Description and taxonomic assessment of fossil Cercopithecidae from the Pliocene Galili Formation (Ethiopia).

The Mount Galili Formation in the Afar region, Ethiopia, samples a critical time in hominin evolution, 4.4 to 3.8 Ma, documenting the last appearance of Ardipithecus and the origin of Australopithecus. This period is also important in the evolution of cercopithecids, especially the origin of Theropithecus in general and Theropithecus oswaldi lineage in particular. Galili has provided a total of 655 cercopithecid specimens that include crania, mandibles, isolated teeth and postcrania. All the fossils were recovered from the Lasdanan (5.3-4.43 Ma), Dhidinley (4.43-3.9 Ma) and Shabeley Laag (∼3.92-3.8 Ma) Members. Here, we described and analyzed 362 fossils employing both qualitative and quantitative methods. Descriptions of the material were supplemented with dental metrics and cranial shape analysis using three-dimensional geometric morphometrics. Results indicate the presence of at least six cercopithecid taxa: Theropithecus oswaldi serengetensis (n = 28), Theropithecus sp. (n = 2), three non-Theropithecus papionin groups (n = 134) and one colobine-size group (n = 58). The T. o. serengetensis represents the earliest form of the lineage, documented from ∼3.9 Ma Galili sediments. The three Galili papionins include a smaller taxon, a medium-sized taxon comparable to Pliopapio alemui and a large papionin overlapping in size with Soromandrillus, Gorgopithecus and Dinopithecus. The majority of Galili colobines have closest affinities to Kuseracolobus aramisi and some overlap with other taxa. Papionins dominate the Galili cercopithecid collection, although colobines are still fairly common (approximately 25% of the sample). Thus, Galili sample is like Kanapoi (4.2-4.1 Ma) and Gona (5.2-3.9 Ma) localities but distinct from Aramis, suggesting paleoecological similarity to the former sites. On the other hand, Theropithecus is less abundant at Galili than geologically younger Hadar (3.4-3.2 Ma) and Woranso-Mille (3.8-3.6 Ma) sites. Whether this difference is due to sampling, time or landscape variation requires further investigation.

Estimating sexual size dimorphism in fossil species from posterior probability densities.

Accurate characterization of sexual dimorphism is crucial in evolutionary biology because of its significance in understanding present and past adaptations involving reproductive and resource use strategies of species. However, inferring dimorphism in fossil assemblages is difficult, particularly with relatively low dimorphism. Commonly used methods of estimating dimorphism levels in fossils include the mean method, the binomial dimorphism index, and the coefficient of variation method. These methods have been reported to overestimate low levels of dimorphism, which is problematic when investigating issues such as canine size dimorphism in primates and its relation to reproductive strategies. Here, we introduce the posterior density peak (pdPeak) method that utilizes the Bayesian inference to provide posterior probability densities of dimorphism levels and within-sex variance. The highest posterior density point is termed the pdPeak. We investigated performance of the pdPeak method and made comparisons with the above-mentioned conventional methods via 1) computer-generated samples simulating a range of conditions and 2) application to canine crown-diameter datasets of extant known-sex anthropoids. Results showed that the pdPeak method is capable of unbiased estimates in a broader range of dimorphism levels than the other methods and uniquely provides reliable interval estimates. Although attention is required to its underestimation tendency when some of the distributional assumptions are violated, we demonstrate that the pdPeak method enables a more accurate dimorphism estimate at lower dimorphism levels than previously possible, which is important to illuminating human evolution.

Canine sexual dimorphism in Ardipithecus ramidus was nearly human-like.

Body and canine size dimorphism in fossils inform sociobehavioral hypotheses on human evolution and have been of interest since Darwin's famous reflections on the subject. Here, we assemble a large dataset of fossil canines of the human clade, including all available Ardipithecus ramidus fossils recovered from the Middle Awash and Gona research areas in Ethiopia, and systematically examine canine dimorphism through evolutionary time. In particular, we apply a Bayesian probabilistic method that reduces bias when estimating weak and moderate levels of dimorphism. Our results show that Ar. ramidus canine dimorphism was significantly weaker than in the bonobo, the least dimorphic and behaviorally least aggressive among extant great apes. Average male-to-female size ratios of the canine in Ar. ramidus are estimated as 1.06 and 1.13 in the upper and lower canines, respectively, within modern human population ranges of variation. The slightly greater magnitude of canine size dimorphism in the lower than in the upper canines of Ar. ramidus appears to be shared with early Australopithecus, suggesting that male canine reduction was initially more advanced in the behaviorally important upper canine. The available fossil evidence suggests a drastic size reduction of the male canine prior to Ar. ramidus and the earliest known members of the human clade, with little change in canine dimorphism levels thereafter. This evolutionary pattern indicates a profound behavioral shift associated with comparatively weak levels of male aggression early in human evolution, a pattern that was subsequently shared by Australopithecus and Homo.

Fossil Cercopithecidae from the Early Pliocene Sagantole Formation at Gona, Ethiopia.

The Early Pliocene Sagantole Fm. in the Gona Project area, Afar State, Ethiopia, is noted for discoveries of the early hominin Ardipithecus ramidus. A large series of fossil cercopithecid primates dated to between 4.8 and 4.3 Ma has also been collected from these sediments. In this paper, we use qualitative analysis and standard dental and postcranial measures to systematically describe the craniodental remains and tentatively allocate postcrania to taxa where we are able to. We then use these data to compare these specimens to fossil assemblages from contemporary sites, interpret their paleobiology, and discuss implications for the paleoecology of the Gona Sagantole Fm. We recognize three cercopithecid species in the Gona Sagantole Fm. Pliopapio alemui makes up approximately two-thirds of the identifiable specimens; nearly all of the rest are allocated to Kuseracolobus aramisi, and a single molar indicates the presence of a second, somewhat larger but morphologically distinct papionin. Among the Early Pliocene cercopithecids from Gona are also a number of postcranial elements. None of the postcranial remains are directly associated with any of the cranial material. Nonetheless, some of the distal humeri and proximal femora can be tentatively allocated to either Pl. alemui or K. aramisi based on a combination of size, as the latter is approximately 50% larger than the former, and morphology. If these assignments are correct, they suggest K. aramisi was primarily arboreal and similar to most extant colobines, whereas Pl. alemui was more mixed in its substrate use, being more terrestrially adapted than K. aramisi, but less so than extant Papio or Theropithecus. Thus, we interpret the predominance of Pl. alemui over K. aramisi is consistent with a somewhat more open environment at Gona than at Aramis.

Ardipithecus ramidus postcrania from the Gona Project area, Afar Regional State, Ethiopia.

Functional analyses of the 4.4 Ma hominin Ardipithecus ramidus postcrania revealed a previously unknown and unpredicted locomotor pattern combining arboreal clambering and a form of terrestrial bipedality. To date, all of the fossil evidence of Ar. ramidus locomotion has been collected from the Aramis area of the Middle Awash Research Project in Ethiopia. Here, we present the results of an analysis of additional early Pliocene Ar. ramidus fossils from the Gona Project study area, Ethiopia, that includes a fragmentary but informative partial skeleton (GWM67/P2) and additional isolated manual remains. While we reinforce the original functional interpretations of Ar. ramidus of having a mixed locomotor adaptation of terrestrial bipedality and arboreal clambering, we broaden our understanding of the nature of its locomotor pattern by documenting better the function of the hip, ankle, and foot. The newly recovered fossils document a greater adaptation to bipedality in the Ar. ramidus ankle and hallux than previously recognized. In addition, a newly discovered scaphoid bone with a fusing os centrale provides further evidence about the nature of hominin hand evolution.

Late Miocene hominin teeth from the Gona Paleoanthropological Research Project area, Afar, Ethiopia.

Since 2000, significant collections of Latest Miocene hominin fossils have been recovered from Chad, Kenya, and Ethiopia. These fossils have provided a better understanding of earliest hominin biology and context. Here, we describe five hominin teeth from two periods (ca. 5.4 Million-years-ago and ca. 6.3 Ma) that were recovered from the Adu-Asa Formation in the Gona Paleoanthropological Research Project area in the Afar, Ethiopia that we assign to either Hominina, gen. et sp. indet. or Ardipithecus kadabba. These specimens are compared with extant African ape and other Latest Miocene and Early Pliocene hominin teeth. The derived morphology of the large, non-sectorial maxillary canine and mandibular third premolar links them with later hominins and they are phenetically distinguishable and thus phyletically distinct from extant apes.

Early Pliocene hominids from Gona, Ethiopia.

Comparative biomolecular studies suggest that the last common ancestor of humans and chimpanzees, our closest living relatives, lived during the Late Miocene-Early Pliocene. Fossil evidence of Late Miocene-Early Pliocene hominid evolution is rare and limited to a few sites in Ethiopia, Kenya and Chad. Here we report new Early Pliocene hominid discoveries and their palaeoenvironmental context from the fossiliferous deposits of As Duma, Gona Western Margin (GWM), Afar, Ethiopia. The hominid dental anatomy (occlusal enamel thickness, absolute and relative size of the first and second lower molar crowns, and premolar crown and radicular anatomy) indicates attribution to Ardipithecus ramidus. The combined radioisotopic and palaeomagnetic data suggest an age of between 4.51 and 4.32 million years for the hominid finds at As Duma. Diverse sources of data (sedimentology, faunal composition, ecomorphological variables and stable carbon isotopic evidence from the palaeosols and fossil tooth enamel) indicate that the Early Pliocene As Duma sediments sample a moderate rainfall woodland and woodland/grassland.

Co-occurrence of Acheulian and Oldowan artifacts with Homo erectus cranial fossils from Gona, Afar, Ethiopia.

Although stone tools generally co-occur with early members of the genus Homo, they are rarely found in direct association with hominins. We report that both Acheulian and Oldowan artifacts and Homo erectus crania were found in close association at 1.26 million years (Ma) ago at Busidima North (BSN12), and ca. 1.6 to 1.5 Ma ago at Dana Aoule North (DAN5) archaeological sites at Gona, Afar, Ethiopia. The BSN12 partial cranium is robust and large, while the DAN5 cranium is smaller and more gracile, suggesting that H. erectus was probably a sexually dimorphic species. The evidence from Gona shows behavioral diversity and flexibility with a lengthy and concurrent use of both stone technologies by H. erectus, confounding a simple "single species/single technology" view of early Homo.

Why Do Knuckle-Walking African Apes Knuckle-Walk?

Among living mammals, only the African apes and some anteaters adopt knuckle-walking as their primary locomotor behavior. That Pan and Gorilla both knuckle-walk has been cited as evidence of their common ancestry and a primitive condition for a combined Homo, Pan, and Gorilla clade. Recent research on forelimb ontogeny and anatomy, in addition to recently described hominin fossils, indicate that knuckle-walking was independently acquired after divergence of the Pan and Gorilla lineages. Although the large-bodied, largely suspensory orangutan shares some aspects of the African ape bauplan, it does not regularly knuckle-walk when terrestrial. While many anatomical correlates of knuckle-walking have been identified, a functional explanation of this unusual locomotor pattern has yet to be proposed. Here, we argue that it was adopted by African apes as a means of ameliorating the consequences of repetitive impact loadings on the soft and hard tissues of the forelimb by employing isometric and/or eccentric contraction of antebrachial musculature during terrestrial locomotion. Evidence of this adaptation can be found in the differential size and fiber geometry of the forearm musculature, and differences in torso shape between the knuckle-walking and non-knuckle-walking apes (including humans). We also argue that some osteological features of the carpus and metacarpus that have been identified as adaptations to knuckle-walking are consequences of cartilage remodeling during ontogeny rather than traits limiting motion in the hand and wrist. An understanding of the functional basis of knuckle-walking provides an explanation of the locomotor parallelisms in modern Pan and Gorilla. Anat Rec, 301:496-514, 2018. © 2018 Wiley Periodicals, Inc.

The Functional Anatomy of the Carpometacarpal Complex in Anthropoids and Its Implications for the Evolution of the Hominoid Hand.

Previously, we described several features of the carpometacarpal joints in extant large-bodied apes that are likely adaptations to the functional demands of vertical climbing and suspension. We observed that all hominids, including modern humans and the 4.4-million-year-old hominid Ardipithecus ramidus, lacked these features. Here, we assess the uniqueness of these features in a large sample of monkey, ape, and human hands. These new data provide additional insights into the functional adaptations and evolution of the anthropoid hand. Our survey highlights a series of anatomical adaptations that restrict motion between the second and third metacarpals (MC2 and MC3) and their associated carpals in extant apes, achieved via joint reorganization and novel energy dissipation mechanisms. Their hamate-MC4 and -MC5 joint surface morphologies suggest limited mobility, at least in Pan. Gibbons and spider monkeys have several characters (angled MC3, complex capitate-MC3 joint topography, variably present capitate-MC3 ligaments) that suggest functional convergence in response to suspensory locomotion. Baboons have carpometacarpal morphology suggesting flexion/extension at these joints beyond that observed in most other Old World monkeys, probably as an energy dissipating mechanism minimizing collision forces during terrestrial locomotion. All hominids lack these specializations of the extant great apes, suggesting that vertical climbing was never a central feature of our ancestral locomotor repertoire. Furthermore, the reinforced carpometacarpus of vertically climbing African apes was likely appropriated for knuckle-walking in concert with other novel potential energy dissipating mechanisms. The most parsimonious explanation of the structural similarity of these carpometacarpal specializations in great apes is that they evolved independently.

Human evolution and osteoporosis-related spinal fractures.

The field of evolutionary medicine examines the possibility that some diseases are the result of trade-offs made in human evolution. Spinal fractures are the most common osteoporosis-related fracture in humans, but are not observed in apes, even in cases of severe osteopenia. In humans, the development of osteoporosis is influenced by peak bone mass and strength in early adulthood as well as age-related bone loss. Here, we examine the structural differences in the vertebral bodies (the portion of the vertebra most commonly involved in osteoporosis-related fractures) between humans and apes before age-related bone loss occurs. Vertebrae from young adult humans and chimpanzees, gorillas, orangutans, and gibbons (T8 vertebrae, n = 8-14 per species, male and female, humans: 20-40 years of age) were examined to determine bone strength (using finite element models), bone morphology (external shape), and trabecular microarchitecture (micro-computed tomography). The vertebrae of young adult humans are not as strong as those from apes after accounting for body mass (p<0.01). Human vertebrae are larger in size (volume, cross-sectional area, height) than in apes with a similar body mass. Young adult human vertebrae have significantly lower trabecular bone volume fraction (0.26±0.04 in humans and 0.37±0.07 in apes, mean ± SD, p<0.01) and thinner vertebral shells than apes (after accounting for body mass, p<0.01). Since human vertebrae are more porous and weaker than those in apes in young adulthood (after accounting for bone mass), even modest amounts of age-related bone loss may lead to vertebral fracture in humans, while in apes, larger amounts of bone loss would be required before a vertebral fracture becomes likely. We present arguments that differences in vertebral bone size and shape associated with reduced bone strength in humans is linked to evolutionary adaptations associated with bipedalism.

Trabecular microarchitecture of hominoid thoracic vertebrae.

Spontaneous vertebral fractures are a common occurrence in modern humans, yet these fractures are not documented in other hominoids. Differences in vertebral bone strength between humans and apes associated with trabecular bone microarchitecture may contribute to differences in fracture incidence. We used microcomputed tomography to examine trabecular bone microarchitecture in the T8 vertebra of extant young adult hominoids. Scaled volumes of interest from the anterior vertebral body were analyzed at a resolution of 46 microm, and bone volume fraction, trabecular thickness, trabecular number, trabecular separation, structure model index, and degree of anisotropy were compared among species. As body mass increased, so did trabecular thickness, but bone volume fraction, structure model index, and degree of anisotropy were independent of body mass. Bone volume fraction was not significantly different between the species. Degree of anisotropy was not significantly different among the species, suggesting similarity of loading patterns in the T8 vertebra due to similar anatomical and postural relationships within each species' spine. Degree of anisotropy was negatively correlated with bone volume fraction (r(2) = 0.85, P < 0.05) in humans, whereas the apes demonstrated no such relationship. This suggested that less dense human trabecular bone was more preferentially aligned to habitual loading. Furthermore, we theorize that trabeculae in ape thoracic vertebrae would not be expected to become preferentially aligned if bone volume fraction was decreased. The differing relationship between bone volume fraction and degree of anisotropy in humans and apes may cause less dense human bone to be more fragile than less dense ape bone.

Paleobiological implications of the Ardipithecus ramidus dentition.

The Middle Awash Ardipithecus ramidus sample comprises over 145 teeth, including associated maxillary and mandibular sets. These help reveal the earliest stages of human evolution. Ar. ramidus lacks the postcanine megadontia of Australopithecus. Its molars have thinner enamel and are functionally less durable than those of Australopithecus but lack the derived Pan pattern of thin occlusal enamel associated with ripe-fruit frugivory. The Ar. ramidus dental morphology and wear pattern are consistent with a partially terrestrial, omnivorous/frugivorous niche. Analyses show that the ARA-VP-6/500 skeleton is female and that Ar. ramidus was nearly monomorphic in canine size and shape. The canine/lower third premolar complex indicates a reduction of canine size and honing capacity early in hominid evolution, possibly driven by selection targeted on the male upper canine.

Careful climbing in the Miocene: the forelimbs of Ardipithecus ramidus and humans are primitive.

The Ardipithecus ramidus hand and wrist exhibit none of the derived mechanisms that restrict motion in extant great apes and are reminiscent of those of Miocene apes, such as Proconsul. The capitate head is more palmar than in all other known hominoids, permitting extreme midcarpal dorsiflexion. Ar. ramidus and all later hominids lack the carpometacarpal articular and ligamentous specializations of extant apes. Manual proportions are unlike those of any extant ape. Metacarpals 2 through 5 are relatively short, lacking any morphological traits associable with knuckle-walking. Humeral and ulnar characters are primitive and like those of later hominids. The Ar. ramidus forelimb complex implies palmigrady during bridging and careful climbing and exhibits none of the adaptations to vertical climbing, forelimb suspension, and knuckle-walking that are seen in extant African apes.

The great divides: Ardipithecus ramidus reveals the postcrania of our last common ancestors with African apes.

Genomic comparisons have established the chimpanzee and bonobo as our closest living relatives. However, the intricacies of gene regulation and expression caution against the use of these extant apes in deducing the anatomical structure of the last common ancestor that we shared with them. Evidence for this structure must therefore be sought from the fossil record. Until now, that record has provided few relevant data because available fossils were too recent or too incomplete. Evidence from Ardipithecus ramidus now suggests that the last common ancestor lacked the hand, foot, pelvic, vertebral, and limb structures and proportions specialized for suspension, vertical climbing, and knuckle-walking among extant African apes. If this hypothesis is correct, each extant African ape genus must have independently acquired these specializations from more generalized ancestors who still practiced careful arboreal climbing and bridging. African apes and hominids acquired advanced orthogrady in parallel. Hominoid spinal invagination is an embryogenetic mechanism that reoriented the shoulder girdle more laterally. It was unaccompanied by substantial lumbar spine abbreviation, an adaptation restricted to vertical climbing and/or suspension. The specialized locomotor anatomies and behaviors of chimpanzees and gorillas therefore constitute poor models for the origin and evolution of human bipedality.

A female Homo erectus pelvis from Gona, Ethiopia.

Analyses of the KNM-WT 15000 Homo erectus juvenile male partial skeleton from Kenya concluded that this species had a tall thin body shape due to specialized locomotor and climatic adaptations. Moreover, it was concluded that H. erectus pelves were obstetrically restricted to birthing a small-brained altricial neonate. Here we describe a nearly complete early Pleistocene adult female H. erectus pelvis from the Busidima Formation of Gona, Afar, Ethiopia. This obstetrically capacious pelvis demonstrates that pelvic shape in H. erectus was evolving in response to increasing fetal brain size. This pelvis indicates that neither adaptations to tropical environments nor endurance running were primary selective factors in determining pelvis morphology in H. erectus during the early Pleistocene.