Significance One of the oldest questions in human evolutionary studies is: why do Neandertals look different from present-day and ancient modern humans? This question can be addressed at different levels, but a critical component of a complete answer is understanding the developmental basis of adult differences. We now know that many skull differences are present by the time of birth. We know less, however, about the developmental basis of differences in the rest of the body. By studying the two most complete Neandertal neonates, we were able to establish that, as for the skull, many differences in body form are present by the time of birth. Neandertals largely look like Neandertals, regardless of age.

Abstract Neandertal and modern human adults differ in skeletal features of the cranium and postcranium, and it is clear that many of the cranial differences—although not all of them—are already present at the time of birth. We know less, however, about the developmental origins of the postcranial differences. Here, we address this deficiency with morphometric analyses of the postcrania of the two most complete Neandertal neonates—Mezmaiskaya 1 (from Russia) and Le Moustier 2 (from France)—and a recent human sample. We find that neonatal Neandertals already appear to possess the wide body, long pubis, and robust long bones of adult Neandertals. Taken together, current evidence indicates that skeletal differences between Neandertals and modern humans are largely established by the time of birth.

It is well established that Neandertal and modern human adults differ in skeletal features of the cranium and postcranium (1⇓⇓⇓⇓⇓–7). Furthermore, it is clear from multiple morphometric studies of the cranium (8⇓⇓⇓⇓–13) that many of the differences in cranial form—although not all of them—are already present around the time of birth. However, there have been only a few morphometric analyses of postcranial form in Neandertals < 1 y of age (11, 14, 15), although we know more about Neandertal children ∼2 y of age or older (16⇓⇓⇓–20).

We would like to know if postcranial diversification followed a similar developmental path to cranial diversification. Additionally, knowing which Neandertal characteristics are present early in development has implications for determining whether postcranial differences between Neandertals and modern humans have evolutionary (e.g., genetic drift, natural selection) or lifetime behavioral (e.g., activity levels, gait patterns) causes (21). Newborn individuals are particularly important in this regard because their skeletons have been subject to only in utero mechanical loading, so it is not possible for their skeletons to have been influenced by locomotion or other habitual activities of adults or older subadults.

Here, we study the postcranial skeletons of the two most complete Neandertal neonates—Mezmaiskaya 1 (from Russia) and Le Moustier 2 (from France)—to quantify the extent to which Neandertal postcranial features are present around the time of birth. We base our analyses on 11 linear measurements (Table S1) of the Neandertals (Table S2) and a recent human sample of African Americans and European Americans (Tables S3 and S4).

Table S1. Measurement descriptions

Table S2. Neandertal measurements

Table S3. Recent human sample

Table S4. Summary statistics for the recent human sample

Discussion We found that many Neandertal postcranial characteristics are present around the time of birth. Neonatal Neandertals already appear to possess the wide body, long pubis, and robust long bones of adult Neandertals. In fact, the only exception we could find was a relatively short radius, which Mezmaiskaya 1 had, whereas Le Moustier 2 had a relatively long radius. This ambiguous result may not be so surprising, given that adult Neandertals show less shortening of the radius relative to the humerus than they do of the tibia relative to the femur (39), and that the Dederiyeh 1 subadult Neandertal has a relatively long radius (18). Unfortunately, the clavicles of Mezmaiskaya 1 and Le Moustier 2 are too fragmentary to reliably estimate the length, but the somewhat older Amud 7 Neandertal seems to already have a clavicle that is long relative to humerus length (14). Consistent with our results, Golovanova et al. (40) concluded that Mezmaiskaya 1 had relatively short distal limb segments and relatively large ends of the radius and femur in comparison with a recent human infant of similar dental age; and Ponce de León et al. (11) found that Mezmaiskaya 1 had absolutely large distal ends of the humerus and femur, absolutely long ilium and pubis, and a relatively short tibia in comparison with the means of measurements collected by Fazekas and Kósa (41) on a recent Hungarian fetal skeletal sample. We focused our analyses on a set of linear measurements, but, based on other studies, Neandertals < 1 y of age already seem to show other distinctive postcranial features, including bowed long bones (Kiik Koba 2, Mezmaiskaya 1, Le Moustier 2) (11, 42, 43); robust, rounded rib shafts (Kiik Koba 2) (42); an incipient dorsal axillary sulcus of the scapula (Kiik Koba 2) (44); a medially directed radial tuberosity (Mezmaiskaya 1) (40); subequal proximal and distal thumb diaphyses (Le Moustier 2) (43); an opponens pollicis flange on the first metacarpal (Kiik Koba 2) (37); and very thick long bones (Le Moustier 2) (15). However, other studies appear to indicate that at least some Neandertals developed elevated long-bone cross-sectional properties (14, 45) and a thin superior pubic ramus (16, 46) later in life. Taken together, current evidence indicates that, with some exceptions [e.g., neurocranial globularity (12, 13), thin superior pubic ramus (16, 18, 46), and perhaps radius/humerus proportions (this study)], skeletal differences between Neandertals and modern humans are largely established by the time of birth. Features that are present on the skeletons of neonatal Neandertals could not have developed in response to mechanical loading associated with adult/older-subadult behaviors (e.g., hunting), so they must either have an evolutionary explanation or result from environmental influences on the fetus (e.g., maternal diet). If we consider that evolutionary changes are a more likely explanation than fetal environment for skeletal differences between Neandertals and modern humans, climatic adaptation is the best-supported explanation for many aspects of Neandertal postcranial form because Neandertals have body proportions close to present-day humans with ancestry in cold climates (24, 30, 31), it appears that multiple generations are necessary for appreciable changes in body proportions (i.e., an evolutionary timescale is needed) (24, 25), a wide variety of taxa exhibit similar ecological relationships (47⇓–49), and laboratory experiments on human subjects demonstrate that body proportions influence heat loss (50) [see also Churchill (51)]. Recent research, however, has cast some doubt on this explanation. Because the modern human expansion from Africa that gave rise to recent human groups had a substantial south-to-north component, differences among recent human groups in body proportions could have more to do with population history than climatic adaptation (52⇓–54). Additionally, a wide body may have been the ancestral condition for Homo (7, 55⇓–57), even though the earliest members of our genus presumably lived in warm climates. Consequently, although it remains likely that many postcranial differences between Neandertals and modern humans stem from contrasts in body proportions (21, 36, 38, 58), further research will be necessary to establish whether climate played an important role in shaping these differences in body proportions. Finally, it is important to note that, even if climatic adaptation explains Neandertal body proportions, climatic adaptation alone cannot explain a long pubis relative to dimensions of the pelvic inlet (59, 60). The alternative explanations for a long pubis include a posteriorly positioned acetabulum related to differences in gait between Neandertals and modern humans (60), or a wide pelvis coupled with a transversely oval outlet of the birth canal (as opposed to the anteroposteriorly oval outlets typical of modern humans), because Neandertals had a different birth process than modern humans (59).

Materials and Methods Mezmaiskaya 1 and Le Moustier 2 Neandertals. Mezmaiskaya Cave is located in the northwestern Caucasus ∼50 km south of the city of Maikop (Russia). Mezmaiskaya 1 consists of 141 identifiable postcranial bones, a cranium and mandible, and 14 dental crowns of deciduous teeth. The skeleton was recovered in anatomical association from the lowermost 3–5 cm of level 3, the oldest Middle Paleolithic layer (Figs. S1 and S2). Detailed stratigraphic assessments clearly indicate that the Mezmaiskaya 1 skeleton and level 3 were deposited at the same time, both dating to very close to or greater than the effective measurement limit of radiocarbon (∼50 ka) and likely to 70–60 ka based on electron spin resonance mean early and late uptake model determinations for level 3 (11, 40, 61, 62). Fig. S1. Mezmaiskaya cave. Stratigraphy of the cave and the stratigraphic position of the Mezmaiskaya 1 skeleton. (A) Plan of the Mezmaiskaya cave indicating bedrock (1), flowstones (2) and limestone blocks (3), grid position (4), measurements of the modern surface along the cave axis (5), datum (6), dripline (7), 1987–2006 excavation area (8), and indicators for the main longitudinal profile along the cave axis (9) shown in Fig. S1B. The vertical red line (10) indicates the position of the microprofile shown in Fig. S1C. (B) Section XZ6 shows the succession of levels: 1–1 and 1–2 (Holocene), 1–3 through 1C (Epi-Paleolithic and Upper Paleolithic), 1D (volcanic ash), 2–3 (Middle Paleolithic), and 4 (sterile). Legend: 1 and 2, level designations and limits of levels; 3 and 4, stones and blocks. (C) Microprofile constructed along the quadrant line M/east, from M26 through M19, which covers the area where the Mezmaiskaya 1 skeleton was found. The profile shows stones, limestone blocks, and stone artifacts found in situ (bones are not shown in this profile because of the very dense concentration of the remains) from the eastern semiquadrant of line M; it documents the exact stratigraphic position of the Mezmaiskaya 1 skeleton relative to the levels excavated in the area. Levels: 1–1 (Holocene); L, erosional stratum; 2–3 (Middle Paleolithic); and 4–5 (sterile strata). Legend: 1, limits of levels; 2, stones; 3, level designations; 4, charcoal lenses; 5–16, stone artifacts of various types; and 17, Mezmaiskaya 1 skeleton. Image courtesy of L.V.G. Fig. S2. Mezmaiskaya 1 Neandertal skeleton. (A) View from the southwest of the 1987–2001 excavation area; the red arrow points to where the Mezmaiskaya 1 skeleton was found in 1993. (B) View from the south-southwest of the Mezmaiskaya 1 skeleton, which was found in quadrant M26 at the bottom of level 3; the red arrow points to the skeleton. (C) View from the west of the Mezmaiskaya 1 skeleton, which is lying in anatomical arrangement; the black arrow points to the north. A and B images courtesy of L.V.G.; image C courtesy of ref. 40, © 1999 by Current Anthropology. The rock shelters of Le Moustier are located in the Dordogne ∼45 km southeast of Périgueux (France). The Le Moustier 2 skeleton comes from layer J through the top of layer H of the lower rock shelter, which contained Typical Mousterian (layer J) and Discoid Mousterian (top of layer H) artifacts (Figs. S3 and S4). Based on thermoluminescence dating of level J, Le Moustier 2 dates to ∼40 ka BP (43, 63⇓⇓–66). Fig. S3. Le Moustier lower rock shelter. View of the upper part of the stratigraphy of the Le Moustier lower rock shelter at the beginning of the 1990s. Following Peyrony’s stratigraphical interpretation (63), Le Moustier 2 was excavated from layer J (“Mousterien typique”) through the top of the layer H (“Mousterien de tradition acheuléenne”) (78⇓–80). Following Gravina and Discamps (66), the upper part of layer H does not contain any Mousterian of Acheulean Tradition; instead, the lithic artifacts should be classified as Discoid Mousterian. Le Moustier 2 is, then, a rare case of a Neandertal primary burial associated with this lithic technocomplex (81). Image courtesy of B.M. Fig. S4. Le Moustier 2 Neandertal skeleton.The 2008 restoration of the Le Moustier 2 Neandertal skeleton (Musée national de Préhistoire, Les Eyzies-de-Tayac Sireuil collections). Note that the right humerus and femur are the two long bones still housed at the Musée de l’Homme under the fossil identification “La Ferrassie 4” (43, 77). Picture Philippe Jugie, Musée national de Préhistoire, Les Eyzies-de-Tayac Sireuil. © MNP (Musée national de Préhistoire-Les Eyzies), Dist.RMN, photograph Philippe Jugie. These two fairly complete skeletons are the best preserved Neandertal neonates, and among the most complete Neandertals of any age (Figs. S2 and S4). We were able to collect the full measurement set on Mezmaiskaya 1 and all of the measurements except pubis length and tibia length on Le Moustier 2 (Table S2). The SI Text includes more details about the context and preservation of the Mezmaiskaya 1 and Le Moustier 2 Neandertals. Recent Human Sample. The recent human sample is from the fetal skeletal collection housed at the National Museum of Natural History (Smithsonian). Various medical practitioners collected the fetuses, mostly from the Baltimore, MD, and Washington, DC, areas, at the end of the 19th and early 20th centuries and donated them to the museum between 1903 and 1917 (67, 68). Based on the documentation associated with the collection, we divided the sample into two groups: African Americans and European Americans, with approximately equal numbers of female and male specimens in each group (Table S3). Age at death is not precisely documented for much of the sample, but, based on femur length (measurement defined in Table S1; minimum, 57 mm; maximum, 102 mm; mean, 79 mm), the individuals ranged from ∼8 mo in utero to ∼4 mo after birth, with the mean approximately birth (41, 69). Data Collection. We collected 11 linear measurements of the humerus, radius, ilium, pubis, femur, and tibia (Table S1) on the left and right sides, preservation permitting, on each of the individuals. We analyzed the mean measurement when both sides could be measured. For Mezmaiskaya 1 and Le Moustier 2 (Table S2), we rounded each measurement to the nearest millimeter and indicated ±0.5 mm on all of the graphs so as not to convey an undue sense of precision when visually comparing these specimens to recent humans. T.D.W. collected the measurements of the recent humans directly with calipers. Mezmaiskaya 1 was scanned with a Skyscan 1172 micro-CT system (resolution ∼35µm for all dimensions), and Le Moustier 2 was scanned with a BIR ACTIS 225/300 industrial CT scanner (resolution of 20–30 µm for all dimensions). H.C., J.-J.H, B.M., and T.D.W. collected the measurements of Mezmaiskaya 1 and Le Moustier 2 directly with calipers and from CT scans with the Avizo (FEI) and Tivmi software packages. Statistical Analyses. We fit nonlinear regressions of the form y = axb (power laws) to the data in the bivariate graphs, where a and b are constants, and y and x are the response and predictor variables, respectively. For each graph, we fit three separate curves: for the African Americans, European Americans, and all of the recent humans (i.e., all individuals except Mezmaiskaya 1 and Le Moustier 2). As with ratios, these curves allow relative dimensions to be compared, but they have the advantage of allowing the ratio to vary with size (i.e., age). (An exponent [b] equal to one indicates that the ratio between the two variables remains constant.) Because relative dimensions are being compared, our analyses are independent of age estimates, which is advantageous given evidence that Neandertals may have matured faster than modern humans (70). Individuals with missing data for one (or both) of the variables were excluded from the particular bivariate analysis. Table S6 provides fit statistics for the bivariate analyses. Table S6. Fit statistics for the bivariate plots To provide a multivariate synthesis of the bivariate analyses, we performed PC analysis (PCA) of the residuals of the individuals from the all-recent-human regressions (i.e., the residuals from a particular bivariate analysis correspond to a variable in the PCA). We performed the PCA on the covariance matrix, and individuals with any missing data were excluded from this analysis. We performed all statistical analyses in Matlab (Mathworks).

SI Text Mezmaiskaya 1. Mezmaiskaya cave is located 1,310 m above sea level along a small tributary of the Kurdjips River, ∼50 km south of the city of Maikop (northwestern Caucasus, Russia). L.V.G. has excavated the site since 1987. Currently, 6 Holocene and 20 Pleistocene strata are identified over an ∼80-m2 excavation area (Fig. S1 A and B), including 7 Middle Paleolithic levels dating to ca. 70–40 ka BP (40, 61, 62, 71, 72), 6 Upper Paleolithic and 2 Epi-Paleolithic levels dating to ca. 39–12 ka calibrated BP (73⇓–75), and 6 post-Paleolithic levels, including a Neolithic level deeper in the cave that was found in 2011. The Neandertal fossils recovered from Mezmaiskaya cave are: the skeleton of a Neandertal neonate (Mezmaiskaya 1), which was discovered in 1993 in level 3, the oldest Middle Paleolithic deposits; an isolated permanent tooth (Mezmaiskaya 3), which was found later and is also from level 3; and skull fragments of a Neandertal child (Mezmaiskaya 2), which were found in 1994 in level 2, the uppermost Middle Paleolithic deposits. The Mezmaiskaya 1 almost-complete skeleton was recovered in situ and in anatomical arrangement from the lowermost 3–5 cm of level 3 in the cave entrance area where most Pleistocene layers were destroyed by erosion (Figs. S1 A and C and S2). The skeleton occupied an area of 20 × 30 cm in quadrant M26, atop a large limestone block, and it was overlain by the Middle Paleolithic levels 3 and 2B–4 and a modern soil (level 1–1). Significantly, level 2B–4 was preserved close to the eastern wall of the cave, including quadrant M26 (Fig. S1C), but it gradually thinned toward the cave axis and is not present on section XZ6 (Fig. S1B). In the area where the skeleton was found, the sediments of levels 3 and 2B–4 underwent a strong calcium-carbonate cementation to the state of a rugged breccia in the lowermost part of level 3. Thanks to strong calcite cementation, which encased large portions of the Mezmaiskaya 1 remains, most of the bones were found in an excellent state of preservation and suffered only minor postdepositional disturbance. The skull was partly damaged and collapsed, but all of the cranial elements were preserved in close anatomical association (Fig. S2C). The left scapula, humerus, radius, most of the vertebral column and ribs, and the pelvis were preserved in anatomical arrangement. The long bones of the legs were disarticulated, and the metatarsals were gnawed by rodents. The body was deposited on the right side in what appears to have been a flexed position, head oriented to the north (inside the cave), with the left arm extended along the trunk and flexed slightly at the elbow. The position of the legs was difficult to determine, but the anatomical association between the spine and pelvis suggests that the legs were bent at the knees. Analyses of linear craniodental and postcranial dimensions of the Mezmaiskaya 1 specimen in comparison with present-day human neonates suggest that the Mezmaiskaya individual died approximately 2 wk after birth (11, 13). No traces of a burial pit were observed, and no artifacts or faunal remains were found in the lowermost part of level 3 in the immediate vicinity of the skeleton. However, small (2–3 mm) charcoal fragments were recovered among the skeleton but were lacking in adjacent parts of level 3. The skeleton’s good preservation with no evidence of scavenger marks on the bones suggest an intentional burial. Several microprofiles constructed across the skeleton area (figures S1C and S2 in ref. 11) indicate that the burial was made in the initial period of Neandertal occupation of the cave (level 3), before a significant accumulation of artifacts and faunal remains in the sediments of this level. Taken together, the evidence suggests that the Mezmaiskaya 1 Neandertal neonate was buried in a flexed position in a shallow pit or directly on the surface of a limestone block and covered with the surrounding sediments, and postdepositional processes completely obliterated traces of the burial. Mezmaiskaya 1 is one of the most complete and best-preserved Neandertal skeletons of any age and the youngest (2 wk after birth) Neandertal individual found in the world. Le Moustier 2. Le Moustier is a small village situated 10 km upriver from Les Eyzies-de-Tayac Sireuil at the crossing of the Vèzère and Vimont valleys in the Dordogne (southwest region of France). There, three different archaeological sites are located on a Coniacian limestone cliff. Two of them are very well known: the Upper (or Classical) and the Lower (or Peyrony) rock shelters (Fig. S3). In May 1914, during his excavations of the Lower shelter, D. Peyrony found a burial of a very young child (Le Moustier 2) within a Mousterian layer (layer H). Very quickly, he sent (at least) two long bones to M. Boule to obtain an age at death estimate for the individual. He received Boule’s answer a few days later: it was a neonate. Following Peyrony’s stratigraphical interpretation, the burial of Le Moustier 2 was excavated from layer J through to the top of the layer H. All of the information recorded by Peyrony during the excavation suggests an intentional Mousterian primary interment (43, 63, 76). Unfortunately, from Peyrony’s records, we do not have any precise data about the skeleton’s position within the burial pit. Then, for a variety of reasons, although Peyrony mentioned Le Moustier 2 in different publications, the fossil was forgotten by the scientific community, or considered to be lost during the first World War (77). In September 1996, one of the present authors (B.M.), while conducting an inventory of the human remains preserved in the collections of the Musée national de Préhistoire at les Eyzies-de-Tayac Sireuil, found small sediment blocks and isolated neonatal human remains in a wooden drawer among the collections belonging to Peyrony’s excavations of the Le Moustier Lower shelter. With the authorization of the French Ministry of Culture, over a period of 150 d (between 1997 and 2001), the sediment blocks containing most of the neonate’s bones were excavated and restored. In the end, it was possible to present to the scientific community one of the best-preserved Neandertal skeletons, including adults (Fig. S4) (65). Today, the Le Moustier 2 original fossil, a Neandertal neonate, which, based on present-day human standards, cannot be older than 4 mo after birth, is one of the most beautiful hominin fossils presented at the permanent exhibition of the Musée national de Préhistoire.

Acknowledgments We thank T. Steele, Y. Rak, and two reviewers for helpful comments and D. Hunt for access to and assistance with collections. This study was funded by the Max Planck Society, the Aquitaine Regional Council (Transitions Program, convention 20051403003AB), and the National Research Agency’s Future Investments program (ANR-10-LABX-52 - Bordeaux Archaeological Sciences LabEx cluster of excellence, NEMO project).

Footnotes Author contributions: T.D.W., H.C., and J.-J.H. designed research; T.D.W., H.C., B.M., and J.-J.H. performed research; T.D.W. analyzed data; T.D.W., H.C., L.V.G., V.B.D., B.M., and J.-J.H. wrote the paper; and L.V.G., V.B.D., and B.M. contributed fossil samples.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission. Y.R. is a guest editor invited by the Editorial Board.

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