New insights on the anatomy and ontogeny of the largest extinct freshwater turtles.

There are many questions regarding the largest freshwater turtle that ever existed, including how its morphology changed during its ontogeny and how a single ecosystem was able to support more than one group of giant turtles. Here, we report the first individual preserving an associated skull and shell for Stupendemys geographica (currently the largest known side-necked turtle) and a nearly complete skull of Caninemys tridentata found in Miocene rocks of the Tatacoa Desert in Colombia. These two specimens indicate that more than two large freshwater turtle species shared a single ecosystem during the middle Miocene in northern South America. We also show the changes in the shell and scutes that occurred along the ontogeny of S. geographica, including a flattening of the carapace, constriction of the vertebral scutes, and increase in the height and thickness of the nuchal upturn wall; some of these changes are also evident in extant representatives of Podocnemididae, and have implications for a better understanding of their phylogeny.

Early anthropoid femora reveal divergent adaptive trajectories in catarrhine hind-limb evolution.

The divergence of crown catarrhines-i.e., the split of cercopithecoids (Old World monkeys) from hominoids (apes and humans)-is a poorly understood phase in our shared evolutionary history with other primates. The two groups differ in the anatomy of the hip joint, a pattern that has been linked to their locomotor strategies: relatively restricted motion in cercopithecoids vs. more eclectic movements in hominoids. Here we take advantage of the first well-preserved proximal femur of the early Oligocene stem catarrhine Aegyptopithecus to investigate the evolution of this anatomical region using 3D morphometric and phylogenetically-informed evolutionary analyses. Our analyses reveal that cercopithecoids and hominoids have undergone divergent evolutionary transformations of the proximal femur from a similar ancestral morphology that is not seen in any living anthropoid, but is preserved in Aegyptopithecus, stem platyrrhines, and stem cercopithecoids. These results highlight the relevance of fossil evidence for illuminating key adaptive shifts in primate evolution.

Investigating the effect of endocranial volume on cranial shape in platyrrhines and the relevance of this relationship to interpretations of the fossil record.

OBJECTIVES: Fossils have been linked to Alouatta based on shared cranial morphology and small brain size. However, the relationship between endocranial volume and cranial shape is unclear; it is possible that any platyrrhine with a small brain may exhibit "Alouatta-like" features due to being "de-encephalized." We test two hypotheses: (a) there are aspects of cranial shape related to encephalization common to all platyrrhines; (b) it is these cranial traits that unite the small-brained "Alouatta-like" fossils. MATERIALS AND METHODS: Three-dimensional cranial shape and endocranial volume (ECV) were measured on 350+ extant platyrrhine crania, Cartelles, Paralouatta, and Antillothrix. Encephalization quotient (EQ) was calculated using regressions of ECV on cranial centroid size. Multivariate regressions were performed using the shape coordinates and EQ and shape changes associated with EQ were visualized. Cranial shape was predicted for a hypothetical primate with an EQ matching the fossils and this shape was compared to the Alouatta mean. RESULTS: There is a significant proportion of cranial shape variation explained by EQ in some taxa. The aspects of shape that are correlated with EQ are shared by several taxa and some have parallel regression vectors, but there is no overall pattern of shape change common to all platyrrhines. However, all taxa look more similar to Alouatta when their EQ is decreased, particularly Pithecia. DISCUSSION: Given that a decrease in encephalization can cause a more Alouatta-like cranial shape in many extant platyrrhines, it should not be automatically assumed that Alouatta-like cranial traits in a small-brained fossil are evidence of a phylogenetic link to the alouattin clade.

Evaluating causes of error in landmark-based data collection using scanners.

In this study, we assess the precision, accuracy, and repeatability of craniodental landmarks (Types I, II, and III, plus curves of semilandmarks) on a single macaque cranium digitally reconstructed with three different surface scanners and a microCT scanner. Nine researchers with varying degrees of osteological and geometric morphometric knowledge landmarked ten iterations of each scan (40 total) to test the effects of scan quality, researcher experience, and landmark type on levels of intra- and interobserver error. Two researchers additionally landmarked ten specimens from seven different macaque species using the same landmark protocol to test the effects of the previously listed variables relative to species-level morphological differences (i.e., observer variance versus real biological variance). Error rates within and among researchers by scan type were calculated to determine whether or not data collected by different individuals or on different digitally rendered crania are consistent enough to be used in a single dataset. Results indicate that scan type does not impact rate of intra- or interobserver error. Interobserver error is far greater than intraobserver error among all individuals, and is similar in variance to that found among different macaque species. Additionally, experience with osteology and morphometrics both positively contribute to precision in multiple landmarking sessions, even where less experienced researchers have been trained in point acquisition. Individual training increases precision (although not necessarily accuracy), and is highly recommended in any situation where multiple researchers will be collecting data for a single project.

Novel 3-dimensional analysis to evaluate temporomandibular joint space and shape.

INTRODUCTION: The purpose of this study was to present and validate a novel semiautomated method for 3-dimensional evaluation of the temporomandibular joint (TMJ) space and condylar and articular shapes using cone-beam computed tomographic data. METHODS: The protocol for 3-dimensional analysis with the Checkpoint software (Stratovan, Davis, Calif) was established by analyzing cone-beam computed tomographic images of 14 TMJs representing a range of TMJ shape variations. Upon establishment of the novel method, analysis of 5 TMJs was further repeated by several investigators to assess the reliability of the analysis. RESULTS: Principal components analysis identified 3 key components that characterized how the condylar head shape varied among the 14 TMJs. Principal component analysis allowed determination of the minimum number of landmarks or patch density to define the shape variability in this sample. Average errors of landmark placement ranged from 1.15% to 3.65%, and none of the 121 landmarks showed significant average errors equal to or greater than 5%. Thus, the mean intraobserver difference was small and within the clinically accepted margin of error. Interobserver error was not significantly greater than intraobserver error, indicating that this is a reliable methodology. CONCLUSIONS: This novel semiautomatic method is a reliable tool for the 3-dimensional analysis of the TMJ including both the form and the space between the articular eminence and the condylar head.

New endemic platyrrhine humerus from Haiti and the evolution of the Greater Antillean platyrrhines.

Much debate surrounds the phylogenetic affinities of the endemic Greater Antillean platyrrhines. Thus far, most phylogenetic analyses have been constructed and tested using craniodental characters. We add to this dialog by considering how features of the distal humerus support or refute existing hypotheses for the origins of fossil Caribbean primates, utilizing three-dimensional geometric morphometric data in combination with character based cladistic analyses. We also add to the sample of fossil platyrrhine humeri with the description of UF 114718, a new distal humerus from Haiti. We reconstruct UF 114718 to be a generalized, arboreal quadruped attributed to the species Insulacebus toussantiana. Our results from phylogenetic analyses lend some support to the idea that some Greater Antillean fossil taxa including Xenothrix mcgregori, Antillothrix bernensis, and Insulacebus toussaintiana could form a monophyletic clade that is sister to either extant Platyrrhini or basal pitheciids. Based on the distal humeral data, we reconstruct the earliest ancestral platyrrhine to be a generalized, arboreal quadruped that potentially emphasized pronated arm postures during locomotion and may have engaged in some limited climbing, most similar in shape to early anthropoids and some of the earliest Antillean forms. However, aspects of shape and standard qualitative characters relating to the distal humerus seem to be variable and prone to both homoplasy and reversals; thus these results must be interpreted cautiously and (where possible) within the context provided by other parts of the skeleton.

Shape Ontogeny of the Distal Femur in the Hominidae with Implications for the Evolution of Bipedality.

Heterochrony has been invoked to explain differences in the morphology of modern humans as compared to other great apes. The distal femur is one area where heterochrony has been hypothesized to explain morphological differentiation among Plio-Pleistocene hominins. This hypothesis is evaluated here using geometric morphometric data to describe the ontogenetic shape trajectories of extant hominine distal femora and place Plio-Pleistocene hominins within that context. Results of multivariate statistical analyses showed that in both Homo and Gorilla, the shape of the distal femur changes significantly over the course of development, whereas that of Pan changes very little. Development of the distal femur of Homo is characterized by an elongation of the condyles, and a greater degree of enlargement of the medial condyle relative to the lateral condyle, whereas Gorilla are characterized by a greater degree of enlargement of the lateral condyle, relative to the medial. Early Homo and Australopithecus africanus fossils fell on the modern human ontogenetic shape trajectory and were most similar to either adult or adolescent modern humans while specimens of Australopithecus afarensis were more similar to Gorilla/Pan. These results indicate that shape differences among the distal femora of Plio-Pleistocene hominins and humans cannot be accounted for by heterochrony alone; heterochrony could explain a transition from the distal femoral shape of early Homo/A. africanus to modern Homo, but not a transition from A. afarensis to Homo. That change could be the result of genetic or epigenetic factors.

1.32 ± 0.11 Ma age for underwater remains constrain antiquity and longevity of the Dominican primate Antillothrix bernensis.

Endemic New World monkeys are an important element of the extinct mammal faunas of the Caribbean's Greater Antilles. Here we report the first geochronometric evidence that the primate Antillothrix bernensis existed in the Dominican Republic during the Pleistocene, based on the uranium-series age of carbonate speleothem that encased a tibia when it was collected in a flooded cave. Three-dimensional geometric morphometrics of laser-scanned living and extinct samples provide evidence to support the hypothesis that this specimen and other Dominican primate tibial remains belong to that same species. U-Th dating of the host cave carbonate returns ages consistently at the 600 ka upper limit of the technique. However, U-Pb, capable of resolving ages of greater antiquity, is more robust in this context, returning a secure age of 1.32 ± 0.11 Ma, which is the oldest chronometric age recorded for a Hispaniolan mammal. While its origins and manner and time of arrival are obscure, the morphometric studies are consistent with phylogenetic analyses that place A. bernensis within the pitheciid clade of the platyrrhines. The species apparently endured for over 1 million years during the climatic perturbations of the Pleistocene, as a frugivorous climbing quadruped, one of two known primate species occupying the hazard prone island of Hispaniola.

Shape analysis of the proximal humerus in orthograde and semi-orthograde primates: correlates of suspensory behavior.

"Suspensory locomotion" is an expression that encompasses a series of specialized forms of locomotion that mainly orthograde primates use to achieve below-branch traveling. It implies a number of features in the entire body associated with the use of the forelimb in overhead positions. The glenohumeral joint is one of the main joints involved in effective suspensory locomotion, being subject to a delicate balance between the high degree of mobility and stabilization needed to successfully engage in suspensory behaviors. Here, we present a 3D geometric morphometric study that explores the form of the proximal humerus of six orthograde and semi-orthograde genera (Hylobates, Pongo, Pan, Gorilla, Ateles, and Lagothrix) and a pronograde genus, Colobus, to determine to what extent suspensory locomotor requirements are driving the shape of this epiphysis. Results show the presence of a morphocline related to degree of suspension in the shape of the articular surface, with highly suspensory taxa (i.e., Hylobates) exhibiting particular morphological traits at the articular surface that provide a greater range of circumduction. The placement and orientation of the rotator cuff muscles' insertion sites on the tubercles appear associated with the divergent forces operating at the joint in quadrupedal or above-head use of the hand.

Phenetic and functional analyses of the distal ulna of Australopithecus afarensis and Australopithecus africanus.

The morphology of the distal portion of the hominoid ulna is poorly studied despite its important functional role at the wrist joint. There are five qualitatively well-described fossil hominin distal ulnae belonging to Australopithecus afarensis and Australopithecus africanus, but there have been few efforts to quantify their morphology or relate it to their functional abilities. This article presents an effort to do so, using three-dimensional geometric morphometrics to analyze the shape of the distal ulna of the Plio-Pleistocene hominins and an extant comparative sample of great apes and humans. For the extant taxa, results show that the morphology of Pan and Pongo is distinct from that of Homo, and that these differences are likely related to climbing, clambering and below-branch suspension in the former, and the release of the limbs from locomotion and (potentially) tool manufacture in the latter. For the australopiths, results indicate that the A. afarensis sample is relatively heterogeneous. These results are driven by the morphology of A.L. 333-12, which is the largest ulna in the sample and has a unique combination of traits when compared with the other two A. afarensis specimens. Overall, the morphology of all the hominins was most consistent with the pattern displayed by extant great apes, and specifically Pan and Pongo; however, large overlap in shape in the distal ulna in the extant sample indicates that other areas of the skeleton may be more informative for functional analyses.

Evaluation of a new method of fossil retrodeformation by algorithmic symmetrization: crania of papionins (Primates, Cercopithecidae) as a test case.

Diagenetic distortion can be a major obstacle to collecting quantitative shape data on paleontological specimens, especially for three-dimensional geometric morphometric analysis. Here we utilize the recently-published algorithmic symmetrization method of fossil reconstruction and compare it to the more traditional reflection & averaging approach. In order to have an objective test of this method, five casts of a female cranium of Papio hamadryas kindae were manually deformed while the plaster hardened. These were subsequently "retrodeformed" using both algorithmic symmetrization and reflection & averaging and then compared to the original, undeformed specimen. We found that in all cases, algorithmic retrodeformation improved the shape of the deformed cranium and in four out of five cases, the algorithmically symmetrized crania were more similar in shape to the original crania than the reflected & averaged reconstructions. In three out of five cases, the difference between the algorithmically symmetrized crania and the original cranium could be contained within the magnitude of variation among individuals in a single subspecies of Papio. Instances of asymmetric distortion, such as breakage on one side, or bending in the axis of symmetry, were well handled, whereas symmetrical distortion remained uncorrected. This technique was further tested on a naturally deformed and fossilized cranium of Paradolichopithecus arvernensis. Results, based on a principal components analysis and Procrustes distances, showed that the algorithmically symmetrized Paradolichopithecus cranium was more similar to other, less-deformed crania from the same species than was the original. These results illustrate the efficacy of this method of retrodeformation by algorithmic symmetrization for the correction of asymmetrical distortion in fossils. Symmetrical distortion remains a problem for all currently developed methods of retrodeformation.

The femur of Orrorin tugenensis exhibits morphometric affinities with both Miocene apes and later hominins.

Orrorin tugenensis (Kenya, ca. 6 Ma) is one of the earliest putative hominins. Its proximal femur, BAR 1002'00, was originally described as being very human-like, although later multivariate analyses showed an australopith pattern. However, some of its traits (for example, laterally protruding greater trochanter, medially oriented lesser trochanter and presence of third trochanter) are also present in earlier Miocene apes. Here, we use geometric morphometrics to reassess the morphological affinities of BAR 1002'00 within a large sample of anthropoids (including fossil apes and hominins) and reconstruct hominoid proximal femur evolution using squared-change parsimony. Our results indicate that both hominin and modern great ape femora evolved in different directions from a primitive morphology represented by some fossil apes. Orrorin appears intermediate between Miocene apes and australopiths in shape space. This evidence is consistent with femoral shape similarities in extant great apes being derived and homoplastic and has profound implications for understanding the origins of human bipedalism.

The distal tibia of Hispanopithecus laietanus: more evidence for mosaic evolution in Miocene apes.

IPS18800 is a partial skeleton attributed to the fossil great ape Hispanopithecus laietanus, and dated to 9.6 Ma (millions of years ago). Previous studies on the postcranial anatomy of this taxon have shown that it displayed a derived, extant great ape-like orthograde body plan with suspensory adaptations, uniquely coupled with adaptations for above-branch pronograde locomotion. Here, for the first time, we describe and analyze in detail the distal tibia of the IPS18800 skeleton of Hispanopithecus with the aid of three-dimensional geometric morphometrics based on 53 landmarks and semilandmarks collected on a broad sample of extant catarrhines and fossil hominoids. Results of principal components and canonical variate analyses reveal that the distal tibia of Hispanopithecus occupies a unique position in the morphospace, similar in some respects to pronograde monkeys, and in other respects to extant apes. The IPS18800 distal tibia combines adaptations for above branch quadrupedalism, such as a keeled trochlear surface and strong intercollicular groove, with adaptations for vertical climbing, such as an anteroposteriorly flattened shaft, enlarged fibular facet and a tibial stop. These results on the distal tibia agree with those from other anatomical regions, indicating that this taxon displayed a locomotor repertoire unlike any extant ape, combining vertical climbing and clambering with above-branch quadrupedalism.

Forelimb to hindlimb shape covariance in extant hominoids and fossil hominins.

Researchers often attempt to use limb proportions to ascertain the locomotor repertoires of fossil hominins. This can be problematic as there are few skeletons in the fossil record that preserve both a full forelimb and hindlimb; therefore, estimates of full limb lengths are typically associated with substantial error. In this study, two-block partial least squares analyses were used to examine covariation between forelimb and hindlimb elements in extant hominoids and fossil hominins. This has the benefit of including both forelimb and hindlimb in a type of functional analysis without necessitating an accurate length estimate. There is a high degree of covariation between forelimb and hindlimb segments in the mixed species sample, particularly in the proximal ulna, distal humerus, and proximal/distal femur and that shape covariation is significantly correlated with intermembral indices in the extant taxa. Overall, the fossil hominins most closely resembled modern humans with the exception of analyses utilizing the distal femur where some occupied a unique morphological position; thus, some fossil hominins likely possessed locomotor capabilities similar to modern humans, whereas others likely represent a unique morphological compromise between terrestrial bipedality and other positional behaviors not present among extant hominoids.

Morphology of the distal radius in extant hominoids and fossil hominins: implications for the evolution of bipedalism.

One of the long-standing arguments about the evolution of bipedality centers on the locomotor pattern used by the last common ancestor (LCA) of apes and humans. In particular, knuckle-walking has been suggested as this locomotor pattern on the basis of shared morphology in the upper limb between African apes and humans and phylogenetic parsimony. Using three-dimensional geometric morphometrics, this study tests whether the distal radius of extant hominoids is sufficient for determining locomotor pattern and the affiliations of Plio-Pleistocene hominins to the extant taxa. Results indicate that while the entire radius differentiates the extant taxa very well by locomotor pattern, the distal radius fails to clearly differentiate the extant taxa. The sigmoid notch of the distal radius is the anatomical feature that differs most among the extant taxa, and its variability broadly correlates with necessary mobility at the wrist joint. Principal components and discriminant function analyses indicate that early hominins are affiliated with a variety of extant taxa with different locomotor patterns. Overall, the bony anatomy of the distal radius of early hominins points towards something adapted for a wide variety of locomotor postures.