Behavioral and phylogenetic correlates of limb length proportions in extant apes and monkeys: Implications for interpreting hominin fossils.

The body proportions of extant animals help inform inferences about the behaviors of their extinct relatives, but relationships between body proportions, behavior, and phylogeny in extant primates remain unclear. Advances in behavioral data, molecular phylogenies, and multivariate analytical tools make it an opportune time to perform comprehensive comparative analyses of primate traditional limb length proportions (e.g., intermembral, humerofemoral, brachial, and crural indices), body size-adjusted long bone proportions, and principal components. In this study we used a mix of newly-collected and published data to investigate whether and how the limb length proportions of a diverse sample of primates, including monkeys, apes, and modern humans, are influenced by behavior and phylogeny. We reconfirm that the intermembral index, followed by the first principal component of traditional limb length proportions, is the single most effective variable distinguishing hominoids and other anthropoids. Combined limb length proportions and positional behaviors are strongly correlated in extant anthropoid groups, but phylogeny is a better predictor of limb length proportion variation than of behavior. We confirm convergences between members of the Atelidae and extant apes (especially Pan), members of the Hylobatidae and Pongo, and a potential divergence of Presbytis limb proportions from some other cercopithecoids, which correlate with adaptations for forelimb-dominated behaviors in some colobines. Collectively, these results substantiate hypotheses indicating that extinct hominins and other hominoid taxa can be distinguished by analyzing combinations of their limb length proportions at different taxonomic levels. From these results, we hypothesize that fossil skeletons characterized by notably disparate limb length proportions are unlikely to have exhibited similar behavioral patterns.

The estimation and evolution of hominin body mass.

Body mass is a critical variable in many hominin evolutionary studies, with implications for reconstructing relative brain size, diet, locomotion, subsistence strategy, and social organization. We review methods that have been proposed for estimating body mass from true and trace fossils, consider their applicability in different contexts, and the appropriateness of different modern reference samples. Recently developed techniques based on a wider range of modern populations hold promise for providing more accurate estimates in earlier hominins, although uncertainties remain, particularly in non-Homo taxa. When these methods are applied to almost 300 Late Miocene through Late Pleistocene specimens, the resulting body mass estimates fall within a 25-60 kg range for early non-Homo taxa, increase in early Homo to about 50-90 kg, then remain constant until the Terminal Pleistocene, when they decline.

Statistical estimates of hominin origination and extinction dates: A case study examining the Australopithecus anamensis-afarensis lineage.

Reliable estimates of when hominin taxa originated and went extinct are central to addressing many paleoanthropological questions, including those relating to macroevolutionary patterns. The timing of hominin temporal ranges can be used to test chronological predictions generated from phylogenetic hypotheses. For example, hypotheses of phyletic ancestor-descendant relationships, based on morphological data, predict no temporal range overlap between the two taxa. However, a fossil taxon's observed temporal range is almost certainly underestimated due to the incompleteness of both the fossil record itself and its sampling, and this decreases the likelihood of observing temporal overlap. Here, we focus on a well-known and widely accepted early hominin lineage, Australopithecus anamensis-afarensis, and place 95% confidence intervals (CIs) on its origination and extinction dates. We do so to assess whether its temporal range is consistent with it being a phyletic descendant of Ardipithecus ramidus and/or a direct ancestor to the earliest claimed representative of Homo (i.e., Ledi-Geraru). We find that the last appearance of Ar. ramidus falls within the origination CI of Au. anamensis-afarensis, whereas the claimed first appearance of Homo postdates the extinction CI. These results are consistent with Homo evolving from Au. anamensis-afarensis, but temporal overlap between Ar. ramidus and Au. anamensis-afarensis cannot be rejected at this time. Though additional samples are needed, future research should extend our initial analyses to incorporate the uncertainties surrounding the range endpoints of Ar. ramidus and earliest Homo. Overall, our findings demonstrate the need for quantifying the uncertainty surrounding the appearances and disappearances of hominin taxa in order to better understand the timing of evolutionary events in our clade's history.

Brain enlargement and dental reduction were not linked in hominin evolution.

The large brain and small postcanine teeth of modern humans are among our most distinctive features, and trends in their evolution are well studied within the hominin clade. Classic accounts hypothesize that larger brains and smaller teeth coevolved because behavioral changes associated with increased brain size allowed a subsequent dental reduction. However, recent studies have found mismatches between trends in brain enlargement and posterior tooth size reduction in some hominin species. We use a multiple-variance Brownian motion approach in association with evolutionary simulations to measure the tempo and mode of the evolution of endocranial and dental size and shape within the hominin clade. We show that hominin postcanine teeth have evolved at a relatively consistent neutral rate, whereas brain size evolved at comparatively more heterogeneous rates that cannot be explained by a neutral model, with rapid pulses in the branches leading to later Homo species. Brain reorganization shows evidence of elevated rates only much later in hominin evolution, suggesting that fast-evolving traits such as the acquisition of a globular shape may be the result of direct or indirect selection for functional or structural traits typical of modern humans.

Pattern and process in hominin brain size evolution are scale-dependent.

A large brain is a defining feature of modern humans, yet there is no consensus regarding the patterns, rates and processes involved in hominin brain size evolution. We use a reliable proxy for brain size in fossils, endocranial volume (ECV), to better understand how brain size evolved at both clade- and lineage-level scales. For the hominin clade overall, the dominant signal is consistent with a gradual increase in brain size. This gradual trend appears to have been generated primarily by processes operating within hypothesized lineages-64% or 88% depending on whether one uses a more or less speciose taxonomy, respectively. These processes were supplemented by the appearance in the fossil record of larger-brained Homo species and the subsequent disappearance of smaller-brained Australopithecus and Paranthropus taxa. When the estimated rate of within-lineage ECV increase is compared to an exponential model that operationalizes generation-scale evolutionary processes, it suggests that the observed data were the result of episodes of directional selection interspersed with periods of stasis and/or drift; all of this occurs on too fine a timescale to be resolved by the current human fossil record, thus producing apparent gradual trends within lineages. Our findings provide a quantitative basis for developing and testing scale-explicit hypotheses about the factors that led brain size to increase during hominin evolution.

Stable isotope-based diet reconstructions of Turkana Basin hominins.

Hominin fossil evidence in the Turkana Basin in Kenya from ca. 4.1 to 1.4 Ma samples two archaic early hominin genera and records some of the early evolutionary history of Paranthropus and Homo. Stable carbon isotopes in fossil tooth enamel are used to estimate the fraction of diet derived from C3 or C4 resources in these hominin taxa. The earliest hominin species in the Turkana Basin, Australopithecus anamensis, derived nearly all of its diet from C3 resources. Subsequently, by ca. 3.3 Ma, the later Kenyanthropus platyops had a very wide dietary range--from virtually a purely C3 resource-based diet to one dominated by C4 resources. By ca. 2 Ma, hominins in the Turkana Basin had split into two distinct groups: specimens attributable to the genus Homo provide evidence for a diet with a ca. 65/35 ratio of C3- to C4-based resources, whereas P. boisei had a higher fraction of C4-based diet (ca. 25/75 ratio). Homo sp. increased the fraction of C4-based resources in the diet through ca. 1.5 Ma, whereas P. boisei maintained its high dependency on C4-derived resources.

Viewpoints: diet and dietary adaptations in early hominins: the hard food perspective.

Recent biomechanical analyses examining the feeding adaptations of early hominins have yielded results consistent with the hypothesis that hard foods exerted a selection pressure that influenced the evolution of australopith morphology. However, this hypothesis appears inconsistent with recent reconstructions of early hominin diet based on dental microwear and stable isotopes. Thus, it is likely that either the diets of some australopiths included a high proportion of foods these taxa were poorly adapted to consume (i.e., foods that they would not have processed efficiently), or that aspects of what we thought we knew about the functional morphology of teeth must be wrong. Evaluation of these possibilities requires a recognition that analyses based on microwear, isotopes, finite element modeling, and enamel chips and cracks each test different types of hypotheses and allow different types of inferences. Microwear and isotopic analyses are best suited to reconstructing broad dietary patterns, but are limited in their ability to falsify specific hypotheses about morphological adaptation. Conversely, finite element analysis is a tool for evaluating the mechanical basis of form-function relationships, but says little about the frequency with which specific behaviors were performed or the particular types of food that were consumed. Enamel chip and crack analyses are means of both reconstructing diet and examining biomechanics. We suggest that current evidence is consistent with the hypothesis that certain derived australopith traits are adaptations for consuming hard foods, but that australopiths had generalized diets that could include high proportions of foods that were both compliant and tough.

Hominin fossils from Kromdraai and Drimolen inform Paranthropus robustus craniofacial ontogeny.

Ontogeny provides critical information about the evolutionary history of early hominin adult morphology. We describe fossils from the southern African sites of Kromdraai and Drimolen that provide insights into early craniofacial development in the Pleistocene robust australopith Paranthropus robustus. We show that while most distinctive robust craniofacial features appear relatively late in ontogeny, a few do not. We also find unexpected evidence of independence in the growth of the premaxillary and maxillary regions. Differential growth results in a proportionately larger and more postero-inferiorly rotated cerebral fossa in P. robustus infants than in the developmentally older Australopithecus africanus juvenile from Taung. The accumulated evidence from these fossils suggests that the iconic SK 54 juvenile calvaria is more likely early Homo than Paranthropus. It is also consistent with the hypothesis that P. robustus is more closely related to Homo than to A. africanus.

Microwear, mechanics and the feeding adaptations of Australopithecus africanus.

Recent studies of dental microwear and craniofacial mechanics have yielded contradictory interpretations regarding the feeding ecology and adaptations of Australopithecus africanus. As part of this debate, the methods used in the mechanical studies have been criticized. In particular, it has been claimed that finite element analysis has been poorly applied to this research question. This paper responds to some of these mechanical criticisms, highlights limitations of dental microwear analysis, and identifies avenues of future research.

Brief communication: Molar development and crown areas in early Australopithecus.

Recent studies suggest that the hypodigms representing the two earliest Australopithecus (Au. anamensis and Au. afarensis) form an ancestor-descendant lineage. Understanding the details of this possible transition is important comparative evidence for assessing the likelihood of other examples of ancestor-descendant lineages within the hominin clade. To this end we have analyzed crown and cusp base areas of high resolution replicas of the mandibular molars of Au. anamensis (Allia Bay and Kanapoi sites) and those of Au. afarensis (Hadar, Laetoli, and Maka). We found no statistically significant differences in crown areas between these hypodigms although the mean of M(1) crowns was smaller in Au. anamensis, being the smallest of any Australopithecus species sampled to date. Intraspecies comparison of the areas of mesial cusps for each molar type using Wilcoxon signed rank test showed no differences for Au. anamensis. Significant differences were found between the protoconid and metaconid of Au. afarensis M(2)s and M(3)s. Furthermore, the area formed by the posterior cusps as a whole relative to the anterior cusps showed significant differences in Au. afarensis M(1)s and in Au. anamensis M(2)s but no differences were noted for M(3)s of either taxon. Developmental information derived from microstructural details in enamel shows that M(1) crown formation in Au. anamensis is similar to Pan and shorter than in H. sapiens. Taken together, these data suggests that the overall trend in the Au. anamensis-Au. afarensis transition may have involved a moderate increase in M(1) crown areas with relative expansion of distal cusps.

The feeding biomechanics and dietary ecology of Australopithecus africanus.

The African Plio-Pleistocene hominins known as australopiths evolved a distinctive craniofacial morphology that traditionally has been viewed as a dietary adaptation for feeding on either small, hard objects or on large volumes of food. A historically influential interpretation of this morphology hypothesizes that loads applied to the premolars during feeding had a profound influence on the evolution of australopith craniofacial form. Here, we test this hypothesis using finite element analysis in conjunction with comparative, imaging, and experimental methods. We find that the facial skeleton of the Australopithecus type species, A. africanus, is well suited to withstand premolar loads. However, we suggest that the mastication of either small objects or large volumes of food is unlikely to fully explain the evolution of facial form in this species. Rather, key aspects of australopith craniofacial morphology are more likely to be related to the ingestion and initial preparation of large, mechanically protected food objects like large nuts and seeds. These foods may have broadened the diet of these hominins, possibly by being critical resources that australopiths relied on during periods when their preferred dietary items were in short supply. Our analysis reconciles apparent discrepancies between dietary reconstructions based on biomechanics, tooth morphology, and dental microwear.

Discrimination of extant Pan species and subspecies using the enamel-dentine junction morphology of lower molars.

Previous research has demonstrated that species and subspecies of extant chimpanzees and bonobos can be distinguished on the basis of the shape of their molar crowns. Thus, there is potential for fossil taxa, particularly fossil hominins, to be distinguished at similar taxonomic levels using molar crown morphology. Unfortunately, due to occlusal attrition, the original crown morphology is often absent in fossil teeth, and this has limited the amount of shape information used to discriminate hominin molars. The enamel-dentine junction (EDJ) of molar teeth preserves considerable shape information, particularly in regard to the original shape of the crown, and remains present through the early stages of attrition. In this study, we investigate whether the shape of the EDJ of lower first and second molars can distinguish species and subspecies of extant Pan. Micro-computed tomography was employed to non-destructively image the EDJ, and geometric morphometric analytical methods were used to compare EDJ shape among samples of Pan paniscus (N = 17), Pan troglodytes troglodytes (N = 13), and Pan troglodytes verus (N = 18). Discriminant analysis indicates that EDJ morphology distinguishes among extant Pan species and subspecies with a high degree of reliability. The morphological differences in EDJ shape among the taxa are subtle and relate to the relative height and position of the dentine horns, the height of the dentine crown, and the shape of the crown base, but their existence supports the inclusion of EDJ shape (particularly those aspects of shape in the vertical dimension) in the systematic analysis of fossil hominin lower molars.

Comparative isotopic evidence from East Turkana supports a dietary shift within the genus Homo.

It has been suggested that a shift in diet is one of the key adaptations that distinguishes the genus Homo from earlier hominins, but recent stable isotopic analyses of fossils attributed to Homo in the Turkana Basin show an increase in the consumption of C4 resources circa 1.65 million years ago, significantly after the earliest evidence for Homo in the eastern African fossil record. These data are consistent with ingesting more C4 plants, more animal tissues of C4 herbivores, or both, but it is also possible that this change reflects factors unrelated to changes in the palaeobiology of the genus Homo. Here we use new and published carbon and oxygen isotopic data (n = 999) taken from large-bodied fossil mammals, and pedogenic carbonates in fossil soils, from East Turkana in northern Kenya to investigate the context of this change in the isotope signal within Homo. By targeting taxa and temporal intervals unrepresented or undersampled in previous analyses, we were able to conduct the first comprehensive analysis of the ecological context of hominin diet at East Turkana during a period crucial for detecting any dietary and related behavioural differences between early Homo (H. habilis and/or H. rudolfensis) and Homo erectus. Our analyses suggest that the genus Homo underwent a dietary shift (as indicated by δ13Cena and δ18Oena values) that is (1) unrelated to changes in the East Turkana vegetation community and (2) unlike patterns found in other East Turkana large mammals, including Paranthropus and Theropithecus. These data suggest that within the Turkana Basin a dietary shift occurred well after we see the first evidence of early Homo in the region.

Inferences regarding the diet of extinct hominins: structural and functional trends in dental and mandibular morphology within the hominin clade.

This contribution investigates the evolution of diet in the Pan-Homo and hominin clades. It does this by focusing on 12 variables (nine dental and three mandibular) for which data are available about extant chimpanzees, modern humans and most extinct hominins. Previous analyses of this type have approached the interpretation of dental and gnathic function by focusing on the identification of the food consumed (i.e. fruits, leaves, etc.) rather than on the physical properties (i.e. hardness, toughness, etc.) of those foods, and they have not specifically addressed the role that the physical properties of foods play in determining dental adaptations. We take the available evidence for the 12 variables, and set out what the expression of each of those variables is in extant chimpanzees, the earliest hominins, archaic hominins, megadont archaic hominins, and an inclusive grouping made up of transitional hominins and pre-modern Homo. We then present hypotheses about what the states of these variables would be in the last common ancestor of the Pan-Homo clade and in the stem hominin. We review the physical properties of food and suggest how these physical properties can be used to investigate the functional morphology of the dentition. We show what aspects of anterior tooth morphology are critical for food preparation (e.g. peeling fruit) prior to its ingestion, which features of the postcanine dentition (e.g. overall and relative size of the crowns) are related to the reduction in the particle size of food, and how information about the macrostructure (e.g. enamel thickness) and microstructure (e.g. extent and location of enamel prism decussation) of the enamel cap might be used to make predictions about the types of foods consumed by extinct hominins. Specifically, we show how thick enamel can protect against the generation and propagation of cracks in the enamel that begin at the enamel-dentine junction and move towards the outer enamel surface.

Hominid mandibular corpus shape variation and its utility for recognizing species diversity within fossil Homo.

Mandibular corpora are well represented in the hominin fossil record, yet few studies have rigorously assessed the utility of mandibular corpus morphology for species recognition, particularly with respect to the linear dimensions that are most commonly available. In this study, we explored the extent to which commonly preserved mandibular corpus morphology can be used to: (i) discriminate among extant hominid taxa and (ii) support species designations among fossil specimens assigned to the genus Homo. In the first part of the study, discriminant analysis was used to test for significant differences in mandibular corpus shape at different taxonomic levels (genus, species and subspecies) among extant hominid taxa (i.e. Homo, Pan, Gorilla, Pongo). In the second part of the study, we examined shape variation among fossil mandibles assigned to Homo (including H. habilis sensu stricto, H. rudolfensis, early African H. erectus/H. ergaster, late African H. erectus, Asian H. erectus, H. heidelbergensis, H. neanderthalensis and H. sapiens). A novel randomization procedure designed for small samples (and using group 'distinctness values') was used to determine whether shape variation among the fossils is consistent with conventional taxonomy (or alternatively, whether a priori taxonomic groupings are completely random with respect to mandibular morphology). The randomization of 'distinctness values' was also used on the extant samples to assess the ability of the test to recognize known taxa. The discriminant analysis results demonstrated that, even for a relatively modest set of traditional mandibular corpus measurements, we can detect significant differences among extant hominids at the genus and species levels, and, in some cases, also at the subspecies level. Although the randomization of 'distinctness values' test is more conservative than discriminant analysis (based on comparisons with extant specimens), we were able to detect at least four distinct groups among the fossil specimens (i.e. H. sapiens, H. heidelbergensis, Asian H. erectus and a combined 'African Homo' group consisting of H. habilis sensu stricto, H. rudolfensis, early African H. erectus/H. ergaster and late African H. erectus). These four groups appear to be distinct at a level similar to, or greater than, that of modern hominid species. In addition, the mandibular corpora of H. neanderthalensis could be distinguished from those of 'African Homo', although not from those of H. sapiens, H. heidelbergensis, or the Asian H. erectus group. The results suggest that the features most commonly preserved on the hominin mandibular corpus have some taxonomic utility, although they are unlikely to be useful in generating a reliable alpha taxonomy for early African members of the genus Homo.

Functional Divergence of the Nuclear Receptor NR2C1 as a Modulator of Pluripotentiality During Hominid Evolution.

Genes encoding nuclear receptors (NRs) are attractive as candidates for investigating the evolution of gene regulation because they (1) have a direct effect on gene expression and (2) modulate many cellular processes that underlie development. We employed a three-phase investigation linking NR molecular evolution among primates with direct experimental assessment of NR function. Phase 1 was an analysis of NR domain evolution and the results were used to guide the design of phase 2, a codon-model-based survey for alterations of natural selection within the hominids. By using a series of reliability and robustness analyses we selected a single gene, NR2C1, as the best candidate for experimental assessment. We carried out assays to determine whether changes between the ancestral and extant NR2C1s could have impacted stem cell pluripotency (phase 3). We evaluated human, chimpanzee, and ancestral NR2C1 for transcriptional modulation of Oct4 and Nanog (key regulators of pluripotency and cell lineage commitment), promoter activity for Pepck (a proxy for differentiation in numerous cell types), and average size of embryological stem cell colonies (a proxy for the self-renewal capacity of pluripotent cells). Results supported the signal for alteration of natural selection identified in phase 2. We suggest that adaptive evolution of gene regulation has impacted several aspects of pluripotentiality within primates. Our study illustrates that the combination of targeted evolutionary surveys and experimental analysis is an effective strategy for investigating the evolution of gene regulation with respect to developmental phenotypes.