http://orcid.org/0000-0003-4550-6913
Figures
Abstract
Immature remains are critical for understanding maturational processes in hominin species as well as for interpreting changes in ontogenetic development in hominin evolution. The study of these subjects is hindered by the fact that associated juvenile remains are extremely rare in the hominin fossil record. Here we describe an assemblage of immature remains of Homo naledi recovered from the 2013–2014 excavation season. From this assemblage, we attribute 16 postcranial elements and a partial mandible with some dentition to a single juvenile Homo naledi individual. The find includes postcranial elements never before discovered as immature elements in the sub-equatorial early hominin fossil record, and contributes new data to the field of hominin ontogeny.
Citation: Bolter DR, Elliott MC, Hawks J, Berger LR (2020) Immature remains and the first partial skeleton of a juvenile Homo naledi, a late Middle Pleistocene hominin from South Africa. PLoS ONE 15(4): e0230440. https://doi.org/10.1371/journal.pone.0230440
Editor: Michael D. Petraglia, Max Planck Institute for the Science of Human History, GERMANY
Received: September 29, 2019; Accepted: February 29, 2020; Published: April 1, 2020
Copyright: © 2020 Bolter et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All data underlying the analyses in this manuscript appear in the manuscript itself. Data include observations of maturational stage and completeness taken on original fossil specimens. In addition, we provide 3D surface models and images of the DH7 elements that are available for public download on Morphosource.org (accession numbers listed under the heading Homo naledi). H. naledi original fossils are curated at the Evolutionary Studies Institute, University of the Witwatersrand in Johannesburg, South Africa, and researchers may apply to study them through the Fossil Access Committee by contacting the University Curator for Fossil and Rock Collections: Bernhard Zipfel, PhD, University Curator of Fossil and Rock Collections, Evolutionary Studies Institute, University of the Witwatersrand, Johannesburg; e-mail: Bernhard.Zipfel@wits.ac.za; Phone: +27-11 717-6683.
Funding: The National Geographic Society--LRB; The Lyda Hill Foundation--LRB; The South African National Research Foundation--LRB; The Gauteng Provincial Government--LRB. Centre for Excellence in the Palaeosciences, University of the Witwatersrand—LRB; University of Wisconsin-Madison—JH; MJC Foundation—DRB.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Our knowledge of maturational processes and life history stages in human evolution is hindered by how extremely rare immature remains are in the hominin fossil record. Further complicating our understanding is that hominin fossil remains rarely combine teeth, cranial and associated postcranial bones, and only a handful of such partial skeletons represent immature individuals. Yet such remains provide important evidence about the maturation of extinct hominins. Apart from recent modern humans and Neanderthals (e.g., [1]), only three hominin species are represented by immature partial skeletons at this time: Australopithecus afarensis [2, 3], Australopithecus sediba [4,5] and Homo erectus [6–9]. Augmenting this limited dataset is of great significance in trying to understand the evolution of human growth and development.
The immature individuals from the Dinaledi and Lesedi assemblages of Homo naledi represent individuals of many juvenile and adult life stages, presenting a unique opportunity to identify and document in particular a range of immature individuals of an extinct species, and contribute data to the study of comparative hominin ontogeny [10–13]. The Lesedi Chamber sample includes an associated partial skeleton of an adult individual, a jaw fragment from a second adult, and the remains of a very young juvenile [12]. The Dinaledi Chamber sample is much richer in fossil material, with the remains of a minimum of 15 individuals, ranging in age from neonates to older adults and dating to between 335,000 and 226,000 years ago [10,11,13,14].
The geology and taphonomy of the Dinaledi Chamber material has been described previously by Dirks et al. [11]. To sum up, the Dinaledi Chamber is an approximately 3 x 5 m chamber located within an interconnected network of cave passages and spaces now designated as the Dinaledi Subsystem [15]. The Subsystem itself is connected to the larger Rising Star Cave System by a narrow, 12 m high vertical passage known as the Chute [11]. Like most other hominin fossil sites in the area, the cave system formed within the stromatolite-rich dolomite of the Monte Christo Formation [16]. The fossils are not encased in hard breccia, but are recovered from largely unconsolidated mudstone sediments that are distinct from those outside the subsystem, suggesting an autochthonous derivation [11]. The presence of some articulated and semi-articulated remains in the Dinaledi deposit, as well as small elements that normally disarticulate and disperse quickly, suggest limited post-mortem disruption and minimal winnowing. Despite this, the high density of material and the lack of stratigraphy within the sediments make the sequence of deposition and disarticulation challenging to determine.
When the Dinaledi Chamber was first assessed, approximately 300 fossil fragments were found scattered across the surface of the chamber floor (Fig 1A). The majority of the remaining assemblage came from a single excavation unit, 0.8 m2, excavated in two sessions in 2013 and 2014, to a depth of c20 cm below the surface. This unit lies midway inside the chamber and was targeted for excavation after fossil material was observed eroding through the surface. In total more than 1800 fossil specimens have been recovered from the Dinaledi Chamber.
A) Schematic of the Dinaledi Chamber floor area, showing the distribution of adult and immature material recovered from the surface during the 2013–2014 expedition; B) All immature postcranial specimens recovered from the excavation pit by accession number and depth level.
Within the primary excavation unit, material is commingled. Detailed analyses of the taphonomy and distribution of the hominin bone accumulations suggested at least some of the bodies were deposited while still fleshed [11,17,18,19]. Further, the deposition of the remains appears to have occurred over a period of time, within different depth locations of the deposits [11]. The assemblage includes cranial and postcranial remains from both immature and adult individuals. Immature bone is less dense and less calcified than adult bone, and typically is less represented in assemblages than adult material [20,21]. Although two immature hemi-mandibles were recovered, in combination with a total of 32 deciduous teeth, immature cranial elements are extremely rare in the assemblage [10,22]. A mass of small fragments and sediment, removed en bloc in 2014 (U.W. 101–1477) appears to contain multiple fragments of an infant cranium. However, analysis of this thin and fragile material has only recently begun and identifications and descriptions are still underway.
While the comingled nature of the assemblage makes it challenging to associate skeletal parts to single individuals, several instances of postcranial elements in direct articulation have been noted [11,17,18]. This information, along with high-resolution data collected from the deposit [18,19], and anatomical assessment of the entire collection have made it possible for us to identify several portions of the skeleton of a single immature individual, which we designate as DH7.
Seventy-six postcranial specimens identified as ‘immature’ were recovered from the 2013–2014 Dinaledi excavations (Fig 1, Table 1). The excavation levels are divided into five levels: surface (surface to 40 mm), depth 1 (41–70 mm), depth 2 (71–100 mm), depth 3 (101–130 mm) and depth 4 (131–160 mm). DH7 is based upon in situ articulated elements excavated from the southwest portion of the excavation unit, approximately 41–100 mm below surface (depths 1 and 2). The articulated elements include an almost complete left tibia (U.W. 101–1070), recovered with unfused epiphyses in place (Fig 2); a partial left fibula (U.W. 101–1045), in three pieces, with heavily eroded surface morphology [23]; a left calcaneus (U.W. 101–907) (Fig 3); and a talus and navicular (recovered together as U.W. 101–910) (Fig 4). The three tarsals were originally designated “Foot 2” [24]. The preservation of the complete left tibia is noteworthy as we are familiar with no other specimen in the hominin fossil record that preserves epiphyses in place with this degree of surface detail. An immature right tibia, U.W. 101–996 (Fig 5) appears to be the antimere of the DH7 left tibia, U.W. 101–1070 [23]. This specimen is a composite of three fragments (U.W.101-996, U.W.101-1074 and U.W.101-1077), which were refit in the lab post-excavation, and accessioned to a single specimen number: U.W.101-996. All three fragments were recovered from depth 2 or 3, within 15 cm of the articulated left lower limb DH7 elements.
Note proximal and distal epiphyses affixed with paraloid.
Considering the number of immature skeletal material recovered from the Dinaledi hominin deposit (Table 1), we set out to test the hypothesis that additional elements of this partial skeleton were present in the sample.
Materials and methods
We assess 70 immature skeletal remains from the 2013–2104 season to identify materials that may belong to the proposed DH7 individual comprised of the six lower limb elements. All fossil analyzed in this study are from the Dinaledi Chamber, accession numbers U.W. 101- (See Table 1). H. naledi original fossils are curated at the Evolutionary Studies Institute, University of the Witwatersrand in Johannesburg, South Africa, and researchers may apply to study them through the Fossil Access Committee by contacting the University Curator for Fossil and Rock Collections. Additionally, 3D surface models and images of DH7 elements are available for public access and download at Morphosource.org (See Table 3). The South African Heritage Resource Agency and Cradle of Humankind UNESCO World Heritage Site Management Authority granted the permits to work on the Rising Star site, excavation permit ID: 952. All necessary permissions were obtained for the described study, which complied with all relevant regulations.
A minimum number of individuals (MNI) was previously assessed from the 2013–2104 season based on dental remains: nine immature individuals, and six adult individuals [10,13] (Table 2). Six of the dental individuals are either ‘Infants’ (deciduous dentition only) or ‘Early Juveniles’ (with first molars erupted). Only a single dental specimen represents a ‘Late Juvenile’ with second molars erupted [13] (Table 2). This ‘Late Juvenile’ is represented by a right mandibular fragment, U.W. 101–377, preserving permanent teeth C, P3, P4, M1 and M2 (canine U.W. 101–1014 refit in lab) [10,11,13,20] (Fig 6). The partial mandible was recovered from depth 1 in the excavation unit.
Right hemi-mandible with permanent teeth C, P3, P4, M1 and M2; canine U.W. 101–1014 refit in lab.
Two additional individuals are present based on MNI, but only approximate age can be determined: One is an adult, and one is an immature [13].
The DH7 associated lower limb represents a ‘Late Juvenile’ in skeletal maturation stage, with unfused but well-developed epiphyses of the hip, knee and ankle, a maturational skeletal pattern that is consistent across apes and hominins [13,25–29].
Criteria for including or excluding elements from association with DH7 include: duplication of element; developmental stage; size difference; spatial proximity (depth and span); refitting of specimens into a single element; and articulation/anatomical position of elements (Table 3). Skeletal maturation continuity was assessed using established standards from the literature [30–33]; cf [5]. Evaluations were made using the original fossils, original excavation notes and photographs, and published descriptions of H. naledi anatomy [17,23,24,34,35,36]. The vertical and horizontal context of immature material within the excavation unit was also used to help identify potentially associated elements [19]. If depth location was not available from the previously collected 3D data [18,19], depth was estimated based on excavation photographs and comparisons with known-depth specimens.
Specimens attributed to DH7 are highlighted in grey. Criteria for determining elements associated with DH7: 1 Duplication of element, 2 Different developmental stage, 3 Size difference, 4 Spatial proximity, 5 Refitting of specimens into single element, 6 Articulation/anatomical position of elements.
In this commingled sample we set a very high evidentiary standard to accept the association of different elements. Anatomical in situ articulation of the left lower limb elements provides certain evidence that these elements represent a single individual, deposited with soft tissue still intact. The U.W. 101–996 tibia meets this standard on the evidence of its mirror-image anatomy to U.W. 101–1070 [23], its identical state of epiphyseal development, and its very close spatial and depth position to the articulated left lower limb elements of DH7. The discovery that all fragments of two antimere elements are very near each other may suggest a low degree of disaggregation of skeletal elements in this part of the deposit.
The evidence for skeletal association here meets the standards linking immature partial skeletons at other hominin sites with commingled individuals [1,4,8,9]. El Sidrón J1 is an Early Juvenile partial skeleton (H. neanderthalensis) recovered mostly from a 1 m2 unit, together with multiple elements from at least one younger and one older immature individual. The consistent developmental stage and some direct articulations support the interpretation that the J1 material represents a single individual [1]. The MH1 immature partial skeleton from Malapa also includes some elements in direct anatomical articulation [4], and of consistent developmental stage, although one adult partial skeleton and another immature individual are known to be present in this assemblage. A sub-adult partial skeleton from Dmanisi, Georgia is evidenced based upon stratigraphic association, with all elements found within a 1 m stratum across 7 m2, along with developmental consistency and lack of element duplication [8,9]. As in the Dinaledi example, the recovery of more skeletal material from any of these active sites may necessitate revisions to the original hypothesis of association.
The 2013–2014 Dinaledi excavations involved a single 0.8 m2 unit, in addition to a small amount of material collected from the chamber surface. While the surface area of the chamber consists of approximately 20 m2, the depth of the sediments within is currently unknown. Consequently, we cannot predict what other remains of this individual may yet be recovered. We further caution that many elements in the collection are too fragmentary to accurately assess developmental stage.
Results
We identified additional skeletal specimens that are developmentally consistent in maturity indicators with the remains of DH7, recovered within 2–20 cm of the articulated lower limb (Figs 7 and 8; Table 4). Consistent with the dental evidence from the Dinaledi Chamber of the ‘Late Juvenile’ age class, postcranial elements that demonstrate a ‘Late Juvenile’ stage of maturation are quite rare within the sample.
A right proximal femur fragment (U.W. 101–1000) was recovered from depth 1 (Fig 9A). The unfused head of this proximal femur fragment refits a right femoral head epiphysis (U.W. 101–1098), located at depth 2 (Fig 9B). A nearly complete right ischium (U.W. 101–1088) was found at the distal end of the articulated lower left limb in the excavation unit, at depth 2 (Fig 10). The distal segment of the left immature fibula (U.W. 101–817) was found adjacent to the articulated in situ ankle, at depth 2 (Figs 11 and 12). Two right humeral shaft pieces were found adjacent to the left tibia, and refit in the lab for a nearly complete humerus (U.W. 101–948) (Fig 13).
a) Proximal fragment with metaphyseal surface (U.W. 101–1000); b) unfused femoral head epiphysis (U.W. 101–1098).
Image showing location of elements of right and left lower limb: U.W. 101–907, U.W. 101–910, U.W. 101–1000, U.W. 101–1070, U.W. 101–1045 and U.W. 101–817.
Composite of two elements, missing epiphyses (U.W. 101–948).
Additional fragmentary hand bones were found near the articulated lower limb and hemi-mandible, and have provisionally been associated with DH7. Despite being small in size, these hand bones are consistent with each other in their developmental morphology and age indicators [17]. Two unsided immature metacarpal shaft fragments (U.W. 101–1633 and U.W. 101–1636), and two immature fragments from a proximal and intermediate phalanx (U.W. 101–1635 and U.W. 101–1664), provisionally attributed to “Hand 5” [17], were recovered en bloc at depth 2, and processed together in the lab (Fig 14A–14D). Two additional metacarpal shafts (U.W. 101–1536 and U.W. 101–1271), also attributed to “Hand 5”, were recovered from depth 2, and in spatial proximity to the partial mandible U.W. 101–377 (Fig 14E and 14F).
Hand remains found en bloc: a) unsided metacarpal shaft U.W. 101–1633; b) unsided metacarpal fragment; c) unsided proximal phalanx, distal shaft U.W. 101–1635; d) unsided intermediate phalanx fragement, U.W. 101–1664; and two additional age-consistent hand bones: e) metacarpal shaft fragment, unsided U.W. 101–1271; and f) metacarpal shaft fragment, unsided U.W. 101–1536.
Although dental MNI indicated only one ‘Late Juvenile’ [10,13], there is postcranial evidence of a second ‘Late Juvenile’ individual in the Dinaledi Chamber deposit [37]. This second ‘Late Juvenile’ is present in the northeastern portion of the excavation pit at depth 3, is not as complete as DH7, and duplicates elements of DH7. The material includes a right femur refit from four pieces (U.W. 101-938a), an epiphyseal head (U.W. 101-938b) and two right pelvic fragments (U.W. 101–1754 and U.W. 101–1755) (Fig 15). This partial lower limb orients towards the periphery of the unit, and the more fragmentary state may be a result of the position of the bones in the commingled pit. Bodies in the more compacted center of commingled deposits from forensic and archaeological mass graves undergo differential taphonomic factors, and may result in differential preservation from those on the outer edges [cf. 38].
Right femur (U.W. 101-938a, b) and pelvic fragments (U.W. 101–1754 and U.W. 101–1755). a) in situ U.W. 101-938a, b and U.W. 101–1754; b) nearly complete femur from four refit pieces; c) articulation of U.W. 101-938b with U.W. 101–1754 and U.W. 101–1755.
Considering the entire fossil collection, we hypothesize that the ‘Late Juvenile’ material from the southwestern portion, and from depths 1–3 of the excavation pit, derive from the same individual as the associated postcranial material. We therefore provisionally attribute all this material to DH7. However, we note that the abundance of material in the present collection may still represent only a small fraction of the total amount of hominin skeletal material in the Dinaledi Chamber as a whole.
Discussion
The conditions inside the Dinaledi Chamber have yielded an unprecedented number of Homo naledi fossils. In this case, the number of immature remains in the Dinaledi assemblage offers the possibility to expand our knowledge of stages of maturational processes in H. naledi. The identification of a partial older juvenile skeleton of H. naledi substantially adds to the database of associated immature partial skeletons in the human evolutionary fossil record.
The skeletal maturation of DH7 places it near the same maturational stage as partial skeletons of two other species, the MH1 holotype of Au. sediba, dated to 1.98 million years old [4,5,39], and the KNM-WT 15000 skeleton attributed to H. erectus, dated to 1.6 million years old [6,40–43]. All three partial skeletons share a combination of unfused long bone epiphyses and pelvic elements, indicating that growth was still occurring at the shoulder, hip, knee and ankle regions. Dentally, all three individuals lack erupted third molars, although the stage of premolar and canine eruptions varies across specimens. The age at death of KNM-WT 15000 is estimated between 8.3 to 8.8 years based on dental microhistology [42]; MH1 has been estimated to have been between 9–11 years old at death [5].
The DH7 partial skeleton (Fig 4) from the Late Middle Pleistocene contributes important new data to the field of hominin ontogeny. As designated, DH7 is consistent in skeletal maturity with MH1 and KNM-WT 15000, both of which exhibit an ape-like (non-human) maturational timing [5,29,41,42]. However, other body systems complicate the characterization of somatic maturity in DH7. Dentally, H. naledi appears to have a pattern of dental eruption which suggests an affinity with H. sapiens, with premolars fully emerged by the time the second molars are fully erupted; however, the pattern of dental root formation is more ape-like [44]. H. naledi has a unique dental pattern of surface enamel deposition unlike any other hominin, and unlike humans [45]. The mosaic of brain size and body size characters in H. naledi further complicates interpretations of the maturation pattern. At 480-610cc, H. naledi has an intermediate brain size between Au. sediba and H. erectus [12,46]. H. naledi has a stature more similar to Au. sediba, estimated at 143.5 cm for adults [5,46]. If Au. sediba, H. erectus and H. naledi shared a similar mode of maturity, this would suggest an age at death for DH7 between ~8–11 years old.
The phylogenetic arrangement of these three species relative to modern humans is uncertain [47,48]. The contrast in brain size among them is striking, raising the possibility of testing whether the maturation pattern in these immature skeletons relates to brain development. The maturational consistency between MH1 and KNM-WT 15000 has been used to support the hypothesis that Early Pleistocene hominins had not experienced the temporal shift in ontogeny that characterizes H. sapiens, irrespective of their brain or body size [5,29,43,49,50].
It remains possible that H. naledi had a slower maturation schedule than earlier hominins, similar to modern humans and Neanderthals. The species did exist contemporaneously with both early modern humans and Neanderthals in the Late Middle Pleistocene, and some evidence suggests that H. naledi may be a phylogenetic sister to these large-brained forms [47]. If so, the DH7 individual might be older than MH1 or KNM-WT 15000, ~11–15 years based on human maturational standards (Table 5). An intermediate pattern of somatic maturity is also possible.
The late Middle Pleistocene age of H. naledi places the species as a possible contemporary in Southern Africa with our own species, H. sapiens (cf. [51]). H. naledi, with its unusual combination of primitive and derived traits, and its relatively recent existence, may shed light on the evolutionary adaptations that drove changes in the tempo of maturity, and possibly life history, in other late members of the Homo genus. The unprecedented assemblage of immature remains, plus the rare juvenile H. naledi partial skeleton, provide new opportunities to further the field of hominin ontogeny, and to explore the factors that shaped the evolution of extended maturity and life history in our own species.
Acknowledgments
We thank our colleagues for comments on early drafts of the paper. We appreciate the collegial dialogue of Ashley Kruger. We thank the University of the Witwatersrand and the Evolutionary Studies Institute for curating the material and the University Curator Bernhard Zipfel for assisting with access to the collections. We thank the South African Heritage Resource Agency and Cradle of Humankind UNESCO World Heritage Site Management Authority for granting the permits to work on the Rising Star site (excavation permit ID: 952); the Jacobs family and Lee R. Berger Foundation for Exploration for granting access to the Rising Star site; past and present exploration team members Pedro Boshoff, Mpume Hlope, Rick Hunter, Maropeng Ramalepa, Dirk van Rooyen, Mathabela Tsikoane and Steven Tucker; other excavators Elen Feuerriegel, K. Lindsay (Eaves) Hunter, Alia Gurtov, Hannah Morris and Becca Peixotto; as well as Wilma Lawrence, Bonita De Klerk, and Sonia Sequeira and Justin Mukanku for their assistance during all phases of the project. We thank the Centre for Excellence in PalaeoSciences.
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