Descriptions of the lower limb skeleton of Homo floresiensis

Bones of the lower extremity have been recovered for up to nine different individuals of Homo floresiensis - LB1, LB4, LB6, LB8, LB9, LB10, LB11, LB13, and LB14. LB1 is represented by a bony pelvis (damaged but now repaired), femora, tibiae, fibulae, patellae, and numerous foot bones. LB4/2 is an immature right tibia lacking epiphyses. LB6 includes a fragmentary metatarsal and two pedal phalanges. LB8 is a nearly complete right tibia (shorter than that of LB1). LB9 is a fragment of a hominin femoral diaphysis. LB10 is a proximal hallucal phalanx. LB11 includes pelvic fragments and a fragmentary metatarsal. LB13 is a patellar fragment, and LB14 is a fragment of an acetabulum. All skeletal remains recovered from Liang Bua were extremely fragile, and some were badly damaged when they were removed temporarily from Jakarta. At present, virtually all fossil materials have been returned, stabilized, and hardened. These skeletal remains are described and illustrated photographically. The lower limb skeleton exhibits a uniquely mosaic pattern, with many primitive-like morphologies; we have been unable to find this combination of ancient and derived (more human-like) features in either healthy or pathological modern humans, regardless of body size. Bilateral asymmetries are slight in the postcranium, and muscle markings are clearly delineated on all bones. The long bones are robust, and the thickness of their cortices is well within the ranges seen in healthy modern humans. LB1 is most probably a female based on the shape of her greater sciatic notch, and the marked degree of lateral iliac flaring recalls that seen in australopithecines such as “Lucy” (AL 288-1). The metatarsus has a human-like robusticity formula, but the proximal pedal phalanges are relatively long and robust (and slightly curved). The hallux is fully adducted, but we suspect that a medial longitudinal arch was absent.     

Liang Bua Homo floresiensis mandibles and mandibular teeth: a contribution to the comparative morphology of a new hominin species

In 2004, a new hominin species, Homo floresiensis, was described from Late Pleistocene cave deposits at Liang Bua, Flores. H. floresiensis was remarkable for its small body-size, endocranial volume in the chimpanzee range, limb proportions and skeletal robusticity similar to Pliocene Australopithecus, and a skeletal morphology with a distinctive combination of symplesiomorphic, derived, and unique traits. Critics of H. floresiensis as a novel species have argued that the Pleistocene skeletons from Liang Bua either fall within the range of living Australomelanesians, exhibit the attributes of growth disorders found in modern humans, or a combination of both. Here we describe the morphology of the LB1, LB2, and LB6 mandibles and mandibular teeth from Liang Bua. Morphological and metrical comparisons of the mandibles demonstrate that they share a distinctive suite of traits that place them outside both the H. sapiens and H. erectus ranges of variation. While having the derived molar size of later Homo, the symphyseal, corpus, ramus, and premolar morphologies share similarities with both Australopithecus and early Homo. When the mandibles are considered with the existing evidence for cranial and postcranial anatomy, limb proportions, and the functional anatomy of the wrist and shoulder, they are in many respects closer to African early Homo or Australopithecus than to later Homo. Taken together, this evidence suggests that the ancestors of H. floresiensis left Africa before the evolution of H. erectus, as defined by the Dmanisi and East African evidence.     

Homo floresiensis: a cladistic analysis

The announcement of a new species, Homo floresiensis, a primitive hominin that survived until relatively recent times is an enormous challenge to paradigms of human evolution. Until this announcement, the dominant paradigm stipulated that: 1) only more derived hominins had emerged from Africa, and 2) H. sapiens was the only hominin since the demise of Homo erectus and Homo neanderthalensis. Resistance to H. floresiensis has been intense, and debate centers on two sets of competing hypotheses: 1) that it is a primitive hominin, and 2) that it is a modern human, either a pygmoid form or a pathological individual. Despite a range of analytical techniques having been applied to the question, no resolution has been reached. Here, we use cladistic analysis, a tool that has not, until now, been applied to the problem, to establish the phylogenetic position of the species. Our results produce two equally parsimonious phylogenetic trees. The first suggests that H. floresiensis is an early hominin that emerged after Homo rudolfensis (1.86 Ma) but before H. habilis (1.66 Ma, or after 1.9 Ma if the earlier chronology for H. habilis is retained). The second tree indicates H. floresiensis branched after Homo habilis.     

Descriptions of the upper limb skeleton of Homo floresiensis

Several bones of the upper extremity were recovered during excavations of Late Pleistocene deposits at Liang Bua, Flores, and these have been attributed to Homo floresiensis. At present, these upper limb remains have been assigned to six different individuals - LB1, LB2, LB3, LB4, LB5, and LB6. Several of these bones are complete or nearly so, but some are quite fragmentary. All skeletal remains recovered from Liang Bua were extremely fragile, but have now been stabilized and hardened in the laboratory in Jakarta. They are now curated in museum-quality containers at the National Research and Development Centre for Archaeology in Jakarta, Indonesia. These skeletal remains are described and illustrated photographically. The upper limb presents a unique mosaic of derived (human-like) and primitive morphologies, the combination of which is never found in either healthy or pathological modern humans.     

Preface: research at Liang Bua, Flores, Indonesia

Excavations at Liang Bua, Flores, Indonesia, have yielded evidence for an endemic human species, Homo floresiensis, a population that occupied the cave between ∼95-17 ka. This discovery has major implications for early hominin evolution and dispersal in Africa and Asia, attracting worldwide interest. This preface describes the rationale for the excavations in historical, geographical, and wider research contexts, as well as the methods used. It also introduces the other papers on aspects of Liang Bua research that feature in this edition of the Journal of Human Evolution.     

Conclusions: implications of the Liang Bua excavations for hominin evolution and biogeography

Excavations at Liang Bua, on the Indonesian island of Flores, have yielded a stratified sequence of stone artifacts and faunal remains spanning the last 95 k.yr., which includes the skeletal remains of two human species, Homo sapiens in the Holocene and Homo floresiensis in the Pleistocene. This paper summarizes and focuses on some of the evidence for Homo floresiensis in context, as presented in this Special Issue edition of the Journal of Human Evolution and elsewhere. Attempts to dismiss the Pleistocene hominins (and the type specimen LB1 in particular) as pathological pygmy humans are not compatible with detailed analyses of the skull, teeth, brain endocast, and postcranium. We initially concluded that H. floresiensis may have evolved by insular dwarfing of a larger-bodied hominin species over 880 k.yr. or more. However, recovery of additional specimens and the numerous primitive morphological traits seen throughout the skeleton suggest instead that it is more likely to be a late representative of a small-bodied lineage that exited Africa before the emergence of Homo erectus sensu lato. Homo floresiensis is clearly not an australopithecine, but does retain many aspects of anatomy (and perhaps behavior) that are probably plesiomorphic for the genus Homo. We also discuss some of the other implications of this tiny, endemic species for early hominin dispersal and evolution (e.g., for the “Out of Africa 1” paradigm and more specifically for colonizing Southeast Asia), and we present options for future research in the region.     

Body size and body shape in early hominins - implications of the Gona Pelvis

Discovery of the first complete Early Pleistocene hominin pelvis, Gona BSN49/P27, attributed to Homo erectus, raises a number of issues regarding early hominin body size and shape variation. Here, acetabular breadth, femoral head breadth, and body mass calculated from femoral head breadth are compared in 37 early hominin (6.0-0.26 Ma) specimens, including BSN49/P27. Acetabular and estimated femoral head sizes in the Gona specimen fall close to the means for non-Homo specimens (Orrorin tugenesis, Australopithecus africanus, Paranthropus robustus), and well below the ranges of all previously described Early and Middle Pleistocene Homo specimens. The Gona specimen has an estimated body mass of 33.2 kg, close to the mean for the non-Homo sample (34.1 kg, range 24-51.5 kg, n = 19) and far outside the range for any previously known Homo specimen (mean = 70.5 kg; range 52-82 kg, n = 17). Inclusion of the Gona specimen within H. erectus increases inferred sexual dimorphism in body mass in this taxon to a level greater than that observed here for any other hominin taxon, and increases variation in body mass within H. erectus females to a level much greater than that observed for any living primate species. This raises questions regarding the taxonomic attribution of the Gona specimen. When considered within the context of overall variation in body breadth among early hominins, the mediolaterally very wide Gona pelvis fits within the distribution of other lower latitude Early and Middle Pleistocene specimens, and below that of higher latitude specimens. Thus, ecogeographic variation in body breadth was present among earlier hominins as it is in living humans. The increased M-L pelvic breadth in all earlier hominins relative to modern humans is related to an increase in ellipticity of the birth canal, possibly as a result of a non-rotational birth mechanism that was common to both australopithecines and archaic Homo.     

Geochronology of cave deposits at Liang Bua and of adjacent river terraces in the Wae Racang valley, western Flores, Indonesia: a synthesis of age estimates for the type locality of Homo floresiensis

A robust timeframe for the extant cave deposits at Liang Bua, and for the river terraces in the adjoining Wae Racang valley, is essential to constrain the period of existence and time of extinction of Homo floresiensis and other biota that have been excavated at this hominin type locality. Reliable age control is also required for the variety of artifacts excavated from these deposits, and to assist in environmental reconstructions for this river valley and for the region more broadly. In this paper, we summarize the available geochronological information for Liang Bua and its immediate environs, obtained using seven numerical-age methods: radiocarbon, thermoluminescence, optically- and infrared-stimulated luminescence (collectively known as optical dating), uranium-series, electron spin resonance, and coupled electron spin resonance/uranium-series. We synthesize the large number of numerical age determinations reported previously and present additional age estimates germane to questions of hominin evolution and extinction.     

Continuities in stone flaking technology at Liang Bua, Flores, Indonesia

This study examines trends in stone tool reduction technology at Liang Bua, Flores, Indonesia, where excavations have revealed a stratified artifact sequence spanning 95 k.yr. The reduction sequence practiced throughout the Pleistocene was straightforward and unchanging. Large flakes were produced off-site and carried into the cave where they were reduced centripetally and bifacially by four techniques: freehand, burination, truncation, and bipolar. The locus of technological complexity at Liang Bua was not in knapping products, but in the way techniques were integrated. This reduction sequence persisted across the Pleistocene/Holocene boundary with a minor shift favoring unifacial flaking after 11 ka. Other stone-related changes occurred at the same time, including the first appearance of edge-glossed flakes, a change in raw material selection, and more frequent fire-induced damage to stone artifacts. Later in the Holocene, technological complexity was generated by “adding-on” rectangular-sectioned stone adzes to the reduction sequence. The Pleistocene pattern is directly associated with Homo floresiensis skeletal remains and the Holocene changes correlate with the appearance of Homo sapiens. The one reduction sequence continues across this hominin replacement.     

The Liang Bua faunal remains: a 95 k.yr. sequence from Flores, East Indonesia

Excavations at Liang Bua, a limestone cave on the island of Flores, East Indonesia, have yielded a well-dated archaeological and faunal sequence spanning the last 95 k.yr., major climatic fluctuations, and two human species - H. floresiensis from 95 to 17 k.yr.¹, and modern humans from 11 k.yr. to the present. The faunal assemblage comprises well-preserved mammal, bird, reptile and mollusc remains, including examples of island gigantism in small mammals and the dwarfing of large taxa. Together with evidence from Early-Middle Pleistocene sites in the Soa Basin, it confirms the long-term isolation, impoverishment, and phylogenetic continuity of the Flores faunal community. The accumulation of Stegodon and Komodo dragon remains at the site in the Pleistocene is attributed to Homo floresiensis, while predatory birds, including an extinct species of owl, were largely responsible for the accumulation of the small vertebrates. The disappearance from the sequence of the two large-bodied, endemic mammals, Stegodon florensis insularis and Homo floresiensis, was associated with a volcanic eruption at 17 ka and precedes the earliest evidence for modern humans, who initiated use of mollusc and shell working, and began to introduce a range of exotic animals to the island. Faunal introductions during the Holocene included the Sulawesi warty pig (Sus celebensis) at about 7 ka, followed by the Eurasian pig (Sus scrofa), Long-tailed macaque, Javanese porcupine, and Masked palm civet at about 4 ka, and cattle, deer, and horse - possibly by the Portuguese within historic times. The Holocene sequence at the site also documents local faunal extinctions - a result of accelerating human population growth, habitat loss, and over-exploitation.     

Mandibular molar root morphology in Neanderthals and Late Pleistocene and recent Homo sapiens

Neanderthals have a distinctive suite of dental features, including large anterior crown and root dimensions and molars with enlarged pulp cavities. Yet, there is little known about variation in molar root morphology in Neanderthals and other recent and fossil members of Homo. Here, we provide the first comprehensive metric analysis of permanent mandibular molar root morphology in Middle and Late Pleistocene Homo neanderthalensis, and Late Pleistocene (Aterian) and recent Homo sapiens. We specifically address the question of whether root form can be used to distinguish between these groups and assess whether any variation in root form can be related to differences in tooth function. We apply a microtomographic imaging approach to visualise and quantify the external and internal dental morphologies of both isolated molars and molars embedded in the mandible (n = 127). Univariate and multivariate analyses reveal both similarities (root length and pulp volume) and differences (occurrence of pyramidal roots and dental tissue volume proportion) in molar root morphology among penecontemporaneous Neanderthals and Aterian H. sapiens. In contrast, the molars of recent H. sapiens are markedly smaller than both Pleistocene H. sapiens and Neanderthals, but share with the former the dentine volume reduction and a smaller root-to-crown volume compared with Neanderthals. Furthermore, we found the first molar to have the largest average root surface area in recent H. sapiens and Neanderthals, although in the latter the difference between M₁ and M₂ is small. In contrast, Aterian H. sapiens root surface areas peak at M₂. Since root surface area is linked to masticatory function, this suggests a distinct occlusal loading regime in Neanderthals compared with both recent and Pleistocene H. sapiens.     

Assessing A.L. 288-1 femur length using computer-aided three-dimensional reconstruction

Fossil reconstruction remains a requisite task for many types of paleoanthropological research. While reconstructions are traditionally accomplished by hand, computer modeling offers a novel and mathematically rigorous approach while providing advantages over the manual process. Computer models of fossil specimens can be reflected, scaled, and aligned in virtual space with relative ease; therefore, it is simple to generate multiple reconstructions to find the "best" one. Here we report on the reconstruction of A.L. 288-1ap (left femur) using three-dimensional computer models. Our "best" reconstruction has a maximum length of 277mm, which is very near both the 280mm originally estimated and the frequently cited 281mm.     

Energetics in Homo erectus and other early hominins: the consequences of increased lower-limb length

Previous studies of daily energy expenditure (DEE) in hominin fossils have estimated locomotor costs using a formula that was based on six species, all 18 kg or less in mass, including no primates, and that has a number of other problems when applied in an ecological context. It is well established that the energetic cost of human walking is lower than that of representative mammals, particularly for individuals with long lower limbs. The current study reevaluates the daily energy expenditures of a variety of hominin species using more appropriate approaches to estimating locomotor costs. To estimate DEE for primates, I relied on published data on body mass, day range, and the percentage of time spent in various activities. Based on those data, I calculated a value for nonlocomotor DEE. I then used a variant of a method that I have suggested elsewhere to calculate the daily cost due to locomotion (DEEL) and summed the two to calculate total DEE. The more up-to-date methods for calculating the cost of travel result in lower estimates of this aspect of the energy budget than seen in previous studies. Values obtained here for DEE in various representatives of Australopithecus are lower than reported previously by around 200 kcal/day. Taking into account the greater economy of human walking, particularly the effect of the longer lower limbs found in many later Homo species, also results in lowered estimates of DEE. Elongation of the lower limbs in H. erectus reduced relative travel costs nearly 50% in comparison to A.L. 288-1 (A. afarensis). The present method for calculating DEE indicates that female H. erectus DEE was 84% greater than that of female Australopithecus; this disparity is even larger than that suggested by previous workers.     

Bone remodeling of the Homo heidelbergensis mandible; the Atapuerca-SH sample.

Growth by bone remodeling is one of the key mechanisms responsible for skeletal morphology. This mechanism consists of the coordinated activity of two cellular groups: osteoblasts and osteoclasts, which are responsible for bone deposition and resorption, respectively. Information obtained from the study of these remodeling growth fields allows us to understand how species-specific craniofacial form is achieved. These data can help to explain the facial growth differences among Primates, both extinct and extant. The aim of this study was to obtain the distribution of growth remodeling fields of the Homo heidelbergensis mandible (Atapuerca-SH sample), and to infer the growth processes responsible for its specific morphology. A Reflected Light Microscope (RLM) was used to identify the microfeatures of the bone surface related to bone deposition and resorption. Results show that H. heidelbergensis presents a specific growth field distribution, which differs slightly between immature and adult individuals. Interpretation of these maps indicates that the mandible of H. heidelbergensis presents noteworthy variability in the symphyseal region. Two distinct patterns of growth are seen, one of those unique for this species and the other similar to that of Homo sapiens. The lingual side of the mandibular corpus has a resorption area found only in this species and one that includes a variable extension in immature and adult individuals. Finally, the mandibular ramus is characterized, among other aspects, by a large resorption field on its buccal surface. Considering the mandible as a whole, the bone remodeling pattern obtained in this work shows that lower facial growth in H. heidelbergensis is dominated mainly by forward growth, illustrated by the strong inward displacement of the ramus, which is in agreement with the Enlow's “V” growth principle.     

Primate brains,the ‘island rule’ and the evolution of Homo floresiensis

The taxonomic status of the small bodied hominin, Homo floresiensis, remains controversial. One contentious aspect of the debate concerns the small brain size estimated for specimen LB1 (Liang Bua 1). Based on intraspecific mammalian allometric relationships between brain and body size, it has been argued that the brain of LB1 is too small for its body mass and is therefore likely to be pathological. The relevance and general applicability of these scaling rules has, however, been challenged, and it is not known whether highly encephalized primates adapt to insular habitats in a consistent manner. Here, an analysis of brain and body size evolution in seven extant insular primates reveals that although insular primates follow the ‘island rule’, having consistently reduced body masses compared with their mainland relatives, neither brain mass nor relative brain size follow similar patterns, contrary to expectations that energetic constraints will favour decreased relative brain size. Brain:body scaling relationships previously used to assess the plausibility of dwarfism in H. floresiensis tend to underestimate body masses of insular primates. In contrast, under a number of phylogenetic scenarios, the evolution of brain and body mass in H. floresiensis is consistent with patterns observed in other insular primates.     

Variation in gestation length among captive reindeer (Rangifer tarandus tarandus)

An estimated 90% of reindeer females are mated in a 10- to 21-d interval and give birth in an equally synchronized manner. Reported gestation length in reindeer is highly variable (range, 203 to 240 d), almost twice the reindeer estrous cycle length. Previously, we identified a significant, negative relationship between gestation length and conception date in a small group of reindeer. In the current study, the negative relationship was investigated in a switchback design, where reindeer were divided into two groups synchronized for early and late mating over a 2-yr trial. Regression analysis of 11 paired observations produced a negative (P < 0.001) association between gestation length and conception date (slope = − 0.31). Dam weight at breeding and prior to parturition, calf birth weight, and calf sex were not significant variables in the regression. Regression analysis of a larger data set from two University of Alaska Fairbanks reindeer herds, where conception date (verified by systemic progesterone) and gestation length were recorded (historical data set), supported previous conclusions (n = 70; slope = −0.37; P < 0.001). Although the calf sex ratio did not differ with gestation length, there was a positive relationship (r² = 0.19; P = 0.014) between male birth weight and gestation length in the larger data set. The negative relationship between conception date and gestation length enhanced calving synchrony, though the limits of gestation plasticity and underlying mechanisms are not clear. The potential role of photoperiod on early embryonic development is discussed.     

Real-time PCR detection of Holophagae (Acidobacteria) and Verrucomicrobia subdivision 1 groups in bulk and leek (Allium porrum) rhizosphere soils

In the light of the poor culturability of Acidobacteria and Verrucomicrobia species, group-specific real-time (qPCR) systems were developed based on the 16S rRNA gene sequences from culturable representatives of both groups. The number of DNA targets from three different groups, i.e. Holophagae (Acidobacteria group 8) and Luteolibacter/Prosthecobacter and unclassified Verrucomicrobiaceae subdivision 1, was determined in DNA extracts from different leek (Allium porrum) rhizosphere soil compartments and from bulk soil with the aim to determine the distribution of the three bacterial groups in the plant-soil ecosystem. The specificity of the designed primers was evaluated in three steps. First, in silico tests were performed which demonstrated that all designed primers 100% matched with database sequences of their respective groups, whereas lower matches with other non-target bacterial groups were found. Second, PCR amplification with the different primer sets was performed on genomic DNA extracts from target and from non-target bacteria. This test demonstrated specificity of the designed primers for the target groups, as single amplicons of expected sizes were found only for the target bacteria. Third, the qPCR systems were tested for specific amplifications from soil DNA extracts and 48 amplicons from each primer system were sequenced. All sequences were > 97% similar to database sequences of the respective target groups. Estimated cell numbers based on Holophagae-, Luteolibacter/Prosthecobacter- and unclassified Verrucomicrobiaceae subdivision 1-specific qPCRs from leek rhizosphere compartments and bulk soils demonstrated higher preference for one or both rhizosphere compartments above bulk soil for all three bacterial groups.