J. theor. Biol. (2002) 218, 129–138 doi:10.1006/yjtbi.3052, available online at http://www.idealibrary.com on

Skeletal Biology, Functional Asymmetry and the Origins of ‘‘Handedness’’ Richard A. Lazenbyn Anthropology Program, University of Northern British Columbia, Prince George, British Columbia, Canada V 2N 4Z9 (Received on 25 April 2001, Accepted in revised form on 4 April 2002)

The past decade has witnessed the (re)emergence of a debate as to whether handedness is apomorphic within hominins. There are both qualitative and quantitative arguments, some which draw non-human primates into the handed sphere and others which exclude them. Ultimate questions concern origins of structural asymmetry of both brain and body and lateralized behaviours with implications for tool use and language. Lateralization is thus an important realm of phylogenetic study, and archaeologists and psychologists alike have sought to identify handedness within material culture. However, hand preference for tool manufacture and use among extant non-human primates, such as Cebus and Pan, suggests that the archaeological record may well be mute regarding the origins of laterality. In this paper, an argument is put forward positioning skeletal biology as a viable approach to the handedness origins issue. Behaviour is a mediator of the complementary processes of geometric modelling (change in size and shape) and histological remodelling (disuse osteopenia; microfracture repair); therefore, directional asymmetry in the pattern of skeletal modelling and remodelling is a putative signal of lateralized activity. r 2002 Elsevier Science Ltd. All rights reserved.

Introduction Prior to 1987 the predominant use of one hand in the performance of diverse tasks, as a population-level phenomenon (‘‘handedness’’), was perceived as a uniquely human trait (McGrew & Marchant, 1997). While earlier studies in experimental psychology had suggested the existence of lateralized hand use in non-human primates (Beck & Barton, 1972), the major assault on the premise of human inimitability for handedness can be traced to MacNeilage et al. (1987, 1988, 1991). They argued that arboreal feeding among early primates lateralized hand function between stability (right hand) and visually guided reaching and feeding n

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(left hand). Their terrestrial successorsFno longer committed to a balancing actFwere subsequently rewarded with a ‘‘freed right hand’’, which was then exapted for fine/skilled manipulation. Revitalized, primate laterality research proliferated through the 1990s, producing numerous research papers, examples of which include Fagot et al. (1991) in rhesus macaques; Byrne & Byrne (1991), in mountain gorillas; Hopkins et al. (1993), Sugiyama et al. (1993) and Marchant & McGrew (1996, 2001) in chimpanzees; and Laska (1996) and Westergaard & Suomi (1996) in New World monkeys. Edited volumes (Preuschoft & Chivers, 1993; Ward & Hopkins, 1993) and reviews and meta-analyses (Marchant & McGrew, 1991; McGrew & Marchant, 1997) have also contributed to a growing body of knowledge surrounding r 2002 Elsevier Science Ltd. All rights reserved.

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primate laterality. Several issues arose from these works, including population vs. individual distinctions, preference vs. handedness, age, sex, and rank-grading of performance, and taskspecific correlates of lateralized behaviour (i.e., tool use vs. ‘‘non-tool’’ activities). The waters were muddied considerably, and for a time it appeared that yet another supposed mainstay of human uniquenessFfunctional asymmetryFhad fallen from grace. Beautiful theory had met ugly factFor so it was supposed. McGrew & Marchant (1996) proposed a fivelevel model of primate laterality, recording the distribution of lateralized behaviour within and between subject and task. Handedness, as we know it in ourselves as a population-level phenomenon, obtains when a hand is employed across tasks and across subjects, while hand preference is the case when individuals favour a given hand for a given task, but the hand so favoured varies among individuals in the population [a model analogous to antisymmetry (Van Valen, 1962) in the structural domain]. For some individuals the dominant hand may be left, and for others, right. Less clear-cut categories are those of task specialization, occurring within tasks across subjects, and hand specialization, within subjects across tasks. Specialization is, of course, a precursor to handedness/preference, and the difference may be more quantitative than qualitative. Ambilaterality obtains when individuals are equally likely to use either left or right hands for any given task. While McGrew & Marchant’s (1994) review of the literature failed to convince them of the existence of handedness in non-human primates, they acknowledged that the antithesisFhandedness as human apomorphyFdid not necessarily follow. The data, they felt, were just too weak. A much stronger stance was taken in a subsequent review (McGrew & Marchant, 1997, p. 227), in which it was concluded that human handedness is a ‘‘highly derived characteristic’’. This conclusion was reinforced by naturalistic studies of wild chimpanzees from Gombe and Mahale (Marchant & McGrew, 1996, 2001) in which a marked absence of laterality was found for pooled and individual observations of non-tool-oriented manual and postural behaviours. Recently, however, McGrew & Marchant (1999) reported a selective

advantage for lateralization of tool use in a food acquisition strategy (termite fishing) at Gombe. They hypothesized that energy-efficient foragers would be selectively favoured over time, leading to ‘‘progressively greater lateralization’’. They found that individual chimpanzees who exclusively used one hand in fishing episodes had a significantly higher success rate (capture per event), as well as higher levels of efficiency and lower error rates (although both statistically non-significant). While they did not consider whether left- or right-hand use was a factor among their more efficient subjects, it is perhaps noteworthy that eight of these ten individuals were 100% left lateralized. However, if an adaptive advantage in fact exists it begs the question as to why preference (individual) has not been transformed into handedness (population/species)? The alternative is to propose that termite fishing is, evolutionarily speaking, a relatively new strategy. Among the more pervasive arguments for handedness being peculiar to humans links lateralization of motor function to cerebral asymmetry and subsequently to the origin of human language (Calvin, 1982; Corballis, 1989; Greenfield, 1991; MacNeilage, 1991; Bradshaw & Rogers, 1993), a position I am not prepared to address here. Interestingly, a recent study (Hepper et al., 1998) identified right-arm movement preference in 10-week-old foetusesF a developmental age preceding cerebral lateralization, prompting the authors to suggest that behaviour stimulated structural asymmetry in the brain. The issue of prehistoric right-hand bias has been a fertile area for archaeologists (Spennemann, 1984; Toth, 1985; Cornford, 1986) and psychologists (Frost, 1980) alike in their examination of the material culture record. Toth (1985) proposed that flake morphology in Lower Paleolithic lithic detritus suggests the presence of predominantly right-handed tool-makers at the origins of the archaeological record. ‘‘Righthanded’’ flakes exhibit a characteristic rightoriented distribution of cortex resulting from a preferential clockwise rotation of a core supported in the left hand. If early hominins had become lateralized along the lines implied by McGrew & Marchant (1999), in which tool-use

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precedes manufacture, material culture demonstrating handedness should be anticipated at the inception of the archaeological record, rather than being perceived to develop within it. This line of reasoning supports Toth’s analysis. Recently, however, Pobiner (1999) has critiqued the use of flake morphology to evaluate handedness in early hominins (to borrow freely from the title of her succinct paper). Her study indicates that on any given day, a left- or right-handed flintknapper may produce exclusively right- or left-handed flakes, or variable proportions of each. Operant factors such as flintknapper skill, raw material type and core shape, and possible preferential curation of ‘‘left-handed’’ flakes could influence a determination of right handedness in such a record. She proposes that hand preference rather than handedness, Sensu McGrew & Marchant (1999), may be a more appropriate characterization for the Lower Paleolithic. Fortunately, the fossil record preserves biology as well as technologyFmost familiar as bone and tooth, both of which can be of greater antiquity than stone tools. Addressing the origins of lateralityFwhich is both interesting and important and a very different problem than demonstrating which living primates exhibit hand preferenceFfalls legitimately, though perhaps not easily, to skeletal biology. The argument has been made that cultural modification of hard tissue may indicate handedness (Berm! udez de Castro et al., 1988, in the case of teeth), although such an approach may overlook the presence of a behaviourally lateralized ‘‘lastcommon ancestor’’ despite the demonstration of population-level complex cultural repertoires among extant chimpanzees (McGrew, 1998; Whiten et al., 1999) presumably also evident in that ancestor. What follows is a biobehavioural model of biomechanical adaptation of bone tissue to lateralized forelimb function. The model is grounded in morphological correlates of quantitative and qualitative variability in activityinduced mechanical loading. It does not, at this time, address demonstrable species-specific differences in genetic (e.g. Akhter et al., 2000; Kodama et al., 2000) or hormonal/metabolic (e.g. Watkins et al., 2001) regulation of physiology of skeletal adaptation.

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A Bone Modelling/Remodelling Model for Handedness Bone is a malleable tissue, and highly responsive at both macroscopic and microscopic levels to its external, mechanical environment throughout the life course. Three decades of basic research in skeletal biology has produced an understanding of functional adaptation that can be distilled thusly: bone adjusts its mass and density in response to unusual, dynamic shortterm loads effecting a functionally adapted organization (Huiskes, 2000; Martin, 2000; Robling et al., 2000; Hazelwood et al., 2001). This is a succinct but specific rendering of opinion that can be traced back to Galileo (Martin & Burr, 1989; Burr & Martin, 1992). We should not be surprised then, that directional asymmetry in skeletal macro- and micro-morphology will be a consequence of behavioural laterality. There are numerous studies on a variety of elements dependent on just this premise in both extant (Roy et al., 1994; Lazenby, 2001) and extinct (Trinkaus et al., 1994) hominin samples. Most notably we see this research applied to long and short limb bones whose size and shape reflects intra- and interspecific variation in locomotor, postural and manipulative behaviours (Lieberman, 1997). The logic here is fairly straightforward: (1) Skeletal modelling (principally the alteration of shape through independent processes of surface resorption and formation by osteoclasts and osteoblasts, respectively) and remodelling (the alteration of histomorphology through coupled intracortical resorption and formation) are threshold effects of a bone’s dynamic and atypical strain environment. Morphology is adjusted as appropriate to accommodate such deformations (Turner, 1998, 1999). (2) Intracortical fatigue microdamage consequential to functional loading is a non-random and site-specific initiator of localized remodelling (Martin & Burr, 1982; Mori & Burr, 1993; Burr et al., 1997; Ramtani & Zidi, 2001). A skeletal biology model predictive of behavioural laterality requires specifying variables indicative of (re)modelling history, shape and mass on the one hand, and be able to relate these

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to the salient features of the strain environment, notably magnitude, rate and direction, on the other. Such variables would include measures of the resistance of an element of a given shape to deformation (and, ultimately, failure), and measures of the history of intracortical remodelling. In cortical bone diaphyses, the former are captured by size and shape quantities, including cross-sectional areas, moments of area, and indicators of loading pattern (departures from circularity suggestive of axes of preferential strain and angles of rotation between anatomical and functional axes, Ruff, 2000). The latter are captured by indicators of intracortical turnover, including porosity, osteon population density, activation frequency and bone formation rate (Martin et al., 1998; Turner, 1999; Martin, 2000). Table 1 provides a phenomenological and qualitative description of the first of these requirements, i.e., which variables may be relevant to behavioural reconstruction? These may be measured at any of a number of locations along a diaphysis, dependent on factors such as muscle and ligament insertion, and joint proximity. The second requirement, relating parameter to strain environment, is less straightforward. Table 2 summarizes an operational relationship, using the dichotomous ordinal strain magnitude

categories of ‘‘higher’’ and ‘‘lower’’ against loading patterns of ‘‘frequent and diverse’’ vs. ‘‘occasional and typical’’. Testing the model will indicate the degree to which this coarseness might be resolved to a finer grain. Examining Table 2 from the perspective of the origins of laterality, however, it is reasonable to expect that cells B and D, inasmuch as they involve relatively low levels of functional loading, would not characterize earlier hominin populations, nor non-human primates if laterality included activities such as nut-cracking or even stone-tool manufacture (e.g. Westergaard & Suomi, 1996). We are thus left with one meaningful functional asymmetry, cells A and C, both of which involve relatively high strain magnitudes but qualitatively different stain rates and patterns. The primary distinction is one of shape and remodelling rate. Here the argument is developed that the dominant limb will be exposed to a greater variety of both normal and abnormal strains, the latter owning to the fact that dominant limbs tend to be stronger (in terms of both bone and muscle mass), and individuals are more likely to perform exceptional tasks using that limb (Peters, 1990). This will generate deviations from circularity, a morphology more characteristic of non-dominant limbs. In human samples, studies of shape asymmetry has demonstrated greater degrees of non-circularity and larger total and

Table 1 Definition of skeletal biological parameters reflective of functional loading (activity), after Ruff (2000, p. 1434) Parameter

Variable

Comment

Size

Total area (TA); Percent cortical area (PCA); maximum bending rigidity (Imax ); torsional rigidity (J)

Shape

Ratio of maximum and minimum bending rigidity (Imax =Imin ); y

TA reflects absolute size, while PCA incorporates differences in medullary cavity area; Imax reflects bending strength and will differentially reflect nonrandom compensatory periosteal bone growth, while J is a general reflection of torsional rigidity Values departing from unity indicate non-circularity and accommodation to directional bending strains; computation of geometric properties such as Imax (above) include measures (y) of the deviation of predominant loading axis from arbitrary anatomical axes (e.g. anterior, medial) Non-random remodelling is indicative of microfracture repair; cortex under higher functional strain will have a higher activation frequency, greater porosity and a larger osteon population density

Remodelling Porosity; osteon population density (OPD); remodelling activation frequency (mrc )

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Table 2 Prediction of modelling and remodelling relationships under alternate loading pattern and strain magnitude scenariosn Loading pattern

Strain magnitude Higher

Frequent and diverse Occasional and typical

Lower

A: Less circular geometry and large bone mass B: Less circular geometry with relatively lower (PCA); high remodellingw and periosteal bone mass (PCA); low remodellingw and little apposition periosteal apposition C: More circular geometry but with large bone D: More circular geometry and lower bone mass (PCA); lower remodellingw and periosteal mass (PCA), low remodellingw and little apposition periosteal apposition

n

Cell A reflects a history of both variable, unusual and heavy loading. This would indicate a limb involved in both skilled and power functions. One-handed throwing, carrying or swinging (e.g. branches, rocks) would fall into this category. Cell B reflects a history of relative unloading; strain is infrequent and random with respect to orientation. Cell C reflects a history of infrequent but typical (cf. repetitive) heavy loading involving dedicated tasks which deform the element. Cell D represents the case of cyclic but comparatively light loading. wHigh or low remodelling refers to the dynamic parameter of activation frequency, rather than a static measure such as osteon population density, the magnitude of which is confounded by normal aging.

cortical bone masses in both historic metacarpals (Lazenby, 1998b, a) and in archaeological (EuroAmerican and Jomon) and Neandertal humerii (Trinkaus et al., 1994). Interestingly, in the case of the metacarpals in which analyses considered age, sex and side effects, older individuals had less circular shapes than younger individuals for both left and right sides, and males less so than females. These outcomes reflect differential loading by sex and the cumulative effect of function over time. This in turn suggests that the identification of laterality in the fossil record would be best discerned from older male limb bones. It is also noteworthy that, as Trinkaus et al. (1994) point out, the immature humerus has a circular midshaft geometry, which becomes progressively non-circular with age (the right more so, as noted). Finally, an additional factor which must be taken into account is the functional complex within which a single element participates. In the case of the ulna, for example, the diaphysis is not functionally independent of the radius, a consequence of the interosseous ligament and its attachment surfaces, a situation which will influence its geometric response to loading. The model predicts that laterality of manual behaviour will be recorded in asymmetry of bone size, shape and pattern of remodelling, through

which it will be possible to identify a dominant limb. (Again, the distinction should be made that handedness exists when a majority of the individuals within a population share limb dominance, i.e., are mostly right or left handed.) There are still many unknowns. For example, what are the effects of grip diversity and grip strength within an over-arching classification such as a power or precision grip (Marzke et al., 1992; Marzke & Wullstein, 1996; Marzke et al., 1998; Susman, 1998)? Can we speculate on the roles of the proximal (strength) and distal (skill) forelimb musculature, a distinction which factors into psychomotor models of lateralized hand use in humans (Peters, 1995)? The greatest difficulty is applying the model to past populations, conditioned by the vagaries of the fossil hominin record which preserves relatively few single, let alone paired, forelimb elements. Niewoehner (2001) has recently indicated variability in some aspects of functional hand morphology for more recent fossil hominins, but did not specifically address the question of side differences. However, comparative analysis of modern human (lateralized) vs. non-human primate (unlateralized) modelling and remodelling patterns in the forelimb should point to unique parameter combinations, Sensu Table 2, observable in isolated fossil remains which may permit characterization of aptitude.

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Some Cautionary Tales There are several caveats in developing a skeletal biological approach to predicting behavioural lateralization from morphological asymmetry. First, not all parts of a given element will equally reflect its behavioural environment. The operative aspect of mechanical loading is the strain induced by the magnitude and frequency of muscle loading with respect to an element’s tendinous, ligamentous, diaphyseal and articular architecture. All else being equal, in the most common dynamic loading scenarios of bending and torsion, strain will be greatest at the periosteal surface. Here, high strain produces new lamellar bone deposition, known as continuing periosteal apposition (Lazenby, 1990), and high rates of intracortical remodelling consistent with fatigue microdamage repair (Burr et al., 1997). Similarly, strain will be distributed differently in the longitudinal axis for bones arranged as cantilevers (e.g. metacarpals) relative to those arranged as columns (e.g. humerus). Thus, biobehavioural models must exercise care in selection of both variables to be measured as well as sites at which to measure them. Second, there is criticism of the presumption that all directional limb bone asymmetries reflect handedness. Helmkamp & Falk (1990) found that, while forelimb directional asymmetry in rhesus macaques consistently favoured the right side, patterns varied by age and sex in a manner suggestive of a more complex etiology than ‘‘handedness’’ alone. They did not explore this suggested etiology, but simply drew attention to the complexity of limb asymmetry ontogeny. Their work recalls earlier studies in the human hand reporting so-called ‘‘paradoxical’’ asymmetry (Garn et al., 1976; Plato et al., 1980), in which the right second metacarpal was larger irrespective of self-reported handedness. Here we might gain some insight from the psychology literature. Coren (1993), for example notes that studies which employ self-reporting for handedness typically record the hand used for writing, which is not necessarily the dominant hand. Also, use of grip strength measures is not consistent with handedness assessed from

multivariate questionnaires: 13% of righthanded individuals tested by Coren had a stronger left-hand grip, and over half of the left-handers tested had a greater grip strength in the right hand. Such differences may reflect hand preference for power and bimanual activities, which distributes differently from that for skilled actions which are most commonly associated with handedness, per se, (Peters, 1990). The paradoxical asymmetry is thus not paradoxical at all, and in fact is an essential element of the model I propose. Third, directional asymmetry (DA) is superimposed over an underlying and etiologically distinct fluctuating asymmetry (FA) which may either moderate or exaggerate DA in any given individual (Van Valen, 1978; Palmer, 1996, 2000). This is seldom considered in analyses of functional asymmetry in skeletal biology [but see Trinkaus et al. (1994)]. It is widely presumed that FA reflects departures from Waddington’s notion of canalized development (e.g. Palmer, 1996). We might anticipate that the magnitude of an FA effect on DA should be comparatively small (within the range of measurement error?) in an otherwise unremarkable skeletal sample, i.e., in which there are no manifest signs of developmental disturbanceFbut it is worth considering. Fourth, it should be expected that the magnitude of directional asymmetry in skeletal remains will characterize a population, not a species. This holds whether we are considering the absolute difference of right vs. left sides, or whether our interest is in the proportion of individuals with rightFor left bias. With respect to the latter, McGrew & Marchant (1994) and Marchant et al. (1995) challenged the notion that 90% dextrality is a species-specific value in humans. In a small survey of the literature, they found that the number of left-handed individuals varied between 0% and 23% cross-culturally. Values considerably higher than 10% have been suggested as the norm for humans in preagricultural contexts (Harris, 1990), reflecting the difference between those born left-handed who subsequently adaptFby choice or coercion (Peters, 1990)Fto a world considerably favouring the dextral individual. Harris (1990) notes that, among liberalized Western states now

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accepting of the sinister individual, handedness studies are consistent in reporting left handedness at 10–12% of the population. Fifth, there is a small but growing literature documenting the effects of various metabolic disease states on the bone remodelling system (Eriksen et al., 1994). Activation frequency, mineralization lag time, erosion depth (affecting osteon size, and thus osteon population density), and other aspects of remodelling can be affected, potentially mimicking behaviourally induced bone remodelling. The key to a differential diagnosis in activity vs. disease etiology will be the distribution of remodelling with respect to other relevant strain-related parameters (size and shape). For example, a localized elevation in activation frequency perpendicular to a crosssection’s Imax axis would be more interpretable as behaviourally induced fatigue microfracture repair, than the pathology of hyperparathyroidism. Finally, in applying a model such as that proposed, there is the question of phenotype. Observation and our own experience tells us that no one uses either hand to the total exclusion of the other. Referencing a large battery of performance tests for both skilled and strength/ power functions, Peters (1990) defined three phenotypes for human handedness. There are consistent right-handers, consistent left-handers, and inconsistent left-handers. Consistently sided individuals used one hand for all tasks measured, while inconsistent left-handers used the designated hand for fine/skilled tasks and the other for strength tasks. To some degree this recalls Fagot & Vauclair’s (1991) distinction between high- and low-level activities. Their review of the primate literature suggested that hand bias is evident for high-level tasks which are both novel and complex, but not for low-level tasks. (They characterize this population-level bias as manual specialization, rather than handedness, a term they reserve to denote individual preferences for hand use in low-level tasksFa usage contra pretty much everyone else.) As noted at the outset, McGrew & Marchant (1996) identify five phenotypes of non-human primate handedness, from ambilateral (no preference; level 1) to handedness of human aspect (a high degree of exclusive left or right handedness; level 5). It is

unlikely that such typologies capture the full diversity of behavioural laterality among human or non-human primates. The practical implication for the model developed here is that of sample size: one is not going to be able to draw definitive conclusions about population-level lateralization from a smattering of hand bones, a conclusion which has profound consequences for prehistoric applications. It would be possible, however, to test the model’s ability to discriminate behavioural asymmetry from skeletal parameters using neontological data from samples of modern primates, as suggested above. Conclusion It is well-established that skeletal morphology is mediated locally by its mechanical loading history against a systemic genetic and endocrinological/metabolic background. Functional adaptation to habitual activity is achieved through osseous modelling and remodelling constructing a particular combination of observable cortical and intracortical attributes. This paper presents a heuristic model which may guide experimental and comparative explication of the predicted patterns. The fundamental question remains, howeverFcan skeletal biology address the origins of a behaviour pattern putatively of great antiquity (e.g. Toth, 1985, but see Pobiner, 1999)? As a general premise the answer is yes; as a practice, it is a very tentative maybe. Success is dependent upon both the existence of an appropriate hominin skeletal record [currently sparse; e.g. Godinot & Beard, 1993)] and the accessibility of the requisite data from that record (currently unknown). While these conditions pose difficult barriers at present, the question is not ipso facto intractable to skeletal biology. Humans are lateralized, and the geometric and histomorphometric patterns specified in Table 2 can be tested in existing skeletal samples. Identifying behavioural laterality from structural asymmetries in non-human primates is differently problematic, as the forelimb is not only manipulative but is also subject to loading differentials in tripedal stance and locomotion (terrestrial and/or arboreal) (Hunt et al., 1996). Chimpanzees are arguably and adaptively the most lateralized non-human primate (McGrew

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& Marchant, 1997, 1999), and it would be of interest to explore the model in skeletal samples of chimpanzees, particularly those of known life histories (cf. Zihlman et al., 1990). To what degree is the pattern present in fossil hominins? Geometric properties are accessible in fossil materials, using non-invasive technologies such as CT and MRI scanning. Humeral diaphyseal strength, for example has been shown to exhibit marked behaviourally mediated asymmetry throughout the Upper Paleolithic and in recent pre-historic samples (summarized in Ruff, 2000). Histomorphology is another matter, though new developments in imaging technologies, along the lines of micro-CT scanning, may offer some promise. McGrew & Marchant (1997, p. 201) have characterized the evolution of behavioural laterality in a mobile organism inhabiting an essential symmetrical world as ‘‘the basic evolutionary question underlying all others’’. If so, it behooves us to develop models and methods that might allow us to explore its origins. Supported by the Natural Sciences and Engineering Research Council of Canada, OPG 0183660.

REFERENCES Akhter, M. P., Iwaniec, U. T., Covey, M. A., Cullen, D. M., Kimmel, D. B. & Recker, R. R. (2000). Genetic variations in bone density, histomorphometry, and strength in mice. Calcif. Tissue Int. 67, 337–344. Beck, C. H. M. & Barton, R. L. (1972). Deviation and laterality of hand preference in monkeys. Cortex 8, 339–363. Berm U´dez de Castro, J. M., Bromage, T. G. & FernaŁ ndez Jalvo, Y. (1988). Buccal striations on fossil human anterior teeth: evidence of handedness in the middle and early Upper Pleistocene. J. Hum. Evol. 17, 403–412. Bradshaw, J. L. & Rogers, L. J. (1993). The Evolution of Lateral Asymmetries, Language, Tool Use and Intellect. San Diego: Academic Press. Burr, D. B., Forwood, M. R. & Fyhrie, D. P. (1997). Bone microdamage and skeletal fragility in osteoporotic and stress fractures. J. Bone Miner. Res. 12, 6–15. Burr, D. B. & Martin, R. B. (1992). Mechanisms of bone adaptation to the mechanical environment. Triangle 31, 59–76. Byrne, R. & Byrne, J. (1991). Hand preferences in the skilled gathering tasks of mountain gorillas (Gorilla g. beringei). Cortex 27, 521–546. Calvin, W. (1982). Did throwing stones shape hominid brain evolution? Ethol. Sociobiol. 3, 115–124.

Corballis, M. (1989). Laterality and human evolution. Psychol. Rev. 96, 492–505. Coren, S. (1993). The Left-Hand Syndrome: The Causes and Consequences of Left-Handedness. New York: Vintage Books. Cornford, J. M. (1986). Specialized resharpening techniques and evidence of handedness. In: Excavations by CBM McBurney, (Callow, P. & Cornford, J., eds), pp. 337–362. La Cotte de St. Brelade, 1961–1978 Norwich: Geobooks. Eriksen, E., Axelrod, D. & Melson, F. (1994). Bone Histomorphometry. New York: Raven Press. Fagot, J., Drea, C. & Walen, K. (1991). Asymmetrical hand use in rhesus monkeys (Macaca mulatta) in tactually and visually regulated tasks. J. Comp. Psychol. 105, 260–268. Fagot, J. & Vauclair, J. (1991). Manual laterality in non-human primates: a distinction betwen handedness and manual specialization. Psychol. Bull. 109, 76–89. Frost, G. T. (1980). Tool behavior and the origins of laterality. J. Hum. Evol. 9, 447–459. Garn, S. M., Mayor, G. H. & Shaw, H. A. (1976). Paradoxical bilateral asymmetry in bone size and bone mass in the hand. Am. J. Phys. Anthropol. 45, 209–210. Godinot, M. & Beard, K. C. (1993). A survey of fossil primate hands. In: Hands of Primates. (Preuschoft, H. & Chivers, D. eds), pp. 335–378. Wein: Springer-Verlag. Greenfield, P. (1991). Language, tools and brain: the ontogeny and phylogeny of hierarchically organized sequential behavior. Behav. Brain Sci. 14, 531–551. Harris, L. J. (1990). Cultural influences on handedness: historical and contemporary theory and evidence. In: Left-Handedness: Behavioral Implications and Anomalies. (Coren, S. ed.), pp. 195–258. Amsterdam: Elsevier Science Publishers, North-Holland. Hazelwood, S. J., Rashid, M. M. & Rodrigo, J. J. (2001). A mechanistic model for internal bone remodelling exhibits different dynamic responses in disuse and overload. J. Biomech. 34, 299–308. Helmkamp, R. C. & Falk, D. (1990). Age-and sexassociated variations in the directional asymmetry of rhesus Macaque forelimb bones. Am. J. Phys. Anthropol. 83, 211–218. Hepper, P. G., McCartney, G. R. & Shannon, E. A. (1998). Lateralised behaviour in first trimester human foetuses. Neuropsychologia 36, 531–534. Hopkins, W., Bard, K., Jones, A. & Bales, S. (1993). Chimpanzee hand preference in throwing and infant cradling: implications for the origins of human handedness. Curr. Anthropol. 34, 786–790. Huiskes, R. (2000). If bone is the answer, then what is the question? J. Anat. 197, 145–156. Hunt, K. D., Cant, J. G. H., Gebo, D. L., Rose, M. D., Walker, S. E. & Youlatos, D. (1996). Standardized descriptions of primate locomotor and postural modes. Primates 37, 363–387. Kodama, Y., Umemura, Y., Nagasawa, S., Beamer, W. G., Donahue, L. R., Rosen, C. R., Baylink, D. J. & Farley, J. R. (2000). Excercise and mechanical loading increase periosteal bone formation and whole bone strength in C57BL/6J mice but not in C3H/Hej mice. Calcif. Tissue Int. 66, 298–306.

SKELETAL BIOLOGY AND LATERALITY

Laska, M. (1996). A study of correlates of hand preferences in squirrel monkeys (Saimiri sciureus). Primates 37, 457–465. Lazenby, R. (1998a). Second metacarpal cross-sectional geometry: rehabilitating a circular argument. Am. J. Hum. Biol. 10, 747–756. Lazenby, R. (1998b). Second metacarpal midshaft geometry in an historic cemetery sample. Am. J. Phys. Anthropol. 106, 157–167. Lazenby, R. (2001). Sex dimorphism and bilateral asymmetry: modeling developmental stability and functional adaptation (abstract). Am. J. Phys. Anthropol. 96, (Supp 32). Lazenby, R. A. (1990). Continuing periosteal apposition I: documentation, hypotheses and interpretation. Am. J. Phys. Anthropol. 82, 451–472. Lieberman, D. L. (1997). Making behavioral and phylogenetic inferences from hominid fossils: considering the developmental influence of mechanical forces. Ann. Rev. Anthropol. 26, 185–210. MacNeilage, P. F. (1991). Linguistic and manual evolution. Behav. Brain Sci. 14, 568–570. MacNeilage, P. F., Studdert-Kennedy, M. G. & Lindblom, B. (1988). Primate handedness: a foot in the door. Behav. Brain Sci. 11, 720–746. MacNeilage, P. F., Studdert-Kennedy, M. G. & Lindblom, B. (1991). Primate handedness: the other theory, the other hand, and the other attitude. Behav. Brain Sci. 14, 338–349. MacNeilage, P. N., Studdert-Kennedy, M. G. & Lindblom, B. (1987). Primate handedness reconsidered. Behav. Brain Sci. 10, 247–303. Marchant, L. F. & McGrew, W. C. (1991). Laterality of function in apes: a meta-analysis of methods. J. Hum. Evol. 21, 425–438. Marchant, L. F. & McGrew, W. C. (1996). Laterality of limb function in wild chimpanzees of Gombe National Park: comprehensive study of spontaneous activities. J. Hum. Evol. 30, 427–443. Marchant, L. F. & McGrew, W. C. (2001). Wild chimpanzees are manually unlateralized: replicative data from the Mahale Mountains, Tanzania (abstract). Am. J. Phys. Anthropol. (Supp 32), 102. Marchant, L. F., McGrew, W. C. & Eibl-Eibesfeldt, I. (1995). Is human handedness universal? Ethological analyses from three traditional cultures. Ethology 101, 239–258. Martin, R. & Burr, D. (1989). Structure, Function and Adaptation of Compact Bone. New York: Raven Press. Martin, R. B. (2000). Toward a unifying theory of bone remodeling. Bone 26, 1–6. Martin, R. B. & Burr, D. B. (1982). A hypothetical mechanism for the stimulation of osteonal remodelling by fatigue damage. J. Biomech. 15, 137–139. Martin, R. B., Burr, D. B. & Sharkey, N. A. (1998). Skeletal Tissue Mechanics. New York: Springer. Marzke, M., Toth, N., Schick, K., Reece, S., Steinberg, K., Hunt, R., Linscheid, R. & An, K. (1998). An EMG study of hand muscle recruitment during hard hammer percussion manufacture of Oldowan tools. Am. J. Phys. Anthropol. 105, 315–332. Marzke, M., Wullstein, K. & Viegas, S. (1992). Evolution of the power (‘‘squeeze’’) grip and its

137

morphological correlates in hominids. Am. J. Phys. Anthropol. 89, 283–298. Marzke, M. W. & Wullstein, K. L. (1996). Chimpanzee and human grips: a new classification with a focus on evolutionary morphology. Int. J. Primatol. 17, 117–139. McGrew, W. C. (1998). Culture in nonhuman primates? Ann. Rev. Anthropol. 27, 301–328. McGrew, W. C. & Marchant, L. F. (1994). Primate ethology: a perspective on human and nonhuman handedness. In: Handbook of Psychological Anthropology. (Bock, P., ed.), pp. 171–184. Westport, CT: Greenwood Press. McGrew, W. C. & Marchant, L. F. (1996). On which side of the apes? Ethological study of laterality of hand use. In: Great Ape Societies. (McGrew, W. C., Marchant, L. F. & Toshisada, N., eds), pp. 255–272. Cambridge: Cambridge University Press. McGrew, W. C. & Marchant, L. F. (1997). On the other hand: current issues in and meta-analysis of the behavioral laterality of hand function in nonhuman primates. Yrbk. Phys. Anthropol. 40, 201–232. McGrew, W. C. & Marchant, L. F. (1999). Laterality of hand use pays off in foraging success for wild chimpanzees. Primates 40, 509–513. Mori, S. & Burr, B. D. (1993). Increased intracortical remodelling following fatigue damage. Bone 14, 103–109. Niewoehner, W. A. (2001). Neandertal, Upper Paleolithic, and recent human hands: what are the differences? (abstract). Am. J. Phys. Anthropol. (Supp 32), 132. Palmer, A. R. (1996). Waltzing with asymmetry. Bioscience 46, 518–532. Palmer, A. R. (2000). Quasi-replication and the contract of error: lessons from sex ratios, heritabilities and fluctuating asymmetry. Annu. Rev. Ecol. Syst. 31, 441–480. Peters, M. (1990). Phenotype in normal left-handers: an understanding of phenotype is the basis for understanding mechanism and inheritance of handedness. In: Left-Handedness. Behavioral Implications and Anomalies. (Coren, S., ed.), pp. 167–192. Amsterdam: Elsevier, North-Holland. Peters, M. (1995). Handedness and its relation to other indices of cerebral lateralization. In: Brain Asymmetry. (Davidson, R. J. & Hughahl, eds.), pp. 183–214. Cambridge: MIT Press. Plato, C. C., Wood, J. L. & Norris, A. H. (1980). Bilateral asymmetry in bone measurements of the hand and lateral hand dominance. Am. J. Phys. Anthropol. 52, 27–31. Pobiner, B. L. (1999). The use of stone tools to determine handedness in hominids. Curr. Anthropol. 40, 90–92. Preuschoft, H. & Chivers, D. (1993). Hands of Primates. Wien: Springer-Verlag. Ramtani, S. & Zidi, M. I. (2001). A theoretical model of the effect of continuum damage on a bone adaptation model. J. Biomech. 34, 471–479. Robling, A. G., Burr, D. B. & Turner, C. H. (2000). Partitioning a daily mechanical stimulus into discrete loading bouts improves the osteogenic response to loading. J. Bone Miner. Res. 15, 1596–1602. Roy, T. A., Ruff, C. B. & Plato, C. C. (1994). Hand dominance and bilateral asymmetry in the structure of the second metacarpal. Am. J. Phys. Anthropol. 94, 203–211.

138

R. A. LAZENBY

Ruff, C. B. (2000). Biomechanical analyses of archaeological human skeletons. In: Biological Anthropology of the Human Skeleton. (Katzenberg, M. A. & Saunders, S. R., eds.), pp. 71–102. New York: Wiley-Liss. Spennemann, D. H. R. (1984). Handedness data on the European Neolithic. Neuropsychologia 22, 613–615. Sugiyama, Y., Fushimi, T., Sakura, O. & Matsuzawa, T. (1993). Hand preference and tool use among wild chimpanzees. Primates 34, 151–159. Susman, R. L. (1998). Hand function and tool behavior in early hominids. J. Hum. Evol. 35, 23–46. Toth, N. (1985). Archaeological evidence for preferential right-handedness in the Lower and Middle Pleistocene, and its possible implications. J. Hum. Evol. 14, 607–614. Trinkaus, E., Churchill, S. E. & Ruff, C. B. (1994). Postcranial robusticity in Homo. II: humeral bilateral asymmetry and bone plasticity. Am. J. Phys. Anthropol. 93, 1–34. Turner, C. H. (1998). Three rules for bone adaptation to mechanical stimuli. Bone 23, 399–407. Turner, C. H. (1999). Toward a mathematical description of bone biology: the principle of cellular accommodation. Calcif. Tissue Int. 65, 466–471.

Van Valen, L. (1962). A study of fluctuating asymmetry. Evolution 16, 125–142. Van Valen, L. (1978). The statistics of variation. Evolutionary Theory 4, 33–43. Ward, J. & Hopkins, W. (1993). Primate Laterality: Current Behavioral Evidence of Primate Asymmetries. New York: Springer. Watkins, B. A., Li, Y. & Seifert, M. F. (2001). Lipids as modulators of bone remodelling. Curr. Opin. Clin. Nutr. Metab. Care 4, 105–110. Westergaard, G. C. & Suomi, S. J. (1996). Hand preference for stone artefact production and tool-use by monkeys: possible implications for the evolution of right-handedness in hominids. J. Hum. Evol. 30, 291–298. Whiten, A., Goodall, J., McGrew, W. C., Nishida, T., Reynolds, V., Sugiyama, Y., Tutin, C. E. G., Wrangham, R. W. & Boesch, C. (1999). Cultures in chimpanzees. Nature 399, 682–685. Zihlman, A. L., Morbeck, M. E. & Goodall, J. (1990). Skeletal biology and life history of Gombe chimpanzees. J. Zool. 221, 37–61.