Temporal labyrinths of eastern Eurasian Pleistocene humans

transcript

Temporal labyrinths of eastern EurasianPleistocene humansXiu-Jie Wua, Isabelle Crevecoeurb, Wu Liua, Song Xinga, and Erik Trinkausc,1

aKey Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences,Beijing 100044, China; bUnité Mixte de Recherche 5199 De la Préhistoire à l’Actuel: Culture, Environnement et Anthropologie, Laboratoire d’Anthropologiedes Populations Passées et Présentes, Centre National de la Recherche Scientifique, Université de Bordeaux 1, 33405 Talence, France; and cDepartment ofAnthropology, Washington University in St. Louis, St. Louis, MO 63130

Contributed by Erik Trinkaus, June 9, 2014 (sent for review April 30, 2014; reviewed by Rolf M. Quam and Fred H. Smith)

One of the morphological features that has been identified asuniquely derived for the western Eurasian Neandertals concernsthe relative sizes and positions of their semicircular canals. Inparticular, they exhibit a relatively small anterior canal, a relativelylarger lateral one, and a more inferior position of the posterior onerelative to the lateral one. These discussions have not included fullpaleontological data on eastern Eurasian Pleistocene human tem-poral labyrinths, which have the potential to provide a broadercontext for assessing Pleistocene Homo trait polarities. We presentthe temporal labyrinths of four eastern Eurasian Pleistocene Homo,one each of Early (Lantian 1), Middle (Hexian 1), and Late (Xujiayao15) Pleistocene archaic humans and one early modern human(Liujiang 1). The labyrinths of the two earlier specimens and themost recent one conform to the proportions seen among westernearly and recent modern humans, reinforcing the modern humanpattern as generally ancestral for the genus Homo. The labyrinthof Xujiayao 15 is in the middle of the Neandertal variation andseparate from the other samples. This eastern Eurasian labyrin-thine dichotomy occurs in the context of none of the distinctiveNeandertal external temporal or other cranial features. As such, itraises questions regarding possible cranial and postcranial morpho-logical correlates of Homo labyrinthine variation, the use of individ-ual “Neandertal” features for documenting population affinities,and the nature of late archaic human variation across Eurasia.

cranium | China | petrous | cochlea

One of the morphological features, which has been used todistinguish the Neandertals from early and recent modern

humans, as well as earlier Pleistocene Homo, is the arrangementof their semicircular canals (or labyrinthine morphology) (1–3).Given its prenatal formation, developmental stability, and min-imal side or sex differences (4–6), labyrinthine morphologyshould provide a direct reflection of one aspect of genetic vari-ation across these samples. It is also frequently preserved pale-ontologically within the petrous portion of the temporal bone. Intheir labyrinths, Neandertals have been shown to have a suite offeatures involving absolute dimensions, proportions, and angu-lations, most which appear to be related to their relatively smallanterior semicircular canals, comparatively larger lateral semi-circular canals, and a more inferior position of the posteriorsemicircular canal relative to the lateral one (1). This pattern ispresent in almost all of the known Neandertal labyrinths; it hasnot been documented among other Pleistocene members of thegenus Homo; and it is rare among recent humans. However, withthe exception of partial data on the labyrinths of three EarlyPleistocene Homo crania (4, 7) that primarily serve to documentthe ancestral Homo configuration, the Pleistocene comparisonshave been limited to western Old World archaic humans (mostlyNeandertal lineage) and modern humans (1, 2, 8–12), plus onecentral Asian late archaic human (13). Given that East Asianarchaic Homo remains are distinctly non-Neandertal in theiroverall configurations (14), it is of interest to assess the laby-rinthine morphology of the available East Asian Pleistocene

humans relative to other PleistoceneHomo (SI Appendix, Table S1).These sufficiently preserved and available eastern Asian humanremains include the Early Pleistocene Lantian (Gongwangling) 1,the Middle Pleistocene Hexian 1, the Late Pleistocene archaicXujiayao 15, and the Late Pleistocene modern Liujiang 1.

ResultsThree of these East Asian Pleistocene Homo temporal labyrinths(Fig. 1) provide configurations that appear generally similar tothose of recent humans (and the apparent ancestral Homo pat-tern), those from Lantian, Hexian, and Liujiang. In particular, inlateral view their lateral canals largely bisect the posterior ones.In contrast, the lateral canal of Xujiayao 15 is positioned in thesuperior portion of its posterior canal. This proportion is re-flected in their sagittal labyrinthine indices (SLIs) of 41.4, 53.5,and 45.5 for the first three, respectively, but one of 61.4 forXujiayao 15. In this feature (Fig. 2), the first three are well withinrecent and early modern human variation and only Hexian 1overlaps the limits of the Neandertal variation (Spy 1). Xujiayao15 is among the Neandertals (who are significantly different fromthe other samples: P < 0.0001), similar to a small minority of therecent humans (7.2% with SLI ≥ 61, n = 180), one Middle Pa-leolithic modern human (Qafzeh 15), and one Middle Pleisto-cene European specimen (Reilingen 1) (Fig. 2). Two of the EarlyPleistocene specimens are within recent human variation, al-though Sangiran 4 has a high value for this feature (4).The Neandertals have also been noted to have relatively small

anterior and large lateral canal radii, and the percent that each

Significance

The assessment of the paleobiology and morphological affini-ties of the Neandertals and other Late Pleistocene archaichumans is central to resolving issues regarding the emergenceand establishment of modern human morphology and di-versity. One feature, which has been used as a distinctive Ne-andertal feature in this context, is the apparently derived shapeof their temporal labyrinths (especially semicircular canals).Analysis of East Asian labyrinths documents the “Neandertal”pattern in the Xujiayao 15 temporal bone, although none ofthe Xujiayao human remains exhibits other distinctly Neandertalfeatures. It therefore raises questions regarding possible bi-ological correlates of labyrinthine morphology, distinctiveNeandertal features, and the nature of late archaic humanvariation across Eurasia.

Author contributions: X.-J.W., I.C., W.L., and E.T. designed research; X.-J.W., I.C., S.X., andE.T. performed research; X.-J.W., I.C., S.X., and E.T. analyzed data; and X.-J.W., I.C., W.L.,and E.T. wrote the paper.

Reviewers: R.M.Q., State University of New York at Binghamton; and F.H.S., IllinoisState University.

The authors declare no conflict of interest.1To whom correspondence should be addressed. E-mail: trinkaus@wustl.edu.

This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1410735111/-/DCSupplemental.

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radius makes up of the three summed radii is significantly dif-ferent across the fossil samples for the anterior and lateral ones(P < 0.0001) but not the posterior canal (P = 0.053) (SI Appendix,Table S2). A comparison of anterior to lateral radii (Fig. 2)confirms the separation of most of the Neandertals from theother samples (including the Early Pleistocene specimens fromLantian and especially from Sangiran and Olduvai). Xujiayao 15is among the Neandertals with the lowest indices, outside of theranges of the other comparative samples. Liujiang 1 and two ofthe European Middle Pleistocene specimens (Reilingen 1 andSteinheim 1) overlap the Neandertal range in this feature.In these two features together, the only Pleistocene specimen

other than Xujiayao 15 that falls within the Neandertal range ofvariation is Reilingen 1, which is poorly dated within the Middleto early Late Pleistocene (15). Hexian 1 overlaps the Neandertalrange of variation in each of these proportions, but it lies along

the margin of that Neandertal distribution and remains withinthe recent human distribution.Therefore, despite some overlap between the Neandertals and

the other comparative samples in the separate indices (Fig. 2), incombination, these two indices separate 56.7% (n = 30) of theNeandertals completely from the distribution of the other sam-ples. All but one Neandertal (Le Moustier 1) are at or beyondthe limits of those other samples (96.7%). Xujiayao 15 is with themajority of the Neandertals in being well outside of the bivariatevariation of the other Pleistocene and recent Homo labyrinths.This proportional similarity of Xujiayao 15 to the Neandertals isalso expressed by the relative proportions of their anterior,posterior, and lateral canals (SI Appendix, Fig. S1).The cochlear dimensions and proportions of the Chinese hu-

man fossils are all within the ranges of the comparative groupvariations (SI Appendix, Table S4). Regarding the torsion of theanterior (ASCtor), posterior (PSCtor), and lateral (LSCtor)semicircular canals, the Xujiayao 15 and other Chinese fossilspecimens show less torsion in ASCtor compared with theMiddle Paleolithic modern humans and the Neandertals (SIAppendix, Table S3).With respect to the shape of the labyrinth, Xujiayao 15 is

separate from the three other East Asian specimens in exhibitingthe hyperrotated morphology apparently derived for the Nean-dertals (1). Compared with recent humans, the ampullar line(APA), the facial nerve canal (FC3), and the posterior petrosalsurface (PPp) are positioned more vertically in relation to the arcof the lateral semicircular canal (LSCm) in the sagittal plane.This conformation is correlated with the low position of theposterior semicircular canal, expressed by SLIs (SI Appendix,Table S3). The angle between the lateral canal plane and theposterior petrosal surface (LSCm < PPp) of Hexian 1 is close tothe Neandertal mean, and the position of the facial nerve canal isalso more vertical than the modern human variation. However,this conformation is not associated with a hyperrotated mor-phology in the Hexian 1 labyrinth (i.e., SLI and LSCm < APAare outside or near the limits of Neandertal variation). FinallyXujiayao 15 is separate from the comparative samples regardingthe position of its cochlea reflected in the angle between thesagittal plane basal turn of the cochlea (COs) and the LSCm,which is oriented more superiorly and whose angle (LSCm < COs)lies close to the upper limits of all of the comparative groups.As previously noted (1), the ranges of variation of many of

these individual labyrinthine measurements overlap across Pleis-tocene and recent human samples, but in combination they largelyseparate the Neandertals (and to a lesser extent European Middle

Fig. 1. Reconstructed temporal labyrinths of East Asian Pleistocene humans from Lantian 1 (reversed), Hexian 1, Xujiayao 15, and Liujiang 1 (reversed), inlateral (Upper) and superior (Lower) views.

Fig. 2. Plot of the index of the anterior to lateral semicircular canal radiiversus the sagittal labyrinthine index for Pleistocene and recent humans.EPleist, Early Pleistocene remains from Sangiran (S2 and S4) and Olduvai; HX,Hexian 1; LJ, Liujiang 1; LT, Lantian 1; M, Le Moustier 1; MPl-Eur, MiddlePleistocene specimens from Europe; MPMH, Middle Paleolithic modernhumans; Neand, western and central Eurasian Neandertals; OR, Obi-Rakhmat1; Recent, global sample of recent modern humans; UPMH, western Old WorldUpper Paleolithic modern humans; and XJY, Xujiayao 15.

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Pleistocene remains) from non-Neandertal human samples.Therefore, a principal component analysis was performed onsix variables of the bony labyrinth (SI Appendix, Table S5), thetwo first principal component (PC) axes (PC 1 and PC 2) rep-resent 73% of the total sample variance. PC 1 reflects the rela-tive proportions of the posterior and lateral semicircular canals,whereas PC 2 accounts for the sagittal shape of the labyrinth.Fig. 3 illustrates the distribution of the individuals following thefirst two principal components. Xujiayao 15 falls in the middle ofthe Neandertal distribution and at the edge of the recent humanone, whereas Lantian 1, Hexian 1, and Liujiang 1 are separatefrom the Neandertals, especially with respect to PC 2. Again, LeMoustier 1 plots with the recent humans.A more comprehensive assessment of the affinities of the

eastern Eurasian labyrinths is provided by a discriminant func-tion analysis with cross-validation on 25 variables (SI Appendix,Table S6). The number of variables was maximized and includedin a step-by-step analysis (ending with 14 active variables). Theanalysis provides an overall success rate of 77.6% across fivesamples (not including the Early Pleistocene one), but if the twoNeandertal lineage samples are combined and the three modernhuman samples are pooled, the success rate rises to 94.5%. Onlyone Neandertal lineage labyrinth (Le Moustier 1) is aligned withmodern humans, for a 94.7% success rate (n = 23), and theremaining misclassified Neandertal lineage vs. modern humanspecimens are all recent humans. In this context, Lantian 1 andHexian 1 group with the Middle Paleolithic modern humans (P =0.985 and 0.999), and Liujiang 1 is with the three modern humansamples (P = 0.326, 0.389, and 0.283, for a total of 0.998).Xujiayao 15 groups with the Neandertals (P = 0.948).These individual proportions and overall morphometrics

therefore align the Lantian, Hexian, and Liujiang labyrinths withearly and recent modern humans, and by extension with EarlyPleistocene Homo (given limited data on the last). Xujiayao 15,in contrast, falls entirely with the Late Pleistocene Neandertals,distinct from the early and recent modern humans and from theEarly and Middle Pleistocene Homo.

DiscussionThese data and comparisons confirm what has been documentedfor the western Old World, that there is a general similarity intemporal labyrinthine proportions through most of the genus

Homo (1, 7). The exception is the western and central EurasianNeandertals (1–3), almost all of whom exhibit a derived mor-phology of their labyrinths. As with many individual features, forwhich the Neandertals are overwhelmingly separate from mod-ern humans but for which their distributions overlap given suf-ficient sample sizes (16), the ranges of variation of these samplesoverlap in their labyrinthine aspects. This minimal distributionaloverlap is evident in the positions of the Le Moustier 1 labyrinthand those of a few recent humans.In eastern Asia, the Early and Middle Pleistocene Lantian 1

and Hexian 1 crania follow the general Homo pattern, and theyjoin Sangiran 2 and 4 in establishing this labyrinthine morphol-ogy as ancestral for Homo across Eurasia. The Late PleistoceneLiujiang 1 has an equally modern labyrinthine configuration, inagreement with its overall modern human morphology (17). Inthis context, the labyrinthine morphology of the Xujiayao 15temporal bone conforms to the derived Neandertal pattern, thefirst documentation of this pattern among Pleistocene Homooutside of the Neandertal geographical range.Despite the similarity of the Xujiayao 15 labyrinth to those of

the Neandertals, its external temporal morphology (Fig. 4 and SIAppendix, Fig. S2) bears little affinity to that of the Neandertals(18, 19). It shares ancestral Homo features with the Neandertals,including a large juxtamastoid eminence and an inferomediallysloping lateral mastoid process. It differs in its other aspects. Thesquamous portion is high and rounded. The zygomatic archextends posteriorly above the auditory porous, continuing intoa supramastoid crest that is horizontal and ends temporally atthe parietal notch. The porous is ovoid, but its long axis is ver-tical. The laterally rugose mastoid process lacks an anteriormastoid tubercle. The parietomastoid suture slopes inferiorly toasterion, and the transverse sinus crossed to the temporal boneacross the posterior parietomastoid suture. Some of theseaspects of Xujiayao 15 can be found on individual Neandertalspecimens, but the constellation of discrete traits of the bone isoutside of the well-documented range of variation in Neandertaltemporal bone external morphology.The same morphological consideration applies to the Xujiayao

human remains generally (SI Appendix, Table S7). A couple oftheir features are common among the Neandertals but notunique to them (the Xujiayao 1 bilevel nasal floor and stronglyshoveled maxillary central incisor (I1) and canine (C1), and theXujiayao 14 enlarged superior medial pterygoid tubercle) (20–22), but the overall configurations of the Xujiayao remains areunlike those of most Neandertals (20–25). The Xujiayao 1 in-ferior nasal margin is broad and rounded, and its M1 has markedcingular development and peripherally placed cusps. TheXujiayao 1 and 13 maxillary first molars (M1s) possess sub-rectangular contours. The Xujiayao 6 and 12 occipital bones areangled at the nuchal torus and lack suprainiac fossae. TheXujiayao 14 mandibular ramus is wide and gonially everted, andit has an open mandibular foramen and a laterally placed man-dibular notch crest. The same pattern holds for other, lateMiddle and early Late Pleistocene archaic human remains fromeastern Asia (14, 26–28). What emerges from these East Asianlater Pleistocene archaic humans, therefore, is a complex mix offeatures, many of them generally ancestral for Homo and a fewfeatures that occur frequently in the Neandertals but need not bediagnostic of them. The Xujiayao 15 labyrinth therefore providesthe first secure evidence of a distinctly derived Neandertal con-figuration in eastern Asia.The geographically closest presence of a similar labyrinthine

configuration is the fragmentary Obi-Rakhmat 1 cranium fromUzbekistan (13), a specimen assigned to the Neandertals on thebasis of its dental morphology (29) despite an apparent mix ofmorphological features in other aspects of the remains (13).The next geographically closest, morphologically “Neandertal”

Fig. 3. Scatter plot of the first two principal components (PC 1 and PC 2)based on six variables in the principal components analysis [the posterior(PSC-R) and lateral (LSC-R) semicircular canal radii, the posterior (PSC-%R)and lateral (LSC-%R) radial proportions, the sagittal labyrinthine index (SLI),and the lateral semicircular canal arc versus ampullar line angle (LSCm <APA)]. The Neandertal in the middle of the recent human distribution is LeMoustier 1. HX, Hexian 1; LJ, Liujiang 1; LT, Lantian 1; and XJY, Xujiayao 15.

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labyrinths are from the eastern Mediterranean littoral (Dederiyeh 1and Tabun 1).The broader implications of the finding, a “Neandertal” lab-

yrinthine morphology in an otherwise distinctly “non-Neandertal”sample of late archaic humans from eastern Eurasia, remainunclear. It is tempting to use it as evidence of population contact(gene flow) between central and western Eurasian Neandertalsand these eastern archaic humans. Indeed, this labyrinthinemorphology has been used repeatedly as a taxonomic marker ofthe Neandertals (1, 3, 11–13). However, there have also beensuggestions (1) that labyrinth shape may be related to otheraspects of Neandertal biology, albeit with reservations, and onlysecondarily a consequence of their phylogenetic history.Spoor et al. (1) suggested a series of Neandertal postcranial

features that might account for at least the dimensions of theiranterior and posterior semicircular canals, as related to overallagility in locomotion (3, 30). None of these postcranial featuresis known for the Xujiayao humans, but they can be assessed forthe Neandertals. However, for them to be relevant to the Ne-andertal (and Xujiayao 15) labyrinthine proportions, they needto be features that distinguish the Neandertals from both modernhumans and the earlier Pleistocene, non-Neandertal, humans wholack this unusual labyrinthine configuration.There is a series of Neandertal features that may be related to

issues of balance and agility (1). Neandertals have relativelyabbreviated limbs (31), yet similarly proportioned modern arctichumans do not appear to differ from other modern humans intheir labyrinths (1). Neandertals have robust necks, especially

with respect to cervical spinous processes (19, 32), but theiroccipital nuchal areas are modest in size for Pleistocene Homo(19, 33, 34). Moreover, their necks were not particularly short(19, 32, 35). Their clavicles are moderately long, but they scale tobody mass in the same manner as other humans (36). Some, butnot all, Neandertals have broad pelves (37), but so apparently doall archaic Homo (38–40). Neandertal (and earlier Homo) fem-oral diaphyseal shape has suggested more mediolateral and lessanteroposterior loading during locomotion; however, properlyscaled, there is no difference through Pleistocene Homo in ante-roposterior femoral strength, only mediolateral variation appar-ently related to pelvic breadth (41, 42). Related are issues of headbalance and momentum in running with a prognathic and platy-cephalic cranium (43); however, the Neandertals had shorter facesthan their Pleistocene Homo predecessors (44, 45), and theirrelative neurocranial heights are similar to all earlier Homo andoverlap the variation of early modern humans (46). Given thecontrast in labyrinth morphology between earlier PleistoceneHomo and the Neandertals, it is therefore difficult to account forthe latter’s (and Xujiayao 15’s) labyrinth configuration frompostcranial and overall cranial proportions.It has also been suggested that labyrinthine variation may be

influenced by cranial base configuration, especially as related toposterior cranial fossa proportions (1), and this interpretationhas been supported by some covariation with cranial base pro-portions among recent humans (47). Neandertals have relativelysmall posterior cranial fossae, yet the same proportions are in atleast one early modern human with a modern labyrinth config-uration (Cro-Magnon 1) (48). It is possible that other neuro-cranial considerations, related to cerebral expansion on anarchaic Homo cranial base (49), given similar endocranial ca-pacity and encephalization across all Late Pleistocene humans(50), are related to the labyrinthine morphology, but that remainsto be evaluated. The endocranial capacity of Xujiayao 15 is un-known, but another individual from the same sample (Xujiayao6) has an estimated cranial capacity ∼1,700 cc, among the largerLate Pleistocene crania; the earlier East Asian crania providinglabyrinthine details have substantially smaller neurocrania (Hexian1: 1,025 cc and Lantian 1: ∼780 cc) (51, 52), making it unlikely thatthe petrous angular similarities between Xujiayao 15 and Hexian 1are due to brain size.It is therefore unclear whether the Neandertal labyrinthine

configuration, and by extension that of Xujiayao 15, can be at-tributed to other aspects of their biology. Moreover, the overallcranial morphology of the Xujiayao sample is incompletelyknown and their postcrania are unknown.These considerations of the Xujiayao 15 labyrinth also raise

questions regarding the use of individual features (whethermorphological or molecular), in the absence of relatively com-plete paleontological remains, to identify the presence ofNeandertals in regions outside of their well-documented corearea of western Eurasia (west of ∼45° E, versus ∼70° E for Obi-Rakhmat and ∼114° E for Xujiayao). Indeed, many of the fea-tures so used are generally ancestral for later Homo (if poorlydocumented other than among the Neandertals), of unknownphylogenetic polarity, of uncertain primacy in morphologicalintegration, and/or isolated features in otherwise non-Neander-tal remains. The Xujiayao 15 labyrinthine morhology, and otherfeatures documented for eastern Eurasian and the earlierPleistocene Homo (e.g., 16, 19, 20, 28, 36, 39, 42, 53), suggestthat many of the purported “Neandertal” features were wide-spread during the Pleistocene, albeit often occurring in higherfrequencies among the Neandertals.Regardless of the ultimate populational and morphofunctional

implications of the Xujiayao 15 and the other East Asian labyrin-thine configurations, they serve to further confirm the generalmodern human pattern as the ancestral Homo one and to docu-ment that the apparently derived Neandertal configuration was not

Fig. 4. Lateral views of the Xujiayao 15 left temporal bone (Upper) and theLa Quina 27 Neandertal right temporal bone (reversed, Lower).

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unique to western Eurasia. Given its presence in Europe, southwestAsia, central Asia, and now eastern Asia, it may well have beenpresent across Eurasia during the later Pleistocene among archaichumans. As such, whether a discrete feature in itself or a secondaryconsequence of other aspects of morphological variation, itbecomes less of a “Neandertal” marker and of broader relevanceto the paleobiology of later Pleistocene Homo.

Materials and MethodsThe petrous portions of the Lantian, Xujiayao, and Liujiang fossils and 26 recentChinese temporal bones were μ-computed tomography (CT) scanned using anindustrial CT scanner (225 kV μCT, made by the Institute of High EnergyPhysics, Chinese Academy of Sciences) in the Institute of Vertebrate Pale-ontology and Paleoanthropology (IVPP) (tube voltage: 150 kV; tube current:110 μA; pixel size: 44 μm for Xujiayao and Lantian, 56 μm for Liujiang, and 48μm for the recent Chinese). Hexian 1 was scanned with a high-resolutionindustrial CT scanner (450 kV) in the IVPP (tube voltage: 450 kV, tube cur-rent: 1.5 mA, pixel size: 0.2 mm), given that it is a full neurocranium and isminerally dense. All specimens were therefore scanned at resolutions morethan adequate to extract and measure their temporal labyrinths (Fig. 1). Thelabyrinthine structures were extracted and measured using Mimics 15.1

(Leuven; Materialise NV). The measurement specifications (SI Appendix,Tables S2–S4) are from Spoor et al. and Spoor (1, 4).

The comparative sample data were compiled from personal research andthe literature (SI Appendix, Table S1). Note that the complete set of labyrinthinevariables (1, 4) is not available for all of the fossil and recent human specimens,due to preservation in some fossils and completeness of measurement col-lection in others. This has resulted in different sample sizes in the variouscomparisons used. The principal component analysis (PCA) was conductedon the six variables (PSC-%R, PSC-R, LSC-R, LSC-%R, SLI, LSCM <APA) thatwere used in Bouchneb and Crevecoeur (2). Multivariate analysis usedstepwise discriminate analysis (ending with active variables) using cross-validation for the comparative samples and the East Asian fossils as separatespecimens. The comparative group classification was computed in “equalsize” to avoid larger groups (such as the recent human sample) being givenmore weight in computing the posterior probabilities. Analyses were doneusing SPSS v.15.0

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Wu et al. PNAS | July 22, 2014 | vol. 111 | no. 29 | 10513

The Temporal Labyrinths of Eastern Eurasian Pleistocene Humans

Supporting Information

Xiu-Jie Wu, Isabelle Crevecoeur, Wu Liu, Song Xing, and Erik Trinkaus Table S1. Pleistocene and recent human comparative labyrinthine samples. Data from this study unless indicated otherwise. Samples Samples Eastern Eurasia Middle Paleolithic modern humans (MPMH)

Lantian (LT) 1 Qafzeh 3,6,7,9,11–13,15,21 (2) Hexian (HX) 1 Skhul 1, 5 (2,4) Xujiayao (XJY) 15 Liujiang (LJ) 1 Upper Paleolithic modern humans (UPMH)

Cro-Magnon 1 (4) Early Pleistocene (EPleist) Lagar Velho 1 (4)

Olduvai OH9 (1) Laugerie Basse 1 (4) Sangiran 2,4 (1) Malaurie 1 (2) Nazlet Khater 2 (2)

Middle Pleistocene Europe (MPl-Eur) Muierii 2 (8) Biache SV1, SV2 (2,3) Oase 2 (9) La Chaise-Suard 3 (4) Pataud 1,3 (4) Reilingen 1 (4) Rochereil 1 (2) Steinheim 1 (4) Recent humans (Recent, n=180)

Neandertals (Neand) China (n=26) Amud 1, 7 (2) Belgium (n=100) (2) Arcy-sur-Cure C7.1544 (5) Worldwide sample (n=54) (1) Dederiyeh 1 (4) Devil’s Tower 1 (4) La Chapelle-aux-Saints 1 (4) Engis 2 (2) La Ferrassie 1–3 (4) Forbes’ Quarry 1 (4) Kebara 1 (2) Krapina 38.1,38.12,38.13,39.1,39.4,39.8,39.13,39.18 (6) Marillac LP01-H02 (2) Le Moustier 1 (4) Obi-Rakhmat 1 (7) Pech de l’Azé 1 (4) Petit-Puymoyen 5 (4) La Quina 5, 27 (4) Spy 1,2 (4) Tabun 1 (4)

Table S2. Measurements and indices of the labyrinths of the east Asian Pleistocene humans and comparative samples: anterior (ASC), posterior (PSC) and lateral (LSC) semicircular canal dimensions. w: width; h: height; R: radius. Measurements and indices following Spoor (1,4). Sample abbreviations as in Table S1. Samples ASC

w ASC h

ASC h/w

ASC -R

PSC h/w

PSC -R

LSC h/w

LSC -R

East Asia LT 6.1 5.1 83.6 2.8 5.1 4.9 96.1 2.5 4.9 3.7 76.2 2.2 41.4

HX 7.4 6.6 88.5 3.5 6.5 6.2 95.4 3.2 6.1 5.4 87.8 2.9 53.5 XJY 6.2 5.4 87.1 2.9 5.7 5.6 98.3 2.8 5.8 4.8 82.8 2.7 61.4

LJ 7.0 5.6 80.0 3.2 5.5 4.9 89.1 2.6 5.7 5.2 91.2 2.7 45.5 EPleist

Mean 7.2 5.5 77.2 3.2 5.9 6.4 108.9 3.1 4.7 3.7 78.4 2.1 53.3 S.D 0.5 0.3 9.5 0.1 0.4 0.6 3.8 0.3 0.5 0.7 13.9 0.2 6.8 max 7.6 5.8 88.0 3.2 6.2 7.0 112.9 3.3 5.2 4.4 88.1 2.4 61.0 min 6.6 5.3 70.0 3.1 5.0 5.8 105.5 3.1 4.2 3.0 62.5 2.0 43.0

n 3 3 3 3 3 3 3 3 3 3 3 3 3 MPl-Eur

Mean 6.0 5.7 95.9 2.9 5.3 5.9 111.6 2.8 5.1 4.7 92.6 2.4 50.9 S.D 0.3 0.3 4.5 0.2 0.4 0.5 13.1 0.2 0.5 0.4 8.3 0.2 8.1 max 6.4 6.1 101.7 3.1 5.8 6.7 131.9 3.1 5.5 5.1 104.4 2.6 60.0 min 5.5 5.2 89.7 2.8 4.7 5.3 96.4 2.7 4.3 4.2 84.0 2.2 40.3

n 5 5 5 5 5 5 5 5 5 5 5 5 4 Neand

Mean 6.2 5.8 92.6 3.0 5.7 5.6 100.7 2.8 5.4 5.0 92.7 2.6 63.5 S.D 0.5 0.4 5.0 0.2 0.4 0.6 8.0 0.2 0.4 0.4 6.7 0.2 5.8 max 7.3 6.6 103.5 3.4 6.8 6.7 114.8 3.4 5.9 5.9 111.7 2.9 76.0 min 5.3 5.1 84.3 2.6 5.1 4.7 87.1 2.5 4.7 4.3 82.7 2.3 52.1

n 22 22 31 31 22 22 30 30 22 22 31 31 30 MPMH

Mean 7.1 6.2 88.5 3.3 6.1 6.0 100.0 3.0 5.2 4.3 83.4 2.4 53.0 S.D 0.5 0.5 6.9 0.2 0.4 0.4 7.9 0.2 0.4 0.5 9.7 0.2 6.2 max 7.7 7.0 97.9 3.7 6.8 6.7 113.9 3.2 5.9 5.1 98.0 2.8 62.5 min 6.1 5.4 71.8 3.0 5.5 5.3 88.1 2.7 4.7 3.7 68.2 2.1 40.2

n 11 11 11 11 11 11 11 11 11 11 11 11 11 UPMH

Mean 7.1 6.3 89.5 3.3 6.1 6.5 106.5 3.1 5.3 5.0 94.0 2.5 43.7 S.D 0.5 0.4 6.7 0.2 0.5 0.4 7.6 0.3 0.4 0.4 6.2 0.2 9.4 max 7.9 6.6 98.0 3.6 6.6 6.9 118.2 3.3 5.8 6.0 104.0 3.0 55.0 min 6.5 5.5 79.7 3.0 5.4 5.7 96.2 2.5 4.7 4.5 85.9 2.2 31.2

n 9 9 9 10 9 9 9 10 9 9 9 10 10 Recent

Mean 6.8 6.1 89.8 3.2 6.1 6.3 104.1 3.1 4.9 4.4 90.8 2.3 50.7 S.D 0.5 0.5 5.1 0.2 0.6 0.7 8.8 0.3 0.4 0.5 7.0 0.2 6.8 max 8.2 7.6 103.6 4.0 7.8 8.3 137.4 3.9 5.9 6.2 109.2 3.0 69.3 min 5.4 4.8 74.0 2.6 4.4 4.3 76.6 2.2 3.8 3.1 67.4 1.8 31.5

n 180 180 180 180 180 180 180 180 180 180 180 180 180

Table S3. Measurements and indices of the labyrinths of the east Asian and comparative samples: semicircular canal radii proportions (%R), torsion angles (tor), lateral canal orientations (LSCm<APA), and lateral canal versus facial nerve canal (LSCm<FC3) and posterior petrosal surface (LSCm<PPp) angles. Measurements and indices following Spoor (1,4). Sample abbreviations as in Table S1. Samples ASC

%R PSC %R

LSC %R

ASC tor

PSC tor

LSC tor

LSCm <APA

LSCm<FC3

LSCm<PPp

East Asia LT 37.6 33.6 28.9 9.0 -5.4 -4.0 33.1 72.9 57.5

HX 36.7 33.2 30.2 11.0 -9.1 1.8 32.1 76.0 65.9 XJY 34.6 33.7 31.6 13.4 -14.9 1.5 46.6 78.5 65.5

LJ 37.2 30.7 32.2 7.0 -12.2 0.9 30.5 63.5 51.2 EPleist

Mean 38.0 37.0 25.0 38.3 S.D 1.0 1.7 2.0 6.1 max 39.0 39.0 27.0 45.0 min 37.0 36.0 23.0 33.0

n 3 3 3 3 MPl-Eur

Mean 35.9 34.4 29.7 23.2 -10.1 -0.5 38.3 81.6 61.6 S.D 1.2 2.5 1.6 1.6 2.8 2.0 3.9 8.4 7.0 max 36.9 38.4 31.0 24.4 -7.2 1.7 41.6 91.8 67.0 min 34.4 32.2 27.2 20.8 -12.8 -2.5 32.6 73.1 53.7

n 5 5 5 4 4 4 4 4 3 Neand

Mean 35.9 33.6 30.5 22.0 -11.3 2.7 45.9 86.6 69.4 S.D 1.5 1.6 1.1 6.5 5.8 5.0 4.6 8.6 7.9 max 41.1 36.0 39.0 32.0 1.9 12.0 55.0 103.5 82.0 min 34.0 29.0 28.0 11.0 -23.0 -6.3 40.3 73.6 55.0

n 30 30 30 21 20 21 21 17 14 MPMH

Mean 38.1 34.7 27.2 14.9 -4.9 1.0 39.2 76.9 60.5 S.D 1.3 1.6 1.6 5.6 6.3 4.0 5.8 7.5 5.1 max 40.8 36.7 29.1 22.9 2.1 10.1 46.7 86.0 67.0 min 35.9 32.6 24.3 3.3 -18.5 -6.0 28.7 67.3 56.1

n 11 11 11 11 10 11 11 6 5 UPMH

Mean 37.2 34.5 28.4 13.6 -13.3 3.5 35.2 73.2 57.5 S.D 1.4 1.7 0.9 2.5 5.4 3.3 3.6 5.4 12.1 max 39.5 37.0 30.1 18.8 -6.0 8.0 41.7 79.0 80.0 min 35.9 32.0 27.2 12.0 -21.0 -0.3 31.9 63.1 45.0

n 10 10 10 7 7 7 6 7 6 Recent

Mean 37.3 36.0 26.8 15.2 -11.4 1.9 39.8 72.4 59.7 S.D 1.3 1.8 1.8 4.8 5.7 4.0 4.7 7.9 8.5 max 41.3 39.9 32.0 28.3 4.4 14.2 56.5 89.8 80.4 min 34.1 30.2 22.6 4.1 -27.8 -7.9 27.4 47.9 34.4

n 180 180 180 180 180 180 180 149 138

Table S4. Measurements and indices of the cochleae (CO) of the east Asian and comparative sample labyrinths. Measurements and indices following Spoor (1,4). Sample abbreviations as in Table S1.

Samples COs<LSCm COw COh COh/w CO-R East Asia

LT 48.9 4.2 5.1 121.6 2.3 HX 52.0 4.4 5.2 119.0 2.4

XJY 71.6 4.1 5.2 127.0 2.3 LJ 58.1 4.0 4.8 121.0 2.2

EPleist Mean 57.7 4.1 5.7 140.9 2.5

S.D 5.0 0.3 0.2 5.7 0.1 max 63.0 4.4 6.0 147.4 2.6 min 53.0 3.8 5.6 136.4 2.4

n 3 3 3 3 3 MPl-Eur

Mean 47.2 3.8 4.8 128.6 2.1 S.D 4.9 0.3 0.8 20.4 0.2 max 54.2 4.1 5.5 145.0 2.3 min 43.3 3.5 3.8 102.6 1.9

n 4 4 4 4 4 Neand

Mean 58.3 3.9 5.1 132.5 2.3 S.D 6.5 0.3 0.3 11.4 0.1 max 70.1 4.4 5.6 154.4 2.5 min 44.8 3.4 4.4 112.5 2.0

n 20 20 20 20 20 MPMH

Mean 54.5 4.3 5.5 129.7 2.5 S.D 7.4 0.26 0.3 7.7 0.1 max 62.1 4.6 6.3 140.0 2.7 min 41.2 3.9 5.2 117.1 2.3

n 11 11 11 11 11 UPMH

Mean 54.5 3.9 5.5 141.5 2.4 S.D 4.0 0.2 0.3 8.7 0.1 max 59.5 4.3 6.0 155.3 2.6 min 49.4 3.7 5.1 130.8 2.3

n 6 7 7 7 7 Recent

Mean 59.0 3.9 5.2 132.7 2.3 S.D 6.6 0.3 0.3 9.1 0.1 max 74.9 4.7 6.1 163.6 2.6 min 36.3 3.3 4.4 112.2 2.0

n 180 180 180 180 180

Figure S1. Graphic representation of the relative proportions of the semicircular canals in Xujiayao 15 (XJY), Lantian 1 (LT), Hexian 1 (HX) and Liujiang 1 (LJ) compared to Middle Pleistocene humans (MPl-Eur), Neandertals (Neand), Middle Paleolithic modern humans (MPMH), Upper Paleolithic modern humans (UPMH), and Recent modern human. Dark gray columns: ACS%R; gray columns: PSC%R; white columns: LSC%R. Table S5. Principal Components Analysis (PCA) loadings with six-variable analyses of Xujiayao 15, Lantian 1, Hexian 1, Liujiang 1 and the five comparative groups.

PC 1 PC 2

SLI 0.496 0.785

PSC-R –0.622 0.351

PSC%R –0.903 0.265

LSC%R 0.921 –0.166

LSC-R 0.597 0.072

LSCm<APA 0.192 0.921

Percent of variance 44.8% 28.2%

Table S6. Posterior probabilities of the eastern Asian labyrinth proportions relative to each of the five comparative samples, using 25 variables. The highest ones are in boldface. MPl-Eur Neand MPMH UPMH Recent Lantian 1 <0.0001 <0.0001 0.9845 0.0023 0.0130 Hexian 1 <0.0001 <0.0001 0.9991 <0.0001 0.0008 Xujiayao 15 <0.0001 0.9485 0.0305 0.0012 0.0197 Liujiang 1 <0.0001 0.0018 0.3261 0.3894 0.2827 The Xujiayao Site and Human Remains

The Xujiayao human remains were discovered during excavations at Locality 74093 (40° 06′ 02″ N, 113° 58′ 39″ E) of the Xujiayao site complex in Houjiayao village, northwestern Nihewan Basin, northern China. The Xujiayao locality is an open-air site comprised of fluviolacustrine deposits. The paleoanthropological remains derive from fluviatile sediments that have been dated to the early Late Pleistocene (most likely Marine Isotope Stage 5) based on associated faunal species (10,11), six Uranium-series dates on Equus sp. and Coelodonta antiquitatis tooth enamel (≈104 to ≈125 ka BP) (12,13), and the presence of an underlying paleomagnetic reversal that most likely represents the Blake Excursion ≈123 ka BP (14,15). Suggestions of an earlier Middle Pleistocene age from the sedimentary paleomagnetism (16,17) are based in unverifiable assumptions of sedimentation rates.

The Xujiayao 15 human fossil was associated with abundant archeological and faunal remains (18,19), as well as sixteen other human craniofacial and dental remains, some of which may derive from the same individuals. They include a juvenile left partial maxilla with six teeth (four unerupted), three isolated molars, fourteen fragments of the neurocranium, and a mandibular ramus (Table S7).

The Xujiayao 15 largely complete adult left temporal bone (Figure S2) was discovered in 1979 (20). The zygomatic process was broken off at the anterior end of the supraglenoid sulcus. The anterosuperior corner of the squamous suture contour is absent, apparently as a result of a missing sutural bone along the sphenotemporal suture extending to pterion in the temporal fossa. The medial tip of the petrous portion is absent, but the petrous portion is intact beyond the internal acoustic meatus and almost to the medial end of the carotid canal. There is neither postmortem distortion nor pathological alteration. Table S7. The human fossil remains from Xujiayao (XJY). XJY No.

IVPP No. Original No.

Discovery date

Preservation Reference

1a PA 1480 1 1976 Immature partial left maxilla with M1 and P3, P4 and M2 germs, all teeth in situ

10,11,21

1b PA 1480 1 1976 Unerupted left I1 (from XJY 1a crypt) 10, 1c PA 1480 1 1976 Unerupted left C1 (from XJY 1a crypt) 10,11 2 PA 1481 2 1976 Right M3 (or possibly M2) 10 3 PA 1482 3 1976 A small section of a parietal bone 10

XJY No.

IVPP No. Original No.

Discovery date

Preservation Reference

4a PA 1483 4 1976 Anterior left parietal bone with coronal suture and stephanion

4b PA 1484 5 1976 Anterior right parietal bone with bregma and adjacent sutures

4c PA 1491 11 1977 Part of left parietal bone close to sagittal suture 22 5 PA

1485/88 6 1976 Largely complete left parietal bone missing

corners (immature) 10,11,23

6a PA 1486 7 1976 Occipital bone with squamous portion and superior nuchal plane

6b PA 1490 10 1977 Largely complete right parietal bone 11,22 7 PA 1487 8 1976 Posterior portion of a left parietal bone (ex situ) 10 8 PA 1489 9 1976 Anterosuperior right parietal bone 10,23 9 PA 1492 12 1977 Inferior half of a right parietal bone 22

10 PA 1493 13 1977 Asterionic corner of a right parietal bone 22 11 PA 1494 14 1977 Right and left posterosuperior parietal bones 22,24 12 PA 1495 15 1977 Occipital bone with nuchal plane and partial

squamous portion 11,22

13 PA 1496 16 1977 Left M1 or M2 11,22 14 PA 1497 10A 1977 Right mandibular ramus 11,22,25 15 PA 1498 1979 Left temporal bone 11,20 16 PA 1499 1979 Right anterior parietal with a part of coronal

suture 22

17 PA 1500 1979 Right M3 (or possibly M2) 22

Figure S2. The Xujiayao 15 temporal bone, in lateral (a), medial (b), posterior (c) and inferior (d) views. The posterior view is slightly posteroinferior. Note that a sutural ossicle in the region of pterion, along the anterior squamous portion, is absent, such that the original squamous contour was probably more rounded anteriorly.

Figure S3. Map of eastern Asia with the locations of the four Pleistocene specimens yielding temporal labyrinthine data. The Lantian, Hexian and Liujiang Human Remains and Comparative Samples The Lantian temporal bone (PA 105(3))

The Lantian 1 cranium was found in 1964, at Gongwangling village, Lantian county, Shanxi province (26). In addition to the eroded frontal and parietal bones (27), there is a separate petrosal portion of the right temporal bone. The petrous portion is fairly well preserved, and the cochlea and the semicircular canals within the pyramid were clearly identified in X-ray films (25). The dating of the Lantian cranium is about ≈1.15 ma BP based on the secure identification of both the Bruhnes/Matuyama paleomagnetic boundary and the Jaramillo event through the stratigraphic sequence (28). The Hexian 1 cranium

The Hexian 1 neurocranium was found in 1982, at Longtandong, Hexian county, Anhui province (29). Although the base of the cranium is largely missing, the petrosal portions of the temporal bones are completely preserved bilaterally. The age of the Hexian hominid was estimated to be ≈412 ka using combined ESR and U-series analyses (30). The Liujiang 1 cranium

The Liujiang 1 cranium was found in Tongtianyan Cave of Liuzhou district, Guangxi Zhuang Autonomous Region (31). The petrosal portion of the right temporal bone is well preserved, while the left petrosal portion is incomplete. Because the exact layer that yielded the fossil is unclear, arguments about

the chronology of the cranium exist (32). Based on the associated mammalian fossils, the Liujiang human fossil is Late Pleistocene in age (11). The Comparative Samples

The comparative human labyrinths providing data are grouped into six samples (Table S1), only one of which (the Early Pleistocene one) includes specimens from the eastern Old World (partial data from the two Sangiran crania from Indonesia). The Middle Pleistocene sample includes mostly later Middle Pleistocene specimens from Europe, which show overall morphological affinities to the Late Pleistocene Neandertals (33-35). The early modern humans are separated into Middle Paleolithic (MIS 5c) southwest Asian remains and later (MIS 3-2) Upper Paleolithic modern humans from Europe plus one MIS 3 northeast African specimen. The pooled recent humans include two regional samples, from northwest Europe and northern China, plus one that includes specimens from across the Old World. Data sources are provided in Table S1. Note that not all of the fossil specimens have the complete series of labyrinthine measurements available for them.

Only two additional Early to Late Pleistocene archaic human remains from eastern Asia retain the temporal bone, Dali 1 (36) and Jinniushan 1 (37). Neither one is available for analysis, and their labyrinthine configurations have not been investigated. They are therefore not included.

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Temporal labyrinths of eastern Eurasian Pleistocene humans

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