Australia: The Land Where Time Began
Human Remains from the Pleistocene-Holocene Transition, Southwest China, Apparent Complex Evolutionary History for East Asians
Human evolution in Late Pleistocene in East Asia is still poorly understood as a result of a scarcity of fossils that are well described, classified reliably and dated accurately. Genetic research has indicated that southwest China is a hotspot of human diversity, containing lineages of ancient mtDNA and Y-DNA, as well as producing a number of human remains believed to derive from deposits of Pleistocene age. Curnoe et al.1 say they have prepared, reconstructed, described and dated a new partial skull from the sediment block that has been consolidated that was collected in 1979 from Longlin Cave, Guangxi Province. New excavations at Maludong, Yunnan Province were undertaken by the authors1 to clarify the stratigraphy and dating of a large sample of human remains from the site that are mostly undescribed.
A detailed comparison was undertaken by the authors1 of crania, including a virtual endocast from the Maludong calotte, mandibular remains from these 2 localities, both samples probably being derived from the same population, which exhibited an unusual combination of traits of modern humans, characters which are probably plesiomorphic for later Homo, as well as some unusual features. They dated charcoal by the AMS radiocarbon and speleothem method with the U-series technique, the results showing that both samples were from the Pleistocene-Holocene transition: ̴ 14.3-11.5 ka.
There are 2 plausible explanations that are suggested by this analysis of the morphology sampled at Longlin Cave and Maludong. The first explanation is that a late-surviving population may possibly parallel the situation of the Dar-es-Soltane and Tamara, North Africa, and maybe also in southern China and Zhirendong. An alternative possibility is that during the Pleistocene multiple waves may have colonised East Asia, with the morphology from Longlin and Maludong possibly reflecting deep population substructure in Africa prior to the dispersal of modern humans into Eurasia.
Europe, Africa and the Levantine corridor connecting them has historically been the focus of human evolution fossil research, resulting in the role of the vast continent of Asia being virtually unknown with regard to the fossil record of humans during this time of the evolution of modern humans. In South Asia the fossil record from the Upper Pleistocene of known human remains contains few human fossils; those that have been found are confined to 2 sites that date from possibly within the 33-25 ka range (Trinkhaus, E., 2005). Human fossils are more numerous in East Asia (Wu, X. & Poirier, 1995), though it has been difficult to assess the significance of these fossils because of the poor knowledge of their geological context and inadequate dating (Trinkhaus, E., 2005, 2-3). East Asia is considered to comprise the region that is bordered by the Ural Mountains in the west, in the southwest by the Himalayan Plateau, Bering Strait in the northwest, as well as extending into island southwest Asia.
The Liujiang skeleton from southern China has been discussed widely as a candidate for the oldest human in East Asia (Wu, X & Poirier, F.E., 1995), though the geological age of this individual has “an everlasting dispute since the discovery of the fossil in 1958” (Brӓuer, G. & Mímisson, K., 2004, p. 62) because of lack of documentation regarding the exact stratigraphic position of the human remains.
Other similarly problematic specimens are the fossils from the Upper Cave, Zhoukoudian, that have been a major source of uncertainty since their discovery in the 1930s, estimates range from ̴33-10 ka (Wu, X & Poirier, F.E., 1995, Brӓuer, G. & Mímisson, K., 2004). Also, the provenance of the child from Niah Cave in East Malaysia is uncertain (Barker et al., 2007). A proposed age of ̴45-39 ka for the cranium has been suggested for this cranium (Barker et al., 2007) as the result of a recent field and lab program that was aimed at assessing the stratigraphy and dating of the deposits at this site.
There is also a problem with most other candidates for the earliest humans in East Asia. The only specimen that is taxonomically diagnostic among the human remains that were recovered from Tabon Cave, Philippines, is a frontal bone that has been assigned to H. sapiens (Dizon, E. et al., 2002), that has been dated to 16.5 ± 2 ka (Détroit et al., 2002). Also, the oldest specimen from the site that has been directly dated to 47+11/-10 ka (Détroit, F. et al., 2004), could possibly be from an orang-utan (Dizon, E. et al., 2002). A hominin metatarsal recovered from Callao Cave, Luzon, has been directly dated to an estimated 66.7 ± 1 ka (Mijares A.M., et al., 2010), though it has been difficult to classify this specimen reliably, which has made its assignment to H. sapiens uncertain (Mijares A.M., et al., 2010). Recently an individual recovered from Tianyuan Cave, not far from Zhoukoudian town, northeast China, has been estimated to be ̴42-36 ka (Shang, H. et al., 2007). The partial skeleton from Tianyuan is comprised of 34 pieces that appear to be from the same individual, the femur of which has been dated directly to 40,328 ± 816 cal. yr BP. The best candidate for the earliest modern human in East Asia appears to be provided by this specimen, though it is significantly younger (>20 kya) than estimates from genetic clocks for the colonisation of the region. Finally, in Zhirendong, southern China, a mandibular fragment has been recovered that has been dated to more than 100 ka based on stratigraphic grounds, though the specimen is fragmentary and is comprised of a mosaic of archaic and modern characters that make its taxonomic status unclear (Liu, W., et al., 2010; Dennell, R., 2010).
Palaeoanthropologists have needed to rely on of genetic sequencing results of samples from living populations to attempt to reconstruct the origins of humans in East Asia because of the uncertainties concerning the human fossil record. It is suggested by genetic research that the earliest modern humans dispersed from Africa into Eurasia about 70-60 ka, after which they spread rapidly into Southeast Asia and Australia (Zhong, H., 2011; Kong, Q-P., 2011; Stoneking M. & Delfin, F., 2010; Rasmussen et al., 2011). Later migrations involved spreading within Eurasia after 40-30 ka adding the founding populations of modern Northeast Asians and Europeans (Rasmussen, M. et al., 2004). The authors1also suggest that there seem to have been several migrations later within the region, some of which were associated with the Neolithic (Zhong, H., 2011; Kong, Q-P., 2011; Stoneking M. & Delfin, F., 2010), and finally a hominin fossil from Denisova Cave, Central Asia, belonging with the Neanderthal lineage that shares features exclusively with Aboriginal Southeast Asians and Australasians (Reich, D. et al., 2010; Reich, D. et al., 2011; Abi-Rached, L., 2011). An interpretation of this has been as 1) evidence that interbreeding occurred between Denisovans and the earliest modern humans colonising the region; and 2) implying that this archaic population occupied Southeast Asia during the Upper Pleistocene (Reich, D. et al., 2010; Reich, D. et al., 2011).
The authors1 began a collaborative research project in 2008 aimed at age determination and to provide detailed comparisons of human remains in southwest China that were possibly from the Pleistocene, as the fossils from East Asia are considered to be of central importance to the testing of the regional and global scenarios of the evolution of humans. In this paper the authors1 have focused on the human remains recovered from 2 localities: Longlin Cave (Longlin or LL) and Malu Cave (Maludong or MLDG).
In 1979 a petroleum geologist, Li Changquing, discovered the human remains opportunistically in a cave near De’e, Longlin County, Guangxi Zhuang Autonomous Region, Guangxi Province. A short time after the discovery a block of consolidated fine-grained sediment that contained the human remains were taken to Kunming in the neighbouring province of Yunnan. At the time it was taken to Kunming a partial mandible and some post-cranial bone were prepared from the block (Wu, X & Poirier, 1995), the remainder of the skull and more post-cranial bones were prepared from the sediment by the authors1 team in 2010. A thin flowstone was found that was adhering to the surface of the vault of the partial LL 1 skeleton, and fragments of charcoal were recovered from the sediment within the endocrinal cavity. The association of the cranium, mandible and postcranial elements, all with similar preservation, in a small block of sediment, less than 1 m3 in volume, suggests there was limited post-depositional disturbance. The cave has been closed to the public and the authors1 have not been able to carry out the research needed to clarify the stratigraphy and geological context of the human remains.
Located near the city of Mengzi, Honghe Prefecture, Hani and Yi Autonomous Region, to the southeast of Yunnan Province, Maludong is a cave that has been partially mined (Wu, X & Poirier, 1995; Zhang et al., 1991). A Chinese team that included 1 of the Authors’1 team, BZ, originally excavated the site in 1989, at which time most of the fossil and archaeological material were recovered (Zhang et al., 1991). A re-evaluation of the remaining stratigraphic section and the collection of a number of samples that were to be used for dating and archaeomagnetic analysis were allowed by excavations undertaken in 2008 by several of the present authors (DC, JX, AH, BK, BZ, ZY and LY). During the current study more human remains were recovered, both during the small-scale excavation by the authors1, 50x50x370 cm, for stratigraphic analysis, as well as from unstudied and unsorted fossils that were recovered during the 1989 field season.
A range of individual features and a composite of characters that have not been seen among populations from the Pleistocene or recent H. sapiens populations are presented by the human skull recovered from Longlin Cave, and the human calotte, partial mandibles and teeth from Maludong. According to the authors1 the remains share no particular affinity with either East Asians from the Pleistocene, such as Liujiang or Upper Cave 101, or recent East Asians. It is also suggested that these features belong to multiple developmental-functional complexes (Enlow, D.H. & Hans, M.G., 2008), which span the neurocranial vault, and include endocranium, cranial base, facial skeleton, mandible and dentition. Where they can be assessed, the metrical dimensions that are involved are mostly characterised by moderate to high heritability (Sjøvold T., 1984; Carson A.E., 2006; Sherwood R.J. et al., 2008; Townsend GC, Brown T., 1978). It seems likely that both samples are from the same population, given their morphological similarity, close geographical proximity, less than 300 km apart, and a geological age that is younger, Pleistocene-Holocene transition.
Multivariate analysis of the shape of the vault, a method which has been shown to track neutral genetic distances (Weaver, T.D., Roseman, C.C. & Stringer, C.B., 2007), indicates that a picture that is somewhat mixed with respect to the phonetic affinities of LL 1 and MLDG 1704. The first principal component, which accounts for 45-46 % of the total variance, indicates that the dominanent phenetic signal in these analyses shows that LL 1 and MLDG 1704 are at the edge of variation within H. sapiens from the Pleistocene, and in some analyses they are also shown to be on the edge of variability of H. erectus. Principal component 3 in particular, ̴12-14 % of total variance, shows them to exhibit a cranial shape that is unique among all hominins from the Pleistocene.
This conclusion that these remains show affinities with H. sapiens is supported by a range of features:
Moderately projecting and laterally thin supraorbital part, which has the bipartite form in MLDG 1704; frontal bone with a moderate chord and arc length, but broad maximum width; and an endocast with long, broad and tall frontal lobes.
Superior facial breadth is narrow; facial skeleton is vertically short (superior facial height and orbit height and nasal length; and nasal breadth relative to height is moderate.
Mental foramen is in mesial position; and a medial pterygoid tubercle is absent.
Anterior dental crowns are small (narrow).
The fossils from Longlin and Maludong also have many features that are either rare or missing from H. sapiens from either the Pleistocene or the present, many of which are plesiomorphies included among later Homo, including :
Endocranial volume is moderate; frontal squama high arched; parietal bones are short; short parietal lobes on endocast; postorbital region is narrow; and bipartite supraorbital morphology is lacking in LL 1.
In LL 1 only there is a long mandibular fossa (A-P), broad (M – L) and deep (S – I).
In LL 1 only: alveolar prognathism is strong; mid-face is flat at both the nasal root and zygomatic process of the maxilla; facial skeleton is broad (interorbital, bizygomatic and bimaxillary); nasal bones very narrow; piriform aperture is broad; canine fossa lacking and deep sulcus maxillaris is present; laterally flared zygomatic arch; strongly angled zygomatic to the extent that its inferior margin is well lateral to the superior part; small zygomatic tubercle that is lateral to a line project from the orbital pillar (anterior aspect); attachment area of anterior masseter marked by broad deep sulcus; lateral orbital pillar (lateral aspect) has strong transverse incurvation; anterior wall of the zygomaticoalveolar root placed anteriorly (above P4/M1).
Sagittal keel and distinct Lateral tubercles absent; chin small (MLDG 1706 Rank 3, LL 1 Rank ?3); mandibular foramen bridging (MLDG 1706); transverse tori thickened; mandibular notch asymmetrical (MLDG 1679); lateral positioning of retromolar space, crest of mandibular notch (MLDG 1679); and anterior symphyseal angle is low (MLDG 1706).
Post-canine crowns broad (BL diameters large); and molars are taurodont.
See Source 1 for a detailed description of features supporting the inclusion of these remains in H. sapiens.
It is unusual, especially in Eurasia to find human remains with such a combination of modern human (H. sapiens) and archaic (putative plesiomorphic) characters. There are several Pleistocene remains in Africa that also display a combination of modern features with plesiomorphies of putative later Homo; from Klasies River Mouth Cave (Smith F.H., 1992) and Hofmeyr (Crevecoeur, I. et al., 2009), South Africa, Iwo Eleru, Nigeria (Harvati, K. et al., 2011), Nazlet Khater, Egypt, and Dar-es-Soltane and Témara, Morocco (Trinkhaus, E., 2005; Trinkhaus, E., 2007; Crevecoeur, I. et al., 2009). Though most of them are much older than Longlin and Maludong: Dar-es-Soltane and Témara are not dated, but they are associated with Aterian lithic assemblages dated recently to between 107 ± 3 ka and 96 ± 4 ka at another site in Morocco, La Grotte des Contrebandiers, (Jacob, Z., et al, 2011); the remains from Klasies River Mouth are from 2 units dating to more than 101 ka and more than 104-64 ka (Millard, A.R., 2008); Nazlet Khater 2 is possibly ≈ 42 ka (Millard, A.R., 2008); and Hofmeyr 36.2 ± 3.3 ka (Grine, F.E. et al., 2007). The Iwo Eleru calvaria has, however, been dated to ~ 16.3-11.7 ka (Harvati, K. et al., 2011), and the authors1 say it is clearly of similar age to the remains from China.
Outside of Africa there are various fossils from the Upper Pleistocene that have also been described as exhibiting an unusual mosaic or characters (e.g. Trinkhaus, e., 2007). Some of them, such as from Israel, Skhul and Qafzeh, and in Romania, Pestera cu Oase were included in the analyses carried out by the authors1, and overall they appear to be metrically well within the range for H. sapiens from the Pleistocene. The former (Levantine) samples, however, exhibit some similarities, in univariate comparisons, to LL 1 and MLDG 1704.
The problem that needs to be answered is how to explain this unusual morphology that is present in the Pleistocene-Holocene transition in East Asia. The authors1 suggest the Longlin and Maludong remains could represent individuals that were very robust within an Epipalaeolithic population that was previously unknown in southwest China. They also consider this explanation to be unsatisfactory because there are several features that are apparently unique that are present, which are combined with an unusual mix of modern and archaic features is seen in several specimens spanning multiple developmental-functional complexes, as mentioned above. The authors1 suggest that this hypothesis could be invoked as an explanation for the morphology seen in the remains recovered from Klasies River Mouth Cave, Hofmeyr, Iwo Eleru, Nazlet Khater, Dar-es-Soltane, Témara and Zhirendong, though it has not been because many of their archaic features are rare or not present among H. sapiens. As is indicated strongly here, the same situation applies to the remains from Longlin and Maludong.
The authors1 suggest there are explanations that are more plausible, a possibility being that the remains from Longlin and Maludong represent an archaic population that were late surviving, possibly similar to that sampled at Dar-es-Soltane, Témara (Trinkhaus, E., 2005; Trinkhaus, E., 2007; Crevecoeur, I. & Trinkhaus, E., 2004) There is problem with this suggestion as the morphology of these remains from North Africa is not well known, and their affinities and taxonomy are uncertain (Trinkhaus, E., 2005; Trinkhaus, E., 2007; Crevecoeur, I. & Trinkhaus, E., 2004). In East Asia the Zhirendong mandibular fragment that has been described recently also has a mosaic of modern and plesiomorphic characters that causes problems with the taxonomy of the fossil (Kaifu, Y. & Fujita, M., 2012; Liu, W. et al., 2010; Dennell, R., 2010). Though it has been dated based on stratigraphy to more than 100 ka (Liu, W. et al., 2010), which is of a similar age to that of the Aterian assemblage from North Africa, but much older than Longlin and Maludong. The site at Salkhit, Mongolia, contains another specimen that has also been described recently has also been described as being of an archaic taxon that is unspecified (Coppens, Y. et al., 2008). A preliminary date of ~20 ka has apparently been reported, though dating is uncertain (Kaifu, Y. & Fujita, M., 2012). Also, there have been expressions of doubts about its archaic affinities (Kaifu, Y. & Fujita, M., 2012), and the authors1 could not include this specimen in their analyses because they found errors in the measurements in this and other specimens in Table 1 of Coppens et al. Coppens, Y. et al., 2008).
It is also possible that the Longlin and Maludong remains retained a large number of ancestral polymorphisms in a population of H. sapiens. Where features of interest are also present in allopatric populations of the same taxon the concept of lineage sorting that is incomplete is often invoked as an explanation (Mavárez, J. & Linares, M., 2008). Related to this it has been suggested by recent morphological studies that H. sapiens were deeply geographically subdivided in the Pleistocene within Africa prior to its dispersal into Eurasia (Gunz, P. et al., 2009). The same explanation has also been invoked to explain the unusual morphology of the Iwo Eleru calvaria (Harvati, K. et al., 2009). At Longlin and Maludong the morphology that has been documented might be interpreted with this hypothesis, the remains from China possibly sampling a human population that was unknown previously (or a migration?) that may not have contributed genetically to recent East Asians. Attempts to extract DNA from a Maludong specimen has to date been unsuccessful, as there is a lack of recoverable genetic material.
Either way, the unusual morphology sampled at Longlin and Maludong during the Pleistocene-Holocene transition indicates that in East Asia human history is more complex than has been suspected previously. It also highlights the need for more research in the region.
PLoS ONE 7(3): e31918. doi:10.1371/journal.pone.0031918 Editor: David Caramelli, University of Florence, Italy
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