Climate and Human Evolution: Insights from Marine Records.

The relationship between climate and human evolution is complex, and the causal mechanisms remain unknown. Here, we review and synthesize what is currently known about climate forcings on African landscapes, focusing mainly on the last 4 million years. We use information derived from marine sediment archives and data-numerical climate model comparisons and integration. There exists a heterogeneity in pan-African hydroclimate changes, forced by a combination of orbitally paced, low-latitude fluctuations in insolation; polar ice volume changes; tropical sea surface temperature gradients; the Walker circulation; and possibly greenhouse gases. Pan-African vegetation changes do not follow the same pattern, which is suggestive of additional influences, such as CO2 and temperature. We caution against reliance on temporal correlations between global or regional climate, environmental changes, and human evolution and briefly proffer some ideas on how pan-African climate trends could help create novel conceptual frameworks to determine the causal mechanisms of associations between climate/habitat change and hominin evolution.

Do rates of dental wear in extant African great apes inform the time of weaning?

Reconstructing the life histories of extinct hominins remains one of the main foci of paleoanthropological inquiry, as an extended juvenile period impacts the social and cognitive development of species. However, the paucity of hominin remains, the lack of comparative hominoid data, and the destructive nature of many life history approaches have limited our understanding of the relationship between dental development (eruption) and weaning in primates. Alternatively, the rate of dental wear in early-forming teeth has been suggested a good proxy for the timing of weaning. Here we test this hypothesis on an ontogenetic series of Gorilla gorilla gorilla and Pan troglodytes troglodytes, using geographic information systems-based shape descriptors of M1s in relation to the nitrogen (δ15N) and carbon (δ13C) isotope composition of their associated hair. Results show that Gorilla g. gorilla are fully weaned considerably later than Pan t. troglodytes, that is, after M1s had been in full functional occlusion for some time. Yet, throughout ontogeny, gorilla dental wear rates are greater than they are in chimpanzees. This refutes the hypothesis that the rates of wear of early-forming teeth inform the time of weaning (i.e., nutritional independence). Instead, dietary breadth and seasonal variation in resource availability are implicated. This finding has implications for interpreting the hominin fossil record and raises questions about the triggers for, and the mechanisms of, life history change in hominin evolution. As a case in point, commonalities in life history patterns between early hominins and Western lowland gorillas seem to be a means to mitigate the effects of recurrent (i.e., seasonal) resource limitations and-conceivably-to prevent high infant mortality rates. Taken further, difference between hominid life histories are likely to be of degree, not kind.

The partial skeleton StW 431 from Sterkfontein - Is it time to rethink the Plio-Pleistocene hominin diversity in South Africa?

The discovery of the nearly complete Plio-Pleistocene skeleton StW 573 Australopithecus prometheus from Sterkfontein Member 2, South Africa, has intensified debates as to whether Sterkfontein Member 4 contains a hominin species other than Australopithecus africanus. For example, it has recently been suggested that the partial skeleton StW 431 should be removed from the A. africanus hypodigm and be placed into A. prometheus. Here we re-evaluate this latter proposition, using published information and new comparative data. Although both StW 573 and StW 431 are apparently comparable in their arboreal (i.e., climbing) and bipedal adaptations, they also show significant morphological differences. Surprisingly, StW 431 cannot be unequivocally aligned with either StW 573 or other hominins from Sterkfontein commonly attributed to A. africanus (nor with Paranthropus robustus and Australopithecus sediba). This finding, together with considerations about the recent dating of Plio-Pleistocene hominin-bearing sites in South Africa and palaeoecological/palaeoclimatic conditions, raises questions whether it is justified to subsume hominins from Taung, Makapansgat and Sterkfontein (and Gladysvale) within a single taxon. Given the wealth of fossil material and analytical techniques now available, we call for a re-evaluation of the taxonomy of South African Plio-Pleistocene hominins. Such an endeavour should however go beyond the current (narrow) focus on establishing an A. africanus-A. prometheus dichotomy.

On the relationship between maxillary molar root shape and jaw kinematics in Australopithecus africanus and Paranthropus robustus.

Plio-Pleistocene hominins from South Africa remain poorly understood. Here, we focus on how Australopithecus africanus and Paranthropus robustus exploited and-in part-partitioned their environment. Specifically, we explore the extent to which first maxillary molar roots (M1) are oriented and thus, by proxy, estimate the direction of loads habitually exerted on the chewing surface. Landmark-based shape analysis of M1 root reconstructions of 26 South African hominins and three East African Paranthropus boisei suggest that A. africanus may have been able to dissipate the widest range of laterally directed loads. Paranthropus robustus and P. boisei, despite having overlapping morphologies, differ in aspects of root shape/size, dento-cranial morphologies, microwear textures and C4 food consumption. Hence, while Paranthropus monophyly cannot be excluded, equivalence of dietary niche can. The South African hominins occupied distinct ecological niches, whereby P. robustus appears uniquely adapted to dissipate antero-posteriorly directed loads.

Pliocene hominin biogeography and ecology.

Australopithecus bahrelghazali, its origin and palaeobiology are not well understood. Reported from only one location some several thousand kilometres away from East African Pliocene hominin sites, it appears to have predominantly fed on C4 sources. Yet, it lacks the morphological adaptations of other primate C4 consumers like Paranthropus boisei and Theropithecus oswaldi. Furthermore, although considered to belong to Australopithecus afarensis by most researchers, A. bahrelghazali appears to differ from the former in a key aspect of its morphology: enamel thickness. To assess the phylogeny and palaeobiology of A. bahrelghazali, I first evaluate the dietary adaptations and energetics of A. bahrelghazali using empirical data of the feeding ecology of extant baboons, Papio cynocephalus. Information published on A. bahrelghazali morphology and habitat preference is used to select C4 foods with the appropriate mechanical properties and availability within the environment to create the models. By altering the feeding time on various food categories, I then test whether A. bahrelghazali could have subsisted on a C4 diet, thus accounting for the δ(13)C composition of its dental tissue. The effects of body mass on the volume of food consumed are taken into account. The outcomes of these simulations indicate that A. bahrelghazali could have subsisted on a diet of predominantly sedges, albeit with limitations. At higher energy requirements, i.e., above 3.5 times the BMR, it would be difficult for a medium-sized primate to obtain sufficient energy from a sedge-based diet. This is apparently due to constraints on foraging/feeding time, not because of the nutritional value of sedges per se. These results are discussed against the backdrop of A. bahrelghazali biogeography, palaeoenvironment, and phylogeny. The combined evidence makes it plausible to suggest that Northern Chad may have been a refugium for migrating mammals, including hominins, and throws new light on the deep history of A. bahrelghazali.

Niche partitioning in sympatric Gorilla and Pan from Cameroon: implications for life history strategies and for reconstructing the evolution of hominin life history.

Factors influencing the hominoid life histories are poorly understood, and little is known about how ecological conditions modulate the pace of their development. Yet our limited understanding of these interactions underpins life history interpretations in extinct hominins. Here we determined the synchronisation of dental mineralization/eruption with brain size in a 20th century museum collection of sympatric Gorilla gorilla and Pan troglodytes from Central Cameroon. Using δ13C and δ15N of individuals' hair, we assessed whether and how differences in diet and habitat use may have impacted on ape development. The results show that, overall, gorilla hair δ13C and δ15N values are more variable than those of chimpanzees, and that gorillas are consistently lower in δ13C and δ15N compared to chimpanzees. Within a restricted, isotopically-constrained area, gorilla brain development appears delayed relative to dental mineralization/eruption [or dental development is accelerated relative to brains]: only about 87.8% of adult brain size is attained by the time first permanent molars come into occlusion, whereas it is 92.3% in chimpanzees. Even when M1s are already in full functional occlusion, gorilla brains lag behind those of chimpanzee (91% versus 96.4%), relative to tooth development. Both bootstrap analyses and stable isotope results confirm that these results are unlikely due to sampling error. Rather, δ15N values imply that gorillas are not fully weaned (physiologically mature) until well after M1 are in full functional occlusion. In chimpanzees the transition from infant to adult feeding appears (a) more gradual and (b) earlier relative to somatic development. Taken together, the findings are consistent with life history theory that predicts delayed development when non-density dependent mortality is low, i.e. in closed habitats, and with the "risk aversion" hypothesis for frugivorous species as a means to avert starvation. Furthermore, the results highlight the complexity and plasticity of hominoid/hominin development.

Baboon feeding ecology informs the dietary niche of Paranthropus boisei.

Hominins are generally considered eclectic omnivores like baboons, but recent isotope studies call into question the generalist status of some hominins. Paranthropus boisei and Australopithecus bahrelghazali derived 75%-80% of their tissues' δ(13)C from C4 sources, i.e. mainly low-quality foods like grasses and sedges. Here I consider the energetics of P. boisei and the nutritional value of C4 foods, taking into account scaling issues between the volume of food consumed and body mass, and P. boisei's food preference as inferred from dento-cranial morphology. Underlying the models are empirical data for Papio cynocephalus dietary ecology. Paranthropus boisei only needed to spend some 37%-42% of its daily feeding time (conservative estimate) on C4 sources to meet 80% of its daily requirements of calories, and all its requirements for protein. The energetic requirements of 2-4 times the basal metabolic rate (BMR) common to mammals could therefore have been met within a 6-hour feeding/foraging day. The findings highlight the high nutritional yield of many C4 foods eaten by baboons (and presumably hominins), explain the evolutionary success of P. boisei, and indicate that P. boisei was probably a generalist like other hominins. The diet proposed is consistent with the species' derived morphology and unique microwear textures. Finally, the results highlight the importance of baboon/hominin hand in food acquisition and preparation.

Intronic tandem repeat in the serotonin transporter gene in Old World monkeys: a new transcriptional regulator?

The serotonin transporter gene (SLC6A4) is heavily involved in the regulation of social behaviour of primates. Old World monkeys (e.g. macaques, baboons) have been used to study interactions between variation in the SLC6A4 gene and behaviour. Correlations of variation at one polymorphism located in the promoter region (known as 5HTTLPR) and variation at SLC6A4 expression levels, serotonin turnover and behaviour has been widely studied. In Old World monkeys, the third intron of the SLC6A4 gene also presents a tandem repeat, which sequence varies across species by a few point substitutions. We predict that in these species, this repeated region also acts as transcriptional regulatory domain and that sequence variation at this polymorphic locus might result in differential levels of expression in gene-environment interactions. For testing these hypotheses, the tandem repeat of Mandrillus sphinx and Cercopithecus aethiops from the third intron were cloned into a reporter gene vector and delivered to either primary cultures of rat neonate frontal cortex or the human cell line (JAr) to analyse their transcriptional activities. These repeated sequences supported significantly different levels of gene expression only when delivered into frontal cortex cultures. Furthermore, we tested in silico if such substitutions could have an effect on their binding profile to RNA- and DNA-binding proteins and on splicing. Taken together our results suggest that the tandem repeat in the third intron of the SLC6A4 gene of Old World monkeys could constitute a second transcriptional regulator as suggested for the 5HTTLPR and therefore contribute to diversification of serotonin-related behaviour in these primates.

An evolutionary conserved region (ECR) in the human dopamine receptor D4 gene supports reporter gene expression in primary cultures derived from the rat cortex.

BACKGROUND: Detecting functional variants contributing to diversity of behaviour is crucial for dissecting genetics of complex behaviours. At a molecular level, characterisation of variation in exons has been studied as they are easily identified in the current genome annotation although the functional consequences are less well understood; however, it has been difficult to prioritise regions of non-coding DNA in which genetic variation could also have significant functional consequences. Comparison of multiple vertebrate genomes has allowed the identification of non-coding evolutionary conserved regions (ECRs), in which the degree of conservation can be comparable with exonic regions suggesting functional significance. RESULTS: We identified ECRs at the dopamine receptor D4 gene locus, an important gene for human behaviours. The most conserved non-coding ECR (D4ECR1) supported high reporter gene expression in primary cultures derived from neonate rat frontal cortex. Computer aided analysis of the sequence of the D4ECR1 indicated the potential transcription factors that could modulate its function. D4ECR1 contained multiple consensus sequences for binding the transcription factor Sp1, a factor previously implicated in DRD4 expression. Co-transfection experiments demonstrated that overexpression of Sp1 significantly decreased the activity of the D4ECR1 in vitro. CONCLUSION: Bioinformatic analysis complemented by functional analysis of the DRD4 gene locus has identified a) a strong enhancer that functions in neurons and b) a transcription factor that may modulate the function of that enhancer.

Ontogenetic changes in the internal and external morphology of the ilium in modern humans.

Trabecular architecture forms an important structural component of bone and, depending on the loading conditions encountered during life, is organised in a systematic, bone- and species-specific manner. However, recent studies suggested that gross trabecular arrangement (e.g. density distribution), like overall bone shape, is predetermined and/or affected by factors other than loading and perhaps less plastic than commonly assumed. To explore this issue further, the present cross-sectional ontogenetic study investigated morphological changes in external bone shape in relation to changes in trabecular bundle orientation and anisotropy. Radiographs of 73 modern human ilia were assessed using radiographic and Geometric Morphometric techniques. The study confirmed the apparently strong predetermination of trabecular bundle development, i.e. prior to external loading, although loading clearly also had an effect on overall morphology. For example, the sacro-pubic bundle, which follows the path of load transmission from the auricular surface to the acetabulum, is well defined and shows relatively high levels of anisotropy from early stages of development; the situation for the ischio-iliac strut is similar. However, while the sacro-pubic strut retains a constant relationship with the external landmarks defining the joint surfaces, the ischio-iliac bundle changes its relationship with the external landmarks and becomes aligned with the iliac tubercle only during late adolescence/early adulthood. It is tentatively proposed that the rearrangement of the ischio-iliac strut may reflect a change in locomotor pattern and/or a shift in positional behavior with increasing mass after growth of external bone dimensions has slowed/ceased.

Kinematic parameters inferred from enamel microstructure: new insights into the diet of Australopithecus anamensis.

The dietary adaptations of Australopithecus anamensis are contentious, with suggestions that range from soft fruits to hard, brittle, tough, and abrasive foods. It is unlikely that all propositions are equally valid, however. Here we extend recent finite element (FE) analyses of enamel microstructure (Shimizu and Macho, 2008) to enquire about the range of loading directions (i.e., kinematics) to which A. anamensis enamel microstructure/molars could safely be subjected. The rationale underlying this study is the observation that hard brittle foods are broken down in crush, while tough foods require shear. The findings are compared with those of Pan and Gorilla. Eighteen detailed FE models of enamel microstructure were created and analysed. The results highlight the uniqueness of A. anamensis dental structure and imply that mastication in this species included a greater shear component than in Pan, as well as a wider range of loading directions; it is similar to that in Gorilla in this respect. These findings are in accord with microwear studies (Grine et al., 2006a). Unlike either of the great apes, however, enamel microstructure of A. anamensis was found to be poorly equipped to withstand loading parallel to the dentino-enamel junction; such loading regimes are associated with mastication of soft fleshy fruits. This, together with broader morphological considerations, raises doubts as to whether A. anamensis was essentially a frugivore that expanded its dietary niche as a result of fluctuations in environmental conditions, e.g., during seasonal food shortages. Instead, it is more parsimonious to conclude that the habitual diet of A. anamensis differed considerably from that of either of the extant African great apes.

An exploratory study on the combined effects of external and internal morphology on load dissipation in primate capitates: its potential for an understanding of the positional and locomotor repertoire of early hominins.

This pilot study explored whether the redirection of stress through trabeculae within morphologically constrained capitates provides information about habitual/positional behaviours unavailable from the study of external morphology alone. To assess this possibility, an experimental finite element approach was taken, whereby no attempt was made to reconstruct the actual magnitudes and loading conditions experienced by the capitates in vivo. Rather, this work addressed fundamental biological questions relating to bone plasticity, i.e. internal versus external bone morphology. The capitates of 7 species with different and - in the case of fossils - inferred locomotor behaviours were selected. Virtual models of capitates were created, scaled to the same size and subjected to the same theoretical load. In the first set of analyses, models were assigned the material properties of bone throughout, whereas in the second set, models were assigned 11 different material properties representing the trabecular architecture derived from high-resolution CT. Species with arboreal behaviours consistently redirected loads towards the ulnar aspect of the capitate when trabeculae were introduced, while terrestrial species, and the bipedal Homo, redirected stress towards the radial side. From these preliminary analyses, it is tentatively concluded that Australopithecus anamensis habitually engaged in arboreal behaviours, whereas Australopithecus afarensis did not.

Dietary adaptations of South African australopiths: inference from enamel prism attitude.

The angle at which enamel prisms approach the wear surface holds information with regard to the stiffness of the tissue, as well as its wear resistance. Hence, analyses of prism orientation may shed light on questions of whether the thick enamel in hominins has evolved to confer stiffness or wear resistance to the teeth and may thus inform about the diet and behavioural ecology of these species. This was explored for Paranthropus robustus and Australopithecus africanus, whereby a distinction was made between prisms at the Phase I and Phase II facets. The results were compared with those obtained for Theropithecus, Macaca, and Potamochoerus for whom behavioural and/or experimental data are available, and were interpreted against simple mechanical principles. The South African hominins differ significantly in their relationships between wear facets and prism angulations. Teeth of P. robustus are better adapted to more vertical loads during mastication (Phase I), whereas those of A. africanus are better adapted to cope with more laterally-directed loads (Phase II) commonly associated with roll-crush and mastication. Overall, teeth of P. robustus appear stiffer, while those of A. africanus seem more wear resistant.

Effect of enamel prism decussation and chemical composition on the biomechanical behavior of dental tissue: a theoretical approach to determine the loading conditions to which modern human teeth are adapted.

This theoretical study explored whether the directions of loads to which modern human molars are commonly subjected to are reflected in the biomechanical behavior of the tissue itself. A detailed finite element model of a piece of decussating enamel (M(3) paracone) was created, taking into account differences in crystal orientation between the prism head and the interprismatic matrix, and was tested under differently angled mediolateral loads (i.e., mimicking various stages of the chewing cycle). Second, although teeth are highly mineralized, they also contain organic material and water, while in modern humans, there are systematic differences in chemical composition from the outer enamel surface to the dentinoenamel junction. To test the biomechanical effects of this gradient in mineralization a second set of models with gradually changing properties was created and subjected to the same loads. Chemically heterogeneous enamel yielded overall lower stress levels than homogenous enamel, especially at extreme loading angles. However, the general trends regarding the increase in tensile stresses at more oblique angles, and the number of nodes exhibiting tension, were comparable between the different set-ups. The findings support suggestions that (a) the biomechanical behavior of dental tissue is the combined result of micromorphology and chemical composition and (b) that the range of loading directions, to which teeth are normally subjected to, can be inferred from dental microanatomy. For (palaeo)biological applications, the findings suggest that the absolute strength of teeth (e.g., bite force) cannot be predicted with certainty, whereas kinematic parameters of the masticatory apparatus can.

Functional significance of the microstructural detail of the primate dentino-enamel junction: a possible example of exaptation.

In primate teeth, the dentino-enamel junction (DEJ) exhibits a scalloped appearance, the functional importance of which has been the subject of various suggestions and speculations. Simplified finite-element (FE) models of DEJ microanatomy were created, both in 2D and 3D, and their biomechanical behavior was tested and compared. Consistently, the models with the scalloped DEJ, although having higher maximum tensile stresses than the straight DEJ models, showed discontinuous concentrations of stress. In straight DEJ models, tensile stresses act at the DEJ over continuous areas in a direction, which would push the two tissues apart, thus leading to delamination of the DEJ. Perhaps even more important, in the scallop model, the net-compression towards the DEJ was consistently higher than net-tension away from it. As a consequence, dentine and enamel would be pushed towards each other during loading (i.e., during mastication). These findings suggest that the scalloped nature of the DEJ confers a biomechanical advantage to the integrity of the tooth during mastication. Furthermore, there exists a correlation between pronounced prism decussation and scallop magnitude, suggesting that scallops may have been selected for in response to high bite forces. However, given the equivocal relationship between scallops and presumed bite force across mammalian taxa, we propose that scallops could in fact be exaptations.

Automated method to measure trabecular thickness from microcomputed tomographic scans and its application.

Trabeculae form the internal bony mesh work and provide strength to the bone; interconnectivity, overall density, and trabecular thickness are important measures of the integrity of the internal architecture. Such strength is achieved only gradually during ontogeny, whereby an increase in trabecular thickness precedes an increase in mineralization. Loss of bone mass later in life may be compensated for by thickening of the remaining trabeculae. These facts, and the role of trabeculae in mineral homeostasis, highlight the importance of investigating trabecular thickness within and between species. While nondestructive imaging techniques (i.e., muCT and MRI) are becoming increasingly popular, quantification of trabecular thickness using nondestructive techniques has proved difficult owing to limitations imposed by scanning parameters, uniform thresholding, and partial volume averaging. Here we present a computer application, which aims to overcome these problems. Validation is carried out against a phantom and against trabecular thickness measured in corresponding histological sections. Good agreement was found between these measurements. Furthermore, when trabecular thickness is recorded for modern human fetal ilia, a trend toward trabecular thickness increase is found and is in line with reports of ontogenetic morphometric changes using histological sections. However, there are discrepancies. These may in part be due to partial volume effects of obliquely oriented structures. More crucial, however, are problems inherent in histological sections, e.g., shrinkage and distortion, especially where differences in mineralization are concerned; this may affect biological interpretations.

Australopithecus anamensis: a finite-element approach to studying the functional adaptations of extinct hominins.

Australopithecus anamensis is the stem species of all later hominins and exhibits the suite of characters traditionally associated with hominins, i.e., bipedal locomotion when on the ground, canine reduction, and thick-enameled teeth. The functional consequences of its thick enamel are, however, unclear. Without appropriate structural reinforcement, these thick-enameled teeth may be prone to failure. This article investigates the mechanical behavior of A. anamensis enamel and represents the first in a series that will attempt to determine the functional adaptations of hominin teeth. First, the microstructural arrangement of enamel prisms in A. anamensis teeth was reconstructed using recently developed software and was compared with that of extant hominoids. Second, a finite-element model of a block of enamel containing one cycle of prism deviation was reconstructed for Homo, Pan, Gorilla, and A. anamensis and the behavior of these tissues under compressive stress was determined. Despite similarities in enamel microstructure between A. anamensis and the African great apes, the structural arrangement of prismatic enamel in A. anamensis appears to be more effective in load dissipation under these compressive loads. The findings may imply that this hominin species was well adapted to puncture crushing and are in some respects contrary to expectations based on macromorphology of teeth. Taking together, information obtained from both finite-element analyses and dental macroanatomy leads us to suggest that A. anamensis was probably adapted for habitually consuming a hard-tough diet. However, additional tests are needed to understand the functional adaptations of A. anamensis teeth fully.

Effect of prism orientation and loading direction on contact stresses in prismatic enamel of primates: implications for interpreting wear patterns.

The ability of prisms to effectively dissipate contact stress at the surface will influence wear rates in teeth. The aim of this investigation was to begin to quantify the effect of prism orientation on surface stresses. Seven finite element models of enamel microstructure were created, each model differing in the angulation of prism orientation with regard to the wear surface. For validation purposes, the mechanical behavior of the model was compared with published experimental data. In order to test the enamel under lateral loads, a compressed food particle was dragged across the surface from the dentino-enamel junction (DEJ) towards the outer enamel surface (OES). Under these conditions, tensile stresses in the enamel model increased with increases in the coefficient of friction. More importantly, stresses were found to be lowest in models in which the prisms approach the surface at lower angles (i.e., more obliquely cut prisms), and highest when the prisms approached the surface at 60 degrees (i.e., less obliquely cut). Finally, the direction of travel of the simulated food particle was reversed, allowing comparison of the difference in behavior between trailing and leading edge enamels (i.e., when the food particle was dragged either towards or away from the DEJ). Stresses at the trailing edge were usually lower than stresses at the leading edge. Taken together with what is known about prism orientation in primate teeth, such findings imply greater wear resistance at the intercuspal region and less wear resistance at the lateral enamel at midcrown. Such findings appear to be supported by archeological evidence.

On the scaling relationship between enamel prism length and enamel thickness in primate molars: a comment.

As part of a larger study we developed a computer programme which allows the recreation of the complex 3-dimensional arrangement of prisms. Data presented in these earlier publications are re-analyzed to assess the relationship between projected prism length (i. e., enamel thickness) and the true prism length. Across primates, proportional prism deviation increases as the enamel becomes thicker. This supports suggestions that prism decussation may be particularly marked in large-bodied and thick-enameled species. There are differences, however, in scaling relationships between species, which correspond to the species' dietary adaptations. Finally, the findings highlight the importance of employing species-specific correction factors for the calculation of prism length (i.e., life-span of the ameloblast) for life history enquiry.