Brain evolution in early Homo
Human brains are larger than and structurally different from the brains of the great apes. Ponce de León et al. explored the timing of the origins of the structurally modern human brain (see the Perspective by Beaudet). By comparing endocasts, representations of the inner surface of fossil brain cases, from early Homo from Africa, Georgia, and Southeast Asia, they show that these structural innovations emerged later than the first dispersal of the genus from Africa, and were probably in place by 1.7 to 1.5 million years ago. The modern humanlike brain organization emerged in cerebral regions thought to be related to toolmaking, social cognition, and language. Their findings suggest that brain reorganization was not a prerequisite for dispersals from Africa, and that there might have been more than one long-range dispersal of early Homo.
The brains of modern humans differ from those of great apes in size, shape, and cortical organization, notably in frontal lobe areas involved in complex cognitive tasks, such as social cognition, tool use, and language. When these differences arose during human evolution is a question of ongoing debate. Here, we show that the brains of early Homo from Africa and Western Asia (Dmanisi) retained a primitive, great ape–like organization of the frontal lobe. By contrast, African Homo younger than 1.5 million years ago, as well as all Southeast Asian Homo erectus, exhibited a more derived, humanlike brain organization. Frontal lobe reorganization, once considered a hallmark of earliest Homo in Africa, thus evolved comparatively late, and long after Homo first dispersed from Africa.
Human brains are substantially larger than those of our closest living relatives, the great apes, and also bear evidence of important structural reorganization, notably in cortical association areas related to higher cognitive functions, such as toolmaking and language capabilities (1, 2). Clarifying when these structural innovations appeared during human evolution remains a major challenge (3, 4). Brains do not fossilize, and so the only direct physical evidence for the actual course of brain evolution comes from natural or virtual fillings of fossil hominin brain cases, so-called endocasts, which show a complex but spatially reliable pattern of imprints representing cerebral gyri and sulci, as well as vascular structures surrounding the brain (5).
The endocranial region that holds key information about frontal lobe reorganization and possible language capabilities is Broca’s cap (BC), a bulge on the lateral fronto-orbital surface of endocasts (Fig. 1). BC is present on both human and great ape endocasts and often assumes similar morphologies (6, 7). However, the underlying brain areas are not the same across groups (7, 8) (Fig. 1). In great apes, BC largely comprises Brodmann area 44, and its inferior border is formed by the fronto-orbital sulcus (fo) (Fig. 1A). In humans, BC largely comprises Brodmann areas 45 and 47, and its inferior delimitation tends to coincide with the lateral orbital sulcus (9) (Fig. 1B). Inferring brain reorganization from the morphology of the BC region of fossil endocasts thus remains ambiguous. The BC of Australopithecus endocasts is typically interpreted as being delimited inferiorly by fo, indicating a great ape–like organization of the underlying brain areas (7). However, endocranial evidence from Australopithecus africanus and Australopithecus sediba has been interpreted as showing incipient reorganization of the frontal lobe (10, 11). This proposition has been challenged on various grounds (12, 13), such that basic questions about the timing and mode of the evolutionary transition from great ape–like to humanlike frontal lobe organization remain largely unanswered.
Cranial sutures are indicated in blue, cerebral sulci in red, and brain regions in other colors. (A) In great apes, the precentral sulcus (pc) crosses the coronal suture (CO), such that its inferior portion (pci) is located anterior to CO. The lunate sulcus (L) marks the anterior border of the primary visual cortex (Brodmann area 17). (B) In humans, evolutionary expansion of the inferior prefrontal cortex (IPF) resulted in a shift of the pci toward the posterior side of CO (red arrowheads). Concomitant expansion of the parietal bone resulted in anterior shift (blue arrowheads) of the apical portion of CO. Expansion of the posterior parietal cortex (PP) resulted in fragmentation and eventual disappearance of L. Numbers indicate Brodmann areas. Neurocranial structures: BC, Broca’s cap; CO, coronal suture; LA, lambdoid suture. Cerebral sulci: c, central; fi, inferior frontal; fs, superior frontal; fo, fronto-orbital; ip, intraparietal; lo, lateral orbital; pc (pcs/pci), precentral (superior/inferior); pt, postcentral; ts, superior temporal; s, Sylvian (lateral); L, lunate; R/Rʹ, ascending/horizontal rami of anterior lateral sulcus. Vascular structures: SS, sigmoid sinus; TS, transverse sinus. Figure was redrawn from (34, 35).
Uncertainties also exist regarding the evolutionary reorganization of the parieto-occipital cortex. All great ape brains exhibit a lunate sulcus (L), which marks the anterior boundary of the primary visual cortex (Brodmann area 17) (Fig. 1A), whereas human brains are characterized by complete loss of L (14), reflecting an expanded parieto-occipital cortex (13, 15) (Fig. 1B). L rarely leaves endocranial imprints (7, 16, 17), such that, in fossil hominin endocasts, absence of evidence of L is not evidence of absence, and it remains unclear when during human evolution this cortical area started expanding (3, 4, 7, 9, 18–20).
Traditionally, it has been assumed that a derived, humanlike organization of the frontal and parieto-occipital lobes (see legend of Fig. 1) characterizes the genus Homo from its beginnings (21–23). However, testing this hypothesis explicitly on fossil endocasts has proven difficult. The African fossil record extends back to the origins of Homo at around 2.8 million years ago (Ma) (24), but critical endocranial evidence is only preserved from ~1.8 Ma onward and represented by single finds dispersed in space and geological time (Table 1). This makes it difficult to identify diachronic trends in brain evolution against a background of interindividual variation in endocranial morphology. Homo erectus from Southeast Asia, on the other hand, is represented by numerous well-preserved neurocrania from a geographically restricted area, but with younger geological dates (25, 26) (Table 1).
The fossil hominins from the early Pleistocene site of Dmanisi, dated to 1.85 to 1.77 Ma (27, 28), play a key role in assessing brain reorganization in early Homo and its potential importance for hominin dispersals from Africa. Dmanisi has yielded five exceptionally well-preserved crania representing individuals from adolescence to old age, which likely represent natural variation in a paleodeme of early Homo (27, 29–32). Also, the site preserves a rich record of faunal remains and Mode I (Oldowan) lithic artifacts co-occurring in taphonomic context, which permits inferences on tool use and site-specific behaviors of the Dmanisi hominins and, more broadly, on subsistence strategies, social organization, and cognitive capabilities of early Homo (28, 30, 31).
Here, we track key changes in brain organization of early Homo from ~1.8 Ma onward by analyzing the endocranial morphology of the five Dmanisi specimens and reevaluating an extended comparative sample of African and Southeast Asian fossil endocasts (33) (Table 1). To identify primitive versus derived aspects of frontal lobe organization in fossil endocasts, we use the highly distinct cranio-cerebral topographies of humans and great apes as a frame of reference (Fig. 1) (34, 35). A characteristic signal of inferior frontal lobe expansion is the posterior shift of the inferior precentral sulcus (pci) relative to the coronal suture (CO) (35) (Fig. 1). Both structures are typically well represented on fossil endocasts, such that their topographical relationships reliably indicate frontal lobe reorganization (supplementary method M3). In addition, we use geometric morphometric methods to identify which endocranial and brain regions underwent differential expansion during frontal lobe reorganization (supplementary methods M4 and M5).
The Dmanisi endocasts
The endocast of the adult individual D2280 (Fig. 2A, fig. S1A, and supplementary text S1) is generally well preserved but lacks parts of the basicranial region. It has a rounded overall shape, with a comparatively wide anterior cranial fossa, and right occipital and left frontal petalia. The cerebellar fossa is large and bulges inferiorly. Imprints of the frontal sulci course toward the precentral sulcus (pc). This latter structure originates near the apex of the endocast, crosses the coronal suture at mid-height, and courses toward BC, such that its inferior portion (pci) lies anterior to the coronal suture.
(A to E) Left and right lateral, posterior, and superior views of (A) D2280, (B) D2282, (C) D2700, (D) D3444, and (E) D4500. Red, sulcal imprints; blue, sutures. Abbreviations are as in Fig. 1. SA, sagittal suture. Scale bar, 5 cm. (See also fig. S2.) In all specimens, the precentral sulcus (pc) crosses the coronal suture (CO), such that its inferior portion (pci) lies anterior to CO, indicating a primitive organization of the frontal lobe (see Fig. 1A).
The cranium of the adult individual D2282 (Fig. 2B, fig. S1B, and supplementary text S1) is fragmentary and exhibits substantial taphonomic distortion, which required digital retrodeformation and reconstruction. Petalial asymmetry cannot be ascertained. Several key endocranial structures are nevertheless visible. Similar to D2280, the endocranium is rounded and exhibits wide frontal lobes. The cerebellar fossa is only moderately bulging. On the left side, the precentral sulcus crosses the coronal suture at mid-height and courses toward the center of BC.
The endocranial cavity of the adolescent individual D2700 (Fig. 2C, fig. S1C, and supplementary text S1) is generally well preserved. Structural detail in the parietal and occipital region is blurred by a thin but dense calcite layer, which tightly adheres to the bone surface. In lateral and posterior views, the endocast appears rounded; in superior view, it presents a marked precoronal constriction, a feature that is often seen in Asian fossils attributed to H. erectus. The endocast exhibits left frontal petalia. The occipital poles are moderately projecting, and the cerebellar fossa is only moderately bulging. On both sides, the imprint of the medial frontal sulcus courses toward the coronal suture, where it reaches the precentral sulcus. The inferior portion of the precentral sulcus (pci) lies in front of the coronal suture and courses toward BC. Preservation of the endocranial base region permits estimation of cranial base angulation. The angle between landmarks basion, sella, and foramen caecum is 135° [cranial base angle CBA1 (36)]. The angle between the clivus plane and the midplane of the anterior cranial fossa (planum sphenoideum) is 124° [cranial base angle CBA4 (36)]. These values are at the upper end or above the range of variation of modern humans of similar dental age [CBA1, 132° to 137°; CBA4, 106° to 118° (37)].
The endocranial cavity of the edentulous cranium D3444 (Fig. 2D, fig. S1D, and supplementary text S1) suffered some taphonomic damage, such as dislocation of the left temporal pyramid, and loss of parts of the anterior cranial base and of the internal table on the left fronto-parietal region. The endocast has a globular shape that is similar to that of some modern human endocasts (Fig. 3) but exhibits precoronal constriction similar to D2700. The endocast exhibits slight right frontal petalia. The frontal sulci are represented by marked endocranial imprints, which course toward the imprint of the precentral sulcus. On both sides, the pci lies anterior to the coronal suture and courses toward the center of BC.
The central graph shows patterns of intragroup and intergroup variation in shape space. The surrounding panels visualize endocranial shapes at the extremes of the distribution. Shape component SC1 accounts for 57% of the total variation in the sample and captures major differences in endocranial shape between great apes and hominins, notably in relative width of frontal lobes (arrows) and in foramen magnum position. Shape component SC2 (10%) captures variation in endocranial length, height, and width relationships (arrows) within and among groups. Green stars, Pongo pygmaeus; red, Pan troglodytes (open squares, P. t. troglodytes; horizontal rectangles, P. t. verus; vertical rectangles, P. t. schweinfurthii); orange dots, P. paniscus; blue diamonds, Gorilla gorilla; filled circles, Australopithecus; open circles, African early Homo; triangles, Asian early Homo (left, upward, and downward triangles indicate Dmanisi, Northeast Asia, and Southeast Asia, respectively); + signs, mid- to late-Pleistocene African and European Homo; × signs, Homo neanderthalensis; black squares, modern Homo sapiens. Light and dark hues indicate immature and adult individuals, respectively. The 90% density ellipses are drawn for great ape species, modern H. sapiens, early Homo between 2 and 1 Ma (black outline), and H. neanderthalensis. For fossil specimen labels, see Table 1. Hexagons indicate the location in shape space of the visualized endocasts.
Cranium D4500, together with mandible D2600, represents the most complete skull of early Homo found to date (32). The endocast is fully preserved, except for a small area of the internal table in the occipital region (Fig. 2E, fig. S1E, and supplementary text S1). Sediment adhering to the middle and anterior cranial fossae was removed using synchrotron imaging and semiautomated image segmentation procedures (supplementary method M2). The D4500 endocast exhibits right occipital petalia. Precoronal constriction is marked, but the frontal lobes remain relatively wide. The frontal sulci are represented by marked imprints; they course toward the precentral sulcus, which is clearly represented on both sides of the endocast. The precentral sulcus crosses the coronal suture at mid-height, such that pci is located anterior to the coronal suture and courses toward BC. The occipital poles are protruding. The internal cranial base of D4500 is substantially less flexed than that of D2700, with a CBA1 of 156° and CBA4 of 144°. Both values are outside the range of variation of adult modern humans.
Altogether, the Dmanisi endocasts indicate a consistent topographic pattern of external cortical morphology, where the precentral sulcus crosses the coronal suture such that its inferior portion is anterior to the suture and courses toward BC (Fig. 2, Table 1, and fig. S1). Using great ape and human cranio-cerebral topographies as a reference (Fig. 1), the Dmanisi individuals largely reflect a great ape pattern of frontal lobe organization, in which BC is delimited inferiorly by the fronto-orbital sulcus and likely housed Brodmann cortical area 44 and parts of area 45 (Fig. 1A).
Endocasts of African and East Asian Homo fossils
A comparative analysis of the endocasts of early to mid-Pleistocene Homo fossils from Africa reveals greater endocranial topographic diversity (Table 1, supplementary text S2, and fig. S2). Specimens KNM-ER1805 and KNM-ER1813, with disputed taxonomic affiliation but dated to before ~1.7 Ma, show endocranial imprints that are compatible with a great ape–like organization of the frontal lobe (fig. S2, A and B). Specimen KNM-ER 1470 (fig. S2C), which has been put forward as key evidence for a derived frontal lobe organization (21), is too fragmented to reveal diagnostic endocranial imprints. The endocasts of fossils dated to ~1.7 to 1.5 Ma, and variably attributed to Homo ergaster or H. erectus, show variation in frontal endocranial topography that suggests a range of primitive to derived frontal lobe morphologies (fig. S2, D to F). By contrast, African fossils younger than ~1.5 Ma exhibit endocranial topographies that are compatible with a derived, modern human–like frontal lobe organization (Table 1 and supplementary text S2).
The endocasts of H. erectus from Java typically exhibit marked imprints of the frontal sulci, whereas imprints of the precentral and central sulci are faint to absent. In all specimens reexamined here, imprints of the inferior and/or middle frontal sulci course anteroposteriorly to reach the coronal suture (Table 1, supplementary text S3, and fig. S3, A to E). This topography constrains the inferior precentral sulcus to a location that either roughly coincides with the coronal suture or is posterior to it, thus representing a derived organization of the frontal lobe. The endocasts of Chinese H. erectus, represented here by Zhoukoudian XII (fig. S3F) and Hexian, exhibit a clearly derived topography of the frontal lobe region (supplementary text S3).
Endocranial shape, size, and topography
Figure 3 shows endocranial shape variation in fossil Homo and in a comparative sample of great apes and modern humans (see supplementary method M4). Great ape endocrania are low but wide in the parietal region and exhibit a tapering frontal region and a posteriorly situated foramen magnum. Modern human endocrania are comparatively high and have wide frontal lobes and an inferiorly situated foramen magnum. The great ape–human contrast in endocranial shape is largely an effect of variation in relative encephalization [measured here as brain size relative to the size of the cranial base and face (38)] (fig. S4). Fossil hominin endocrania occupy the region in morphospace between great apes and humans. Endocranial shape in the genus Homo between 2 and 1 Ma shows wide intragroup and intergroup variation (Fig. 3). Variation in the Dmanisi sample is congruent in range and pattern with intragroup variation in other taxa (fig. S5).
Correlating our data about endocranial topography (Table 1) with geological dates permits inferences on the timing of frontal lobe reorganization and its possible correlation with brain expansion and changes in brain shape (Fig. 4). The transition from primitive to derived frontal lobe morphologies likely took place during the time between 1.7 and 1.5 Ma, with derived morphologies largely established in the fossil record after 1.5 Ma. During that time interval, frontal lobe reorganization occurred in tandem with brain expansion (Fig. 4A and Table 1) [mean endocranial volume (ECV) increased from 650 to 830 cm3]. It is likely that the two processes had similar evolutionary causes. However, the possible presence of derived frontal lobe morphologies in small-brained (ECV ~460 cm3) but geologically younger fossils, such as H. floresiensis and H. naledi (9) (supplementary text S4), suggests that frontal lobe organization is not mechanistically linked to large brain volumes.
(A) Changes in ECV and craniocerebral topography over the past 2 Ma. Orange, gray, and turquoise symbols indicate the position of the inferior precentral sulcus (pci) anterior to, coincident with, and posterior to the coronal suture (CO), respectively (see inset graph). White symbols indicate missing or indeterminate data. Circles indicate Africa, left-facing triangles indicate Western Asia and Europe, and upward and downward triangles indicate Northeast and Southeast Asia, respectively (see inset world map). Dashed symbols indicate immature specimens, and horizontal lines indicate geological age ranges. (B) Endocranial shape change associated with frontal lobe reorganization (left lateral view). Colors denote above-average expansion (green) and bulging (yellow) of the endocranial surface, indicating differential enlargement of labeled brain regions (IPF, inferior prefrontal cortex; 45/47, Brodmann areas 45/47; PP, posterior parietal cortex; T, temporal lobe, O, occipital lobe). Also note endocranial surface expansion along the transverse sinus (TS). Brain sulci (red): fs/fi, superior/inferior frontal; pc/c/pt, precentral/central/postcentral; s, Sylvian; ip, intraparietal.
Our data further indicate that the transition from primitive to derived frontal lobe organization was accompanied by specific changes in endocranial shape (Fig. 4B and supplementary method M5). The posterior shift of pci (Fig. 4A) is associated with differential expansion of the inferior prefrontal (IPF) region (Figs. 1 and 4B). Furthermore, expansion of IPF is correlated with marked expansion of the posterior parietal (PP) and occipital (O) cortical regions.