Moving beyond the adaptationist paradigm for human evolution, and why it matters.

The Journal of Human Evolution (JHE) was founded 50 years ago when much of the foundation for how we think about human evolution was in place or being put in place, providing the main framework for how we consider our origins today. Here, we will explore historical developments, including early JHE outputs, as they relate to our understanding of the relationship between phenotypic variation and evolutionary process, and use that as a springboard for considering our current understanding of these links as applied to human evolution. We will focus specifically on how the study of variation itself has shifted us away from taxonomic and adaptationist perspectives toward a richer understanding of the processes shaping human evolutionary history, using literature searches and specific test cases to highlight this. We argue that natural selection, gene exchange, genetic drift, and mutation should not be considered individually when considering the production of hominin diversity. In this context, we offer suggestions for future research directions and reflect on this more complex understanding of human evolution and its broader relevance to society. Finally, we end by considering authorship demographics and practices in the last 50 years within JHE and how a shift in these demographics has the potential to reshape the science of human evolution going forward.

Morphological integration in the hominid midfoot.

The calculation of morphological integration across living apes and humans may provide important insights into the potential influence of integration on evolutionary trajectories in the hominid lineage. Here, we quantify magnitudes of morphological integration among and within elements of the midfoot in great apes and humans to examine the link between locomotor differences and trait covariance. We test the hypothesis that the medial elements of the great ape foot are less morphologically integrated with one another compared to humans based on their abducted halluces, and aim to determine how adaptations for midfoot mobility/stiffness and locomotor specialization influence magnitudes of morphological integration. The study sample is composed of all cuneiforms, the navicular, the cuboid, and metatarsals 1-5 of Homo sapiens (n = 80), Pan troglodytes (n = 63), Gorilla gorilla (n = 39), and Pongo sp. (n = 41). Morphological integration was quantified using the integration coefficient of variation of interlandmark distances organized into sets of a priori-defined modules. Magnitudes of integration across these modules were then compared against sets of random traits from the whole midfoot. Results show that all nonhuman apes have less integrated medial elements, whereas humans have highly integrated medial elements, suggesting a link between hallucal abduction and reduced levels of morphological integration. However, we find considerable variation in magnitudes of morphological integration across metatarsals 2-5, the intermediate and lateral cuneiform, the cuboid, and navicular, emphasizing the influence of functional and nonfunctional factors in magnitudes of integration. Lastly, we find that humans and orangutans show the lowest overall magnitudes of integration in the midfoot, which may be related to their highly specialized functions, and suggest a link between strong diversifying selection and reduced magnitudes of morphological integration.

Common evolutionary patterns in the human nasal region across a worldwide sample.

OBJECTIVES: Variation in the external nasal region among human populations has long been proposed in the literature to reflect adaptations to facilitate thermoregulation, air conditioning, and moisture retention in local climates and environments. More specifically, adaptations in populations living in colder climates have often been assumed due to correlational relationships found between variation in the nasal region and climatic variables. Here, we test this hypothesis by applying a quantitative genetics approach based on the Lande model to assess whether variation in the nasal region can be explained by random neutral processes (e.g., genetic drift) or if non-random forces (i.e., adaptation) have contributed significantly to its diversity. MATERIALS AND METHODS: A mixed-sex sample representing 28 population groups from Howells' craniometric dataset were analyzed (n = 2504). Twenty standard measurements were chosen to reflect the external skeletal morphology of the nasal region. We apply statistical tests developed from evolutionary quantitative genetics theory to analyze patterns of within- and between-population divergence under a null hypothesis of genetic drift. RESULTS: This study finds a rejection of genetic drift in all analyses, across tests that involve all 28 populations, exclusively cold-climate populations, and with cold-climate populations excluded, indicating that non-random evolutionary forces have contributed significantly to variation in the nasal region overall. DISCUSSION: These results show that nasal region adaptation is not exclusive to cold-climate populations, which have often been implicated in the literature to drive nasal variation, instead suggesting that the propensity for adaptation in the nasal region is shared among all human populations.

Type of unanticipated stimulus affects lower extremity kinematics and kinetics during sidestepping.

Including an unanticipated stimulus has significant impacts on lower extremity biomechanics during dynamic movements. It is unknown how a live, human defender affects lower extremity biomechanics. The purpose of this study was thus to determine the effects of two types of unanticipated stimuli (visual stimulus; defensive opponent) on lower extremity kinematics and kinetics in males and females during 45° sidestepping trials. Eight males and eight females completed two unanticipated stimuli sidestepping conditions. Numeric visual analog scales for reaction difficulty and movement realism were collected and analysed using a 2 × 2 mixed-model ANOVA. Three-dimensional hip, knee, and ankle kinematics and kinetics were measured during the stance phase of the sidestep and analysed using statistical parametric mapping. Participants reported greater difficulty and less realistic movements with the visual stimulus. Unanticipated stimulus main effects were observed for knee abduction angle, and hip extension and adduction, and knee extension and adduction moments. Sex main effects were observed for hip flexion, hip abduction, and ankle dorsiflexion angles, as well as hip abduction, ankle plantarflexion and ankle eversion moments and vertical ground reaction forces. Participants responded differently to two unanticipated stimuli. Careful consideration should be used when determining the type of unanticipated stimulus used.

Increased Ankle Range of Motion Reduces Knee Loads During Landing in Healthy Adults.

Decreased dorsiflexion range of motion (DROM) can be modified using static stretching and joint mobilizations and may attenuate known knee anterior cruciate ligament injury risk factors. It is not known how these interventions compare to each other and how they improve knee landing mechanics. This study's purpose was to determine the immediate effects of static stretching and joint mobilization interventions on DROM measurement changes and right-leg drop jump knee landing mechanics. Eighteen females and 7 males, all recreationally active, completed 2 study sessions. Active and passive DROM, the weight-bearing lunge test, the anterior reach portion of the Star Excursion Balance Test, and a right-leg drop jump landing task were completed before and after the intervention. Change in DROM (ΔDROM) was calculated for DROM assessments between preintervention and postintervention. Pairwise dependent t tests determined no differences in ΔDROM between interventions, and statistical parametric mapping determined increased knee flexion (P = .004) and decreased anterior shear force (P = .015) during landing after both interventions. Increased DROM improves sagittal plane displacement and loading at the knee. Stretching may be a more feasible option in a healthy population for those wanting to maintain range of motion and decrease knee injury risk without physical therapist involvement.

Overground Walking Biomechanics of Dissatisfied Persons With Total Knee Replacements.

Patient dissatisfaction following total knee replacement (TKR) procedures is likely influenced by both subjective and objective aspects. Increased pain and reduced performance on clinical tests have been shown in persons who are dissatisfied with the outcome of their surgery. However, it is unknown how overground walking kinematics and kinetics might differ in the dissatisfied versus satisfied patients following TKR surgery. This study compared the lower-extremity walking kinematics and kinetics of patients dissatisfied with their TKR to that of satisfied patients and healthy controls. Thirty nine subjects completed walking trials, including nine dissatisfied and 15 satisfied TKR patients and 15 healthy controls. A 2 × 3 repeated -measures analysis of variance was used to assess differences between groups and limbs (P < .05). Dissatisfied persons showed significantly reduced loading-response and push-off peak vertical ground reaction forces, flexion range of motion, loading-response extension moments, and loading-response abduction moments compared to the controls. Peak loading-response and push-off vertical ground reaction forces and flexion range of motion were reduced in the replaced limb of dissatisfied patients compared with their nonreplaced limb. Push-off plantar flexion moments were reduced in the dissatisfied patients compared with the satisfied and healthy controls. Dissatisfied patients also reported increased knee joint pain and reduced preferred gait speed. Moreover, dissatisfied patients experienced mechanical limb asymmetries not present in those satisfied with their surgery result. Thus, patients dissatisfied with their total knee replacement outcome were found to be experiencing significant negative physiological changes.

Hybridization in human evolution: Insights from other organisms.

During the late Pleistocene, isolated lineages of hominins exchanged genes thus influencing genomic variation in humans in both the past and present. However, the dynamics of this genetic exchange and associated phenotypic consequences through time remain poorly understood. Gene exchange across divergent lineages can result in myriad outcomes arising from these dynamics and the environmental conditions under which it occurs. Here we draw from our collective research across various organisms, illustrating some of the ways in which gene exchange can structure genomic/phenotypic diversity within/among species. We present a range of examples relevant to questions about the evolution of hominins. These examples are not meant to be exhaustive, but rather illustrative of the diverse evolutionary causes/consequences of hybridization, highlighting potential drivers of human evolution in the context of hybridization including: influences on adaptive evolution, climate change, developmental systems, sex-differences in behavior, Haldane's rule and the large X-effect, and transgressive phenotypic variation.

Comparing Anterior Cruciate Ligament Injury Risk Variables Between Unanticipated Cutting and Decelerating Tasks.

To examine the relationship between anterior cruciate ligament injury risk factors in unanticipated cutting and decelerating. Three-dimensional kinematics and ground reaction forces were collected on 11 females (22 [2] y, 1.67 [0.08] m, and 68.5 [9.8] kg) during 2 unanticipated tasks. Paired samples t tests were performed to compare dependent variables between tasks. Spearman rank correlation coefficients were calculated to analyze the relationship between peak internal knee adduction moment and peak anterior tibial shear force (ASF) during 2 unanticipated tasks. Significantly greater knee abduction angles, peak knee adduction moments, and peak ASFs were observed during cutting (P ≤ .05). A strong positive correlation existed between decelerating ASF and cutting ASF (ρ = .67), while correlations between decelerating knee adduction moment and cutting knee adduction moment and decelerating ASF and cutting knee adduction moment were not significant. In situations where time management is a necessity and only one task can be evaluated, it may be more appropriate to utilize an unanticipated cutting task rather than an unanticipated deceleration task because of the increased knee adduction moment and ASF. These data can help future clinicians in better designing more effective anterior cruciate ligament injury risk screening methods.

Morphological integration of anatomical, developmental, and functional postcranial modules in the crab-eating macaque (Macaca fascicularis).

OBJECTIVES: Integration and modularity reflect the coordinated action of past evolutionary processes and, in turn, constrain or facilitate phenotypic evolvability. Here, we analyze magnitudes of integration in the macaque postcranium to test whether 20 a priori defined modules are (1) more tightly integrated than random sets of postcranial traits, and (2) are differentiated based on mode of definition, with developmental modules expected to be more integrated than functional or anatomical modules. MATERIALS AND METHODS: The 3D morphometric data collected for eight limb and girdle bones for 60 macaques were collated into anatomical, developmental, and functional modules. A resampling technique was used to create random samples of integration values for each module for statistical comparison. RESULTS: Our results found that not all a priori defined modules were more strongly integrated than random samples of postcranial traits and that specific types of modules did not present consistent patterns of integration. Rather, girdle and joint modules were consistently less integrated than limb modules, and forelimb elements were less integrated than hindlimbs. DISCUSSION: The results suggest that morphometrically complex modules tend to be less integrated than simple limb bones, irrespective of the number of available traits. However, differences in integration of the fore- and hindlimb more likely reflects the multitude of locomotory, feeding, and social functions involved. It remains to be tested whether patterns of integration identified here are primate universals, and to what extent they vary depending on phylogenetic or functional factors.

Evolutionary processes shaping diversity across the Homo lineage.

Recent fossil finds have highlighted extensive morphological diversity within our genus, Homo, and the co-existence of a number of species. However, little is known about the evolutionary processes responsible for producing this diversity. Understanding the action of these processes can provide insight into how and why our lineage evolved and diversified. Here, we examine cranial and mandibular variation and diversification from the earliest emergence of our genus at 2.8 Ma until the Late Pleistocene (0.126-0.0117 Ma), using statistical tests developed from quantitative genetics theory to evaluate whether stochastic (genetic drift) versus non-stochastic (selection) processes were responsible for the observed variation. Results show that random processes can account for species diversification for most traits, including neurocranial diversification, and across all time periods. Where selection was found to shape diversification, we show that: 1) adaptation was important in the earliest migration of Homo out of Africa; 2) selection played a role in shaping mandibular and maxillary diversity among Homo groups, possibly due to dietary differences; and 3) Homo rudolfensis is adaptively different from other early Homo taxa, including the earliest known Homo specimen. These results show that genetic drift, and, likely, small population sizes were important factors shaping the evolution of Homo and many of its novel traits, but that selection played an essential role in driving adaptation to new contexts.

Skull diversity in the Homo lineage and the relative position of Homo naledi.

The discovery of Homo naledi has expanded the range of phenotypic variation in Homo, leading to new questions surrounding the mosaic nature of morphological evolution. Though currently undated, its unique morphological pattern and possible phylogenetic relationships to other hominin taxa suggest a complex evolutionary scenario. Here, we perform geometric morphometric analyses on H. naledi cranial and mandibular remains to investigate its morphological relationship with species of Homo and Australopithecus. We use Generalized Procrustes analysis to place H. naledi within the pattern of known hominin skull diversity, distributions of Procrustes distances among individuals to compare H. naledi and Homo erectus, and neighbor joining trees to investigate the potential phenetic relationships between groups. Our goal is to address a set of hypotheses relating to the uniqueness of H. naledi, its affinity with H. erectus, and the age of the fossils based on skull morphology. Our results indicate that, cranially, H. naledi aligns with members of the genus Homo, with closest affiliations to H. erectus. The mandibular results are less clear; H. naledi closely associates with a number of taxa, including some australopiths. However, results also show that although H. naledi shares similarities with H. erectus, some distances from this taxon - especially small-brained members of this taxon - are extreme. The neighbor joining trees place H. naledi firmly within Homo. The trees based on cranial morphology again indicate a close relationship between H. naledi and H. erectus, whereas the mandibular tree places H. naledi closer to basal Homo, suggesting a deeper antiquity. Altogether, these results emphasize the unique combination of features (H. erectus-like cranium, less derived mandible) defining H. naledi. Our results also highlight the variability within Homo, calling for a greater focus on the cause of this variability, and emphasizing the importance of using the total morphological package for species diagnoses.

The skull of Homo naledi.

The species Homo naledi was recently named from specimens recovered from the Dinaledi Chamber of the Rising Star cave system in South Africa. This large skeletal sample lacks associated faunal material and currently does not have a known chronological context. In this paper, we present comprehensive descriptions and metric comparisons of the recovered cranial and mandibular material. We describe 41 elements attributed to Dinaledi Hominin (DH1-DH5) individuals and paratype U.W. 101-377, and 32 additional cranial fragments. The H. naledi material was compared to Plio-Pleistocene fossil hominins using qualitative and quantitative analyses including over 100 linear measurements and ratios. We find that the Dinaledi cranial sample represents an anatomically homogeneous population that expands the range of morphological variation attributable to the genus Homo. Despite a relatively small cranial capacity that is within the range of australopiths and a few specimens of early Homo, H. naledi shares cranial characters with species across the genus Homo, including Homo habilis, Homo rudolfensis, Homo erectus, and Middle Pleistocene Homo. These include aspects of cranial form, facial morphology, and mandibular anatomy. However, the skull of H. naledi is readily distinguishable from existing species of Homo in both qualitative and quantitative assessments. Since H. naledi is currently undated, we discuss the evolutionary implications of its cranial morphology in a range of chronological frameworks. Finally, we designate a sixth Dinaledi Hominin (DH6) individual based on a juvenile mandible.

The evolutionary relationships and age of Homo naledi: An assessment using dated Bayesian phylogenetic methods.

Homo naledi is a recently discovered species of fossil hominin from South Africa. A considerable amount is already known about H. naledi but some important questions remain unanswered. Here we report a study that addressed two of them: "Where does H. naledi fit in the hominin evolutionary tree?" and "How old is it?" We used a large supermatrix of craniodental characters for both early and late hominin species and Bayesian phylogenetic techniques to carry out three analyses. First, we performed a dated Bayesian analysis to generate estimates of the evolutionary relationships of fossil hominins including H. naledi. Then we employed Bayes factor tests to compare the strength of support for hypotheses about the relationships of H. naledi suggested by the best-estimate trees. Lastly, we carried out a resampling analysis to assess the accuracy of the age estimate for H. naledi yielded by the dated Bayesian analysis. The analyses strongly supported the hypothesis that H. naledi forms a clade with the other Homo species and Australopithecus sediba. The analyses were more ambiguous regarding the position of H. naledi within the (Homo, Au. sediba) clade. A number of hypotheses were rejected, but several others were not. Based on the available craniodental data, Homo antecessor, Asian Homo erectus, Homo habilis, Homo floresiensis, Homo sapiens, and Au. sediba could all be the sister taxon of H. naledi. According to the dated Bayesian analysis, the most likely age for H. naledi is 912 ka. This age estimate was supported by the resampling analysis. Our findings have a number of implications. Most notably, they support the assignment of the new specimens to Homo, cast doubt on the claim that H. naledi is simply a variant of H. erectus, and suggest H. naledi is younger than has been previously proposed.

Testing the equivalence of modern human cranial covariance structure: Implications for bioarchaeological applications.

OBJECTIVES: Estimation of the variance-covariance (V/CV) structure of fragmentary bioarchaeological populations requires the use of proxy extant V/CV parameters. However, it is currently unclear whether extant human populations exhibit equivalent V/CV structures. MATERIALS AND METHODS: Random skewers (RS) and hierarchical analyses of common principal components (CPC) were applied to a modern human cranial dataset. Cranial V/CV similarity was assessed globally for samples of individual populations (jackknifed method) and for pairwise population sample contrasts. The results were examined in light of potential explanatory factors for covariance difference, such as geographic region, among-group distance, and sample size. RESULTS: RS analyses showed that population samples exhibited highly correlated multivariate responses to selection, and that differences in RS results were primarily a consequence of differences in sample size. The CPC method yielded mixed results, depending upon the statistical criterion used to evaluate the hierarchy. The hypothesis-testing (step-up) approach was deemed problematic due to sensitivity to low statistical power and elevated Type I errors. In contrast, the model-fitting (lowest AIC) approach suggested that V/CV matrices were proportional and/or shared a large number of CPCs. Pairwise population sample CPC results were correlated with cranial distance, suggesting that population history explains some of the variability in V/CV structure among groups. DISCUSSION: The results indicate that patterns of covariance in human craniometric samples are broadly similar but not identical. These findings have important implications for choosing extant covariance matrices to use as proxy V/CV parameters in evolutionary analyses of past populations.

Further evidence for phenotypic signatures of hybridization in descendant baboon populations.

Hybridization may have played a substantial role in shaping the diversity of our evolving lineage. Although recent genomic evidence has shown that hybridization occurred between anatomically modern humans (AMHS) and Neanderthals, it remains difficult to pin down precisely where and when this gene flow took place. Investigations of the hybrid phenotype in primates and other mammals are providing models for identifying signatures of hybridization in the fossil record. However, our understanding of intra- and inter-taxon variation in hybrids is still limited. Moreover, there is little evidence from these studies that is pertinent to the question of how long hybrid skeletal traits persist in descendants, and therefore it is not clear whether observed hybrid phenotypes are evidence of recent (e.g., F1) or much earlier hybridization events. Here, we present an analysis updating a previous study of cranial variation in pedigreed olive and yellow baboons and their hybrids. Results suggest that traits previously associated with hybrids in baboons and other mammalian species are also present in this expanded data set; many of these traits are highly heritable, confirming a genetic basis for their variation in this mixed population. While F1 animals - and especially F1 males - still have the highest number of dental anomalies, these and other atypical traits persist into later hybrid generations (such as F2 and B1). Moreover, non-F1 recombinants also show extremely rare trait variations, including reduced canines and rotated teeth. However, these results must be considered in light of the possibility that some founding individuals may have themselves been unrecognized hybrids. Despite this, the data are compelling, and indicate once again that further controlled research remains to be done on primates and other mammals in order to better understand variation in the hybrid phenotype.

Skull variation in Afro-Eurasian monkeys results from both adaptive and non-adaptive evolutionary processes.

Afro-Eurasian monkeys originated in the Miocene and are the most species-rich modern primate family. Molecular and fossil data have provided considerable insight into their evolutionary divergence, but we know considerably less about the evolutionary processes that underlie these differences. Here, we apply tests developed from quantitative genetics theory to a large (n > 3000) cranio-mandibular morphometric dataset, investigating the relative importance of adaptation (natural selection) and neutral processes (genetic drift) in shaping diversity at different taxonomic levels, an approach applied previously to monkeys of the Americas, apes, hominins, and other vertebrate taxa. Results indicate that natural selection, particularly for differences in size, plays a significant role in diversifying Afro-Eurasian monkeys as a whole. However, drift appears to better explain skull divergence within the subfamily Colobinae, and in particular the African colobine clade, likely due to habitat fragmentation. Small and declining population sizes make it likely that drift will continue in this taxon, with potentially dire implications for genetic diversity and future resilience in the face of environmental change. For the other taxa, many of whom also have decreasing populations and are threatened, understanding adaptive pressures similarly helps identify relative vulnerability and may assist with prioritising scarce conservation resources.

Effects of foot progression angle on knee mechanics during an anticipated cutting task: A statistical parametric mapping approach.

Cutting is considered a "high-risk" movement for anterior cruciate ligament (ACL) injuries. It has been established that sex differences exist during cutting, placing females at greater ACL injury risk. Foot progression angle (FPA) during landing has been shown to influence lower extremity mechanics, yet little is known how FPA influences mechanics during cutting. The purpose of this study was to compare two FPA conditions during cutting between males and females. Twenty-four males and females were tested using two FPA conditions: toe-in 15° (TI15) and toe-out 15° (TO15). Right knee joint kinematic and kinetic variables were measured using a motion capture system and force plate. Five successful trials were collected and compared between FPA conditions. One-dimensional statistical parametric mapping was used to assess changes in knee mechanics between males and females over the entire stance phase. The only sex × FPA effect found was knee flexion angle. Females cutting at TI15 had decreased knee flexion angle compared TO15 (p = 0.019). Significant sex main effects included knee abduction and rotation angles, and knee flexion and rotation moments. Significant FPA main effects included knee flexion, abduction and rotation angles. The results show cutting with a toe-in FPA of 15° is enough to induce changes in knee abduction angle while cutting with 15° toe-out FPA influenced knee flexion and rotation angles. These data suggest that different cutting FPAs may be influential on known ACL injury risk variables. However, more research is warranted on cutting FPA before FPA is targeted as part of ACL injury prevention protocols.

The activity patterns of nonworking and working sled dogs.

There are limited studies investigating the combined effects of biological, environmental, and human factors on the activity of the domestic dog. Sled dogs offer a unique opportunity to examine these factors due to their close relationship with handlers and exposure to the outdoors. Here, we used accelerometers to measure the activity of 52 sled dogs over 30 days from two locations in Canada. The two locations differ in the working demands of dogs, therefore we used linear mixed effects models to assess how different factors impact daytime and nighttime activity of working versus nonworking dogs. During the daytime, we found that males were more active than females among nonworking dogs and younger dogs were more active than older dogs among working dogs. Alaskan huskies had higher activity levels than non-Alaskan husky breeds in working sled dogs during the day. Nonworking dogs were slightly more active during colder weather, but temperature had no effect on working dogs' activity. The strongest predictor of daytime activity in working dogs was work schedule. These results indicate that the influence of biological factors on activity varied depending on dogs' physical demands and human activity was the most powerful driver of activity in working dogs.

Ovariectomized rat model and shape variation in the bony labyrinth.

Postmenopausal osteoporosis is a serious concern in aging individuals, but has not been explored for its potential to alter the shape of the inner ear by way of increased remodeling in the otic capsule. The otic capsule, or bony labyrinth, is thought to experience uniquely limited remodeling after development due to high levels of osteoprotegerin. On this basis, despite the widespread remodeling that accompanies osteoporosis, we hypothesize that both the shape and volume of the semicircular canals will resist such changes. To test this hypothesis, we conducted three-dimensional geometric morphometric shape analysis on microcomputed tomographic data collected on the semicircular canals of an ovariectomized (OVX) rat model. A Procrustes ANOVA found no statistically significant differences in shape between surgery and sham groups, and morphological disparity testing likewise found no differences in shape variation. Univariate testing found no differences in semicircular volume between OVX and control groups. The range of variation in the OVX group, however, is greater than in the sham group but this difference does not reach statistical significance, perhaps because of a combination of small effect size and low sample size. This finding suggests that labyrinthine shape remains a tool for assessing phylogeny and function in the fossil record, but that it is possible that osteoporosis may be contributing to intraspecific shape variation in the bony labyrinth. This effect warrants further exploration at a microstructural level with continued focus on variables related to remodeling.