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.     

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.     

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.     

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.     

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.     

New evidence for a 67,000-year-old human presence at Callao Cave, Luzon, Philippines

Documentation of early human migrations through Island Southeast Asia and Wallacea en route to Australia has always been problematic due to a lack of well-dated human skeletal remains. The best known modern humans are from Niah Cave in Borneo (40-42 ka), and from Tabon Cave on the island of Palawan, southwest Philippines (47 ± 11 ka). The discovery of Homo floresiensis on the island of Flores in eastern Indonesia has also highlighted the possibilities of identifying new hominin species on islands in the region. Here, we report the discovery of a human third metatarsal from Callao Cave in northern Luzon. Direct dating of the specimen using U-series ablation has provided a minimum age estimate of 66.7 ± 1 ka, making it the oldest known human fossil in the Philippines. Its morphological features, as well as size and shape characteristics, indicate that the Callao metatarsal definitely belongs to the genus Homo. Morphometric analysis of the Callao metatarsal indicates that it has a gracile structure, close to that observed in other small-bodied Homo sapiens. Interestingly, the Callao metatarsal also falls within the morphological and size ranges of Homo habilis and H. floresiensis. Identifying whether the metatarsal represents the earliest record of H. sapiens so far recorded anywhere east of Wallace’s Line requires further archaeological research, but its presence on the isolated island of Luzon over 65,000 years ago further demonstrates the abilities of humans to make open ocean crossings in the Late Pleistocene.     

The fellowship of the hobbit: the fauna surrounding Homo floresiensis

The Late Pleistocene Flores fauna shows a pattern observed on many other islands. It is neither aberrant nor exclusive, but the result of non‐random selective forces acting upon an impoverished and disharmonic insular fauna. By comparing the Flores vertebrate fauna with other fossil insular biotas, it is apparent that the evolution of Homo floresiensis is part of a general pattern affecting all the inhabitants of Pleistocene Flores. Vertebrate evolution on Flores appears to have been characterized by phylogenetic continuity, low species richness and a disharmonic fauna. All three aspects stem from the isolated position of the island and have resulted in the distinct morphological characteristics of the Flores fauna. Evidence reviewed herein shows that features exhibited by H. floresiensis, such as small stature, a small brain, relatively long arms, robust lower limbs and long feet, are not unique, but are shared by other insular taxa. Therefore, the evolution of H. floresiensis can be explained by existing models of insular evolution and followed evolutionary pathways similar to those of the other terrestrial vertebrates inhabiting Pleistocene Flores.     

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.     

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.     

The evolving landscape and climate of western Flores: an environmental context for the archaeological site of Liang Bua

The rapidly changing landscape of the eastern Indonesian archipelago has evolved at a pace dictated by its tropical climate and its geological and tectonic history. This has produced accelerated karstification, flights of alluvial terraces, and complex, multi-level cave systems. These cave systems sometimes contain a wealth of archaeological evidence, such as the almost complete skeleton of Homo floresiensis found at the site of Liang Bua in western Flores, but this information can only be understood in the context of the geomorphic history of the cave, and the more general geological, tectonic, and environmental histories of the river valley and region. Thus, a reconstruction of the landscape history of the Wae Racang valley using speleothems, geological structure, tectonic uplift, karst, cave, and terrace development, provides the necessary evidence to determine the formation, age, evolution, and influences on the site. This evidence suggests that Liang Bua was formed as two subterranean chambers ∼600 ka, but could not be occupied until ∼190 ka when the Wae Racang wandered to the southern side of the valley, exposing the chamber and depositing alluvial deposits containing artifacts. During the next ∼190 k.yr., the chambers coalesced and evolved into a multi-level and interconnected cave that was subjected to channel erosion and pooling events by the development of sinkholes. The domed morphology of the front chamber accumulated deep sediments containing well stratified archaeological and faunal remains, but ponded water in the chamber further prevented hominin use of the cave until ∼100 ka. These chambers were periodically influenced by river inundation and volcanic activity, whereas the area outside the cave was greatly influenced by glacial phases, which changed humid forest environments into grassland environments. This combined evidence has important implications for the archaeological interpretation of the site.     

LB1 and LB6 Homo floresiensis are not modern human (Homo sapiens) cretins

Excavations in the late Pleistocene deposits at Liang Bua cave, Flores, have uncovered the skeletal remains of several small-bodied and small-brained hominins in association with stone artefacts and the bones of Stegodon. Due to their combination of plesiomorphic, unique and derived traits, they were ascribed to a new species, Homo floresiensis, which, along with Stegodon, appears to have become extinct ∼17 ka (thousand years ago). However, recently it has been argued that several characteristics of H. floresiensis were consistent with dwarfism and evidence of delayed development in modern human (Homo sapiens) myxoedematous endemic (ME) cretins. This research compares the skeletal and dental morphology in H. floresiensis with the clinical and osteological indicators of cretinism, and the traits that have been argued to be associated with ME cretinism in LB1 and LB6. Contrary to published claims, morphological and statistical comparisons did not identify the distinctive skeletal and dental indicators of cretinism in LB1 or LB6 H. floresiensis. Brain mass, skeletal proportions, epiphyseal union, orofacial morphology, dental development, size of the pituitary fossa and development of the paranasal sinuses, vault bone thickness and dimensions of the hands and feet all distinguish H. floresiensis from modern humans with ME cretinism. The research team responsible for the diagnosis of ME cretinism had not examined the original H. floresiensis skeletal materials, and perhaps, as a result, their research confused taphonomic damage with evidence of disease, and thus contained critical errors of fact and interpretation. Behavioural scenarios attempting to explain the presence of cretinous H. sapiens in the Liang Bua Pleistocene deposits, but not unaffected H. sapiens, are both unnecessary and not supported by the available archaeological and geochronological evidence from Flores.     

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.     

LB1’s virtual endocast, microcephaly, and hominin brain evolution

Earlier observations of the virtual endocast of LB1, the type specimen for Homo floresiensis, are reviewed, extended, and interpreted. Seven derived features of LB1's cerebral cortex are detailed: a caudally-positioned occipital lobe, lack of a rostrally-located lunate sulcus, a caudally-expanded temporal lobe, advanced morphology of the lateral prefrontal cortex, shape of the rostral prefrontal cortex, enlarged gyri in the frontopolar region, and an expanded orbitofrontal cortex. These features indicate that LB1's brain was globally reorganized despite its ape-sized cranial capacity (417 cm³). Neurological reorganization may thus form the basis for the cognitive abilities attributed to H. floresiensis. Because of its tiny cranial capacity, some workers think that LB1 represents a Homo sapiens individual that was afflicted with microcephaly, or some other pathology, rather than a new species of hominin. We respond to concerns about our earlier study of microcephalics compared with normal individuals, and reaffirm that LB1 did not suffer from this pathology. The intense controversy about LB1 reflects an older continuing dispute about the relative evolutionary importance of brain size versus neurological reorganization. LB1 may help resolve this debate and illuminate constraints that governed hominin brain evolution.     

Body size and its consequences: Allometry and the lower limb length of Liang Bua 1 (Homo floresiensis)

Bivariate femoral length allometry in recent humans, Pan, and Gorilla is investigated with special reference to the diminutive Liang Bua (LB) 1 specimen (the holotype of Homo floresiensis) and six early Pleistocene femora referred to the genus Homo. Relative to predicted body mass, Pan and Gorilla femora show strong negative length allometry while recent human femora evince isometry to positive allometry, depending on sample composition and line-fitting technique employed. The allometric trajectories of Pan and Homo show convergence near the small body size range of LB 1, such that LB 1 manifests a low percentage deviation (d_yx of Smith [1980]) from the Pan allometric trajectory and falls well within the 95% confidence limits around the Pan individuals (but also outside the 95% confidence limits for recent Homo). In contrast, the six early Pleistocene Homo femora, belonging to larger individuals, show much greater d_yx values from both Pan and Gorilla and fall well above the 95% confidence limits for these taxa. All but one of these Pleistocene Homo specimens falls within the 95% confidence limits of the recent human sample. Similar results are obtained when femoral length is regressed on femoral head diameter in unlogged bivariate space. Regardless of the ultimate taxonomic status of LB 1, these findings are consistent with a prediction made by us (Franciscus and Holliday, 1992) that hominins in the small body size range of A.L. 288-1 (“Lucy”), including members of the genus Homo, will tend to possess short, ape-like lower limbs as a function of body size scaling.     

Human talus bones from the Middle Pleistocene site of Sima de los Huesos (Sierra de Atapuerca,Burgos, Spain)

Here we present and describe comparatively 25 talus bones from the Middle Pleistocene site of the Sima de los Huesos (SH) (Sierra de Atapuerca, Burgos, Spain). These tali belong to 14 individuals (11 adult and three immature). Although variation among Middle and Late Pleistocene tali tends to be subtle, this study has identified unique morphological characteristics of the SH tali. They are vertically shorter than those of Late Pleistocene Homo sapiens, and show a shorter head and a broader lateral malleolar facet than all of the samples. Moreover, a few shared characters with Neanderthals are consistent with the hypothesis that the SH population and Neanderthals are sister groups. These shared characters are a broad lateral malleolar facet, a trochlear height intermediate between modern humans and Late Pleistocene H. sapiens, and a short middle calcaneal facet. It has been possible to propose sex assignment for the SH tali based on their size. Stature estimates based on these fossils give a mean stature of 174.4 cm for males and 161.9 cm for females, similar to that obtained based on the long bones from this same site.     

Unique Dental Morphology of Homo floresiensis and Its Evolutionary Implications

Homo floresiensis is an extinct, diminutive hominin species discovered in the Late Pleistocene deposits of Liang Bua cave, Flores, eastern Indonesia. The nature and evolutionary origins of H. floresiensis’ unique physical characters have been intensively debated. Based on extensive comparisons using linear metric analyses, crown contour analyses, and other trait-by-trait morphological comparisons, we report here that the dental remains from multiple individuals indicate that H. floresiensis had primitive canine-premolar and advanced molar morphologies, a combination of dental traits unknown in any other hominin species. The primitive aspects are comparable to H. erectus from the Early Pleistocene, whereas some of the molar morphologies are more progressive even compared to those of modern humans. This evidence contradicts the earlier claim of an entirely modern human-like dental morphology of H. floresiensis, while at the same time does not support the hypothesis that H. floresiensis originated from a much older H. habilis or Australopithecus-like small-brained hominin species currently unknown in the Asian fossil record. These results are however consistent with the alternative hypothesis that H. floresiensis derived from an earlier Asian Homo erectus population and experienced substantial body and brain size dwarfism in an isolated insular setting. The dentition of H. floresiensis is not a simple, scaled-down version of earlier hominins.     

Nacurrie 1: Mark of ancient Java, or a caring mother’s hands, in terminal Pleistocene Australia?

There has been a protracted debate over the evidence for intentional cranial modification in the terminal Pleistocene Australian crania from Kow Swamp and Coobool Creek. Resolution of this debate is crucial to interpretations of the significance of morphological variation within terminal Pleistocene-early Holocene Australian skeletal materials and claims of a regional evolutionary sequence linking Javan Homo erectus and Australian Homo sapiens. However, morphological comparisons of terminal Pleistocene and recent Australian crania are complicated by the significantly greater average body mass in the former. Raw and size-adjusted metric comparisons of the terminal Pleistocene skeleton from Nacurrie, south-eastern Australia, with modified and unmodified H. sapiens and H. erectus, identified a suite of traits in the frontal, parietal, and occipital bones associated with intentional modification of a neonate’s skull. These traits are also present in some of the crania from Kow Swamp and Coobool Creek, which are in close geographic proximity to Nacurrie, but not in unmodified H. sapiens or Javan H. erectus. Frontal bone morphology in H. erectus was distinct from all of the Australian H. sapiens samples. During the first six months of life, Nacurrie’s vault may have been shaped by his mother’s hands, rather than though the application of fixed bandages. Whether this behaviour persisted only for several generations, or hundreds of years, remains unknown. The reasons behind the shaping of Nacurrie’s head, aesthetics or otherwise, and why this cultural practice was adopted and subsequently discontinued, will always remain a matter of speculation.