Evolution of early Homo: An integrated biological perspective

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Science  04 Jul 2014:
Vol. 345, Issue 6192, 1236828
DOI: 10.1126/science.1236828

Structured Abstract


Until recently, the evolution of the genus Homo has been interpreted in the context of the onset of African aridity and the expansion of open grasslands. Homo erectus was considered to be a bona fide member of the genus Homo, but opinions diverged on the generic status of earlier, more fragmentary fossils traditionally attributed to Homo habilis and Homo rudolfensis. Arguments about generic status of these taxa rested on inferred similarities and differences in adaptive plateau. However, there was near-universal agreement that the open-country suite of features inferred for Homo erectus had evolved together and provided the adaptations for dispersal beyond Africa. These features foreshadowed those of more recent Homo sapiens and included large, linear bodies, elongated legs, large brain sizes, reduced sexual dimorphism, increased carnivory, and unique life history traits (e.g., extended ontogeny and longevity) as well as toolmaking and increased social cooperation.

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Hominin evolution from 3.0 to 1.5 Ma. (Species) Currently known species temporal ranges for Pa, Paranthropus aethiopicus; Pb, P. boisei; Pr, P. robustus; A afr, Australopithecus africanus; Ag, A. garhi; As, A. sediba; H sp., early Homo >2.1 million years ago (Ma); 1470 group and 1813 group representing a new interpretation of the traditionally recognized H. habilis and H. rudolfensis; and He, H. erectus. He (D) indicates H. erectus from Dmanisi. (Behavior) Icons indicate from the bottom the first appearance of stone tools (the Oldowan technology) at ~2.6 Ma, the dispersal of Homo to Eurasia at ~1.85 Ma, and the appearance of the Acheulean technology at ~1.76 Ma. The number of contemporaneous hominin taxa during this period reflects different strategies of adaptation to habitat variability. The cultural milestones do not correlate with the known first appearances of any of the currently recognized Homo taxa.


Over the past decade, new fossil discoveries and new lines of interpretation have substantially altered this interpretation. New environmental data sets suggest that Homo evolved against a background of long periods of habitat unpredictability that were superimposed on the underlying aridity trend. New fossils support the presence of multiple groups of early Homo that overlap in body, brain, and tooth size and challenge the traditional interpretation of H. habilis and H. rudolfensis as representing small and large morphs, respectively. Because of a fragmentary and distorted type specimen for H. habilis two informal morphs are proposed, the 1813 group and the 1470 group, that are distinguished on the basis of facial anatomy but do not contain the same constituent fossils as the more formally designated species of early Homo. Furthermore, traits once thought to define early Homo, particularly H. erectus, did not arise as a single package. Some features once considered characteristic of Homo are found in Australopithecus (e.g., long hind limbs), whereas others do not occur until much later in time (e.g., narrow pelves and extended ontogeny). When integrated with our understanding of the biology of living humans and other mammals, the fossil and archaeological record of early Homo suggests that key factors to the success and expansion of the genus rested on dietary flexibility in unpredictable environments, which, along with cooperative breeding and flexibility in development, allowed range expansion and reduced mortality risks.


Although more fossils and archaeological finds will continue to enhance our understanding of the evolution of early Homo, the comparative biology of mammals (including humans) will continue to provide valuable frameworks for the interpretation of existing material. This comparative context enables us to formulate and test robust models of the relationships between energetics, life history, brain and body size, diet, mortality, and resource variability and thereby yield a deeper understanding of human evolution.

Pleistocene people and environments

In the past few decades, hundreds of hominin fossils have been recovered from well-dated sites in East Africa. In addition, early representatives from far outside Africa have been found in Asia and Europe. Recently, discoveries at Malapa in South Africa and at Dmanisi in western Asia have brought important new fossils and archaeological residues to light. Analyses of local stratigraphy, windblown dust, sea and lake cores, and stable isotopic analyses have improved the reconstruction of ancient environments inhabited by early humans. Antón et al. review recent evidence and arguments about the evolution of early Homo, arguing that habitat instability and fragmentation imposed an important selective force.

Science, this issue p. 10.1126/science.1236828


Integration of evidence over the past decade has revised understandings about the major adaptations underlying the origin and early evolution of the genus Homo. Many features associated with Homo sapiens, including our large linear bodies, elongated hind limbs, large energy-expensive brains, reduced sexual dimorphism, increased carnivory, and unique life history traits, were once thought to have evolved near the origin of the genus in response to heightened aridity and open habitats in Africa. However, recent analyses of fossil, archaeological, and environmental data indicate that such traits did not arise as a single package. Instead, some arose substantially earlier and some later than previously thought. From ~2.5 to 1.5 million years ago, three lineages of early Homo evolved in a context of habitat instability and fragmentation on seasonal, intergenerational, and evolutionary time scales. These contexts gave a selective advantage to traits, such as dietary flexibility and larger body size, that facilitated survival in shifting environments.

The evolution of the genus Homo has long been linked to the onset of African aridity, and the evolution of key features such as increased carnivory, brain enlargement, long-distance mobility, and prolonged life history. These features have been explained as a response to the progressive expansion of open, grassland habitats (1, 2). However, new environmental data challenge this interpretation, and archaeological research has identified behaviors in early toolmakers that aided flexible responses to dynamic environments (3, 4). Furthermore, comparative studies of mammalian development, energetics, ecology, and behavior offer new interpretive models. In this context, new fossils have also expanded the known range of morphological variation, raising questions about the number of species of early Homo and the distinction between inter- and intraspecific adaptations (510).

The East African fossil record continues to command much attention because of a unique combination of factors. The history of East African rift volcanism enables precise geochronological analyses through long stratigraphic sequences rich in fossil and archaeological remains. The temporal sequence of morphological and behavioral innovations in early Homo is thus more finely resolved in East Africa than elsewhere. Environmental indicators can also be measured in lengthy stratigraphic order, enabling researchers to assess climate and habitat dynamics at a variety of time scales rather than relying on more limited environmental snapshots or broadly time-averaged portraits of the environment. Uncertainties over stratigraphic correlation and dating have arisen that directly affect an understanding of early Homo, yet East African rift basins typically offer opportunities to resolve the geological debates [e.g., (11, 12)]. Beyond this region, important recent finds pertinent to the evolution of Homo have been made at Malapa, South Africa (6, 7, 9, 13), and Dmanisi, Georgia (8), which expand how hominin morphological variation and the dispersal of early Homo beyond Africa are understood. This review begins with a focus on morphological variation and environmental dynamics because these topics have strongly affected analyses of the adaptive shifts distinctive to early Homo (Fig. 1).

Fig. 1 Hominin evolution, diet, landscape vegetation, and climate dynamics from 3.0 to 1.5 Ma.

(A) Currently known species temporal ranges for Pa, Paranthropus aethiopicus; Pb, P. boisei; Pr, P. robustus; Aafr, Australopithecus africanus; Ag, A. garhi; As, A. sediba; H sp., early Homo > 2.1 Ma; 1470 and 1813 groups, see text for definitions (traditionally classified as H. rudolfensis and H. habilis, respectively); and He, H. erectus. The temporal position of Dmanisi H. erectus, He (D), is indicated. (B) Icons representing the first appearance of (from bottom) Oldowan technology (~2.6 Ma), Homo dispersal to Eurasia (~1.85 Ma), and Acheulean technology (~1.76 Ma). Horizontal pale green lines mark these times across (A) to (D). (C) Homo tooth δ13C. Carbon isotopic values measured on tooth enamel of East African specimens assigned to Homo and P. boisei (21); the mean and range of dental δ13C for A. africanus is also shown (22). (D) East African paleosol δ13C: compilation of δ13C values for East African fossil soil carbonates [data compiled in (74)]. Values range from those typical of woodland (40 to 80% woody cover) to wooded grassland (10 to 40% woody cover) to grassland (0 to 10% woody cover). Woody cover estimates based on (2). (E) Climate variability. Alternating intervals of high (lighter color bands) and low (darker color bands) climate variability based on predicted insolation resulting from the modulation of orbital precession by eccentricity, where low variability is defined by eccentricity ε ≤ 0.0145, (i.e., 1 SD below mean ε for the past 5 million years) (67). White circles show the standard deviations for terrigenous dust flux values at Ocean Drilling Project sites 721 and 722, western Arabian Sea (64, 69). Change between eolian dust standard deviations (adjacent white circles) follows the predicted direction between alternating high (larger SD, further to the right) and low (smaller SD, further to the left) climate variability for 13 of the 16 variability transitions. For example, the large SD in the two predicted high climate variability intervals, 2.79 to 2.47 and 2.37 to 2.08 Ma, is further to the right of the plot than is the intervening small SD in the predicted low-variability interval 2.47 to 2.37 Ma.

Who was early Homo?

Throughout the 20th century, the definition of Homo was expanded to accommodate fossil specimens increasingly remote from Homo sapiens in both time and morphology [e.g., (14, 15)]. Landmarks include collapsing multiple genera into Homo erectus in the 1940s, naming Homo habilis in 1964, and establishing Homo rudolfensis in 1986 (14, 16, 17). However, the status of pre-erectus Homo has always been controversial, and by the late 1990s the perceived similarities between fossil remains of Australopithecus (especially A. afarensis, e.g., A.L. 288-1; “Lucy”) and non-erectus early Homo (e.g., fossil specimens KNM-ER 1470 and 1813) led some to reclassify both H. habilis and H. rudolfensis as Australopithecus (18, 19) and more recently to suggest that they might belong to a new, unspecified genus (20). Alternatively, anatomical variation within early H. erectus at Dmanisi has been used to argue not only for the inclusion of these specimens in early Homo but for the inclusion of all early Homo in a single species, H. erectus (8).

The argument for excluding non-erectus Homo from the genus rested heavily on differences in adaptive plateau, particularly dietary adaptation, and locomotor efficiency inferred from aspects of postcranial anatomy. However, for all hominins subsequent to ~3.5 million years ago (Ma) new isotopic studies identify a diverse diet incorporating a broad range of plants using the C3 and C4 photosynthetic pathways (21, 22) (Fig. 1C). Furthermore, large-bodied finds of Australopithecus (23) and small-bodied Homo show no difference in hind limb proportions or inferred bipedal efficiency; this is because locomotor efficiency in walking and running is a function of leg length, which is allometrically related to body size (24). Similarly, the A. afarensis foot possessed close-packed arches, another sign of bipedal adequacy (25, 26). Although there may have been multiple modes of bipedality among the early hominins, long legs and efficient bipedal locomotion were in place well before the origin of the genus Homo and cannot necessarily be used to distinguish among genera or species. Regardless of the taxonomy of early Homo or morphological differences between species, recent fossil finds and new analytical techniques suggest that all early Homo differ from Australopithecus in having larger average body and brain sizes (Table 1).

Table 1 Comparative brain and body size of Australopithecus and Homo based on the most complete specimens in each group.

See Box 1 for a discussion of how body and brain size ranges may change based on the size of more fragmentary remains in each assemblage. The 1470 and 1813 groups in particular are skewed to larger and smaller sizes, respectively, by considering only their more complete members. Individual data points included in these species’ means can be found in table S2. Sources for endocranial capacity data are as follows: A. sediba (6); A. africanus (127); A. afarensis (128); Homo, as indicated in table S2 of this paper. The apparent difference in cranial capacity between the 1470 and 1813 groups is due to the fact that only a single large cranium, KNM-ER 1470, contributes to the capacity for that group. Dental measurement definitions and most data are from (41); A. afarensis, from (129); A. sediba, as above; newer Homo data not in 41 follow (5, 32, 130). I1, upper incisor 1; I1, lower incisor 1. Body mass estimates from orbital dimensions are from (131, 132). The values presented are the range of individual predicted values; the mean of individual predicted values rounded to whole values; and the total range of the 95% confidence intervals for all individual values. The Kappelman values are predicted from orbital area. The Aiello and Wood values are predicted from orbital height dimensions and hominoid predictive equations. The apparent difference in body mass between 1470 and 1813 groups is because only a single large cranium, KNM-ER 1470, contributes to the body mass estimate for that group. Postcranial body mass estimates follow (24) and table S2 of this paper. The East Africa unattributed non-erectus Homo group includes H. habilis. CV, coefficient of variation; CI, confidence interval; dash entries, not applicable or no fossils or data available.

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Given these observations, what is the evidence for distinct morphological groups in the fossil record of Homo before and contemporaneous with H. erectus? The earliest fossils assignable to Homo are fragmentary and identified by reduced tooth and jaw size and the shape and reorganization of craniofacial morphology (supplementary materials) (5, 10, 2732). Among the oldest and most complete are likely to be the A.L. 666 maxilla from Ethiopia (~2.33 Ma), which has some affinities to hominins traditionally called H. habilis (33), and the UR–501 mandible [2.5 to 1.9 Ma; (29, 34)] from Malawi, which is more robust and similar to mandibles (i.e., KNM-ER 1802) often included in H. rudolfensis. A few South African fossils over 2.1 Ma also may be attributed to early Homo, although they are usually considered Australopithecus (3539). Brain size and postcranial anatomy are largely unknown for this period.

There are many more early Homo specimens between 2.1 and 1.5 Ma, as well as new contenders for relatives of Homo. The recently discovered Australopithecus sediba (~1.98 Ma) from Malapa, South Africa, is argued to possess a unique relationship to the origin of Homo because of a number of Homo-like features of its cranial and postcranial anatomy, particularly a reduction in dental size and aspects of its pelvis and lower thorax, although it differs from Homo in cranial capacity, facial shape, and aspects of the postcranial skeleton (6, 7, 13). In addition to A. sediba, at least one group of early Homo is likely present in South Africa, based on dental anatomy (35, 39), although the highly fragmentary nature of the remains make associations with East African forms speculative.

East African non-erectus Homo from this period has been assigned previously to either H. habilis or H. rudolfensis, which were often considered to represent small- and large-brained (and -bodied) species, respectively (19, 32, 40, 41). New fossils from Lake Turkana, Kenya (KNM-ER 60000 and 62000), suggest multiple species of non-erectus Homo just after 2.1 Ma but show that the two species cannot be distinguished on the basis of cranial size (5). The new Kenyan fossils suggest that palate and mandibular shape, especially the relative position of the anterior dentition, differentiate among the two better known groups of early Homo; yet taphonomic damage to the OH 7 mandible, the type specimen for H. habilis, and the fact that size may no longer be a distinguishing feature of different species of early Homo preclude an easy answer to the attribution of the type. This poses nomenclatural problems because it is unclear to which group, if either, the nomen H. habilis applies (5). We therefore recommend informally calling the morphological groups of early non-erectus Homo after their most iconic specimens (10). Thus, the 1470 group (2.09 to 1.78 Ma, table S1) is named for KNM-ER 1470 and is distinguished particularly by its short and flat anterior dental arcade (with a short premolar row and flat anterior tooth row) and by a relatively tall, flat face. The 1813 group (2.09 to 1.44 Ma) has a more primitive face with a round and more projecting anterior palate and is named for KNM-ER 1813.

We emphasize that these groups do not comprise the same fossils as previously attributed to H. rudolfensis and H. habilis. Fossils with large teeth but primitive arcade structures (such as KNM-ER 1802) are definitively excluded from the 1470 group, and large fossils (such as KNM-ER 1590) that were once grouped with KNM-ER 1470 on the basis of size alone are now unaffiliated because they do not preserve critical anatomical areas. As a result of these reassignments, both the 1813 and 1470 groups exhibit considerable and overlapping size variation. In particular, molar size, facial size (but not shape), and very likely endocranial and body size cannot be used to distinguish the 1813 and 1470 groups (Box 1, supplementary text, and table S2) as they once were used to distinguish H. habilis and H. rudolfensis.

Box 1

Anatomical features of early Homo groups

Fragmentary fossils provide the hard evidence for the anatomy and variation within early Homo. Making inferences regarding the number of groups is a nontrivial exercise that relies on careful assessments of anatomical similarity and the recognition of differences in morphological traits and their patterning across fossil assemblages. The main anatomical features of the three groups of early Homo and their fossil group members are summarized below, and in the supplementary text we provide additional discussion of the fossils that compose these groups and those that we currently cannot assign to a group because of missing evidence.

(A) The 1470 group is defined by the derived shape of the face, which is relatively tall and flat with the incisor/canine row squared off and the upper third premolar forming the corner of the anterior palate. Lower incisors are narrow. Premolars are mesiodistally narrow and molars are large but just slightly larger than average for all early Homo. There is no third molar reduction. The vault is rounded and lacks a posttoral/supratoral gutter. The posterior mandible (bigonial/bicondylar breadths) is wide relative to arcade breadth, and the corpus is relatively tall. Only the largest specimen, KNM-ER 1470, allows actual estimates of brain size (750 cm3) or body size (43 to 63 kg, from the orbit), but differences in size between KNM-ER 1470 and the more fragmentary KNM-ER 62000 suggest that the lower range of brain and body size is substantially less. Given that facial dimensions of KNM-ER 62000 are between 75 and 80% of those of KNM-ER 1470, we cautiously suggest ranges of 560 to 750 cm3 and 35 to 50 kg for this group.

Key members: cranium KNM-ER 1470; partial face 62000; mandibles KNM-ER 1482 and 60000. No postcranial remains are affiliated with this group.

Important exclusions: Mandibles KNM-ER 1802 and Uraha 501 are definitively excluded from this group on the basis of arcade shape and a mismatch with the palate of KNM-ER 62000 (5). Cranial specimens once included with the group on the basis of large cranial and dental size, especially KNM-ER 1590, have insufficient preservation in key areas (mandible and face) to allow an assessment of palate or mandibular shape. These certain and probable exclusions remove evidence for extremely large molar size in this group.

(B) The 1813 group presents a more primitive facial architecture with a rounded anterior palate and more parallel and narrow posterior tooth rows. Lower incisors are broader than in the 1470 group (uppers are unknown for the 1470 group). Molars are about the size of or slightly smaller than the 1470 group; however, if the large-molared KNM-ER 1802 is included, as we suspect it should be, these differences disappear entirely. There is no third molar reduction. Mandibular height and width are similar; rami are essentially unknown. The vault is rounded with some posterior occipital cresting in some individuals (e.g., KNM-ER 1805). Brain size estimates from the best preserved of these yield a range of 510 to 660 cm3; however, because the OH 65 palate (which does not preserve the cranial vault) is about 15% bigger than that of OH 13 (which is associated with a vault of 660 cm3), we cautiously suggest that the upper range may increase to as much as 775 cm3. Cross-sectional data indicate the group had relatively strong upper limbs compared with lower limb strength, suggesting a sustained arboreal component (perhaps related to nesting) in addition to their terrestrial locomotor repertoire (134). Body size estimates are available from only the smallest specimens (e.g., KNM-ER 1813 from orbital dimensions and OH 62 from the postcranial skeleton) and suggest ranges of 30 to 35 kg. The size of OH 65 relative to KNM-ER 1813 suggests that the upper range of these should be extended to at least 42 kg.

Key members: crania KNM-ER 1813, OH 24; partial crania and mandible KNM-ER 1805, OH 13; palate OH 65; fragmentary cranial and postcranial KNM-ER 3735, OH 62.

Likely members: Mandible KNM-ER 1802 and Uraha 501 are definitively excluded from the 1470-group and are consistent with palate shape in the 1813 group. However, because they are more robust and because OH 7 remains unaffiliated, leaving open the possibility of a third group of non-erectus Homo, we suggest they are likely but not certain members of the 1813 group.

Important unknowns: OH 7 cannot be definitively affiliated with any group. Although the specimen retains a mandible and dentition, extensive postmortem deformation and distortion to the mandibular symphysis and body leave the relationships among and between the anterior and posterior tooth rows unresolved. It is thus currently impossible to assess the fossil for the key features of arcade shape and orientation that distinguish the 1813 and 1470 groups.

(C) Early H. erectus is a represented by a greater number of fossil crania and a larger geographic distribution of samples. The face and dental arcade lacks the derived anatomy of the 1470 group arcade, being in some ways more similar to the 1813 group with the rounded anterior palate and large incisors. However, unlike this group posterior arcade shape is more derived, with broader more parabolic tooth rows and third molar crown reduction. The canines (especially roots) and premolars are also reduced relative to the condition in the 1813 group (but the premolars are not narrow as in 1470 group). The mandibular body is more gracile than in the 1813 group. The vault is rounded but presents a variable series of superstructures (some size-related) including supraorbital tori and posttoral/supratoral gutter, bregmatic and sagittal keels, and angular and occipital tori; however, cresting is not seen. The petrous temporal is angulated around the glenoid fossa. Shaft cross-sectional data suggest relatively less strong upper limb to lower limb development, which has been suggested to reflect greater terrestriality than in the 1813 group (133). Between 1.9 and 1.5 Ma, substantial regional population variation in size exists, but taken together the brain size estimates from the best preserved of these yield a range of 546 to 1067 cm3, and postcranial body mass estimates suggest ranges of 40 to 68 kg.

Key members from Africa and Georgia: crania and calvaria KNM-ER 3733, KNM-ER 3883, and KNM-ER 42700, OH 9, and Dmanisi 2280; crania and associated mandibles Dmanisi 2282/211, 2700/2735, and 3444/3900; crania and associated postcrania KNM-ER 1808 and 15000.

In contrast with these groups, but partly overlapping them in time, is early African H. erectus (~1.89 to 0.90 Ma), which has been traditionally distinguished from non-erectus early Homo on the basis of dental anatomy, craniofacial morphology, and average cranial and body size [e.g., (10, 42, 43); see Box 1]. Cranial fossils KNM-ER 42700 and KNM OG 45500 substantially extend the lower end of the size range, overlapping with non-erectus early Homo (32, 44). Postcranial fossils from Gona, Ethiopia (45), and reevaluation of the KNM–WT 15000 skeleton (46) suggest small-size individuals, as well as a less-linear body form than previously thought. Early H. erectus is best known from East Africa, although there are hints of its presence in South Africa (39, 44, 4751). Shortly after its appearance in Africa, H. erectus is also found at Dmanisi, Georgia (52); Java, Indonesia (53, 54); and possibly Yuanmou, China (55); providing evidence of range expansion across Asia. Individual and regional variations exist, including substantial variation in size, especially between the Georgian and some African fossils (32, 44, 56). However, there is growing consensus that these represent regional morphs of a single species (42, 57, 58).

New fossils from Dmanisi, Georgia (~1.8 Ma), exhibit a range of variation that is argued to encompass not only that seen in early African H. erectus but also that of all other early African Homo as well (8). The five Dmanisi crania, some with associated postcranial remains, exhibit derived characters of H. erectus but also retain some primitive characteristics, including small brain sizes (538 to 750 cm3), suggesting they are part of an early dispersal of that species. A global analysis of craniofacial size and shape was used to argue that this expanded range of variation encompassed all three morphs of African Homo (i.e., 1470 and 1813 groups and H. erectus) (8) and thus that only a single lineage of Homo existed and perhaps even originated at Dmanisi. However, this metric analysis of overall cranial shape misses the specific characters, as described above (supplementary materials and Box 1), that distinguish these groups and cannot, therefore, be used to disprove their existence (20, 59). Although we concur that a more robust fossil record is surely necessary, we conclude that three distinct lineages of early Homo in Africa remains the most compelling hypothesis.

Thus, the East African fossil record provides evidence of at least three partly contemporary species of Homo from ~2 to 1.5 Ma, all of which exhibit, on average, larger brains and bodies than Australopithecus (Table 1). Non-erectus early Homo (i.e., both 1470 and 1813 groups) is about 30% bigger in brain and 10% bigger in body size than Australopithecus. Early African and Georgian H. erectus together are about 40% bigger in brain and 25% in body size than Australopithecus. Early H. erectus is 20% bigger in brain and 15% in body than the combined 1470 and 1813 groups. Importantly, ranges of variation overlap substantially, and there is also no discernible difference in sexual dimorphism between species or genera (24, 6062) (Tables 2 and 3).

Table 2 Differences between Australopithecus and Homo and within early Homo based on empirical fossil and archaeological evidence.

These differences may relate to life history inferences made in Table 3. A. afarensis is used as a conservative comparator because it has the largest average brain (128) and body sizes (24) of the more complete Australopithecus species. Non-erectus early Homo includes specimens in the 1470 and 1813 groups and non-erectus early Homo fossils not yet attributed to either of the former groups. Early H. erectus values are the combined means for Dmanisi and early African H. erectus as a conservative comparison with A. afarensis, followed by the early African H. erectus–only values. Age at M1 eruption is available only for the early African H. erectus remains. Basal metabolic rate (BMR) is calculated by using the Oxford equations for prime adults (18 to 30 years) and the average body weight of each species. The average of male (16 × weight + 545) and female (13.1 × weight + 558) equations is used (61). TDEE range is calculated as TDEE = BMR * PAL (physical activity level). A range of PALs from apelike (1.7) (137) to humanlike (1.9; the mean of male, 1.98, and female, 1.82, averages for subsistence populations) (138) are used. Lower mean values for Pan have been reported (1.5) (139), but given the high range of variation we use the more conservative values.

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Table 3 Inferences regarding physiological, behavioral, and ecological differences between Australopithecus and Homo.

These comparisons have their basis in empirical evidence noted in Table 2 and comparative biological models noted in the text.

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The Dmanisi fossils, as well as A. sediba, highlight the importance and the difficulties of recognizing and distinguishing two important aspects of variation in early Homo: variation within and between species. The Dmanisi remains, along with small-sized remains from East Africa, have expanded the range of size variation within H. erectus, highlighted the notion of population-level variation within that taxon, and blurred at least the size distinctions among morphological groups of early Homo. The mosaic of features in A. sediba (~1.98 Ma) and variation in the Dmanisi H. erectus sample (~1.8 Ma), both of which are contemporaneous with the three African groups, suggest that the early diversification of Homo was a period of morphological experimentation. The potential malleability of developmental processes and the role of vicariance and hybridization in evolving and testing reproductive and correlated morphological distinctions remain important sources of uncertainty, although ones potentially ripe for future evaluation through integration of data from extant biological forms.

Environmental instability as an evolutionary paradigm

The intra- and intertaxon diversity observed in early hominins cannot be understood apart from its environmental context. A long-standing view is that human evolution was linked to the onset of global cooling, progressive African aridity, and C4 grass–dominated open vegetation habitats (1, 6365). Accordingly, the spread of African savanna grasslands set the selection pressures that favored stone toolmaking, increased carnivory, and other adaptive characteristics of early Homo as a member of the African arid-adapted fauna (6466). However, a current synthesis of stratigraphic, eolian dust, lake, faunal, stable isotopic, volcanologic, and tectonic data results in a far more dynamic picture of East African environments in which fluctuating moisture and aridity, shifting resource regimes, and spatial heterogeneity were the dominant features of the settings in which early Homo evolved (4, 6770). In contrast to the traditional model of a stable or progressively arid savanna, evidence of climate and landscape variability highlights a different set of adaptive problems in which capacities to buffer and adjust to environmental dynamics at diverse temporal and spatial scales were at a premium in hominin and other contemporaneous animal populations (67, 71).

Although eolian dust in marine drill cores and limited isotopic data sets from the Turkana Basin, Kenya, have previously been used to emphasize the aridity trend between 3.0 and 1.5 Ma (64), the broader range of data now available emphasizes the wide diversity of vegetational settings and moisture regimes in which Homo emerged (7276) (Fig. 1, D and E). Improved efforts to quantify past and present East African habitats consider savanna to comprise from 5 to 80% woody cover (2), illustrating the potential role of highly diverse habitats in creating speciation opportunities and selective conditions favoring hominin adaptive versatility (4, 73, 77, 78).

Large lake fluctuations during times of strengthened monsoon intensity (68, 77, 79, 80) along with volcanism and tectonic impacts (81) were sources of instability in East African landscapes and ecological settings. The tempo of wet-dry variability for tropical Africa was governed by ~20,000-year cycles of orbital precession, whereas variation in Earth’s eccentricity on cycles ~100,000 and 413,000 years long altered the long-term pattern of seasonal precipitation intensity and duration. There is thus a causal connection between seasonal variability and longer phases of climate variability over evolutionary time. The modulation of precession by eccentricity defines a predictive pattern of episodic increases and decreases in seasonal monsoon intensity and alternating periods of high climate variability and shorter periods of relative stability over the past several million years in East Africa (67, 69, 72) (Fig. 1E). Arabian Sea eolian dust flux and Mediterranean sapropel intensity are two high-resolution data sets that exhibit this pattern (69, 72), and stratigraphic sequences at well-studied, early to mid-Pleistocene Homo sites at East Turkana, Olduvai, and Olorgesailie indicate that this high/low-variability pattern was imprinted on the geological landscapes of East Africa (67, 8285).

Although certain data sets [e.g., eolian dust and carbon isotope ratio (δ13C) of soil carbonates] are keenly sensitive to aridity and others (e.g., distribution of lacustrine deposits and diatom stratigraphies) to moisture and lake expansion, the shifting pattern of environmental dynamics over seasonal-to-orbital time scales becomes apparent when uniting the multiple indicators (67). The alternation of high and low climate variability implies that periods of relatively stable environment and the aridity trend were interrupted by lengthy intervals of pronounced habitat unpredictability and resource uncertainty. Although individual organisms experienced extensive seasonal fluctuation, persistent gene pools evolved in the context of long-term revamping of resource landscapes and inconsistent timing and intensity of seasonal rainfall in tropical Africa. Accordingly, environmental instability, which included heightened aridity and humidity phases, defined the overall adaptive setting in which key benchmarks of dietary, developmental, cognitive, and social adaptability evolved in early Homo.

The paleobiology of early Homo

We argue that the origin and evolution of early Homo is related to the accommodation of these novel and/or unpredictable environments over time and space. Specifically, increases in average body and brain size and changing dental size coupled with increased toolmaking and stone transport suggest dietary expansion, developmental plasticity, cognitive evolution, and social investments (see Tables 1 to 3 for relevant data). Together these features and behaviors enabled successful accommodation of these changing environments.

Diet, stone transport, and toolmaking

Isotopic analysis indicates a shift from reliance on C3-based foods in early Australopithecus (~4 Ma) to a more diverse diet incorporating a broader range of C3- and C4-based foods in both Australopithecus and Homo lineages but in different proportions (21, 22) (Fig. 1C). In the same geographical area, East African Homo has a diet that is 78% broader than contemporaneous Paranthropus, which specialized in more C4 [and/or crassulacean acid metabolism (CAM)] foods. However, East African Homo has a dietary breadth that is only 63% that of A. afarensis and 79% that of A. africanus. This suggests that it is not dietary breadth as reflected in isotopic breadth that was important in the evolution of Homo, but rather the inclusion of a broader range of food stuffs within a narrower isotopic range. Hard evidence for this in early Homo dental morphology suggests a shift toward incisal preparation and molar shearing, which may indicate the incorporation of tough-plant products or animal tissues (86). In H. erectus, smaller incisors and molars, together with a broader range of microwear textural complexity and a smaller average feature size (Table 1), implies a more diverse diet, including the incorporation of increased meat consumption and/or other tough foods as well as tool use in food preparation.

The archaeological record is consistent with this interpretation. Although tool cut marks have been found on large animal bones by 2.58 Ma (87) and possibly earlier (88), evidence of stone tool–assisted foraging is intermittent (stratigraphically discontinuous) before 2.0 Ma (2). Core-flake-hammerstone technology (Oldowan) is temporally persistent beginning ~2.0 Ma; along with the acquisition of large animal tissues at least partly by hunting and butchery, the exploitation of diverse terrestrial and aquatic resources, and tool-edge wear consistent with processing underground tubers and roots (8992). Stone tools were transported from as far away as 12 km from source (93), which underscores the energetic trade-off between the cost of stone transport and the energetic returns from tool use. The Oldowan also provided the technological basis for expansion into southern and northern Africa and western Asia by 1.85 Ma, and the appearance of the Acheulean by 1.76 Ma (94) may have further enhanced adaptive potential.

These fossil, isotopic, and archaeological features suggest substantial differences between early Homo and earlier hominins, as well as contemporaneous Paranthropus, that imply flexibility in accommodating to habitat and resource diversity and unpredictability in eastern Africa and beyond. This trend, which begins with early Homo and intensifies in H. erectus, is also consistent with niche partitioning and the existence of contemporaneous hominin taxa in this period (Box 2).

Box 2

Sympatry and niche partitioning in early Homo

The number of contemporaneous species of early Homo has proved controversial because of differing approaches to species definition and assumptions concerning niche breadth. A single-species or linear hypothesis of hominin phylogeny prevailed through much of the 20th century, underpinned by the idea that a cultural, toolmaking niche was so broad as to competitively exclude multiple species within Homo (140142). Recent interpretation of the fossil crania from Dmanisi, Georgia, as evidence of a single evolving lineage incorporating all early Homo, including H. erectus (8), is consistent with this assumption. Following their anatomical analyses, the authors suggested that a tool-mediated widening of the dietary niche in early Homo may have impeded niche differentiation.

However, carbon isotopic values for teeth of broadly sympatric representatives of early Homo in the Turkana Basin, Kenya (~1.99 to 1.46 Ma), call into question the idea that tool use precludes niche differentiation. These carbon isotopic values range from –2.6 to –9.9 per mil (‰) for all early Homo, indicating sufficient resource space to sustain dietary differentiation. This range exceeds the isotopic separation of 3.5 to 4.3‰ seen in sympatric lineages of fossil murine rodents in the late Miocene Siwalik sequence of Pakistan (143) and the 1.3‰ separation in the means for hair samples of sympatric West African chimpanzees and gorillas (combined range for the two species is 3.7‰) (144). Furthermore, an isotopic difference of 2.8‰ between the means for H. erectus (N = 10; = –4.3‰) and non-erectus Homo (N = 15; = –7.1‰) in the Turkana Basin is nearly identical to the difference of 2.9‰ between the means of Turkana Basin H. erectus and Paranthropus boisei: N = 27; = –1.4‰) (18), which suggests the potential for niche partitioning within early Homo, all of whom may have been toolmakers.

Additionally, ecological and genetic studies in other organisms provide models for the coexistence of closely related taxa with similar diets and have potential implications for taxonomic diversity in early Homo. For example, widespread and highly mobile populations of large-bodied East African giraffe are now considered to compose at least two and possibly five to eight distinct species (145147). They exhibit relatively deep genetic differentiation in mitochondrial and nuclear DNA consistent with trait differences (e.g., ossicone number) and reproductive isolation in the absence of obvious geographic barriers (148). Maintenance of sympatric taxonomic diversity in the face of overlapping diets is also evident in diverse ungulates and carnivores [e.g., (149, 150)].

These observations, taken together with evidence that H. erectus continues in both Africa and Asia after 1.4 Ma yet does not include the morphologies of either the 1470 or 1813 group and that the 1813 group lasts to at least 1.4 Ma in Africa (32), support the view that taxonomic diversity sustained by ecological differentiation did characterize Homo between ~2.0 and 1.4 Ma. We thus conclude that tool-assisted dietary flexibility in early Homo need not have led to competitive exclusion of multiple species of Homo. Such flexibility could instead have favored opportunities for niche differentiation through, for example, seasonal resource partitioning, population size variations in multiple taxa in response to different climate regimes, and differential use of the habitats [including mesic refugia (151) and dry grasslands (152)] that are evident during the time of East African early Homo.

Body size and developmental plasticity

Body-size increase and developmental accommodation as inferred from intrataxon variation in body size also indicate adaptive flexibility. There is an increase in average body size from Australopithecus to early Homo to H. erectus (Table 1), as well as substantial intrataxon size variation. The range in body size across paleopopulations, particularly in H. erectus, is similar to that found in modern humans, where it is known to be a complex reflection of mortality probability and nutrition (95, 96). In living humans, these variables interact to affect both the duration and the speed of ontogeny, and this developmental flexibility allows a large reaction norm of body sizes. Relatively large size in humans is found in environments of high nutritional sufficiency, and selection for later maturation and extended longevity occur only in situations of relatively low extrinsic mortality risk (e.g., low predation risk or parasite load). H. erectus ontogeny was likely somewhat slower than in Australopithecus or non-erectus early Homo but considerably faster than in modern humans (97, 98). This suggests that H. erectus may have been able to reduce mortality risk in relation to other hominins through social or other factors.

Larger body size in Homo in relation to Australopithecus undoubtedly reflects nutritional sufficiency resulting from tool use, social cooperation, and a higher-quality diet. This interspecific size increase does not preclude the effect of habitat variation among populations of, for example, H. erectus, where low-quality habitats would be associated with smaller body size, as is the case in other primates (99101). Once established, larger body size provides a greater range of phenotypic adaptive flexibility in response to environmental circumstances. Across mammals, larger body size also equates with larger home range sizes, which would have been exaggerated further if the Homo diet was at the more carnivorous end of the omnivorous spectrum (43, 102). Large home ranges imply increased total daily energy expenditure (TDEE) in relation to body size and a greater reproductive investment (greater lifetime reproductive output) (24, 103). TDEE may have been even higher in H. erectus because of larger brain size in this species, implying efficiency in obtaining a high-quality calorie-rich diet.

Encephalization, cognitive evolution, and social investment

Average brain size also increases from Australopithecus to early Homo to H. erectus. Large brains require an increase in total energy and/or a reduction in energy allocation to other expensive functions, such as maintenance (smaller guts), locomotion (efficient bipedal locomotion), or production (slower growth and reproduction) (104110). All of these factors are observed or inferred in the evolution of Homo.

There is also some indication that cooperation in the form of allocare is directly related to increased brain size. For example, social carnivores show a tendency in this direction, where a modest amount of cooperation is correlated with larger brain sizes in social carnivores compared with their more isolationist congeners (111). New work also suggests that, because of the extended ontogenetic periods necessary for the growth of larger-bodied and -brained offspring, the great apes are at the demographic limit for brain size increase. Larger-brained hominins (over about 700 cm3 in average size) could not reproduce fast enough to sustain population numbers without greater cooperative care that would provide extra resources to the mother and result in earlier weaning, shorter interbirth intervals, and higher overall fertility (105). Other factors, such as adiposity, may also have been important to brain growth early in ontogeny (112). Although we are currently limited in our ability to gauge soft-tissue features from the fossil record, adiposity and sex differences in relative adiposity are critical components of human abilities to disperse into myriad environments.

Thus, the increase in average body and brain size from Australopithecus to early Homo to H. erectus is consistent with a greater control over or amelioration of mortality risk and increased nutritional sufficiency. Increasing cultural mediation and enhanced niche construction (4, 71, 113, 114), through technology and social factors such as food sharing or allocare, would be essential to buffer against fluctuating climatic conditions, reduce predation pressure and extrinsic mortality risk, and insure greater food availability.

Niche construction and dispersal

These lines of reasoning suggest that there were a variety of strategies available to early Homo that enabled adaptive flexibility in the context of climatic variability and dispersal to new habitats. We emphasize that flexibility is just one possible reaction to these environmental challenges and need not be the one that all or even most animals took at this time. Lessons from extant comparators suggest that intraspecific phenotypic plasticity provides a more rapid response to environmental challenges than genetic change but that genetic change can follow (95). We expect that this is precisely what occurred with the evolution of Homo. Different species (1470 group, 1813 group, and H. erectus) used different strategies. In the face of a dynamic and fluctuating environment, we suggest that the unique combination of larger brain size, the potential for diverse body sizes, inferred dietary flexibility, and cooperation enabled H. erectus to attain a level of niche construction and adaptive versatility that allowed this species to outpace its congeners.

This same adaptive flexibility was likely essential to the expansion of Homo out of Africa and into Eurasia. The limited available fossil evidence is consistent with this in suggesting that H. erectus was the first hominin to leave Africa, reaching Dmanisi (Georgia) by 1.85 Ma and Sangiran (Java, Indonesia) by 1.66 Ma (Fig. 2) (115, 116). Two incisors from Yuanmou (Yunnan, China; 1.71 Ma) are similar to those of KNM-ER 15000 (Nariokotome, West Turkana, Kenya; 1.6 Ma) and have also been assigned to H. erectus, although their hominin affinities are contested (55, 57). Regardless, archaeological sites in the Nihewan basin of northern China (Hebei Province) at 1.66 Ma confirm that hominins in eastern Asia spanned a variety of habitats from 40°N (Nihewan basin) to 7°S (Sangiran, Java, Indonesia) (116).

Fig. 2 Key sites and first appearances in the dispersal of early Homo from Africa.

Given the sparse record, the possibility remains, of course, that H. erectus was not the first or only hominin to disperse from Africa. Primitive aspects of the postcranial skeleton of the relatively recent island hominin Homo floresiensis raise the possibility of a pre-erectus hominin in eastern Asia (117), although more-recent work suggests that H. floresiensis was derived from an H. erectus ancestor (118121). The fossil and archaeological evidence to date as well as inferred features of adaptive flexibility all point to H. erectus as the first disperser.

Reduction of mortality risk and increased nutritional sufficiency implied by increasing body and brain sizes, and enhanced niche construction and ranging implied by both the archaeological and fossil records, suggest a level of adaptive flexibility that ultimately allowed the dispersal and range expansion by H. erectus. However, we caution that, even if H. erectus was the first and only to disperse, that geographic expansion was likely to have been episodic and to have involved multiple populations and back migrations. Figure 2 implies only the ultimate direction of dispersal initially from west to east, not the specific mechanism or complexity of that dispersal.

Conclusion: New frameworks and unresolved questions

A suite of morphological and behavioral traits once considered to define the origin of the genus Homo or of earliest H. erectus evolved not as an integrated package but over a prolonged time frame that encompassed species of Australopithecus, early Homo, H. erectus, and later Homo. The idea of an integrated package of traits in early Homo has been thought to anticipate the adaptive characteristics of H. sapiens and to include reduced face and teeth, a substantial increase in brain size, body proportions characterized by an elongated hind limb and shortened forelimb, essentially modern hand functional morphology, dependence on toolmaking and culture with incipient language capabilities, dietary expansion, persistent carnivory and systematic hunting, narrow hips with implications for the birth of altricial young, prolonged life history compared with extant apes, and cooperative food-sharing focused at a home base (15, 122125). New fossil and archaeological data summarized here allow refined perspectives on the morphological variation and pacing of evolutionary change in the Homo clade. These empirical findings, coupled with interpretive models drawn from developmental and comparative biology and behavioral ecology, now require the disentangling of this package of traits (Fig. 3).

Fig. 3 Evolutionary timeline of important anatomical, behavioral, and life history characteristics that were once thought to be associated with the origin of the genus Homo or earliest H. erectus.

An important, continuing goal is to develop a more refined understanding of exactly what adaptive features did originate with early Homo. According to present data, facial and dental reduction defines the earliest members of the genus between 2.4 and 2.0 Ma. Cranial capacity expanded by 2.0 Ma. A greater yet varied degree of brain enlargement correlated with body size increase is expressed in early H. erectus between 1.9 and 1.5 Ma, although estimates of the degree of encephalization overlap with those of Australopithecus. However, brain expansion independent of body size appears to be most strongly expressed later, between 800 and 200 thousand years ago. A relatively elongated hind limb is present in A. afarensis (by 3.9 Ma) and in later Australopithecus (A. africanus, A. garhi, and A. sediba) but not in Ardipithecus (4.4 Ma). Absolutely longer and strongly built femora evolved between 1.9 and 1.5 Ma, coinciding with early H. erectus. Stone technology at ~2.6 Ma may predate the origin of Homo, whereas cultural capabilities of the early Pleistocene led to highly persistent traditions of toolmaking rather than an innovative, cumulative culture linked to symbolic behavior typical of the latter part of the Pleistocene. Transversely oriented hips and a broad pelvis persisted until H. sapiens, although a brain consistently >700 cm3, which occurred after ~1.8 Ma, connotes altricial neonates and heightened cooperation among H. erectus adults. Based on first molar dental histology and eruption, the tempo of life history was slower in H. erectus than in Australopithecus yet was similar to that of extant great apes. Far more prolonged phasing of growth typical of H. sapiens, with implications for intensive social cooperation, is evident in the middle Pleistocene, which is also when definitive evidence of hearths and shelters occurs in the archaeological record, implying strong centrally located social cooperation. The traits associated with the origin of Homo and of H. erectus thus evidently did not approximate the integrated complex of adaptations found in H. sapiens.

The evolution of early Homo, moreover, was associated with recurrent periods of intensified moist-dry variability (Fig. 1E). Dynamic environments favored evolutionary experimentation and the coupling and uncoupling of biological variables (71, 126), which governed against any simple transition from Australopithecus to Homo. We maintain that the East African record to date preserves three distinct taxa of early Homo, including H. erectus, although the issues that arise from recent discoveries elsewhere at Malapa and Dmanisi hint at the intriguing shuffling of derived and plesiomorphic traits and biological variables that likely characterized the early evolution of Homo.

Developmental plasticity and ecological versatility were at a premium in the habitats in which early Homo evolved. Although plasticity across biological levels (molecular to behavioral) was favored in dynamic habitats, both extrinsic (e.g., environmental) factors as well as biological and social feedback mechanisms were complexly entwined in the evolution of Homo and can no longer stand as alternative explanatory hypotheses (4, 61). Understanding the processes by which adaptability evolved in Homo and exactly how various traits contributed to plasticity during the evolution of the genus are important future challenges.

Critical foci for future research on the paleobiology of early Homo are numerous. To cite four examples, first, the field is always well served by new fossil and archaeological finds. Larger fossil samples between 2.5 and 1.5 Ma will be necessary to assess the taxonomic diversity of early Homo and to determine the temporal and spatial integrity of the morphological groups. Second, comparative mammalian studies focused on population structure, genetic isolation, niche differentiation, and the variables enabling the coexistence of congeneric taxa will help build more effective models for understanding morphological groups and diversity in early Homo. Third, much remains to be learned about encephalization in early Homo, the degree of plasticity in body and brain size, and how these variables were related to paleoenvironmental variables (e.g., shifting resource abundance). Last, interpretations concerning early Homo rely on the comparative biology of a wide range of mammals (including humans) in order to test and develop robust models of the intricate relationships between energetics, life history, brain and body size, diet, mortality, and resource variability across temporal and spatial scales. A refined understanding of these relationships will enable the union of many disciplines to yield a deeper understanding of human evolution.

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References and Notes

  1. Acknowledgments: We thank the participants of the Wenner-Gren Symposium “Human Biology and the Origin of Homo”; our field and laboratory collaborators for contributing stimulating conversation and ideas; J. B. Clark, who assisted in creating the figures; and E. R. Middleton, who provided bibliographic assistance. Funding provided by the Wenner-Gren Foundation for Anthropological Research (S.C.A. and L.C.A.), New York University (S.C.A.), the Peter Buck Fund for Human Origins Research, and the Human Origins Program (Smithsonian) (R.P.). The authors contributed equally to this work.
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