U-series dating Owing to the poor provenance, we attempted to directly date this fossil cranium using a U-series method. Fossil bones are less desirable than carbonates for U-series dating, because fossil bones readily take up uranium from groundwater after deposition. However, if the incorporated uranium has not been leached out at some time after bone deposition, the U-series apparent age can provide the minimum age of the fossil.26
To minimize destruction on the Harbin fossil cranium, the samples (n = 10) for U-series dating were hand drilled on the broken surfaces of the bones with 0.3 mm carbide-tipped drill bits, and the powdered sample size was kept between 0.1 and 0.5 mg (Figure 5). The U and Th isotopic measurements were performed on an MC-ICPMS (Thermo Fisher Neptune). The U-series dating results are summarized in Table S3. All samples lie within a narrow 234U/238U activity ratio range (1.481–1.576), but show large variations in 230Th/234U activity ratio (0.474–1.039). The corrected U-series apparent ages are highly scattered, ranging from 62 ± 3 to 296 ± 8 ka, and the back-calculated initial 234U/238U activity ratio (234U/238Ui) ranged from 1.652 to 2.161 (Table S3).
Figure 5 Sampling locations on the Harbin cranium for U-series dating analyses
The results can roughly be divided into two groups. The first group includes five samples that have relatively younger U-series apparent ages (from 62 ± 3 to 148 ± 2 ka), red data points in the isotope evolution diagram (Figure 6). Their isotopic data randomly scatter around the U-series evolution curve for an initial 234U/238Ui of 1.70 (Figure 6). This pattern suggests that the source of uranium in these samples remained the same, but U-uptake took place over different time intervals without obvious evidence for post-burial U-leaching. The two youngest U-series apparent ages are 62 ± 3 and 85 ± 4 ka (HH19-1, 2), both obtained on the exposed dentine from the tooth roots of the surviving molar (M2). The young ages are probably caused by a delayed U-uptake, because the cementum and dentine of the tooth roots are much denser than the bones and probably obstructed uranium migration into the dentine. The other three U-series apparent ages, 106 ± 1, 129 ± 1, and 148 ± 2 ka, were obtained on HH19-6, 20-2, and 19-4, respectively. This group of data has no obvious evidence for U-leaching and is reasonable for estimating the minimum age of the Harbin cranium. The best minimum age estimate derived from this data group is the maximum value of the data group: that is 148 ± 2 ka.
Figure 6 U-series evolution diagram showing the activity ratios observed on the Harbin cranium
The second group (green data points in Figure 6) includes five samples with relatively older U-series apparent ages (185 ± 2 to 296 ± 8 ka). This older age group shows higher 230Th/234U isotope ratios and more widely scattered initial 234U/238Ui ratios than the younger age group. It can be expected that, for a bone that experienced continuous U-uptake process, its 230Th/234U activity ratio should be less than 1, but the occurrence of U-leaching can result in a shift of the 230Th/234U activity ratio to higher values, even beyond isotopic equilibrium.27 The subsample HH19-3 shows the oldest apparent U-series age of ∼296 ka, but it has 230Th activities in excess of 234U (230Th/234U = 1.031 ± 0.006), suggesting that this old age is very likely the result of U-leaching. The other four subsamples with older ages (HH19-5, 19-7, 20-1, and 20-3) have 230Th/234U ratios close to isotopic equilibrium (0.943 on average), suggesting that a slight U-leaching has occurred to these samples. Leached samples do not provide any useful age information, we therefore regard the age of 146 ka from the younger age group as the most conservative age (minimum age) estimate for the Harbin cranium.
The U-series apparent ages of the mammalian/human fossils from the Harbin area (Figures S1 and S2; Table S3) can be seen as the minimum ages of the corresponding fossil samples, except for the samples V23288 and F12, because their 230Th activities are in excess of 234U, and thus the occurrence of U-leaching cannot be excluded. All these samples show initial 234U/238Ui (1.467–2.063) comparable with the values measured in the Harbin cranium (1.652–2.161), which provide another line of evidence that the Harbin cranium was probably from a similar burial environment as these fossils analyzed for comparison.
Discussion and conclusions Our analyses reveal that the Harbin cranium has XRF element distribution patterns and REE concentration patterns like those of the mammalian and human fossils recovered from the Pleistocene sediments in the Harbin area. The 87Sr/86Sr ratio of the Harbin cranium (0.709423) also falls in the range of these mammalian and human fossils for comparison (ranging from 0.709066 to 0.709574). All these 87Sr/86Sr ratios are within the range of the regional bioavailable Sr isotope ratio values in the Harbin areas. The sediments adhered in the nasal cavity of the Harbin cranium show a 87Sr/86Sr ratio of 0.711898, very close to the values measured at the upper part of the DJ core at a depth of ∼12 m. The regional stratigraphic correlations based on Sr isotopic data and lithostratigraphic characters indicate that the Harbin cranium probably was recovered from the upper part of the Upper Huangshan Formation. Direct U-series dating on the cranium (n = 10) suggests that one group of the samples suffered U-leaching, and one group of the samples experienced continuous or delayed U-uptake without obvious evidence of U-leaching. The group without U-leaching yielded an apparent age of ∼146 ka as the most conservative age (minimum age) estimate for the Harbin cranium. This minimum age is consistent with the regional stratigraphic correlation. While the multiple lines of evidence from our experiments cannot pin the Harbin cranium to an exact site and layer, they consistently support the conclusion that this human specimen is from the late Middle Pleistocene of the Harbin area.
The late Middle Pleistocene Harbin archaic human (>146 ka) is roughly contemporaneous with some other Middle Pleistocene archaic humans from China, such as Xiahe (≥160 ka),28 Jinniushan (≥200 ka),29 Dali (327–240 ka),30,31 and Hualongdong (345–265 ka).32 This age span also overlaps with the early H. sapiens from Africa and the Mideast. If these East Asian archaic humans indeed belong to a monophyletic evolutionary lineage sister to the H. sapiens lineage,1 this human lineage must have been as successful as the early H. sapiens populations in Africa and the Mideast, because they distributed in a very large area, including some extreme environments (high altitude and high latitude). Material and methods
Provenance test We used non-destructive XRF analyses, following the procedures of Li et al.,33 to examine the element distribution of the Harbin cranium and a range of mammalian fossils (n = 6) collected from submerged sediments near the Dongjiang Bridge (Figure 1). The mammalian fossils are Middle-Late Pleistocene in age. Two mammalian fossils from sites in southern China were used as control samples. All the fossil specimens are under the oversight of the institutional review board of the Hebei GEO University or the Institute of Vertebrate Paleontology and Paleoanthropology. XRF analyses were performed on the M4 TORADO PLUS Micro-SRF analyzer at the Institute of Geology and Geophysics, Chinese Academy of Sciences. One area of about ∼1–2 cm2 for each sample was randomly selected for collecting the XRF signals. Measuring parameters were set at 50 kV of high voltage and 40 μm of pixel size. For semi-quantitative comparisons, each XRF spectrum was normalized with the signal of the Rh-Lα peak, which is generated by a Rh X-ray source.
Small bone pieces (∼100 mg) from the nasal cavity of the Harbin cranium were carefully collected for REE and Sr isotopic analyses. For comparison, fossil fragments from mammals (Figure S1, n = 6) and late Pleistocene-Holocene human individuals (Figures S2 and S3, n = 2) recovered from the Dongjiang Bridge area were analyzed. The sediment samples adhering in the nasal cavity of the Harbin cranium (n = 1) and from a core (n = 45) drilled near the Dongjiang Bridge were also used for Sr isotopic analyses.
REE analyses were performed at the State Key Laboratory for Mineral Deposits Research, Nanjing University. A Thermo Fisher Element XR HR-ICP-MS was used for the REE analyses. The samples were processed using the method in Trueman et al.34 The rhodium solution (10 ppb) was dropped into the sample solutions for instrument drift correction. Analytical precision was <5% for each element. An MC-ICPMS (multiple collector inductively coupled plasma mass spectrometer, Thermo Fisher Neptune) in Nanjing Normal University was used for the Sr isotopic analyses. Sample preparation and measurement methods followed that of Lei et al.35 The measured 87Sr/86Sr ratio was corrected for mass fractionation by normalization to a constant 86Sr/88Sr ratio of 0.1194 using an exponential law. The isobaric interference of 87Rb on 87Sr was corrected using a natural 87Rb/85Rb ratio of 0.3857. Replicate measurements of the NIST SRM 987 standard yielded a mean value of 87Sr/86Sr = 0.710263 ± 0.000014 (2σ, n = 11) during the analytical period.
U-series analysis We carried out the U-series analysis directly on the Harbin cranium. Sample preparation followed that of Shao et al.36 The U and Th isotopic measurements were performed on an MC-ICPMS (Thermo Fisher Neptune) in Nanjing Normal University. It is equipped with nine Faraday cups and a secondary electron multiplier (SEM). A retarding potential quadrupole energy filter was positioned in front of the SEM. An Aridus-II desolvator system (Cetac) couple with an ESI-50 nebulizer and an AutoSampler (ASX-520) was used for sample introduction. The U-series analysis results are summarized in Table S3. The isotopic variation and age distribution indicate that the U-uptake histories are heterogeneous in the Harbin cranium. A group of samples showing no evidence of U-leaching26 had a U-series apparent age range of 62 ± 3 to 148 ± 2 ka. We consider that the oldest U-series apparent age (148 ± 2 ka) is a minimum age estimate for the Harbin cranium.
Massive cranium from Harbin in northeastern China establishes a new Middle Pleistocene human lineage
Xijun Ni Qiang Ji Wensheng Wu Qiang Li Rainer Grün Chris Stringer
Published:June 25, 2021
DOI:https://doi.org/10.1016/j.xinn.2021.100130
Public summary •More than 100,000 years ago, several human species coexisted in Asia, Europe, and Africa •A completely preserved fossil human cranium discovered in the Harbin area provides critical evidence for understanding the evolution of humans and the origin of our species •The Harbin cranium has a large cranial capacity (∼1,420 mL) falling in the range of modern humans, but is combined with a mosaic of primitive and derived characters •Our comprehensive phylogenetic analyses suggest that the Harbin cranium represents a new sister lineage for Homo sapiens •A multi-directional “shuttle dispersal model” is more likely to explain the complex phylogenetic connections among African and Eurasian Homo species/populations
It has recently become clear that several human lineages coexisted with Homo sapiens during the late Middle and Late Pleistocene. Here, we report an archaic human fossil that throws new light on debates concerning the diversification of the Homo genus and the origin of H. sapiens. The fossil was recovered in Harbin city in northeastern China, with a minimum uranium-series age of 146 ka. This cranium is one of the best preserved Middle Pleistocene human fossils. Its massive size, with a large cranial capacity (∼1,420 mL) falling in the range of modern humans, is combined with a mosaic of primitive and derived characters. It differs from all the other named Homo species by presenting a combination of features, such as long and low cranial vault, a wide and low face, large and almost square orbits, gently curved but massively developed supraorbital torus, flat and low cheekbones with a shallow canine fossa, and a shallow palate with thick alveolar bone supporting very large molars. The excellent preservation of the Harbin cranium advances our understanding of several less-complete late Middle Pleistocene fossils from China, which have been interpreted as local evolutionary intermediates between the earlier species Homo erectus and later H. sapiens. Phylogenetic analyses based on parsimony criteria and Bayesian tip-dating suggest that the Harbin cranium and some other Middle Pleistocene human fossils from China, such as those from Dali and Xiahe, form a third East Asian lineage, which is a part of the sister group of the H. sapiens lineage. Our analyses of such morphologically distinctive archaic human lineages from Asia, Europe, and Africa suggest that the diversification of the Homo genus may have had a much deeper timescale than previously presumed. Sympatric isolation of small populations combined with stochastic long-distance dispersals is the best fitting biogeographical model for interpreting the evolution of the Homo genus.
Introduction The origin of modern humans (Homo sapiens, our own species) has long been a controversial topic. During the late Middle and Late Pleistocene, several human lineages, evidently at species level, coexisted with H. sapiens across Africa and Eurasia. These extinct hominins include H. heidelbergensis/H. rhodesiensis, Homo naledi, Homo floresiensis, H. luzonensis, Denisovans, Neanderthals (Homo neanderthalensis), and Homo erectus.1, 2, 3, 4, 5 The phylogenetic relationship between these coexisting hominins and H. sapiens has long been debated. Before the appearance of undoubted modern humans in Asia, some archaic fossils, such as those from Narmada, Maba, Dali, Jinniushan, Xuchang, and Hualongdong show mosaic combinations of features present in H. erectus, H. heidelbergensis/H. rhodesiensis, Neanderthals, and H. sapiens. Therefore, it is widely believed that these Asian hominins are critical for studying the later evolution of the genus Homo and the origin of H. sapiens. The incomplete preservation of these fossils and the fact that they have largely been described by advocates of regional continuity have made it difficult to integrate them into the wider picture of human evolution. For example, Xuchang, Dali, and Hualongdong have all been described as transitional forms between Chinese H. erectus and H. sapiens, whose affinities can be understood in the context of a braided stream network model of gene flow.6, 7, 8, 9 Here, we report a fossil human cranium that is characterized by a combination of large cranial capacity, short face, and small check bones as in H. sapiens, but also a low vault, strong browridges, large molars, and alveolar prognathism as in most archaic humans. Through phylogenetic and biogeographic analyses, we argue that this fossil is the most complete representative of a distinct Middle Pleistocene lineage, with a separate evolutionary history in East Asia.
The Harbin human fossil is represented by a single cranium (HBSM2018-000018(A), housed in the Geoscience Museum of Hebei GEO University, Shijiazhuang, Hebei Province, China), which was reportedly discovered in 1933 during construction work when a bridge (Dongjiang Bridge) was built over the Songhua River in Harbin city (Figure 1). Because of a long and confused history since the discovery (see the supplemental information), the exact site of the find is uncertain. We tested the concentrations of rare earth elements (REEs) and the Sr isotopic composition of the human fossil and a range of mammalian fossils collected from deposits of the Songhua River near the supposed locality (Dongjiang Bridge), and used non-destructive X-ray fluorescence analyses to examine the element distributions of these human and mammalian fossils. The results of our experiments show that element distributions and REE concentrations of the Harbin cranium and the mammalian fossils found near Dongjiang Bridge have similar distribution patterns.10 The Sr isotopic composition of the Harbin cranium falls in the range of the local Middle Pleistocene-Early Holocene human and mammalian fossils.10 We also directly dated the Harbin fossil cranium by the uranium-series disequilibrium (U-series) method. The results suggest a minimum age for the cranium of ∼146 ka.10 While these results cannot pin the Harbin cranium to an exact site and layer, they are consistent with the conclusion that the cranium is from the late Middle Pleistocene of the Harbin area.10
Figure 1 Geographic location of the Harbin cranium
Morphology The Harbin cranium is undistorted and almost intact, with the main losses being all but one tooth (the left M2), and slight damage to the left zygomatic arch (Figure 2). It is massive in size, showing the largest values in our comparative fossil database (see the supplemental information) for measurements, such as maximum cranial length, nasio-occipital length, and supraorbital torus breadth, and the second largest values for measurements, such as biauricular breadth, frontal chord, zygomatic breadth, and biorbital breadth. Detailed morphological descriptions and comparisons of the cranium are given in the supplemental information, and are summarized below.
Figure 2 The Harbin cranium in standard views
The cranial vault is voluminous (∼1,420 mL capacity, measured using high-resolution computed tomography [CT] scanning and three-dimensional reconstruction of the endocranial cast). However, the braincase is clearly archaic, with a very wide supraorbital torus, base and palate, and a long and low shape in lateral view, with a receding frontal and evenly curved parietal contour. Nevertheless, it lacks both the angulated occipital with a strong transverse torus found in H. erectus and H. heidelbergensis/H. rhodesiensis crania, and the protruding occipital region with a central suprainiac fossa typical of Neanderthals. In posterior view the unkeeled cranium is widest in the supramastoid area, below which the well-developed mastoid processes slope inward. The temporals and parietals do not converge strongly as in H. erectus fossils, but there is no upper parietal expansion, as found in recent H. sapiens, nor the “en bombe” shape typical of Neanderthals. In lateral view the face is relatively low in height and retracted under the cranial vault, lacking the total anterior projection typical of H. erectus and H. heidelbergensis/H. rhodesiensis. The upper face and nasal aperture are very wide, but the zygomaxillary region is transversely flat and faces anteriorly, with a morphology like that of H. sapiens.
The combination of an archaic but large-brained cranial vault and a wide but H. sapiens-like face is striking, and is also found in the less-complete Middle Pleistocene Chinese fossils from Dali and Jinniushan, although they differ in details of morphology (see the supplemental information and Video S1. Virtual reconstruction of the Harbin cranium based on CT scanning, yaw movie, Video S2. Virtual reconstruction of the Harbin cranium based on CT scanning, pitch movie, Video S3. Virtual Reconstruction of the Harbin Cranium based on CT scanning, roll movie). The less-complete Hualongdong cranium resembles Dali more closely in several respects, and some of its differences may be due to its immaturity, while the Xuchang and Maba partial crania appear more distinct (see the supplemental information for more details and comparative data).
Overall, the Harbin cranium shows an individual combination of traits, and probably represents a distinct species of Homo from other designated Middle-Late Pleistocene human taxa, such as H. sapiens, H. neanderthalensis, and H. heidelbergensis/H. rhodesiensis. Its enormous overall size sets it apart from nearly every other fossil but, in terms of cranial vault proportions, the braincase clearly overlaps in shape with those of other large-sized late archaic Homo species. However, the face, despite its enormous breadth dimensions, is relatively low in height and has an H. sapiens and H. antecessor-like zygomaxillary shape that is also found in the Middle Pleistocene Chinese fossils from Dali and Jinniushan. It is also hafted onto the braincase with reduced prognathism, as in recent humans. In its combination of traits, the Harbin cranium is more like fossils attributed to early H. sapiens, such as Jebel Irhoud 1 and Eliye Springs, than to later members of our lineage. Finally, and perhaps significantly, the morphology and large size of the surviving Harbin M2 (Figure S1, mesiodistal length 13.6 mm and buccolingual width 16.6 mm) are matched most closely in the Late Pleistocene record by the permanent molars from Denisova Cave (Denisovan 4: M2/3, mesiodistal length 13.1 mm, and buccolingual width 14.7 mm; Denisovan 8: M3, mesiodistal length 14.3 mm, and buccolingual width 14.65 mm).11,12