrane, the pericranium, switch to sures to maintain thick vaults, presumably depositing vascularized lamellar bone, form- because thin vaults are metabolically less ing the inner and outer tables of the neuro- expensive to grow or support. Similar argu- cranium (Sperber, 1989). Osteoclasts and ments are found in Brace (1979:67), Stringer then osteoblasts begin to invade the center (1988:268), and elsewhere. of the vault at around age four, resorbing and A second hypothesis is that differences in remodeling the woven bone and the earliest CVT reflect nonheritable, in vivo responses formed lamellae into the trabecular bone of to mechanical force. Bone tissue interacts the diploe, which comes to contain haemo- dynamically with its mechanical environ- poietic cells (Williams et al., 1989). It is im- ment. Force applied to a bone (quantified portant to note that, unlike most limb bones per unit area as stress, a), generates strain and other cranial bones, both the endocran- (deformation, E) whose cumulative effects, ial and pericranial surfaces of the superior if sufficient in magnitude, can damage its half of the vault constitute depository microstructure and mechanical integrity growth fields in human and nonhuman pri- (Carter, 1987; Martin and Burr, 1989, Mar- mates (Duterloo and Enlow, 1970; Enlow, tin, 1992.). Controlled experiments on both 1990).Consequently, the vast majority of the limb bones that form endochondrally (e.g., neurocranial cavity does not expand though Biewener et al., 1986;Woo et al., 1981;Rubin drift (resorption of the inner layer and depo- and Lanyon, 1984, 1985) and facial bones sition of the outer layer) but instead expands that form intramembranously (e.g., Corruc- from tension-induced growth within the su- cini and Beecher, 1982, 1984; Bouvier and tures of the vault. A small amount of drift Hylander, 1981;Yamada and Kimmel, 1991) does occur, however, at the sutural margins demonstrate that high levels of strains in- of the neurocranial bones, preventing duce local osteoblastic responses that in- steeply angled sutures (Enlow, 1990). The crease cortical bone mass. Such remodeling bones of the superior half of the vault, there- can be adaptive because it increases the dis- fore, can grow only thicker and do so inde- tribution of mass in the plane(s) of deforma- pendently of any increases in cranial ca- tion, thereby reducing the amount of strain pacity. generated by a given force (Biewener et al., This paper asks to what extent as a char- 1986; Frost, 1986,1987,1988). The most im- acter CVT is strongly linked to the genome portant sources of mechanical force on the and to what extent it reflects epigenetic re- cranial vault are clearly those from chewing. sponses to exogenetic stimuli. Despite infor- It is a reasonable hypothesis that strains mation on the proximate cellular processes from the tension produced by the m. tempo- by which CVT develops, there is little under- rulis on the outer table of the vault or strains standing of the mechanisms that cause some generated from other chewing-related forces individuals or taxa to have thicker cranial generated elsewhere in the cranium may af- vaults than others. Three hypotheses have been proposed to account for variability in nonpathological cranial vault thickness in ‘A variety of pathologies, including haemolytic blood dysplasias humans.l The most common hypothesis is associated with sickle cell anemia and thalassemia, can cause unusual thickening of the diploic layer of the cranial vault (Webb, that CVT is subject to selection. Wolpoff 1990). Such cases, however, are rare in the fossil record and are (1980:333),for example, points out that thick not considered here. CRANIAL. VAULT THICKNESS 2 19 fect the rate of bone growth in the cranial selection. If, however, CVT variation is an vault (Weidenreich, 1941; Washburn, 1947; in vivo, exogenetic response to higher me- Moss, 1954; Moss and Young, 1960; Naw- chanical forces, then such strains should be rocki, 1991, 1992). As Hylander (1986) has sufficient to replicate them in laboratory shown, chewing harder foods generates more conditions. In addition, this hypothesis strain in the mandible and face than chew- would predict that humans who eat soft diets ing soft foods, so variation in CVT may re- will have thinner vaults than those who eat flect responses to diets of different hardness. harder diets. Finally, if CVT is merely a con- Locomotion may also generate strains in the sequence of elevated circulating hormones cranium, resulting in the prediction that hu- that stimulate osteogensis, then thickened mans who run more may have thicker skulls cranial vaults will develop in laboratory ani- (Bhanba, 1961). mals who have elevated GH levels, and such Finally, a few researchers (e.g., Twiessel- individuals will also have an overall high mann, 1941; Kennedy, 1985; Nawrocki, degree of cortical robusticity. An additional, 1991; Nelson and Gauld, 1994) have pointed related question is whether a thin cranial out that differences in the levels of certain vault is a derived character of anatomically circulating hormones may also influence modern humans or whether it is a more re- CVT. All bone growth is mediated by hor- cent phenomenon. Although generally cited mones on both local and systemic levels. as a defining character of modern humans, Growth hormone (GH) in particular has there has been little systematic investiga- well-documented effects on CVT and overall tion of variability in CVT among recent
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