Variation in human functional eccrine gland density and its implications for the evolution of human sweating.

OBJECTIVES: We aim to test three questions regarding human eccrine sweat gland density, which is highly derived yet poorly understood. First, is variation in functional eccrine gland density ("FED") explained by childhood climate, suggesting phenotypic plasticity? Second, is variation in FED explained by genetic similarity (a proxy for "geographic ancestry"), implying divergent evolutionary pathways in this trait of ancestral populations? Third, what is the relationship between FED and sweat production? MATERIALS AND METHODS: To test questions one and two, we measured FED in 68 volunteers aged 18-39 with varied childhood climate regimes and geographic ancestries. To test question three, we compared sweat production to FED in our n = 68 sample. In addition, we examined the relationship between FED and whole-body sweat loss during cycling in warm conditions using a sample of eight heat-acclimated endurance athletes. RESULTS: Interindividual variation in six-site FED was more than twofold, ranging from 60.9 to 132.7 glands/cm2 . Variation in FED was best explained by body surface area and limb circumferences (negative associations) and poorly explained by childhood climatic conditions and genetic similarity. Pilocarpine-induced sweat production was unrelated to FED while whole-body sweat loss during cycling was significantly, though modestly, associated with FED. DISCUSSION: We hypothesize that gland-level phenotypic plasticity, rather than changes in eccrine gland density, was sufficient to permit thermal adaptation to novel environments as humans colonized the globe. Future research should measure effects of FED in dehydrated states and the relationship between FED and salt loss, and control for effects of microclimate to rule out phenotypic plasticity effects.

Archery's signature: an electromyographic analysis of the upper limb.

Non-technical summary: Bow and arrow technology plays a significant role in the recent evolutionary history of modern humans, but limitations of preservation make it challenging to identify archaeological evidence of early archery. Since bone structure can change in response to muscle force, archers of the past can potentially be identified through analysis of upper arm bones. However, there is limited research on how archery impacts upper limb musculature. This study offers initial insights into how archery impacts humeral musculature and highlights the need for additional research focused on archery's direct impact on humeral morphology. Technical summary: Humeral morphology has been used to support behaviour reconstructions of archery in past populations. However, the lack of experimental research concerning the impacts that archery has on the upper limb weakens skeletal morphological approaches. The goal of this study was to determine how archery impacts the activation of upper limb musculature. More specifically, this study tested: (a) whether the relative muscle activations are similar between arms; and (b) what muscles were activated on the dominant (draw) arm compared with the non-dominant (bow) arm. Data on upper arm muscle activation were collected bilaterally for nine archers using surface electromyography (EMG). Results show similar levels of muscle activation bilaterally with different muscles being activated in each arm. There were significantly higher integrated EMG and peak muscle activations of the biceps brachii muscles in the draw arm compared with the bow arm. In contrast, the lateral deltoid and the triceps brachii muscles had significantly higher integrated EMG and peak muscle activations on the bow arm compared with the draw arm. This work offers initial insights into how archery impacts humeral musculature and highlights the need for additional research focused on archery's direct impact on humeral morphology.

The impact of terrain on lower limb bone structure.

OBJECTIVES: Lower limb diaphyseal geometry is often used to evaluate mobility in past populations. Diaphyseal dimensions such as high shape (IX /IY ) indices generally thought to reflect high mobility may also result from walking over rough terrain. This study investigates the possible effects of terrain on lower limb diaphyseal cross-sectional geometric dimensions. MATERIALS: The sample (N = 3,195) comprises adult skeletons from Europe, Africa, North America, and Asia, spanning from around 30,000 BP to mid-twentieth century. METHODS: Femoral and tibial shape and bending/torsional strength dimensions were gathered either as part of a previous project or were generously provided by researchers. Local terrain for each site was quantified with ArcGIS mapping software using geographic coordinates and USGS elevation data, and characterized as flat, hilly, or mountainous. RESULTS: Analysis of variance shows significant differences (p < .05) in midshaft femoral and tibial shape ratio and relative bending/torsional strength among the three terrain categories, with more AP oriented diaphyseal shapes and greater relative strength in hilly and mountainous groups, even after correcting for the effect of subsistence. As expected, the impact of terrain is much more marked for hunter-gatherers and agriculturalists than for more mechanized recent populations. Interestingly, the effect of terrain is confounded in higher latitude individuals that exhibit increased ML bending strength, probably reflecting larger body breadth. DISCUSSION: This study underscores the mechanical significance of traveling over rough terrain and highlights the complex interactions of mobility, terrain, and body shape that contribute to shaping lower limb bone diaphyseal structure.

Bone functional adaptation does not erase neutral evolutionary information.

OBJECTIVES: To investigate whether diaphyseal and craniofacial variation similarly reflect neutral genetic variation among modern European and South Africans. MATERIALS AND METHODS: Diaphyseal and craniofacial data were collected on English, South European, and South African samples. The Relethford-Blangero model was used to compare predicted among-population relationships generated by limb bones relative to those generated by the crania and, further, to test whether adaptive plasticity affected these predicted relationships. Evidence of adaptive plasticity was confirmed by comparing J, an indicator of limb bone robusticity, among individuals who worked different occupations in industrializing Lisbon (Portugal) and Bologna (Italy). RESULTS: Diaphyses were more variable than were crania and more robust in individuals with physically demanding occupations-both consistent with expectations of adaptive plasticity. However, diaphyseal variation still generated among-population relationships consistent with neutral genetic predictions and Mantel tests confirmed a high, significant correlation between diaphyseal and craniofacial distance matrices. This pattern was not strongly affected by adaptive plasticity. DISCUSSION: Among-population patterns of diaphyseal variation are consistent with neutral expectations and are consistent with historical data on population composition, genetics, and migration. Furthermore, plasticity induced by Industrial-era levels of physical activity does not erase these neutral signatures. Diaphyseal variation may therefore be useful to infer neutral (presumably genetic) information across populations, and controlling for existing relationships may strengthen inferences of physical activity made when comparing limb bone structure across populations.

Can we refine body mass estimations based on femoral head breadth?

Femoral head breadth is widely used in body mass estimation in biological anthropology. Earlier research has demonstrated that reduced major axis (RMA) equations perform better than least squares (LS) equations. Although a simple RMA equation to estimate body size from femoral head breadth is sufficient in most cases, our experiments with male skeletons from European data (including late Pleistocene and Holocene skeletal samples) and the Forensic Anthropology Data Bank data (including the W. M. Bass Donated Skeletal Collection sample) show that including femoral length or anatomically estimated stature in an equation with femoral head breadth improves body mass estimation precision. More specifically, although directional bias related to body mass is not reduced within specific samples, the total estimation error range, directional bias related to stature, and temporal fluctuation in estimation error are markedly reduced. The overall body mass estimation precision of individuals representing different temporal periods and ancestry groups (e.g., African and European ancestry) is thus improved.

The effect of age and body composition on body mass estimation of males using the stature/bi-iliac method.

The stature/bi-iliac breadth method provides reasonably precise, skeletal frame size (SFS) based body mass (BM) estimations across adults as a whole. In this study, we examine the potential effects of age changes in anthropometric dimensions on the estimation accuracy of SFS-based body mass estimation. We use anthropometric data from the literature and our own skeletal data from two osteological collections to study effects of age on stature, bi-iliac breadth, body mass, and body composition, as they are major components behind body size and body size estimations. We focus on males, as relevant longitudinal data are based on male study samples. As a general rule, lean body mass (LBM) increases through adolescence and early adulthood until people are aged in their 30s or 40s, and starts to decline in the late 40s or early 50s. Fat mass (FM) tends to increase until the mid-50s and declines thereafter, but in more mobile traditional societies it may decline throughout adult life. Because BM is the sum of LBM and FM, it exhibits a curvilinear age-related pattern in all societies. Skeletal frame size is based on stature and bi-iliac breadth, and both of those dimensions are affected by age. Skeletal frame size based body mass estimation tends to increase throughout adult life in both skeletal and anthropometric samples because an age-related increase in bi-iliac breadth more than compensates for an age-related stature decline commencing in the 30s or 40s. Combined with the above-mentioned curvilinear BM change, this results in curvilinear estimation bias. However, for simulations involving low to moderate percent body fat, the stature/bi-iliac method works well in predicting body mass in younger and middle-aged adults. Such conditions are likely to have applied to most human paleontological and archaeological samples.

Correction: Trabecular bone in the calcaneus of runners.

[This corrects the article DOI: 10.1371/journal.pone.0188200.].

Trabecular bone in the calcaneus of runners.

Trabecular bone of the human calcaneus is subjected to extreme repetitive forces during endurance running and should adapt in response to this strain. To assess possible bone functional adaptation in the posterior region of the calcaneus, we recruited forefoot-striking runners (n = 6), rearfoot-striking runners (n = 6), and non-runners (n = 6), all males aged 20-41 for this institutionally approved study. Foot strike pattern was confirmed for each runner using a motion capture system. We obtained high resolution peripheral computed tomography scans of the posterior calcaneus for both runners and non-runners. No statistically significant differences were found between runners and nonrunners or forefoot strikers and rearfoot strikers. Mean trabecular thickness and mineral density were greatest in forefoot runners with strong effect sizes (<0.80). Trabecular thickness was positively correlated with weekly running distance (r2 = 0.417, p<0.05) and years running (r2 = 0.339, p<0.05) and negatively correlated with age at onset of running (r2 = 0.515, p<0.01) Trabecular thickness, mineral density and bone volume ratio of nonrunners were highly correlated with body mass (r2 = 0.824, p<0.05) and nonrunners were significantly heavier than runners (p<0.05). Adjusting for body mass revealed significantly thicker trabeculae in the posterior calcaneus of forefoot strikers, likely an artifact of greater running volume and earlier onset of running in this subgroup; thus, individuals with the greatest summative loading stimulus had, after body mass adjustment, the thickest trabeculae. Further study with larger sample sizes is necessary to elucidate the role of footstrike on calcaneal trabecular structure. To our knowledge, intraspecific body mass correlations with measures of trabecular robusticity have not been reported elsewhere. We hypothesize that early adoption of running and years of sustained moderate volume running stimulate bone modeling in trabeculae of the posterior calcaneus.

The impact of subsistence changes on humeral bilateral asymmetry in Terminal Pleistocene and Holocene Europe.

Analyses of upper limb bone bilateral asymmetry can shed light on manipulative behavior, sexual division of labor, and the effects of economic transitions on skeletal morphology. We compared the maximum (absolute) and directional asymmetry in humeral length, articular breadth, and cross-sectional diaphyseal geometry (CSG) in a large (n > 1200) European sample distributed among 11 archaeological periods from the Early Upper Paleolithic through the 20(th) century. Asymmetry in length and articular breadth is right-biased, but relatively small and fairly constant between temporal periods. Females show more asymmetry in length than males. This suggests a low impact of behavioral changes on asymmetry in length and breadth, but strong genetic control with probable sex linkage of asymmetry in length. Asymmetry in CSG properties is much more marked than in length and articular breadth, with sex-specific variation. In males, a major decline in asymmetry occurs between the Upper Paleolithic and Mesolithic. There is no further decline in asymmetry between the Mesolithic and Neolithic in males and only limited variation during the Holocene. In females, a major decline occurs between the Mesolithic and Neolithic, with resulting average directional asymmetry close to zero. Asymmetry among females continues to be very low in the subsequent Copper and Bronze Ages, but increases again in the Iron Age. Changes in female asymmetry result in an increase of sexual dimorphism during the early agricultural periods, followed by a decrease in the Iron Age. Sexual dimorphism again slightly declines after the Late Medieval. Our results indicate that changes in manipulative behavior were sex-specific with a probable higher impact of changes in hunting behavior on male asymmetry (e.g., shift from unimanual throwing to use of the bow-and-arrow) and food grain processing in females, specifically, use of two-handed saddle querns in the early agricultural periods and one-handed rotary querns in later agricultural periods.

Gradual decline in mobility with the adoption of food production in Europe.

Increased sedentism during the Holocene has been proposed as a major cause of decreased skeletal robusticity (bone strength relative to body size) in modern humans. When and why declining mobility occurred has profound implications for reconstructing past population history and health, but it has proven difficult to characterize archaeologically. In this study we evaluate temporal trends in relative strength of the upper and lower limb bones in a sample of 1,842 individuals from across Europe extending from the Upper Paleolithic [11,000-33,000 calibrated years (Cal y) B.P.] through the 20th century. A large decline in anteroposterior bending strength of the femur and tibia occurs beginning in the Neolithic (∼ 4,000-7,000 Cal y B.P.) and continues through the Iron/Roman period (∼ 2,000 Cal y B.P.), with no subsequent directional change. Declines in mediolateral bending strength of the lower limb bones and strength of the humerus are much smaller and less consistent. Together these results strongly implicate declining mobility as the specific behavioral factor underlying these changes. Mobility levels first declined at the onset of food production, but the transition to a more sedentary lifestyle was gradual, extending through later agricultural intensification. This finding only partially supports models that tie increased sedentism to a relatively abrupt Neolithic Demographic Transition in Europe. The lack of subsequent change in relative bone strength indicates that increasing mechanization and urbanization had only relatively small effects on skeletal robusticity, suggesting that moderate changes in activity level are not sufficient stimuli for bone deposition or resorption.

Tall guys and fat ladies: Grimaldi's Upper Paleolithic burials and figurines in an historical perspective.

The importance of the Grimaldi complex of caves and rock shelters is twofold: scientific and historical. Scientifically, it is one of the major Upper Paleolithic sites, considering the variety of mobiliary and parietal art, the number of single and multiple burials and associated grave goods, and the abundant lithic and fauna remains. Historically, the documentation of activity that took place in this site starting from the second half of the 19 th century and the studies carried out on the materials that have been recovered in the decades between 1870s-1910s, provide instructive examples of methods and goals of Paleolithic archeology and anthropology of the epoch. This paper combines the scientific and the historic interest of the site through a chronicle of the events that took place during the period of the most sensational discoveries, i.e. beginning with the identification in 1872 of the first Upper Paleolithic burial and ending with the results of the excavations carried out in 1901 at Grotte des Enfants published in four volumes a few years later. The paper discusses early interpretations and modern views on the different findings and documents changes in perspectives and goals of paleoanthropological research in over a century, raising some of the major issues of contemporary Upper Paleolithic studies.

The timing and spatiotemporal patterning of Neanderthal disappearance.

The timing of Neanderthal disappearance and the extent to which they overlapped with the earliest incoming anatomically modern humans (AMHs) in Eurasia are key questions in palaeoanthropology. Determining the spatiotemporal relationship between the two populations is crucial if we are to understand the processes, timing and reasons leading to the disappearance of Neanderthals and the likelihood of cultural and genetic exchange. Serious technical challenges, however, have hindered reliable dating of the period, as the radiocarbon method reaches its limit at ∼50,000 years ago. Here we apply improved accelerator mass spectrometry (14)C techniques to construct robust chronologies from 40 key Mousterian and Neanderthal archaeological sites, ranging from Russia to Spain. Bayesian age modelling was used to generate probability distribution functions to determine the latest appearance date. We show that the Mousterian ended by 41,030-39,260 calibrated years bp (at 95.4% probability) across Europe. We also demonstrate that succeeding 'transitional' archaeological industries, one of which has been linked with Neanderthals (Châtelperronian), end at a similar time. Our data indicate that the disappearance of Neanderthals occurred at different times in different regions. Comparing the data with results obtained from the earliest dated AMH sites in Europe, associated with the Uluzzian technocomplex, allows us to quantify the temporal overlap between the two human groups. The results reveal a significant overlap of 2,600-5,400 years (at 95.4% probability). This has important implications for models seeking to explain the cultural, technological and biological elements involved in the replacement of Neanderthals by AMHs. A mosaic of populations in Europe during the Middle to Upper Palaeolithic transition suggests that there was ample time for the transmission of cultural and symbolic behaviours, as well as possible genetic exchanges, between the two groups.

Stature and body mass estimation from skeletal remains in the European Holocene.

Techniques that are currently available for estimating stature and body mass from European skeletal remains are all subject to various limitations. Here, we develop new prediction equations based on large skeletal samples representing much of the continent and temporal periods ranging from the Mesolithic to the 20th century. Anatomical reconstruction of stature is carried out for 501 individuals, and body mass is calculated from estimated stature and biiliac breadth in 1,145 individuals. These data are used to derive stature estimation formulae based on long bone lengths and body mass estimation formulae based on femoral head breadth. Prediction accuracy is superior to that of previously available methods. No systematic geographic or temporal variation in prediction errors is apparent, except in tibial estimation of stature, where northern and southern European formulae are necessary because of the presence of relatively longer tibiae in southern samples. Thus, these equations should bebroadly applicable to European Holocene skeletal samples.

Hunters of the Ice Age: The biology of Upper Paleolithic people.

The Upper Paleolithic represents both the phase during which anatomically modern humans appeared and the climax of hunter-gatherer cultures. Demographic expansion into new areas that took place during this period and the diffusion of burial practices resulted in an unprecedented number of well-preserved human remains. This skeletal record, dovetailed with archeological, environmental, and chronological contexts, allows testing of hypotheses regarding biological processes at the population level. In this article, we review key studies about the biology of Upper Paleolithic populations based primarily on European samples, but integrating information from other areas of the Old World whenever possible. Data about cranial morphology, skeletal robusticity, stature, body proportions, health status, diet, physical activity, and genetics are evaluated in Late Pleistocene climatic and cultural contexts. Various lines of evidence delineate the Last Glacial Maximum (LGM) as a critical phase in the biological and cultural evolution of Upper Paleolithic populations. The LGM, a long phase of climatic deterioration culminating around 20,000 BP, had a profound impact on the environment, lifestyle, and behavior of human groups. Some of these effects are recorded in aspects of skeletal biology of these populations. Groups living before and after the LGM, Early Upper Paleolithic (EUP) and Late Upper Paleolithic (LUP), respectively, differ significantly in craniofacial dimensions, stature, robusticity, and body proportions. While paleopathological and stable isotope data suggest good health status throughout the Upper Paleolithic, some stress indicators point to a slight decline in quality of life in LUP populations. The intriguing and unexpected incidence of individuals affected by congenital disorders probably indicates selective burial practices for these abnormal individuals. While some of the changes observed can be explained through models of biocultural or environmental adaptation (e.g., decreased lower limb robusticity following decreased mobility; changes in body proportions along with climatic change), others are more difficult to explain. For instance, craniodental and upper limb robusticity show complex evolutionary patterns that do not always correspond to expectations. In addition, the marked decline in stature and the mosaic nature of change in body proportions still await clarifications. These issues, as well as systematic analysis of specific pathologies and possible relationships between genetic lineages, population movements and cultural complexes, should be among the goals of future research.

Biomechanical approach to the reconstruction of activity patterns in Neolithic Western Liguria, Italy.

This paper investigates the changes in upper and lower limb robusticity and activity patterns that accompanied the transition to a Neolithic subsistence in western Liguria (Italy). Diaphyseal robusticity measures were obtained from cross-sectional geometric properties of the humerus and femur in a sample of 16 individuals (eight males and eight females) dated to about 6,000-5,500 BP. Comparisons with European Late Upper Paleolithics (LUP) indicate increased humeral robusticity in Neolithic Ligurian (NEOL) males, but not in females, with a significant reduction in right-left differences in both sexes. Sexual dimorphism in robusticity increases in upper and lower limb bones. Regarding the femur, while all female indicators of bending strength decrease steadily through time, values for NEOL males approach those of LUP. This suggests high, and unexpected, levels of mechanical stress for NEOL males, probably reflecting the effects of the mountainous terrain on lower limb remodeling. Comparisons between NEOL males and a small sample of LUP hunter-gatherers from the same area support this interpretation. In conclusion, cross-sectional geometry data indicate that the transition to Neolithic economies in western Liguria did not reduce functional requirements in males, and suggest a marked sexual division of labor involving a more symmetrical use of the upper limb, and different male-female levels of locomotory stress. When articulated with archaeological, faunal, paleopathological, and ethnographic evidence, these results support the hypothesis of repetitive, bimanual use of axes tied to pastoral activities in males, and of more sedentary tasks linked to agriculture in females.

Body size, body proportions, and mobility in the Tyrolean "Iceman".

Body mass and structural properties of the femoral and tibial midshafts of the "Iceman," a late Neolithic (5,200 BP) mummy found in the Tyrolean Alps, are determined from computed tomographic scans of his body, and compared with those of a sample of 139 males spanning the European early Upper Paleolithic through the Bronze Age. Two methods, based on femoral head breadth and estimated stature/bi-iliac (pelvic) breath, yield identical body-mass estimates of 61 kg for the Iceman. In combination with his estimated stature of 158 cm, this indicates a short but relatively wide or stocky body compared to our total sample. His femur is about average in strength compared to our late Neolithic (Eneolithic) males, but his tibia is well above average. His femur also shows adaptations for his relatively broad body (mediolateral strengthening), while his tibia shows adaptations for high mobility over rough terrain (anteroposterior strengthening). In many respects, his tibia more closely resembles those of European Mesolithic rather than Neolithic males, which may reflect a more mobile lifestyle than was characteristic of most Neolithic males, perhaps related to a pastoral subsistence strategy. There are indications that mobility in general declined between the European Mesolithic and late Neolithic, and that body size and shape may have become more variable throughout the continent following the Upper Paleolithic.

Who's afraid of the big bad Wolff?: "Wolff's law" and bone functional adaptation.

"Wolff's law" is a concept that has sometimes been misrepresented, and frequently misunderstood, in the anthropological literature. Although it was originally formulated in a strict mathematical sense that has since been discredited, the more general concept of "bone functional adaptation" to mechanical loading (a designation that should probably replace "Wolff's law") is supported by much experimental and observational data. Objections raised to earlier studies of bone functional adaptation have largely been addressed by more recent and better-controlled studies. While the bone morphological response to mechanical strains is reduced in adults relative to juveniles, claims that adult morphology reflects only juvenile loadings are greatly exaggerated. Similarly, while there are important genetic influences on bone development and on the nature of bone's response to mechanical loading, variations in loadings themselves are equally if not more important in determining variations in morphology, especially in comparisons between closely related individuals or species. The correspondence between bone strain patterns and bone structure is variable, depending on skeletal location and the general mechanical environment (e.g., distal vs. proximal limb elements, cursorial vs. noncursorial animals), so that mechanical/behavioral inferences based on structure alone should be limited to corresponding skeletal regions and animals with similar basic mechanical designs. Within such comparisons, traditional geometric parameters (such as second moments of area and section moduli) still give the best available estimates of in vivo mechanical competence. Thus, when employed with appropriate caution, these features may be used to reconstruct mechanical loadings and behavioral differences within and between past populations.

Mobility in Upper Paleolithic and Mesolithic Europe: evidence from the lower limb.

A growing body of archeological evidence suggests that the dramatic climatic events of the Last Glacial Maximum in Europe triggered important changes in foraging behavior, involving a significant decrease in mobility. In general, changes in mobility alter patterns of bending of the midshaft femur and tibia, resulting in changes in diaphyseal robusticity and shape. This relationship between levels of mobility and lower limb diaphyseal structure was used to test the hypothesized decrease in mobility. Cross-sectional geometric data were obtained for 81 Upper Paleolithic and Mesolithic European femora and tibiae. The sample was divided into three time periods: Early Upper Paleolithic (EUP), Late Upper Paleolithic (LUP), and Mesolithic (Meso). In addition, because decreased mobility often results in changes in sex roles, males and females were analyzed separately. All indicators of bending strength decrease steadily through time, although few of the changes reach statistical significance. There is, however, a highly significant change in midshaft femur shape, with LUP and Meso groups more circular in cross-section than the EUP sample, supporting archeologically based predictions of decreased mobility. Sexual dimorphism levels in diaphyseal strength remain low throughout the three time periods, suggesting a departure in Upper Paleolithic and Mesolithic foragers away from the pattern of division of labor by sex observed in modern hunter-gatherers. Results confirm that the onset of the Last Glacial Maximum represents a crucial stage in Late Pleistocene human evolution, and signals the appearance of some of the behavioral adaptations that are usually associated with the Neolithic, such as sedentism.