Variation in body form among human groups is structured by a blend of natural selection driven by local climatic conditions and random genetic drift. However, attempts to test ecogeographic hypotheses have not distinguished between adaptive traits (i.e., those that evolved as a result of selection) and those that evolved as a correlated response to selection on other traits (i.e., nonadaptive traits), complicating our understanding of the relationship between climate and morphological distinctions among populations. Here, we use evolutionary quantitative methods to test if traits previously identified as supporting ecogeographic hypotheses were actually adaptive by estimating the force of selection on individual traits needed to drive among-group differentiation. Our results show that not all associations between trait means and latitude were caused by selection acting directly on each individual trait. Although radial and tibial length and biiliac and femoral head breadth show signs of responses to directional selection matching ecogeographic hypotheses, the femur was subject to little or no directional selection despite having shorter values by latitude. Additionally, in contradiction to ecogeographic hypotheses, the humerus was under directional selection for longer values by latitude. Responses to directional selection in the tibia and radius induced a nonadaptive correlated response in the humerus that overwhelmed its own trait-specific response to selection. This result emphasizes that mean differences between groups are not good indicators of which traits are adaptations in the absence of information about covariation among characteristics.natural selection | ecogeographic variation | Bergmann's rule | Allen's rule | evolutionary constraints
Considerable research has shown that modern human pelvic dimensions, especially of the birth canal, are sexually dimorphic. Studies also suggest that females with younger ages-at-death have narrower canal dimensions than those who die at older ages, possibly due to continued independent growth of the pubis. A recent examination of this pattern argued that it is unlikely that these differences relate to mortality, but the source of the difference in pelvic dimensions with age remains unresolved. We use pelvic dimensions to assess differences in magnitudes of morphological integration between adult females and males across agesat-death. We first ascertain whether the sexes have different strengths of integration, and then assess if differences in magnitudes of integration are associated with age-at-death. Pelvic dimensions of all groups were moderately integrated. Females and males have similar magnitudes of integration, and there is no change in the strength of integration with age. Examining individual regions of the pelvis indicates that the ilium, pubis, and pelvic inlet and outlet have stronger integration than the overall pelvis. This was particularly true of the pelvic outlet, which demonstrated the strongest integration. Our findings suggest that regions of the pelvis are more strongly integrated internally, and less integrated with each other, which would allow for proportional growth among regions of the pelvis with age that do not affect its overall integration. No single region of the pelvis appears to be motivating the difference in pelvic dimensions between age groups. We further consider the implications of these findings on evolutionary constraints. Anat Rec, 300:666-674, 2017. V C 2017 Wiley Periodicals, Inc.
Objectives: Though recent quantitative genetic analyses have indicated that directional selection appears to be acting on limb lengths and measures of body size in modern humans, these studies assume equal evolvability across modern human groups. However, differences in trait covariance structure due to ancient migration patterns and/or selection may limit the evolvability of populations further from Africa. This study therefore explores patterns of human evolvability across ecogeographic regions. Materials and Methods: Mean evolvability, respondability, conditional evolvability, and autonomy were calculated from variance-covariance matrices of limb length and body size measures representing 14 human groups spanning four ecogeographic regions. Measures of evolvability were compared across groups and regions, and the minimum sample size, inaccuracy, and bias were calculated for each. Results: When compared between regions, humans demonstrate significant differences between indices of evolvability across regions. Despite the relatively recent evolution of modern humans, several measures of evolvability show a strong negative correlation with latitude across regions, demonstrating a reduction in genetic variance that is potentially reflective of human migration and/or response to selection.Conclusions: These results demonstrate the importance of establishing patterns of evolvability prior to additional quantitative genetic analyses, and emphasize the influence of sample size on the accuracy of estimated evolvability measures. These findings also suggest that while modern human groups share similar covariance structures, there is evidence for emergent differentiation in evolvability and respondability between human groups across ecogeographic regions, further complicating our ability to apply results derived from modern human groups to ancient hominin lineages.
Objectives:The global distribution of human body proportions has long been attributed to thermoregulatory adaptation to climate. However, latitude has been the most common proxy for climate across ecogeographic studies. If thermoregulation was driving post-cranial evolution, temperature should provide a better explanation for the morphological patterns observed than latitude, which encompasses temperature and other variables, as well as major events in human migration history. We investigate relationships between latitude, temperature, and postcranial form by distinguishing the strength of these potential selective factors from population structure.Materials & Methods: Quantitative genetic multivariate mixed models were used to estimate morphological effects associated with latitude, minimum temperature, and maximum temperature using osteometric data from 31 globally distributed groups, geographically matched genetic data from 54 groups, and geographically matched temperature data. Results: Dimensions reflecting body size (bi-iliac breadth/femoral head size) show independent evolutionary responses from limb lengths. In models including population history, only dimensions reflecting body size show evidence of response to directional selection. Model results indicate that selection in response to minimum temperature has shaped evolution in body breadth and femoral head size. Models for limb length evolution accounting for population history match results of prior studies, but do not indicate responses to temperature-driven directional selection. Conclusions: This study highlights the importance of considering multiple potential sources of selection within a multivariate evolutionary model, demonstrating the possible synergistic effects of selective pressures. These results complicate the classic thermoregulatory model of human postcranial evolution and show that factors other than temperature may have shaped post-cranial evolution in humans.
The general adherence of modern human body proportions to ecogeographic rules is frequently argued to be the result of thermoregulatory adaptation to climate. However, much of the history of human migrations follows the same clines that are associated with trends in body form. It is therefore important to test hypotheses about human adaptation to climate with approaches that account for population history and structure.In this project, we investigate the relationship between latitude and post‐cranial form in modern humans, with the goal of accounting for population history/structure and providing estimates of effects sizes and error. Using a multivariate quantitative genetics mixed model, we estimate morphological effects associated with latitude for long bone lengths and body size using osteometric data from 121 globally‐distributed populations and geographically matched genetic data representing 28 populations. The model includes a random effect for population structure (genetic relatedness) and a fixed effect for latitude. We found that among‐group variation was tightly correlated between limb lengths and body size measures respectively, but that these trait groups were fairly independent of each other. In addition, only bi‐iliac breadth demonstrates a clear directional effect once population history is taken into consideration, though directional trends skew positive for humeral length and negative for distal limb lengths, supporting previous research.By disentangling latitudinal effects from population structure using a mixed model approach, we add to the growing body of research exploring these strong underlying associations, and allow for a better understanding of the relationship between environmental and post‐cranial morphological diversity.This abstract is from the Experimental Biology 2018 Meeting. There is no full text article associated with this abstract published in The FASEB Journal.
This study examines morphological integration (MI) in the human pelvis with respect to sex and age. Anatomists and biological anthropologists have often cited the flair of the iliac blades, sub‐pubic angle, and breadth between the ischia among the morphologies that distinguish females and males, though the magnitude of difference between the sexes varies among groups. Despite these differences, it is assumed that patterns of MI within the human pelvis are the same between the sexes; the few studies of evolvability and integration in the pelvis to date remove effects of sexual dimorphism on the variance‐covariance matrix. In addition, the age of adult individuals is never considered a factor in quantitative genetic studies of the evolution of the pelvis, as the pelvis is thought to reach its definitive morphology with the cessation of primary growth. However, studies by Tague (1994) and Auerbach et al. (in review) show that older adult females have mediolaterally wider pelvic outlets (MLPO) and anteroposteriorly deeper pelvic inlets (APPI), while no age‐related differences in pelvic dimensions are observed among males. Though covariation within the pelvis should be similar between the sexes and among age groups within the sexes, no assessment of overall integration within the pelvis has been compared in light of these factors.In this study, 18 linear dimensions were measured from the rearticulated pelves of 327 adult human skeletons (188 females, 139 males) recovered from archaeological sites in North America dating from the last millennium. Fusion of the iliac crest was the criterion for inclusion. We aged the skeletons based on diagnostic changes in pelvic articular morphology, and placed the skeletons into two groups: “Young” (<~25 years) and “Not Young” (>~25 years). MI was measured by comparing relative eigenvalue variances between sex and age‐and‐sex groups, following Pavličev et al. (2009. Evol Biol 36:157–170), as well as by comparing mean‐scaled covariance matrices of the traits within each group. Relative eigenvalue variances have a scale of zero to one and higher values indicate more integration.Results indicate that MI differs notably between age groups within sex, but not between the sexes. Both females and males have similar relative eigenvalues (females = 0.162; males = 0.172). The slightly lower value for females may be driven by the influence of the Young female group, which has a relative eigenvalue variance of 0.139. In contrast, the Not Young female group has relative eigenvalue variance of 0.202. This is a stark difference, and indicates that younger females have less integration than older females. Examination of the covariance matrices indicates lower covariances among most traits, but especially between MLPO and APPI. This indicates that covariation of traits within the pelvis continue to change in adults, and older females have more integrated pelves. Further developmental and evolutionary implications are considered.Support or Funding InformationNational Science Foundation, BCS Grant #0962752
Recent work by Roseman and Auerbach (in press) indicates that the ecogeographic distribution of human body proportions is driven by a combination of neutral evolutionary forces and natural selection. This contrasts with assumptions that natural selection produces morphological variance along ecogeographic clines (i.e., Bergmann's and Allen's “rules”). Roseman and Auerbach's approach, however, does not distinguish between direct and indirect responses to the natural selection acting on these morphologies. This study uses retrospectively estimated selection gradients for limb lengths, femoral head size, and body breadth to assess the nature of selective forces on ecogeographic variance in human morphology.We estimated the vectors of selection gradients required to evolve one group into another for pairs of populations across major climate regions, and used parametric bootstraps to determine 95% confidence intervals. Equatorial African populations are assumed to have been drifting atop a plateau on the adaptive landscape, reflecting a tropically‐adapted human state. Results indicate that strong selection on distal limb lengths, femoral head size, and body breadth effected an evolutionary transition to morphologies found in arctic populations. The patterns of selection necessary to effect a transition to proportions found in more temperate regions (i.e. North Africa and Europe) were qualitatively similar but much less strong. These results in part support the findings of Roseman and Auerbach, but suggest that the action of natural selection may be entangled with random genetic drift, gene flow, and neutral mutation.
Since Washburn's New Physical Anthropology, researchers have sought to understand the complexities of morphological evolution among anatomical regions in human and non‐human primates. Researchers continue, however, to preferentially use comparative and functional approaches to examine complex traits, but these methods cannot address questions about evolutionary process and often conflate function with fitness. Moreover, researchers also tend to examine anatomical elements in isolation, which implicitly assumes independent evolution among different body regions. In this paper, we argue that questions asked in primate evolution are best examined using multiple anatomical regions subjected to model‐bound methods built from an understanding of evolutionary quantitative genetics. A nascent but expanding number of studies over the last two decades use this approach, examining morphological integration, evolvability, and selection modeling. To help readers learn how to use these methods, we review fundamentals of evolutionary processes within a quantitative genetic framework, explore the importance of neutral evolutionary theory, and explain the basics of evolutionary quantitative genetics, namely the calculation of evolutionary potential for multiple traits in response to selection. Leveraging these methods, we demonstrate their use to understand non‐independence in possible evolutionary responses across the limbs, limb girdles, and basicranium of humans. Our results show that model‐bound quantitative genetic methods can reveal unexpected genetic covariances among traits that create a novel but measurable understanding of evolutionary complexity among multiple traits. We advocate for evolutionary quantitative genetic methods to be a standard whenever appropriate to keep studies of primate morphological evolution relevant for the next seventy years and beyond.
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