Thoracic skeletal morphology and high-altitude hypoxia in Andean prehistory

Living humans from the highland Andes exhibit antero-posteriorly and medio-laterally enlarged chests in response to high-altitude hypoxia. This study hypothesizes that morphological responses to high-altitude hypoxia should also be evident in pre-Contact Andean groups. Thoracic skeletal morphology in four groups of human skeletons (N = 347) are compared: two groups from coastal regions (Ancón, Peru, n = 79 and Arica, Chile, n = 123) and two groups from high altitudes (San Pedro de Atacama, Chile, n = 102 and Machu Picchu and Cuzco, Peru, n = 43). Osteometric variables that represent proportions of chest width and depth include sternal and clavicular lengths and breadths and rib length, curvature, and area. Each variable was measured relative to body size, transformed into logarithmic indices, and compared across sex-specific groups using ANOVA and Tukey multiple comparison tests. Atacama highlanders have the largest sternal and clavicular proportions and ribs with the greatest area and least amount of curvature, features that suggest an antero-posteriorly deep and mediolaterally wide thoracic skeleton. Ancón lowlanders exhibit proportions indicating narrower and shallower chests. Machu Picchu and Cuzco males cluster with the other highland group in rib curvature and area at the superior levels of the thorax, whereas chest proportions in Machu Picchu and Cuzco females resemble those of lowlanders. The variation in Machu Picchu and Cuzco males and females is interpreted as the result of population migrations. The presence of morphological traits indicative of enlarged chests in some highland individuals suggests that high-altitude hypoxia was an environmental stressor shaping the biology of highland Andean groups during the pre-Contact period.     

Geographic variation in body form of prehistoric Jomon males in the Japanese archipelago: Its ecogeographic implications

Diversity of human body size and shape is often biogeographically interpreted in association with climatic conditions. According to Bergmann's and Allen's rules, populations in regions with a cold climate are expected to display an overall larger body and smaller/shorter extremities than those in warm/hot environments. In the present study, the skeletal limb size and proportions of prehistoric Jomon hunter‐gatherers, who extensively inhabited subarctic to subtropical areas in the ancient Japanese archipelago, were examined to evaluate whether or not the inter‐regional differences follow such ecogeographic patterns. Results showed that the Jomon intralimb proportions including relative distal limb lengths did not differ significantly among five regions from northern Hokkaido to the southern Okinawa Islands. This suggests a limited co‐variability of the intralimb proportions with climate, particularly within genealogically close populations. In contrast, femoral head breadth (associated with body mass) and skeletal limb lengths were found to be significantly and positively correlated with latitude, suggesting a north‐south geographical cline in the body size. This gradient therefore comprehensively conforms to Bergmann's rule, and may stem from multiple potential factors such as phylogenetic constraints, microevolutionary adaptation to climatic/geographic conditions during the Jomon period, and nutritional and physiological response during ontogeny. Specifically, the remarkably small‐bodied Jomon in the Okinawa Islands can also be explained as an adjustment to subtropical and insular environments. Thus, the findings obtained in this study indicate that Jomon people, while maintaining fundamental intralimb proportions, displayed body size variation in concert with ambient surroundings. Am J Phys Anthropol, 2012. © 2012 Wiley Periodicals, Inc.     

Morphological integration versus ecological plasticity in the avian pelvic limb skeleton

Understanding patterns and distributions of morphological traits is essential for discerning underpinning processes of morphological variation. We report on the variation in the avian pelvic limb skeleton. Length and width variables were measured in the skeletons of 236 avian species in order to examine the importance of body mass, ecological factors, phylogeny and integration in the formation of specific hindlimb morphology. Scaling relationships with body mass were analyzed across Aves and in individual avian subclades. Principal component analysis and multiple regressions were performed to examine the relationship between morphology, ecology, and phylogeny. Finally, the occurrence of within‐limb morphological integration was tested by partial correlation analysis of the residuals from element lengths vs. body mass and correlation analysis of avian hindlimb proportions. Body mass is the greatest contributor to variation, and it strongly influences variation in avian skeletal lengths. Lengthening of the leg typically comes from disproportionate increases in tibiotarsal and tarsometatarsal length. Partial correlation analysis showed that only these two elements are distinctly integrated consistently across all bird taxa, whereas relation of femur and third toe to other limb elements displays no clear pattern. Hence, morphological integration of all elements is not a prerequisite for limb design, and variation between taxa is mainly to be found in femoral and digital length. Furthermore, variation in tibiotarsal relative length is much lower than in other elements likely due to geometric constrains. Clear ecological adaptations are obscured by multifunctionality of the avian hindlimb, and phylogeny significantly constrains the morphology. Finally, when looking at relative lengths segmented limbs meet the requirements of many‐to‐one‐mapping of phenotype to functional property, in line with a common concept of evolvability of function and morphology. J. Morphol., 2013. © 2013 Wiley Periodicals, Inc.     

Early hominin limb proportions

Recent analyses and new fossil discoveries suggest that the evolution of hominin limb length proportions is complex, with evolutionary reversals and a decoupling of proportions within and between limbs. This study takes into account intraspecific variation to test whether or not the limb proportions of four early hominin associated skeletons (AL 288-1, OH 62, BOU-VP-12/1, and KNM-WT 15000) can be considered to be significantly different from one another. Exact randomization methods were used to compare the differences between pairs of fossil skeletons to the differences observed between all possible pairs of individuals within large samples of Gorilla gorilla, Pan troglodytes, Pongo pygmaeus, and Homo sapiens. Although the difference in humerofemoral proportions between OH 62 and AL 288-1 does not exceed variation in the extant samples, it is rare. When humerofemoral midshaft circumferences are compared, the difference between OH 62 and AL 288-1 is fairly common in extant species. This, in combination with error associated with the limb lengths estimates, suggests that it may be premature to consider H. (or Australopithecus) habilis as having more apelike limb proportions than those in A. afarensis. The humerofemoral index of BOU-VP-12/1 differs significantly from both OH 62 and AL 288-1, but not from KNM-WT 15000. Published length estimates, if correct, suggest that the relative forearm length of BOU-VP-12/1 is unique among hominins, exceeding those of the African apes and resembling the proportions in Pongo.Evidence that A. afarensis exhibited a less apelike upper:lower limb design than A. africanus (and possibly H. habilis) suggests that, if A. afarensis is broadly ancestral to A. africanus, the latter did not simply inherit primitive morphology associated with arboreality, but is derived in this regard. The fact that the limb proportions of OH 62 (and possibly KNM-ER 3735) are no more human like than those of AL 288-1 underscores the primitive body design of H. habilis.     

Birth month associations with height,head circumference,and limb lengths among peruvian children

Associations between season of birth and body size, morbidity, and mortality have been widely documented, but it is unclear whether different parts of the body are differentially sensitive, and if such effects persist through childhood. This may be relevant to understanding the relationship between early life environment and body size and proportions. We investigated associations between birth month and anthropometry among rural highland (n = 162) and urban lowland (n = 184) Peruvian children aged 6 months to 8 years. Stature; head‐trunk height; total limb, ulna, tibia, hand, and foot lengths; head circumference; and limb measurements relative to head‐trunk height were converted to internal age‐sex‐specific z scores. Lowland and highland datasets were then analyzed separately for birth month trends using cosinor analysis, as urban conditions likely provide a more consistent environment compared with anticipated seasonal variation in the rural highlands. Among highland children birth month associations were significant most strongly for tibia length, followed by total lower limb length and stature, with a peak among November births. Results were not significant for other measurements or among lowland children. The results suggest a prenatal or early postnatal environmental effect on growth that is more marked in limb lengths than trunk length or head size, and persists across the age range studied. We suggest that the results may reflect seasonal variation in maternal nutrition in the rural highlands, but other hypotheses such as variation in maternal vitamin D levels cannot be excluded. Am J Phys Anthropol 154:115–124, 2014. © 2014 The Authors. American Journal of Physical Anthropology Published by Wiley Periodicals, Inc.     

Ontogenetic and individual variation in size, shape and speed in the Australian agamid lizard Amphibolurus nuchalis

The present study investigates relationships among size, shape and speed in the Australian agamid lizard Amphibolurus nuchalis . Maximal running speed, body mass, snout-vent length, tail length, fore- and hind limb spans and thigh muscle mass were measured in 68 field-fresh individuals spanning the entire ontogenetic size range (1.3 48 g). Relative lengths of both foreand hind limbs decrease with increasing body mass (= negative allometry), whereas relative tail length and thigh muscle mass increase with body mass (= positive allometry). Repeatable and significant differences in maximal running speed exist among individuals. Maximal running speed scales as (body mass)^0.161, and 59% of the variation in maximal speed was related to body mass. Based on the results of the present and previous studies, data on scaling of body proportions alone appear inadequate to infer scaling relationships of functional characters such as top speed.
Surprisingly, individual variation in maximal speed is not related to individual variation in shape (relative limb, tail and body lengths). These components of overall shape are not independent; individuals tended to have either relatively long or relatively short limbs, tails and bodies for their body mass. Even the significant difference in multivariate shape between adult males and females has no measurable consequences for maximal speed. Speeds of field-fresh animals did not vary on a seasonal basis, and eight weeks of captivity had no effect on maximal running speeds. Gravid females and long-term (obese) captive lizards were both approximately 12% slower than field-fresh lizards.     

Developmental variation in ecogeographic body proportions

While ecogeographic variation in adult human body proportions has been extensively explored, relatively less attention has been paid to the effect of Bergmann's and Allen's rules on human body shape during growth. The relationship between climate and immature body form is particularly important, as immature mortality is high, mechanisms of thermoregulation differ between young and mature humans, and immature body proportions fluctuate due to basic parameters of growth. This study explores changes in immature ecogeographic body proportions via analyses of anthropometric data from children included in Eveleth and Tanner's (1976) Worldwide Variation in Human Growth, as well as limb proportion measurements in eight different skeletal samples. Moderate to strong correlations exist between climatic data and immature stature, weight, BMI, and bi-iliac breadth; these relationships are as strong, if not stronger, in immature individuals as they are in adults. Correlations between climate and trunk height relative to stature are weak or nonexistent. Altitude also has significant effects on immature body form, with children from higher altitudes displaying smaller statures and lower body weights. Brachial and crural indices remain constant over the course of growth and display consistent, moderate correlations with latitude across ontogeny that are just as high as those detected in adults. The results of this study suggest that while some features of immature body form, such as bi-iliac breadth and intralimb indices, are strongly dictated by ecogeographic principles, other characteristics of immature body proportions are influenced by intrinsic and extrinsic factors such as nutrition and basic constraints of growth.     

Crab louse infestation in pre-Columbian America

Until now, Pthirus pubis infestation in ancient human populations had only been recorded in the Old World. We found crab lice on South American mummified bodies from the Atacama Desert region. Crab louse eggs were found attached to the pubic hairs of a 2,000-yr-old Chilean mummy. Well-preserved adults were found in sediment and clothing from a Peruvian mummy dated 1,000 yr ago. Paleoparasitological evidence expands the knowledge of the distribution of this ectoparasite in ancient populations. As with many other parasites, pubic lice recorded in Andean populations show the antiquity of this parasite in the New World. It is likely that P. pubis entered the continent with early human migration to the New World.     

Thoracic morphology in Near Eastern Neandertals and early modern humans compared with recent modern humans from high and low altitudes

Paleoanthropologists have long noted the unique "hyper-barrel-shaped" Neandertal thorax as inferred from fragmentary ribs, clavicles, and sterna. Yet scholars disagree whether the Neandertal thorax represents an adaptation to cold climates or elevated activity levels. Given the difficulties of reconstructing overall chest shape from isolated and fragmentary thoracic skeletal elements, it is worthwhile comparing Neandertals and contemporaneous early modern human fossils from the same geographic region to recent modern human skeletons that are known to have enlarged chests. This study compares thoracic skeletal morphology in two Near Eastern Neandertals (Tabūn C1 and Shanidar 3) and two early modern humans from the same region (Skhūl IV and V) with four samples of recent modern human skeletons from the Andes (n=347): two coastal groups and two groups from high altitudes. The two highland groups, similar to their living descendants, exhibit morphological evidence of anteroposteriorly deep and mediolaterally wide chests as part of respiratory adaptations to high-altitude hypoxia. I calculated the percentage of deviation of each Neandertal and early modern human fossil from the means of the four recent modern human samples for clavicle and rib lengths and curvatures. Shanidar 3 and Tabūn C1 exhibit ribs that are slightly larger and less curved than the Andean samples, indicating slightly larger thoracic skeletons than modern humans who are known to have enlarged chests in response to increased respiratory demands. Skhūl IV and V have significantly shorter ribs with greater curvature suggesting especially narrow thoracic skeletons. Comparisons with Andean populations suggest that the enlarged thoraces of Neandertals may reflect high activity levels, although results from this study do not exclude cold adaptation as an explanatory factor.     

Bio-cultural effects in medieval populations

Male skeletons from medieval archaeological sites are analysed to assess differences in stature and body proportions related to the bio-cultural environment, such as social, economic, and health factors. Environmental factors, such as climate change in the course of the Middle Ages, did not have statistically significant effect on body proportions in these samples. The results show a relationship between bio-cultural factors and physique in the analysed populations that indicate stunted growth in height and weight in a leprosarium population with a low socio-economic and health status. A high-status monastic population is characterised by a stocky build, i.e., increased weight for height and relatively shorter limbs, while a medieval parish population has a linear build, i.e., relatively long limbs for height and decreased weight for height. These characteristics, relative weight for height and relative limb length, changed during the course of the Middle Ages, as did stature.     

Functional and ecological significance of relative growth in Alligator

Allometric coefficients are calculated for 27 cranial and 39 postcranial measurements of a growth series of Alligator mississipiensis that spans a size range of an order of magnitude. Developmental patterns are quite-well canalized, as expressed in coefficients of variation of 8 to 10 for isometric variables. A multivariate expression of allometry is discovered using principal components analysis. A number of allometric coefficients have expression in known aspects of the life history of Alligator. Negative allometry of limb lengths and limb proportions shows an ontogenetic decrease in importance of the limbs throughout life, and observations show large animals to be more dependent on water than small ones. Isometry of skull length with respect to body length represents an adaptation to ever-increasing size of prey items as body size increases. Positive allometry of snout length and size of the upper temporal fenestrae finds parallel in the structure of the highly aquatic gavial.     

Variation in the growth and development of the hind limbs in frogs of the genus Telmatobius (Anura: Telmatobiidae)

There are remarkable interspecific differences in the sizes of the larvae of Andean frogs of the genus Telmatobius. This size variation seems to be associated with the duration of the larval stage and may affect the hind-limb morphology in Telmatobius. Larval, juvenile, and adult Telmatobius rubigo and T. oxycephalus were examined to determine the variation in relative sizes of hind-limb elements, their growth patterns during postmetamorphic life, and skeletal ontogeny. The results showed that the proportionately shorter hind limbs of T. rubigo relative to those of T. oxycephalus are associated with the protracted development and ossification of hind limbs during the prolonged larval life of T. rubigo. Postmetamorphically, the hind limbs grew faster than the body in juveniles of both species in contrast to the relative growth rates of the hind limbs and bodies of the adults. The growth phase of juvenile T. rubigo seems shorter than that of juvenile T. oxycephalus; possibly, this heightens the difference in the relative lengths of hind limbs after metamorphosis. Temperature affects the effects of thyroid hormone on growth and development, and T. rubigo lives at much higher, colder elevations than does T. oxycephalus. It is not clear whether the developmental differences described here are plastic (i.e., environmentally induced) or genetically fixed in each species.     

中国现代人群上、下肢形态与环境温度的相关性分析

观察中国不同区域内现代人群四肢形态变化是否与艾伦法则相一致。本文搜集中国各区域102处地点的现代人群上、下肢测量性状中17项指标,探讨其与温度(年平均温度、年最高温度、年最低温度和气温年较差)间的线性关系。结果表明,随着环境温度降低,中国现代人的上肢相对长度逐渐变短,前臂和手则逐渐增粗;下肢(下肢全长、大腿长和小腿长)逐渐变长,且下肢相对长度同样渐增。手长、手宽、上臂围和前臂围与气温年较差呈正相关,而身高上肢长指数与气温年较差呈负相关;下肢全长、大腿长、足长和小腿围与气温年较差呈正相关。环境温度作为一项选择性压力,作用于上肢发育或形态塑造过程的显著程度上要高于下肢。中国现代人群的四肢形态变化规律并不完全符合艾伦法则,可能与遗传、地理环境、功能性需求、生存策略和营养等因素共同影响现代人群的四肢发育密切相关。     

Artificial selection sheds light on developmental mechanisms of limb elongation

Species diversity in limb lengths and proportions is thought to have evolved adaptively in the context of locomotor and habitat specialization, but the heritable cellular processes that drove this evolution within species are poorly understood. In this study, we take a novel “micro‐evo‐devo” approach, using artificial selection on relative limb length to amplify phenotypic variation in a population of mice, known as Longshanks, to examine the cellular mechanisms of postnatal limb development that contribute to intraspecific limb length variation. Cross‐sectional growth data indicate that differences in bone length between Longshanks and random‐bred controls are not due to prolonged growth, but to accelerated growth rates. Histomorphometric and cell proliferation assays on proximal tibial growth plates show that Longshanks’ increased limb bone length is associated with an increased number of proliferative chondrocytes. In contrast, we find no differences in other growth plate cellular features known to underlie interspecific differences in limb bone size and shape, such as the rates of chondrocyte proliferation or the size and number of hypertrophic cells in the growth plate. These data suggest that small differences among individuals in the number of proliferating chondrocytes are a potentially important determinant of selectable intraspecific variation in individual limb bone lengths, independent of body size.     

Altitude,heredity and body proportions in northern Chile

Recent studies of the effects of hypoxia on human growth and adult size have focused mainly on the variability of single measurements. In this paper we explore changes with altitude and ethnicity (Spanish-Aymara ancestry) in body proportions of permanent residents of an altitudinal gradient (0–4000 meters) in northern Chile. Body proportion or shape is assessed by anthropometric indices and principal components of 14 bone measurements. Ethnicity independent of altitude had its major effect on proportions and a lesser effect on size. Aymara had larger relative sitting heights, broader builds and prominent facial development as compared to non-Aymara (Spanish). Altitude also affected head and chest proportions during growth. On the whole, the effects of altitude and Aymara ancestry on the measurements and indices were independent (not necessarily of similar direction or magnitude), in spite of a correlation of ethnicity and altitude in Andean populations.     

Body size and host range co-determine the altitudinal distribution of Neotropical tephritid flies

Aim We addressed the following questions: (1) Does tephritid body size tend to increase in species found at higher elevations, as predicted by Bergmann's rule? (2) Do tephritids conform to Rapoport's rule, so that species found at higher elevations tend to have broader altitudinal ranges? (3) More generally, how do body size and host range jointly affect the patterns of altitudinal distribution among Neotropical tephritid flies? Location The Mantiqueira mountain range, south‐eastern Brazil, at sites ranging from c. 700 to 2500 m a.s.l. Methods At each site we collected flower heads of all Asteraceae species to rear out endophagous immatures (from January to June in 1998 and 1999). We used structural equation models (SEM) to evaluate jointly the relationships between body size, host range and altitudinal distribution (range and mid‐point). Results Neotropical tephritid body size showed a negative relationship with altitudinal distribution. SE modelling showed no significant direct effect of body size on altitudinal range; however, it had significant indirect negative effects through host range and altitudinal mid‐point. The SE model was a good predictor of observed correlations and accounted for 84% of the variation in tephritid altitudinal range. Main conclusions The altitudinal range of flower‐head‐feeding tephritids is related to host range and is indirectly affected by body size via host range and altitudinal mid‐point. As predicted by Rapoport's rule, tephritids that occur at higher elevations also present wider altitudinal ranges. Bergmann's rule does not apply to Neotropical tephritids along a tropical elevational gradient, but rather its converse was found. Body size may determine host range by imposing a restriction upon large individuals using small flower heads. Host species turnover along the altitudinal gradient may be the main factor explaining the strong relationship between host range and insect elevational distribution.     

Adult body size = <Emphasis Type="Italic">f</Emphasis> (initial size + growth rate × age): explaining the proximate cause of Bergman’s cline in a toad along altitudinal gradients

Animals that exhibit indeterminate growth obey such a functional relationship: adult body size = f (initial size + growth rate × age). Using this framework, we investigated how and why body sizes of a toad species (Bufo andrewsi) covaried across six altitudes (760–2,100 m) in western China. Towards high altitudes, toads tended to produce large eggs, attain large sizes at metamorphism and have great average age, but grow slowly. This indicated that the former three variables contributed more to the observed altitudinal increase in body size than did the last one. The altitudinal variation in these life-history traits should be adaptive to increased climate harshness and decreased predation risks at higher altitudes. We suggest that the relative significance of responses of these size-related parameters to local environments may provide critical cues to explaining considerable variability in geographic size pattern among ectothermic vertebrates.     

Limb proportions in climbing and ground-dwelling geckos (Lepidosauria, Gekkonidae): a phylogenetically informed analysis

Biomechanical considerations predict that limb proportions should differ between animals with climbing and ground-dwelling lifestyles. Ground-dwellers should have relatively long, parasagittal hind limbs, with high tibia:femur ratios, and relatively short fore limbs. Climbers should have relatively short limbs, with low tibia:femur ratios, and equally long hind and fore limbs. We tested these predictions using gecko species with different locomotion habits (climbing versus ground-dwelling). We measured snout-vent length and lengths of limb segments in 29 species of geckos and analysed them using both non-phylogenetic statistics (nested analysis of variance and principal component analysis) and phylogenetic statistics (analysis of covariance). Neither approach allowed us to find any consistent relationship between habitat use and the morphometric variables. We conclude that either relative limb lengths and limb proportions in geckos have not evolved in response to the physical demands of the microhabitat, or our understanding of those demands is insufficient. Accepted: 22 February 2001     

Adult proportionality in small-bodied foragers: a test of ecogeographic expectations

If predictable, ecogeographic patterning in body size and proportions of human populations can provide valuable information regarding human biology, adaptation to local environments, migration histories, and health, now and in the past. This paper evaluates the assumption that small-bodied Later Stone Age (LSA) foragers of Southern Africa show the adult proportions that would be expected of warm-adapted populations. Comparisons are also made with small-bodied foragers from the Andaman Islands (AI). Indices including brachial, crural, limb element length to skeletal trunk height, and femoral head and bi-iliac breadth to femoral length were calculated from samples of LSA (n = 124) and AI (n = 31) adult skeletons. Samples derived from the literature include those from high (Europe), middle (North Africa), and low (Sub-Saharan Africa) latitude regions. The LSA and AI samples match some but not all expected ecogeographic patterns for their particular regions of long term habitation. For most limb length to skeletal trunk height indices the LSA and AI are most similar to the other mid-latitude sample (North Africans). However, both groups are similar to low latitude groups in their narrow bi-iliac breadths, and the AI display relatively long radii. Proportions of LSA and AI samples also differ from those of African pygmies. In regions like southern-most Africa, that do not experience climatic extremes of temperature or humidity, or where small body size exists through drift or selection, body size, and proportions may also be influenced by nonclimatic variables, such as energetic efficiency.     

Altitudinal variation in age and body size in Yunnan pond frog (Pelophylax pleuraden)

Large-scale systematic patterns of body size are a basic concern of evolutionary biology. Identifying body size variation along altitudinal gradients may help us to understand the evolution of life history of animals. In this study, we investigated altitudinal variation in body size, age and growth rate in Chinese endemic frog, Pelophylax pleuraden. Data sampled from five populations covering an altitudinal span of 1413 to 1935 m in Sichuan province revealed that body size from five populations did not co-vary with altitudes, not following Bergmann's rule. Average adult SVL differed significantly among populations in males, but not in females. For both sexes, average adult age differed significantly among populations. Post-metamorphic growth rate did not co-vary with altitude, and females grew faster than males in all populations. When controlling the effect of age, body size did not differ among populations in both sexes, suggesting that age did not affect variation in body size among populations. For females, there may be other factors, such as the allocation of energy between growth and reproduction, that eliminated the effect of age on body size. To our minds, the major reason of body size variation among populations in male frogs may be related to individual longevity. Our findings also suggest that factors other than age and growth rate may contribute to size differences among populations.