Morphological and morphometric analyses of a late Middle Pleistocene hominin mandible from Hualongdong, China.

Excavations in Hualongdong (HLD), East China, have yielded abundant hominin fossils dated to 300 ka. There is a nearly complete mandible that fits well with a partial cranium, and together they compose the skull labeled as HLD 6. Thus far, detailed morphological description and comparisons of the mandible have not been conducted. Here we present a comprehensive morphological, metric, and geometric morphometric assessment of this mandible and compare it with both adult and immature specimens of Pleistocene hominins and recent modern humans. Results indicate that the HLD 6 mandible exhibits a mosaic morphological pattern characterized by a robust corpus and relatively gracile symphysis and ramus. The moderately developed mental trigone and a clear anterior mandibular incurvation of the HLD 6 mandible are reminiscent of Late Pleistocene hominin and recent modern human morphology. However, the weak expression of all these features indicates that this mandible does not possess a true chin. Moreover, a suite of archaic features that resemble those of Middle Pleistocene hominins includes pronounced alveolar planum, superior transverse torus, thick corpus, a pronounced endocondyloid crest, and a well-developed medial pterygoid tubercle. The geometric morphometric analysis further confirms the mosaic pattern of the HLD 6 mandible. The combination of both archaic and modern human features identified in the HLD 6 mandible is unexpected, given its late Middle Pleistocene age and differs from approximately contemporaneous Homo members such as Xujiayao, Penghu, and Xiahe. This mosaic pattern has never been recorded in late Middle Pleistocene hominin fossil assemblages in East Asia. The HLD 6 mandible provides further support for the high morphological diversity during late Middle Pleistocene hominin evolution. With these findings, it is possible that modern human morphologies are present as early as 300 ka and earlier than the emergence of modern humans in East Asia.

Reassessment of the human mandible from Banyoles (Girona, Spain).

Since the discovery of a human mandible in 1887 near the present-day city of Banyoles, northeastern Spain, researchers have generally emphasized its archaic features, including the lack of chin structures, and suggested affinities with the Neandertals or European Middle Pleistocene (Chibanian) specimens. Uranium-series and electron spin resonance dating suggest the mandible dates to the Late Pleistocene (Tarantian), approximately ca. 45-66 ka. In this study, we reassessed the taxonomic affinities of the Banyoles mandible by comparing it to samples of Middle Pleistocene fossils from Africa and Europe, Neandertals, Early and Upper Paleolithic modern humans, and recent modern humans. We evaluated the frequencies and expressions of morphological features and performed a three-dimensional geometric morphometric analysis on a virtual reconstruction of Banyoles to capture overall mandibular shape. Our results revealed no derived Neandertal morphological features in Banyoles. While a principal component analysis based on Euclidean distances from the first two principal components clearly grouped Banyoles with both fossil and recent Homo sapiens individuals, an analysis of the Procrustes residuals demonstrated that Banyoles did not fit into any of the comparative groups. The lack of Neandertal features in Banyoles is surprising considering its Late Pleistocene age. A consideration of the Middle Pleistocene fossil record in Europe and southwest Asia suggests that Banyoles is unlikely to represent a late-surviving Middle Pleistocene population. The lack of chin structures also complicates an assignment to H. sapiens, although early fossil H. sapiens do show somewhat variable development of the chin structures. Thus, Banyoles represents a non-Neandertal Late Pleistocene European individual and highlights the continuing signal of diversity in the hominin fossil record. The present situation makes Banyoles a prime candidate for ancient DNA or proteomic analyses, which may shed additional light on its taxonomic affinities.

Evolution of Homo in the Middle and Late Pleistocene.

The Middle and Late Pleistocene is arguably the most interesting period in human evolution. This broad period witnessed the evolution of our own lineage, as well as that of our sister taxon, the Neanderthals, and related Denisovans. It is exceptionally rich in both fossil and archaeological remains, and uniquely benefits from insights gained through molecular approaches, such as paleogenetics and paleoproteomics, that are currently not widely applicable in earlier contexts. This wealth of information paints a highly complex picture, often described as 'the Muddle in the Middle,' defying the common adage that 'more evidence is needed' to resolve it. Here we review competing phylogenetic scenarios and the historical and theoretical developments that shaped our approaches to the fossil record, as well as some of the many remaining open questions associated with this period. We propose that advancing our understanding of this critical time requires more than the addition of data and will necessitate a major shift in our conceptual and theoretical framework.

Modern human teeth unearthed from below the ∼128,000-year-old level at Punung, Java: A case highlighting the problem of recent intrusion in cave sediments.

The emergence of modern humans in the eastern edge of the Eurasian Continent is debated between two major models: early (∼130-70 ka) and late (∼50 ka) dispersal models. The former view is grounded mainly on the claims that several cave sites in Southeast Asia and southern China yielded modern human fossils of those early ages, but such reports have been disputed for the lack of direct dating of the human remains and insufficient documentation of stratigraphy and taphonomy. By tracing possible burial process and conducting direct dating for an early Late Pleistocene paleontological site of Punung III, East Java, we here report a case that demonstrates how unexpected intrusion of recent human remains into older stratigraphic levels could occur in cave sediments. This further highlights the need of direct dating and taphonomic assessment before accepting either model. We also emphasize that the state of fossilization of bones and teeth is a useful guide for initial screening of recent intrusion and should be reported particularly when direct dating is unavailable. Additionally, we provide a revised stratigraphy and faunal list of Punung III, a key site that defines the tropical rainforest Punung Fauna during the early Late Pleistocene of the region.

Morphological description and evolutionary significance of 300 ka hominin facial bones from Hualongdong, China.

Late Middle Pleistocene hominins in Africa displaying key modern morphologies by 315 ka are claimed as the earliest Homo sapiens. Evolutionary relationships among East Asian hominins appear complex due to a growing fossil record of late Middle Pleistocene hominins from the region, reflecting mosaic morphologies that contribute to a lack of consensus on when and how the transition to modern humans transpired. Newly discovered 300 ka hominin fossils from Hualongdong, China, provide further evidence to clarify these relationships in the region. In this study, facial morphology of the juvenile partial cranium (HLD 6) is described and qualitatively and quantitatively compared with that of other key Early, Middle, and Late Pleistocene hominins from East Asia, Africa, West Asia, and Europe and with a sample of modern humans. Qualitatively, facial morphology of HLD 6 resembles that of Early and Middle Pleistocene hominins from Zhoukoudian, Nanjing, Dali, and Jinniushan in China, as well as others from Java, Africa, and Europe in some of these features (e.g., supraorbital and malar regions), and Late Pleistocene hominins and modern humans from East Asia, Africa, and Europe in other features (e.g., weak prognathism, flat face and features in nasal and hard plate regions). Comparisons of HLD 6 measurements to group means and multivariate analyses support close affinities of HLD 6 to Late Pleistocene hominins and modern humans. Expression of a mosaic morphological pattern in the HLD 6 facial skeleton further complicates evolutionary interpretations of regional morphological diversity in East Asia. The prevalence of modern features in HLD 6 suggests that the hominin population to which HLD 6 belonged may represent the earliest pre-modern humans in East Asia. Thus, the transition from archaic to modern morphology in East Asian hominins may have occurred at least by 300 ka, which is 80,000 to 100,000 years earlier than previously recognized.

The ripples of modernity: How we can extend paleoanthropology with the extended evolutionary synthesis.

Contemporary understandings of paleoanthropological data illustrate that the search for a line defining, or a specific point designating, "modern human" is problematic. Here we lend support to the argument for the need to look for patterns in the paleoanthropological record that indicate how multiple evolutionary processes intersected to form the human niche, a concept critical to assessing the development and processes involved in the emergence of a contemporary human phenotype. We suggest that incorporating key elements of the Extended Evolutionary Synthesis (EES) into our endeavors offers a better and more integrative toolkit for modeling and assessing the evolution of the genus Homo. To illustrate our points, we highlight how aspects of the genetic exchanges, morphology, and material culture of the later Pleistocene complicate the concept of "modern" human behavior and suggest that multiple evolutionary patterns, processes, and pathways intersected to form the human niche.

Trajectories of cultural innovation from the Middle to Later Stone Age in Eastern Africa: Personal ornaments, bone artifacts, and ocher from Panga ya Saidi, Kenya.

African Middle Stone Age (MSA) populations used pigments, manufactured and wore personal ornaments, made abstract engravings, and produced fully shaped bone tools. However, ongoing research across Africa reveals variability in the emergence of cultural innovations in the MSA and their subsequent development through the Later Stone Age (LSA). When present, it appears that cultural innovations manifest regional variability, suggestive of distinct cultural traditions. In eastern Africa, several Late Pleistocene sites have produced evidence for novel activities, but the chronologies of key behavioral innovations remain unclear. The 3 m deep, well-dated, Panga ya Saidi sequence in eastern Kenya, encompassing 19 layers covering a time span of 78 kyr beginning in late Marine Isotope Stage 5, is the only known African site recording the interplay between cultural and ecological diversity in a coastal forested environment. Excavations have yielded worked and incised bones, ostrich eggshell beads (OES), beads made from seashells, worked and engraved ocher pieces, fragments of coral, and a belemnite fossil. Here, we provide, for the first time, a detailed analysis of this material. This includes a taphonomic, archeozoological, technological, and functional study of bone artifacts; a technological and morphometric analysis of personal ornaments; and a technological and geochemical analysis of ocher pieces. The interpretation of the results stemming from the analysis of OES beads is guided by an ethnoarcheological perspective and field observations. We demonstrate that key cultural innovations on the eastern African coast are evident by 67 ka and exhibit remarkable diversity through the LSA and Iron Age. We suggest the cultural trajectories evident at Panga ya Saidi were shaped by both regional traditions and cultural/demic diffusion.

Hybridization in human evolution: Insights from other organisms.

During the late Pleistocene, isolated lineages of hominins exchanged genes thus influencing genomic variation in humans in both the past and present. However, the dynamics of this genetic exchange and associated phenotypic consequences through time remain poorly understood. Gene exchange across divergent lineages can result in myriad outcomes arising from these dynamics and the environmental conditions under which it occurs. Here we draw from our collective research across various organisms, illustrating some of the ways in which gene exchange can structure genomic/phenotypic diversity within/among species. We present a range of examples relevant to questions about the evolution of hominins. These examples are not meant to be exhaustive, but rather illustrative of the diverse evolutionary causes/consequences of hybridization, highlighting potential drivers of human evolution in the context of hybridization including: influences on adaptive evolution, climate change, developmental systems, sex-differences in behavior, Haldane's rule and the large X-effect, and transgressive phenotypic variation.

Population structure and the evolution of Homo sapiens in Africa.

It has been proposed that a multiregional model could describe how Homo sapiens evolved in Africa beginning 300,000 years ago. Multiregionalism would require enduring morphological or behavioral differences among African regions and morphological or behavioral continuity within each. African fossils, archeology, and genetics do not comply with either requirement and are unlikely to, because climatic change periodically disrupted continuity and reshuffled populations. As an alternative to multiregionalism, I suggest that reshuffling produced novel gene constellations, including one in which the additive or cumulative effect of newly associated genes enhanced cognitive or communicative potential. Eventual fixation of such a constellation in the lineage leading to modern H. sapiens would explain the abrupt appearance of the African Later Stone Age 50-45 thousand years ago, its nearly simultaneous expansion to Eurasia in the form of the Upper Paleolithic, and the ability of fully modern Upper Paleolithic people to swamp or replace non-modern Eurasians.

Cranial measures and ancient DNA both show greater similarity of Neandertals to recent modern Eurasians than to recent modern sub-Saharan Africans.

OBJECTIVES: Ancient DNA analysis has shown that present-day humans of Eurasian ancestry are more similar to Neandertals than are present-day humans of sub-Saharan African ancestry, reflecting interbreeding after modern humans first left Africa. We use craniometric data to test the hypothesis that the crania of recent modern humans show the same pattern. MATERIALS AND METHODS: We computed Mahalanobis squared distances between a published Neandertal centroid based on 37 craniometric traits and each of 2,413 recent modern humans from the Howells global data set (N = 373 sub-Saharan Africans, N = 2,040 individuals of Eurasian descent). RESULTS: The average distance to the Neandertal centroid is significantly lower for Eurasian crania than for sub-Saharan African crania as expected from the findings of ancient DNA (p < 0.001). This result holds when examining distances for separate geographic regions of humans of Eurasian descent (Europeans, Asians, Australasians, Native Americans, and Pacific Islanders). Most of these results are also seen when examining distances partitioning size and shape variation. DISCUSSION: Our results show that the genetic difference in Neandertal ancestry seen in the DNA of present-day sub-Saharan Africans and Eurasians is also found in patterns of recent modern human craniometric variation.

Late Pleistocene age and archaeological context for the hominin calvaria from GvJm-22 (Lukenya Hill, Kenya).

Kenya National Museums Lukenya Hill Hominid 1 (KNM-LH 1) is a Homo sapiens partial calvaria from site GvJm-22 at Lukenya Hill, Kenya, associated with Later Stone Age (LSA) archaeological deposits. KNM-LH 1 is securely dated to the Late Pleistocene, and samples a time and region important for understanding the origins of modern human diversity. A revised chronology based on 26 accelerator mass spectrometry radiocarbon dates on ostrich eggshells indicates an age range of 23,576-22,887 y B.P. for KNM-LH 1, confirming prior attribution to the Last Glacial Maximum. Additional dates extend the maximum age for archaeological deposits at GvJm-22 to >46,000 y B.P. (>46 kya). These dates are consistent with new analyses identifying both Middle Stone Age and LSA lithic technologies at the site, making GvJm-22 a rare eastern African record of major human behavioral shifts during the Late Pleistocene. Comparative morphometric analyses of the KNM-LH 1 cranium document the temporal and spatial complexity of early modern human morphological variability. Features of cranial shape distinguish KNM-LH 1 and other Middle and Late Pleistocene African fossils from crania of recent Africans and samples from Holocene LSA and European Upper Paleolithic sites.

Genomic and cranial phenotype data support multiple modern human dispersals from Africa and a southern route into Asia.

Despite broad consensus on Africa as the main place of origin for anatomically modern humans, their dispersal pattern out of the continent continues to be intensely debated. In extant human populations, the observation of decreasing genetic and phenotypic diversity at increasing distances from sub-Saharan Africa has been interpreted as evidence for a single dispersal, accompanied by a series of founder effects. In such a scenario, modern human genetic and phenotypic variation was primarily generated through successive population bottlenecks and drift during a rapid worldwide expansion out of Africa in the Late Pleistocene. However, recent genetic studies, as well as accumulating archaeological and paleoanthropological evidence, challenge this parsimonious model. They suggest instead a "southern route" dispersal into Asia as early as the late Middle Pleistocene, followed by a separate dispersal into northern Eurasia. Here we test these competing out-of-Africa scenarios by modeling hypothetical geographical migration routes and assessing their correlation with neutral population differentiation, as measured by genetic polymorphisms and cranial shape variables of modern human populations from Africa and Asia. We show that both lines of evidence support a multiple-dispersals model in which Australo-Melanesian populations are relatively isolated descendants of an early dispersal, whereas other Asian populations are descended from, or highly admixed with, members of a subsequent migration event.

Archaeological shellfish size and later human evolution in Africa.

Approximately 50 ka, one or more subgroups of modern humans expanded from Africa to populate the rest of the world. Significant behavioral change accompanied this expansion, and archaeologists commonly seek its roots in the African Middle Stone Age (MSA; ∼200 to ∼50 ka). Easily recognizable art objects and "jewelry" become common only in sites that postdate the MSA in Africa and Eurasia, but some MSA sites contain possible precursors, especially including abstractly incised fragments of ocher and perforated shells interpreted as beads. These proposed art objects have convinced most specialists that MSA people were behaviorally (cognitively) modern, and many argue that population growth explains the appearance of art in the MSA and its post-MSA florescence. The average size of rocky intertidal gastropod species in MSA and later coastal middens allows a test of this idea, because smaller size implies more intense collection, and more intense collection is most readily attributed to growth in the number of human collectors. Here we demonstrate that economically important Cape turban shells and limpets from MSA layers along the south and west coasts of South Africa are consistently and significantly larger than turban shells and limpets in succeeding Later Stone Age (LSA) layers that formed under equivalent environmental conditions. We conclude that whatever cognitive capacity precocious MSA artifacts imply, it was not associated with human population growth. MSA populations remained consistently small by LSA standards, and a substantial increase in population size is obvious only near the MSA/LSA transition, when it is dramatically reflected in the Out-of-Africa expansion.

Paleoenvironmental context of the Middle Stone Age record from Karungu, Lake Victoria Basin, Kenya, and its implications for human and faunal dispersals in East Africa.

The opening and closing of the equatorial East African forest belt during the Quaternary is thought to have influenced the biogeographic histories of early modern humans and fauna, although precise details are scarce due to a lack of archaeological and paleontological records associated with paleoenvironmental data. With this in mind, we provide a description and paleoenvironmental reconstruction of the Late Pleistocene Middle Stone Age (MSA) artifact- and fossil-bearing sediments from Karungu, located along the shores of Lake Victoria in western Kenya. Artifacts recovered from surveys and controlled excavations are typologically MSA and include points, blades, and Levallois flakes and cores, as well as obsidian flakes similar in geochemical composition to documented sources near Lake Naivasha (250 km east). A combination of sedimentological, paleontological, and stable isotopic evidence indicates a semi-arid environment characterized by seasonal precipitation and the dominance of C4 grasslands, likely associated with a substantial reduction in Lake Victoria. The well-preserved fossil assemblage indicates that these conditions are associated with the convergence of historically allopatric ungulates from north and south of the equator, in agreement with predictions from genetic observations. Analysis of the East African MSA record reveals previously unrecognized north-south variation in assemblage composition that is consistent with episodes of population fragmentation during phases of limited dispersal potential. The grassland-associated MSA assemblages from Karungu and nearby Rusinga Island are characterized by a combination of artifact types that is more typical of northern sites. This may reflect the dispersal of behavioral repertoires-and perhaps human populations-during a paleoenvironmental phase dominated by grasslands.

The origins and significance of coastal resource use in Africa and Western Eurasia.

The systematic exploitation of marine foods by terrestrial mammals lacking aquatic morphologies is rare. Widespread ethnographic and archaeological evidence from many areas of the world shows that modern humans living on coastlines often ratchet up the use of marine foods and develop social and technological characteristics unusual to hunter-gatherers and more consistent with small scale food producing societies. Consistent use of marine resources often is associated with reduced mobility, larger group size, population packing, smaller territories, complex technologies, increased economic and social differentiation, and more intense and wide-ranging gifting and exchange. The commitment to temporally and spatially predictable and dense coastal foods stimulates investment in boundary defense resulting in inter-group conflict as predicted by theory and documented by ethnography. Inter-group conflict provides an ideal context for the proliferation of intra-group cooperative behaviors beneficial to the group but not to the altruist (Bowles, 2009). The origins of this coastal adaptation marks a transformative point for the hominin lineage in Africa since all previous adaptive systems were likely characterized by highly mobile, low-density, egalitarian populations with large territories and little boundary defense. It is important to separate occasional uses of marine foods, present among several primate species, from systematic and committed coastal adaptations. This paper provides a critical review of where and when systematic use of coastal resources and coastal adaptations appeared in the Old World by a comparison of the records from Africa and Europe. It is found that during the Middle Stone Age in South Africa there is evidence that true coastal adaptations developed while there is, so far, a lack of evidence for even the lowest levels of systematic coastal resource use by Neanderthals in Europe. Differences in preservation, sample size, and productivity between these regions do not explain the pattern.

Brief communication: Artificial cranial modification in Kow Swamp and Cohuna.

The crania from Kow Swamp and Cohuna have been important for a number of debates in Australian paleoanthropology. These crania typically have long, flat foreheads that many workers have cited as evidence of genetic continuity with archaic Indonesian populations, particularly the Ngandong sample. Other scientists have alleged that at least some of the crania from Kow Swamp and the Cohuna skull have been altered through artificial modification, and that the flat foreheads possessed by these individuals are not phylogenetically informative. In this study, several Kow Swamp crania and Cohuna are compared to known modified and unmodified comparative samples. Canonical variates analyses and Mahalanobis distances are generated, and random expectation statistics are used to calculate statistical significance for these tests. The results of this study agree with prior work indicating that a portion of this sample shows evidence for artificial modification of the cranial vault. Many Kow Swamp crania and Cohuna display shape similarities with a population of known modified individuals from New Britain. Kow Swamp 1, 5, and Cohuna show the strongest evidence for modification, but other individuals from this sample also show evidence of culturally manipulated changes in cranial shape. This project provides added support for the argument that at least some Pleistocene Australian groups were practicing artificial cranial modification, and suggests that caution should be used when including these individuals in phylogenetic studies.

A demographic perspective on the Middle to Later Stone Age transition from Nasera rockshelter, Tanzania.

Increased population density is among the proposed drivers of the behavioural changes culminating in the Middle to Later Stone Age (MSA-LSA) transition and human dispersals from East Africa, but reliable archaeological measures of demographic change are lacking. We use Late Pleistocene-Holocene lithic and faunal data from Nasera rockshelter (Tanzania) to show progressive declines in residential mobility-a variable linked to population density-and technological shifts, the latter associated with environmental changes. These data suggest that the MSA-LSA transition is part of a long-term pattern of changes in residential mobility and technology that reflect human responses to increased population density, with dispersals potentially marking a complementary response to larger populations.This article is part of the themed issue 'Major transitions in human evolution'.

The shaping of human diversity: filters, boundaries and transitions.

The evolution of modern humans was a complex process, involving major changes in levels of diversity through time. The fossils and stone tools that record the spatial distribution of our species in the past form the backbone of our evolutionary history, and one that allows us to explore the different processes-cultural and biological-that acted to shape the evolution of different populations in the face of major climate change. Those processes created a complex palimpsest of similarities and differences, with outcomes that were at times accelerated by sharp demographic and geographical fluctuations. The result is that the population ancestral to all modern humans did not look or behave like people alive today. This has generated questions regarding the evolution of human universal characters, as well as the nature and timing of major evolutionary events in the history of Homo sapiens The paucity of African fossils remains a serious stumbling block for exploring some of these issues. However, fossil and archaeological discoveries increasingly clarify important aspects of our past, while breakthroughs from genomics and palaeogenomics have revealed aspects of the demography of Late Quaternary Eurasian hominin groups and their interactions, as well as those between foragers and farmers. This paper explores the nature and timing of key moments in the evolution of human diversity, moments in which population collapse followed by differential expansion of groups set the conditions for transitional periods. Five transitions are identified (i) at the origins of the species, 240-200 ka; (ii) at the time of the first major expansions, 130-100 ka; (iii) during a period of dispersals, 70-50 ka; (iv) across a phase of local/regional structuring of diversity, 45-25 ka; and (v) during a phase of significant extinction of hunter-gatherer diversity and expansion of particular groups, such as farmers and later societies (the Holocene Filter), 15-0 ka.This article is part of the themed issue 'Major transitions in human evolution'.