Automated morphological phenotyping using learned shape descriptors and functional maps: A novel approach to geometric morphometrics.

The methods of geometric morphometrics are commonly used to quantify morphology in a broad range of biological sciences. The application of these methods to large datasets is constrained by manual landmark placement limiting the number of landmarks and introducing observer bias. To move the field forward, we need to automate morphological phenotyping in ways that capture comprehensive representations of morphological variation with minimal observer bias. Here, we present Morphological Variation Quantifier (morphVQ), a shape analysis pipeline for quantifying, analyzing, and exploring shape variation in the functional domain. morphVQ uses descriptor learning to estimate the functional correspondence between whole triangular meshes in lieu of landmark configurations. With functional maps between pairs of specimens in a dataset we can analyze and explore shape variation. morphVQ uses Consistent ZoomOut refinement to improve these functional maps and produce a new representation of shape variation, area-based and conformal (angular) latent shape space differences (LSSDs). We compare this new representation of shape variation to shape variables obtained via manual digitization and auto3DGM, an existing approach to automated morphological phenotyping. We find that LSSDs compare favorably to modern 3DGM and auto3DGM while being more computationally efficient. By characterizing whole surfaces, our method incorporates more morphological detail in shape analysis. We can classify known biological groupings, such as Genus affiliation with comparable accuracy. The shape spaces produced by our method are similar to those produced by modern 3DGM and to auto3DGM, and distinctiveness functions derived from LSSDs show us how shape variation differs between groups. morphVQ can capture shape in an automated fashion while avoiding the limitations of manually digitized landmarks, and thus represents a novel and computationally efficient addition to the geometric morphometrics toolkit.

Hip extensor mechanics and the evolution of walking and climbing capabilities in humans, apes, and fossil hominins.

The evolutionary emergence of humans' remarkably economical walking gait remains a focus of research and debate, but experimentally validated approaches linking locomotor capability to postcranial anatomy are limited. In this study, we integrated 3D morphometrics of hominoid pelvic shape with experimental measurements of hip kinematics and kinetics during walking and climbing, hamstring activity, and passive range of hip extension in humans, apes, and other primates to assess arboreal-terrestrial trade-offs in ischium morphology among living taxa. We show that hamstring-powered hip extension during habitual walking and climbing in living apes and humans is strongly predicted, and likely constrained, by the relative length and orientation of the ischium. Ape pelves permit greater extensor moments at the hip, enhancing climbing capability, but limit their range of hip extension, resulting in a crouched gait. Human pelves reduce hip extensor moments but permit a greater degree of hip extension, which greatly improves walking economy (i.e., distance traveled/energy consumed). Applying these results to fossil pelves suggests that early hominins differed from both humans and extant apes in having an economical walking gait without sacrificing climbing capability. Ardipithecus was capable of nearly human-like hip extension during bipedal walking, but retained the capacity for powerful, ape-like hip extension during vertical climbing. Hip extension capability was essentially human-like in Australopithecus afarensis and Australopithecus africanus, suggesting an economical walking gait but reduced mechanical advantage for powered hip extension during climbing.

The influence of mobility strategy on the modern human talus.

OBJECTIVES: The primate talus is known to have a shape that varies according to differences in locomotion and substrate use. While the modern human talus is morphologically specialized for bipedal walking, relatively little is known on how its morphology varies in relation to cultural and environmental differences across time. Here we compare tali of modern human populations with different subsistence economies and lifestyles to explore how cultural practices and environmental factors influence external talar shape. MATERIALS AND METHODS: The sample consists of digital models of 142 tali from 11 archaeological and post-industrial modern human groups. Talar morphology was investigated through 3D (semi)landmark based geometric morphometric methods. RESULTS: Our results show distinct differences between highly mobile hunter-gatherers and more sedentary groups belonging to a mixed post-agricultural/industrial background. Hunter-gatherers exhibit a more "flexible" talar shape, everted posture, and a more robust and medially oriented talar neck/head, which we interpret as reflecting long-distance walking strictly performed barefoot, or wearing minimalistic footwear, along uneven ground. The talus of the post-industrial population exhibits a "stable" profile, neutral posture, and a less robust and orthogonally oriented talar neck/head, which we interpret as a consequence of sedentary lifestyle and use of stiff footwear. DISCUSSION: We suggest that talar morphological variation is related to the adoption of constraining footwear in post-industrial society, which reduces ankle range of motion. This contrasts with hunter-gatherers, where talar shape shows a more flexible profile, likely resulting from a lack of footwear while traversing uneven terrain. We conclude that modern human tali vary with differences in locomotor and cultural behavior.

Dental microwear profilometry of African non-cercopithecoid catarrhines of the Early Miocene.

The Early Miocene of Kenya has yielded the remains of many important stem catarrhine species that provide a glimpse of the East African primate radiation at a time of major faunal turnover. These taxa have been subject to innumerable studies, yet there is still no consensus on their dietary niches. Here we report results of an analysis of dental microwear textures of non-cercopithecoid catarrhines from the Early Miocene of Kenya. Scanning confocal profilometry of all available molar specimens with undamaged occlusal surfaces revealed 82 individuals with unobscured antemortem microwear, representing Dendropithecus, Micropithecus, Limnopithecus, Proconsul, and Rangwapithecus. Scale-sensitive fractal analysis was used to generate microwear texture attributes for each individual, and the fossil taxa were compared with each other using conservative non-parametric statistical tests. This study revealed no discernible variation in microwear texture among the fossil taxa, which is consistent with results from a previous feature-based microwear study using smaller samples. Our results suggest that, despite their morphological differences, these taxa likely often consumed foods with similar abrasive and fracture properties. However, statistical analyses of microwear texture data indicate differences between the Miocene fossil sample and several extant anthropoid primate genera. This suggests that the African non-cercopithecoid catarrhines included in our study, despite variations in tooth form, had generalist diets that were not yet specialized to the degree of many modern taxa.

Ecological divergence and medial cuneiform morphology in gorillas.

Gorillas are more closely related to each other than to any other extant primate and are all terrestrial knuckle-walkers, but taxa differ along a gradient of dietary strategies and the frequency of arboreality in their behavioral repertoire. In this study, we test the hypothesis that medial cuneiform morphology falls on a morphocline in gorillas that tracks function related to hallucial abduction ability and relative frequency of arboreality. This morphocline predicts that western gorillas, being the most arboreal, should display a medial cuneiform anatomy that reflects the greatest hallucial abduction ability, followed by grauer gorillas, and then by mountain gorillas. Using a three-dimensional methodology to measure angles between articular surfaces, relative articular and nonarticular areas, and the curvatures of the hallucial articular surface, the functional predictions are partially confirmed in separating western gorillas from both eastern gorillas. Western gorillas are characterized by a more medially oriented, proportionately larger, and more mediolaterally curved hallucial facet than are eastern gorillas. These characteristics follow the predictions for a more prehensile hallux in western gorillas relative to a more stable, plantigrade hallux in eastern gorillas. The characteristics that distinguish eastern gorilla taxa from one another appear unrelated to hallucial abduction ability or frequency of arboreality. In total, this reexamination of medial cuneiform morphology suggests differentiation between eastern and western gorillas due to a longstanding ecological divergence and more recent and possibly non-adaptive differences between eastern taxa.

Variation in brown rat cranial shape shows directional selection over 120 years in New York City.

Urbanization exposes species to novel environments and selection pressures that may change morphological traits within a population. We investigated how the shape and size of crania and mandibles changed over time within a population of brown rats (Rattus norvegicus) living in Manhattan, New York, USA, a highly urbanized environment. We measured 3D landmarks on the cranium and mandible of 62 adult individuals sampled in the 1890s and 2010s. Static allometry explained approximately 22% of shape variation in crania and mandible datasets, while time accounted for approximately 14% of variation. We did not observe significant changes in skull size through time or between the sexes. Estimating the P-matrix revealed that directional selection explained temporal change of the crania but not the mandible. Specifically, rats from the 2010s had longer noses and shorter upper molar tooth rows, traits identified as adaptive to colder environments and higher quality or softer diets, respectively. Our results highlight the continual evolution to selection pressures. We acknowledge that urban selection pressures impacting cranial shape likely began in Europe prior to the introduction of rats to Manhattan. Yet, our study period spanned changes in intensity of artificial lighting, human population density, and human diet, thereby altering various aspects of rat ecology and hence pressures on the skull.

Exploring sexual dimorphism of the modern human talus through geometric morphometric methods.

Sex determination is a pivotal step in forensic and bioarchaeological fields. Generally, scholars focus on metric or qualitative morphological features, but in the last few years several contributions have applied geometric-morphometric (GM) techniques to overcome limitations of traditional approaches. In this study, we explore sexual dimorphism in modern human tali from three early 20th century populations (Sassari and Bologna, Italy; New York, USA) at intra- and interspecific population levels using geometric morphometric (GM) methods. Statistical analyses were performed using shape, form, and size variables. Our results do not show significant differences in shape between males and females, either considering the pooled sample or the individual populations. Differences in talar morphology due to sexual dimorphism are mainly related to allometry, i.e. size-related changes of morphological traits. Discriminant function analysis using form space Principal Components and centroid size correctly classify between 87.7% and 97.2% of the individuals. The result is similar using the pooled sample or the individual population, except for a diminished outcome for the New York group (from 73.9% to 78.2%). Finally, a talus from the Bologna sample (not included in the previous analysis) with known sex was selected to run a virtual resection, followed by two digital reconstructions based on the mean shape of both the pooled sample and the Bologna sample, respectively. The reconstructed talus was correctly classified with a Ppost between 99.9% and 100%, demonstrating that GM is a valuable tool to cope with fragmentary tali, which is a common occurrence in forensic and bioarchaeological contexts.

Snapshots of human anatomy, locomotion, and behavior from Late Pleistocene footprints at Engare Sero, Tanzania.

Fossil hominin footprints preserve data on a remarkably short time scale compared to most other fossil evidence, offering snapshots of organisms in their immediate ecological and behavioral contexts. Here, we report on our excavations and analyses of more than 400 Late Pleistocene human footprints from Engare Sero, Tanzania. The site represents the largest assemblage of footprints currently known from the human fossil record in Africa. Speed estimates show that the trackways reflect both walking and running behaviors. Estimates of group composition suggest that these footprints were made by a mixed-sex and mixed-age group, but one that consisted of mostly adult females. One group of similarly-oriented trackways was attributed to 14 adult females who walked together at the same pace, with only two adult males and one juvenile accompanying them. In the context of modern ethnographic data, we suggest that these trackways may capture a unique snapshot of cooperative and sexually divided foraging behavior in Late Pleistocene humans.

Stratigraphic interpretation of the Kulu Formation (Early Miocene, Rusinga Island, Kenya) and its implications for primate evolution.

Early Miocene fossils from Rusinga Island, Kenya, provide some of the best evidence for catarrhine evolution and diversification, and, together with more than eighty-five other mammalian species, form an important comparative reference for understanding faunal succession in East Africa. While there is consensus over the stratigraphic position of most of Rusinga's volcaniclastic deposits, the lacustrine Kulu Formation has been placed in various parts of the geological sequence by different researchers. To resolve this discrepancy, we conducted detailed geological analyses which indicate that the Kulu Formation was formed in the Early Miocene during a period of volcanic inactivity and subsidence following the early, mainly explosive hyper-alkaline phase of the Kisingiri complex and prior to the final eruptions of nephelinitic lavas. The underlying Hiwegi and older formations were locally deformed and deeply eroded before sedimentation began in the Kulu basin, so that the Kulu sediments may be significantly younger than the 17.8 Ma Hiwegi Formation and not much older than the overlying Kiangata Agglomerata-Lunene Lava series, loosely dated to ca. 15 Ma. The overall similarities between Kulu and Hiwegi faunas imply long-term ecological stability in this region. Our stratigraphic interpretation suggests that the Kulu fauna is contemporaneous with faunas from West Turkana, implying that differences between these assemblages-particularly in the primate communities--reflect paleobiogeographic and/or paleocological differences. Finally, the position of the Kulu Formation restricts the time frame during which the substantial faunal turnover seen in the differences between the primate and mammalian communities of Rusinga and Maboko Islands could have occurred.

Scythes, sickles and other blades: defining the diversity of pectoral fin morphotypes in Pachycormiformes.

The traditional terminology of 'scythe' or 'sickle' shaped is observed to be flawed as an effective descriptor for pectoral fin shape in pachycormids. The diversity of pachycormid pectoral fin shapes is assessed across the 14 recognised genera that preserve complete pectoral fins, and improved terms are defined to more effectively describe their form, supported by anatomical observation and aspect ratio analysis of individual fins, and corroborated by landmark analysis. Three clear and distinct pectoral fin structural morphotypes emerge (falceform, gladiform, falcataform), reflecting a diversity of pachycormid lifestyles throughout the Mesozoic, from agile pursuit predator to slow-cruising suspension feeder.

Early hominin diversity and the emergence of the genus Homo.

Bipedalism is a defining trait of hominins, as all members of the clade are argued to possess at least some characters indicative of this unusual form of locomotion. Traditionally the evolution of bipedalism has been treated in a somewhat linear way. This has been challenged in the last decade or so, and in this paper I consider this view in light of the considerable new fossil hominin discoveries of the last few years. It is now apparent that there was even more locomotor diversity and experimentation across hominins than previously thought, and with the discovery of taxa such as H. floresiensis and H. naledi, that diversity continues well into the genus Homo. Based on these findings,we need to reevaluate how we define members of the genus Homo, at least when considering postcranial morphology, and accept that the evolution of hominin bipedalism was a complex and messy affair. It is within that context that the modern human form of bipedal locomotion emerged.

Homo naledi, a new species of the genus Homo from the Dinaledi Chamber, South Africa.

Homo naledi is a previously-unknown species of extinct hominin discovered within the Dinaledi Chamber of the Rising Star cave system, Cradle of Humankind, South Africa. This species is characterized by body mass and stature similar to small-bodied human populations but a small endocranial volume similar to australopiths. Cranial morphology of H. naledi is unique, but most similar to early Homo species including Homo erectus, Homo habilis or Homo rudolfensis. While primitive, the dentition is generally small and simple in occlusal morphology. H. naledi has humanlike manipulatory adaptations of the hand and wrist. It also exhibits a humanlike foot and lower limb. These humanlike aspects are contrasted in the postcrania with a more primitive or australopith-like trunk, shoulder, pelvis and proximal femur. Representing at least 15 individuals with most skeletal elements repeated multiple times, this is the largest assemblage of a single species of hominins yet discovered in Africa.

Remnants of an ancient forest provide ecological context for Early Miocene fossil apes.

The lineage of apes and humans (Hominoidea) evolved and radiated across Afro-Arabia in the early Neogene during a time of global climatic changes and ongoing tectonic processes that formed the East African Rift. These changes probably created highly variable environments and introduced selective pressures influencing the diversification of early apes. However, interpreting the connection between environmental dynamics and adaptive evolution is hampered by difficulties in locating taxa within specific ecological contexts: time-averaged or reworked deposits may not faithfully represent individual palaeohabitats. Here we present multiproxy evidence from Early Miocene deposits on Rusinga Island, Kenya, which directly ties the early ape Proconsul to a widespread, dense, multistoried, closed-canopy tropical seasonal forest set in a warm and relatively wet, local climate. These results underscore the importance of forested environments in the evolution of early apes.

Laetoli footprints preserve earliest direct evidence of human-like bipedal biomechanics.

BACKGROUND: Debates over the evolution of hominin bipedalism, a defining human characteristic, revolve around whether early bipeds walked more like humans, with energetically efficient extended hind limbs, or more like apes with flexed hind limbs. The 3.6 million year old hominin footprints at Laetoli, Tanzania represent the earliest direct evidence of hominin bipedalism. Determining the kinematics of Laetoli hominins will allow us to understand whether selection acted to decrease energy costs of bipedalism by 3.6 Ma. METHODOLOGY/PRINCIPAL FINDINGS: Using an experimental design, we show that the Laetoli hominins walked with weight transfer most similar to the economical extended limb bipedalism of humans. Humans walked through a sand trackway using both extended limb bipedalism, and more flexed limb bipedalism. Footprint morphology from extended limb trials matches weight distribution patterns found in the Laetoli footprints. CONCLUSIONS: These results provide us with the earliest direct evidence of kinematically human-like bipedalism currently known, and show that extended limb bipedalism evolved long before the appearance of the genus Homo. Since extended-limb bipedalism is more energetically economical than ape-like bipedalism, energy expenditure was likely an important selection pressure on hominin bipeds by 3.6 Ma.