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Endocast Morphology of Homo Naledi from the Dinaledi Chamber, South Africa

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Endocast Morphology of Homo Naledi from the Dinaledi Chamber, South Africa Endocast morphology of Homo naledi from the Dinaledi Chamber, South Africa Ralph L. Hollowaya,1,2, Shawn D. Hurstb,1, Heather M. Garvinc,d, P. Thomas Schoenemannb,e, William B. Vantif, Lee R. Bergerd, and John Hawksd,g,2 aDepartment of Anthropology, Columbia University, New York, NY 10027; bDepartment of Anthropology, Indiana University, Bloomington, IN 47405; cDepartment of Anatomy, Des Moines University, Des Moines, IA 50312; dEvolutionary Studies Institute, University of Witwatersrand, Johannesburg 2000, South Africa; eStone Age Institute, Bloomington, IN 47405; fScience and Engineering Library, Columbia University, New York, NY 10027; and gDepartment of Anthropology, University of Wisconsin–Madison, Madison, WI 53706 Contributed by Ralph L. Holloway, April 5, 2018 (sent for review December 1, 2017; reviewed by James K. Rilling and Chet C. Sherwood) Hominin cranial remains from the Dinaledi Chamber, South Africa, We examined the endocast morphology of H. naledi from the represent multiple individuals of the species Homo naledi. This Dinaledi Chamber and compared this morphology with other species exhibits a small endocranial volume comparable to Aus- hominoids and fossil hominins. The skeletal material from the tralopithecus, combined with several aspects of external cranial Dinaledi Chamber includes seven cranial portions that preserve anatomy similar to larger-brained species of Homo such as Homo substantial endocranial surface detail, representing partial crania habilis and Homo erectus. Here, we describe the endocast anat- of at least five individuals. The external morphology of these omy of this recently discovered species. Despite the small size of specimens has been described and illustrated (13). All are the H. naledi endocasts, they share several aspects of structure in morphologically consistent with an adult developmental stage. common with other species of Homo, not found in other hominins Collectively, the remains document nearly the entire cortical sur- or great apes, notably in the organization of the inferior frontal face (SI Appendix,Fig.S1) with a high degree of gyral and sulcal and lateral orbital gyri. The presence of such structural innovations detail. The DH1 calvaria preserves portions of the left and right in a small-brained hominin may have relevance to behavioral evo- parietal lobes, complete left and mostly complete right occipital lution within the genus Homo. lobes, and a small portion of both cerebellar lobes. The endocranial surface of the DH3 calvaria preserves a mostly complete left brain evolution | human evolution | South Africa | Homo | hemisphere with most of the frontal, temporal, and parietal lobes. paleoanthropology Additional fragments, including the DH2 and DH4 calvariae, du- plicate some of this morphology and in no case contradict the uman brains are larger than those of the living great apes, morphology observable in the relatively more complete specimens. Hand they also exhibit many differences in organization from The DH1 (Fig. 1 and SI Appendix, Fig. S2) and DH2 (SI Ap- those primates. Understanding when and how these changes pendix, Figs. S3 and S4) calvariae represent individuals with took place is the key challenge of paleoneurology (1, 2). The size approximately the same ECV, while the DH3 (Fig. 2 and SI of the brain and several externally visible aspects of brain anat- Appendix, Fig. S5) calvaria is smaller. Previously, virtual re- omy can be assessed in fossil hominins based upon evidence from construction of these crania yielded volume estimates of 560 mL endocasts, which are natural or artificial impressions of the for a composite model based on DH1 and DH2 elements and endocranial surface. Endocasts do not perfectly reflect the un- 465 mL for the DH3/DH4 composite (6). Here, we have carried derlying cerebral cortex, in part because three tissue layers sep- out physical reconstructions of the DH1 and DH3 specimens (SI arate the endocranial surface from the brain itself and in part because many fossils present insufficient surface detail to pre- Significance serve clear evidence of gyral and sulcal impressions. Neverthe- less, some endocasts provide enough sulcal morphology to The new species Homo naledi was discovered in 2013 in a re- enable reliable identification of features with salience for func- mote cave chamber of the Rising Star cave system, South Africa. tional interpretations (1–5). This species survived until between 226,000 and 335,000 y ago, Hominin skeletal material from the Dinaledi Chamber, South placing it in continental Africa at the same time as the early Africa, represents the species Homo naledi (6). This fossil ancestors of modern humans were arising. Yet, H. naledi was assemblage represents at least 15 individuals, both adults and strikingly primitive in many aspects of its anatomy, including the juveniles across all stages of development (7). The Dinaledi small size of its brain. Here, we have provided a description of Chamber assemblage was deposited between 236,000 and endocast anatomy of this primitive species. Despite its small 335,000 y ago (8), meaning that this sample of H. naledi existed brain size, H. naledi shared some aspects of human brain orga- at the same time as some archaic humans within Africa (9), in- nization, suggesting that innovations in brain structure were cluding those that some workers identify as “early Homo sapiens” ancestral within the genus Homo. (10). The cranial, dental, and postcranial remains of H. naledi Author contributions: R.L.H., S.D.H., H.M.G., P.T.S., W.B.V., L.R.B., and J.H. designed re- exhibit a mosaic of derived, humanlike traits combined with search, performed research, analyzed data, and wrote the paper. primitive traits shared with Australopithecus and other stem Reviewers: J.K.R., Emory University; and C.C.S., George Washington University. hominins (6, 11). This morphological pattern makes it difficult to Conflict of interest statement: R.L.H. and C.C.S. are coauthors on a 2018 paper published determine the phylogenetic placement of H. naledi relative to in PNAS. other species within Homo: For example, Bayes factor tests on This open access article is distributed under Creative Commons Attribution-NonCommercial- cranial and dental traits clearly place H. naledi within the Homo NoDerivatives License 4.0 (CC BY-NC-ND). clade, but do not exclude it as a sister taxon of Homo antecessor, 1R.L.H. and S.D.H. contributed equally to this work. Asian Homo erectus, Homo floresiensis, Homo habilis, or even H. 2To whom correspondence may be addressed. Email: [email protected] or jhawks@ sapiens (12). The small endocranial volume (ECV) of H. naledi, wisc.edu. which is within the range known for australopiths, is one of many This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. primitive traits that contrast with other, more humanlike, cranial 1073/pnas.1720842115/-/DCSupplemental. and dental traits. Published online May 14, 2018. 5738–5743 | PNAS | May 29, 2018 | vol. 115 | no. 22 www.pnas.org/cgi/doi/10.1073/pnas.1720842115 Downloaded by guest on September 27, 2021 parallel each other. The entire frontal bends sharply in an an- terior–inferior direction toward the ventral edge (SI Appendix, Fig. S5), rather than more directly anteriorly toward the frontal pole, which is also a derived trait (18). Hominin endocasts differ from great apes in the extent of frontal and occipital petalial asymmetry (25, 26). None of the endocasts of H. naledi from the Dinaledi Chamber preserve both frontal poles and lateral prefrontal surfaces, preventing an as- sessment of frontal petalia. The left frontal pole of DH3 suggests a somewhat greater lateral width. The DH1 occipital shows a left occipital petalia, with the left occipital lobe both markedly larger and more posteriorly projecting than the right (Fig. 1). U.W. 101-200 is a less complete occipital fragment but is consistent with a left occipital petalia equally marked as DH1 (SI Appendix, Fig. 1. Posterior oblique view of 3D model of the positive endocranial surface of the DH1 occipital fragment with oblique lighting applied and Fig. S12). This pattern is commonly seen in modern humans and features labeled: 1, tempero-occipital fissure; 2, parietal lobe; 3, beginning fossil hominins, including both Homo and Australopithecus, al- of sigmoid sulcus; 4, possible lunate sulcus; 5, inferior occipital sulcus; 6, though the greater degree of petalial asymmetry seen in H. naledi possible dorsal remnant of the lunate sulcus; 7, possible occipital polar sul- is most like that seen in modern humans and the larger fossil cus; 8, transverse sinus; 9, occipital pole; 10, midsagittal plane; and 11, cer- endocasts of later Homo. Greater variation in asymmetry within ebellar lobe. the human brain has been suggested to reflect a degree of adaptive plasticity than other living primates (27). In modern humans, left occipital petalia with right frontal petalia is asso- Appendix), resulting in water-displacement volumes of 555 mL ciated with righthandedness (28). for DH1 and 460 mL for DH3, both in good agreement with the One indicator of the posterior organization of the brain is the virtual reconstructions. position of the lunate sulcus. This sulcus is relatively well-marked The most notable morphological differences of the frontal in many endocasts of great apes, where its high, transversely lobes between humans and apes involve the inferior frontal and extensive and relatively rostral position marks the extent of the lateral orbital gyri. In apes, this area of the frontal lobes includes primary visual cortex. In living humans, the overall cortex is the fronto-orbital sulcus, which is usually well preserved on ape substantially larger, but the primary visual cortex is relatively less endocasts. A fronto-orbital sulcus is also evident on the MH1 enlarged than the cortex as a whole. The lunate sulcus in humans endocast of Australopithecus sediba (14) and on some endocasts is variable and less well represented on the cortical surface, but of Australopithecus africanus (15, 16).
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