Evolutionary Anthropology 17:22–37 (2008)

ARTICLES

The Origin of Modern Anatomy: By Speciation or Intraspecific Evolution?

GU¨ NTER BRA¨ UER

‘‘Speciation remains the special case, the less frequent and more elusive Over the , the chronological phenomenon, often arising by default’’ (p 164).1 framework for had to be Over the last thirty years, great progress has been made regarding our under- somewhat revised due to new dating standing of sapiens evolution in Africa and, in particular, the origin of ana- evidence and other discoveries. For tomically modern . However, in the mid-1970s, the whole process of example, in 1997, we presented a re- Homo sapiens evolution in Africa was unclear and confusing. At that time it was vised scheme14 in which the time widely assumed that very archaic-looking hominins, also called the ‘‘Rhode- periods of both the early archaic and sioids,’’ which included the specimens from (), Saldanha (South the late archaic groups had to be Africa), and Eyasi (), were spread over wide parts of the continent as somewhat extended because of new recently as 30,000 or 40,000 years ago. Yet, at the same time, there were also absolute dates for the Bodo and Flo- indications from the Omo Kibish skeletal remains () and the Border risbad hominins, among others. The specimens () that anatomically modern humans had already been current updated version (Fig. 1) present somewhat earlier than 100,000 years B.P.2,3 Thus, it was puzzling how includes the most recently discovered such early moderns could fit in with the presence of very still specimens from Ethiopia as as existing in Eastern and Southern Africa only 30,000 years ago. the latest dating evidence. Looking back over about two and a half deca- des, no evidence has emerged so far that disproves or contradicts the sug- gested early origin of modern anatomy During the 1970s, new field work, archeo-chronology of the African in Africa and the continuously evolv- faunal analyses, and absolute dating and to a dramatic exten- ing lineage during the Middle Pleisto- began to reveal more and more that sion in time of the Middle and Later cene.15–19 Also, the current framework the late dates for archaic specimens Stone Age, and thus to older dates of appears now to be rather well founded were incorrect.4–7 Intensive research the associated hominins.8,9 The on quite a number of diagnostic homi- also led to a drastic revision of the 1970s also saw important Middle nin specimens, as well as absolute hominin discoveries, dates (Table 1, Fig. 2).17 such as the crania from Ndutu and Gu¨ nter Bra¨ uer is a professor of biological anthropology at the Department of Laetoli (Tanzania) and Bodo Biology, University of Hamburg, (Ethiopia). In 1978, in view of the . As a paleoanthropologist, he accumulating evidence, I started a EVOLVING LINEAGE carried out many studies of Pleistocene hominin in Africa, , Indone- morphological analysis of the Middle The anatomical modernization sia, and Europe. He is a major proponent and hominin mate- process can be divided into three of the Out-of-Africa model of modern human origins. His research also has rial from Africa. This research finally largely diachronic grades of Homo contributed to the problem of taxonomic led to a framework of Homo sapiens sapiens (Fig. 1), each including hom- diversity in African and Asian Homo evolution suggesting a mosaic-like, erectus. E-mail: guenter.braeuer@uni- inin specimens of similar evolution- 12,13,15,16,20 hamburg.de continuous anatomical process of ary level. The specimens Department of Human Biology, University modernization, from an early archaic in the early archaic Homo sapiens of Hamburg, Allende-Platz 2, 20146 Hamburg, Germany grade via a more derived late archaic category are clearly derived relative grade to anatomically modern to , sharing apomor- humans.10–13 This result was a cen- phies with later Homo sapiens espe- Key words: Africa; archaic Homo sapiens; Homo tral element of an early version of cially regarding their enlarged brain- heidelbergensis; Neandertals; species; cladistics the Out-of-Africa model,11 also sug- case, more vertically oriented lateral gesting that the modernization pro- walls, expanded frontal bone, less VC 2008 Wiley-Liss, Inc. cess in Africa occurred largely in strongly angulated occipital bone, DOI 10.1002/evan.20157 Published online in Wiley InterScience parallel to the Neandertalization pro- more vertically oriented upper (www.interscience.wiley.com). cess in Europe. scale, higher temporal squama, and ARTICLES The Origin of Modern Anatomy 23

is associated with some parietal bossing, a coronally expanded fron- tal, and derived features of the tem- poral. The supraorbital torus even appears to show some division into a medial and a lateral portion.25 Still, the massive face looks rather ar- chaic. Another specimen of similar or slightly younger age17 is the Sal- danha (or Elandsfontein) cranium from South Africa (Fig. 3). Having an estimated cranial capacity of about 1,225 cm3, the parietals are well arched and show some bossing. With regard to the parietal arch shape index, the specimen is even close to that of early modern humans from Qafzeh.26 In addition, the frontal squama is coronally enlarged. The occipital is less angu- lated than generally is seen in Homo erectus and the transverse torus is reduced. Another specimen grouped with the early archaics is the cra- nium from Ndutu (Tanzania), which is about 400,000 years old or possi- bly somewhat older.17,27 In posterior view, the parietal walls are vertically oriented, exhibiting well-developed bossing (Fig. 4). The occipital is clearly derived relative to Homo erec- tus due to its more rounded shape, the relatively long and slightly poste- Figure 1. Scheme of Homo sapiens evolution in Africa. riorly inclined upper scale, and the reduced torus morphology. Other well-preserved early archaic reduced development of the supraor- whether there are parts of the line- crania from Kabwe (Zambia), Eyasi bital and occipital tori. The late ar- age that show more intensive (Tanzania), and Sale´ () date chaic Homo sapiens is clearly more changes toward the modern mor- from the same time span between derived as compared to the morpho- phology than do others. Thus, factor 600,000 and 300,000 years ago and logical pattern of the early archaics, analysis and other studies such as are similar regarding most of their as is especially evident in the large those carried out, for example, by derived conditions.15,16 The Kabwe cranial capacity, the more reduced Lieberman and coworkers21,22 are specimen (Fig. 4) exhibits an supraorbital torus, and the near- useful in trying to identify major enlarged cranial capacity of ca. 1,280 modern or modern face, including structural elements of this process, cm3, increased sagittal curvature of canine fossa and inframalar incurva- such as neurocranial globularity and the parietal, and coronal expansion ture. This grade of evolution is fol- facial retraction.23 Indeed, it must be of the frontal regions. Other derived lowed by the anatomically modern expected that many of the features features include the vertically ori- Homo sapiens. The use of these tem- and aspects characterizing the ented upper scale of the occipital porally and morphologically overlap- grades are connected with more gen- bone, the high and superiorly curved ping entities is just a way to describe eral changes or shifts. temporal squama, and the gracile the continuous mosaic-like modern- tympanic nearly aligned with pet- ization process.19 I also favor a grad- rous.28 The Eyasi 1 cranium has an EARLY ARCHAICS ual pattern for this part of hominin estimated capacity similar to that of evolution because we are certainly Key evidence of the presence of Kabwe and rather vertical parietal dealing here with diachronic changes early archaic Homo sapiens (Fig. 3) walls with some bossing. Its occipital within one species. The use of the comes from the hominin specimen is rounded with a relatively vertically grade pattern does not suggest any- from Bodo (Ethiopia), dated by Ar/Ar oriented upper scale and a weak thing about the underlying factors to ca. 600,000 years B.P.24 The large transverse torus. In spite of patholog- of anatomical modernization nor cranial capacity of nearly 1,300 cm3 ical changes in the nuchal area and 24 Bra¨ uer ARTICLES

TABLE 1. Major Middle and Early Late Pleistocene Cranial and Mandibular Remains From Africa Site Country Fossils Age (Myr) Eastern Africa Bodo Ethiopia Partial cranium, temporal fragment 0.6 Ndutu Tanzania Partial cranium 0.4 Eyasi Tanzania Partial cranium, cranial fragments 0.4–0.3 Olduvai Tanzania Maxilla, palate (OH 11) 0.4–0.3 Kapthurin/Baringo 2 mandibles 0.5 Laetoli Tanzania Cranium (LH 18) 0.3–0.2 Wadi Dagadle´ Djibouti Maxilla 0.25 Ileret Kenya Partial cranium (ER 3884) 0.27 Eliye Springs Kenya Cranium >0.2 Omo Kibish Ethiopia Partial cranium, mandible (Omo 1) 0.2 Partial cranium (Omo 2) 0.2 Cranial fragment (Omo 3) 0.1 Herto Ethiopia Cranium (BOU-VP-16/1) 0.16 Cranial fragment (16/2, 16/43) 0.16 Child’s cranium (16/5) 0.16 Singa Sudan Partial cranium 0.15 Mumba Tanzania Teeth 0.13–0.1 Aduma Ethiopia Cranial fragment 0.1–0.07 Dire´ -Dawa Ethiopia Partial mandible 0.08–0.06 Bouri Ethiopia Cranial fragment >0.05 Southern Africa Saldanha South Africa Partial cranium, mandibular fragment 0.6–0.4 Kabwe Zambia Cranium () 0.35–0.25 Maxilla (Kabwe 2) 0.35–0.25 Cave of South Africa Partial mandible 0.35–0.25 Florisbad South Africa Partial cranium 0.26 Klasies River South Africa Several cranial and mandibular fragments 0.12–0.08 South Africa Partial cranium (BC 1), mandible (BC 2) 0.12–0.09 Die Kelders South Africa Teeth 0.08–0.06 Northern Africa Thomas Quarry Morocco Mandible, cranial fragment 0.6–0.5 Sidi Abderrahman Morocco Mandible 0.4 Sale´ Morocco Cranium 0.4 Ke´bibat Morocco Cranial fragment 0.25 Morocco Cranium (JI 1), partial cranium (JI 2), mandible (JI 3) 0.19–0.17 2 partial mandibles 0.2–0.08 Zouhra Cave Morocco Mandible 0.13–0.04 Te´ mara Morocco Cranial and mandibular fragments 0.13–0.04 Dar-es-Soltane Morocco Partial cranium, mandible 0.13–0.04

its relatively small cranial capacity, of ca. 270,000 years.14 A previous The Florisbad specimen (Fig. 5) the Sale´ cranium exhibits a rather analysis30 showed that most of the could be directly dated by ESR to ca. convex frontal, expanded parietals cranial vault falls both metrically 260,000 years B.P.31 Its derived mor- and other similarities to the Ndutu and nonmetrically close to the range phology is evident in the great coro- hominin.29,72 of Holocene Africans. However, the nal expansion of the frontal bone, cranium also exhibits a continuous which is associated with a continu- supraorbital torus that deviates from ous but only slightly projecting LATE ARCHAICS the generally rather modern impres- supraorbital torus, and the modern The late archaic grade comprises sion of the specimen. As a whole, the facial shape with a well-developed specimens spreading from northern cranium is rather close in morphology canine fossa. For the LH 18 cranium to southern Africa that are more to that of modern humans (Fig. 5).15 (Fig. 6), a date of more than 200,000 derived toward the modern morphol- During the mid-1990s, further sup- to 300,000 years was determined by ogy than are the early archaics. An port for the early presence of late ar- a combined approach using Ar/Ar example of these near-moderns is the chaic Homo sapiens emerged based analysis and the AMS-calibrated cranium KNM-ER 3884 from Ileret, on new absolute dates for the Floris- amino acid method.32 This well-pre- East Turkana. This specimen was bad hominin from South Africa and served specimen exhibits a modern- directly dated by gamma-ray spec- the Laetoli Hominid 18 from the looking face with a canine fossa and trometry, which yielded, an U/Th age Ngaloba Beds in Northern Tanzania. a near-modern braincase with a ARTICLES The Origin of Modern Anatomy 25

Figure 2. Middle and early late Pleistocene hominin sites.

capacity of about 1,350 cm3,a its combination of archaic and appears to have a morphology simi- rounded occipital bone, and well- derived conditions.19,33 A CT-based lar to that of Jebel Irhoud 1. developed parietal bossing. It is three-dimensional analysis of the mainly the frontal that exhibits vari- matrix-filled cranium revealed that ous archaic features. Among these its cranial capacity measures ca. EARLY MODERNS are the flat, narrow squama and the 1,210 cm3.34 supraorbital torus, which is rather Important late archaic specimens The continuous mosaic-like transi- thick and rounded in its lateral seg- also exist from Northern Africa, such tion from late archaic to early ana- ment. However, the torus shows indi- as the crania from Jebel Irhoud (Mo- tomically modern Homo sapiens is cations of an incipient division in the rocco), dated to about 170,000 years also obvious in the available speci- mid-orbital region, which might be a B.P.35,36 The better-preserved cra- mens from Ethiopia. The Omo Kib- tendency toward the fully modern nium Jebel Irhoud 1 (Fig. 6) exhibits ish remains include two reasonably pattern. Although it is not as well near-modern morphology of the well-preserved crania, Omo 1 and dated as the previous three late vault and face.37 Here again, the Omo 2. Recent field work at the two archaics, the cranium from Eliye most obvious archaic is the sites and new Ar/Ar dating suggests Springs, West Lake Turkana, might continuous supraorbital torus. Jebel that both the Omo 1 skeleton and also belong to this group based on Irhoud 2, although lacking a face, the Omo 2 cranium date to around 26 Bra¨ uer ARTICLES

and modern face combined with a somewhat angulated occipital bone. This feature, however, appears to vary considerably within these early modern or near-modern populations as indicated by the less angled occi- pital in the other adult specimen, BOU-VP-16/2.39 The Singa cranium from Sudan, with an age of around 150,000 years B.P.,41 also belongs to this transitional earliest modern human spectrum.15 Other early moderns are known from Southern Africa, especially the Klasies River Mouth on the south coast. Here are the oldest human remains derived from the LBS Member, the lowest member of the Klasies deposits, dated to ca. 120,000 years B.P. These maxillary fragments fall both metrically and morphologically within the range of variation of Holocene Africans.42 A nearly complete mandible from the Lower SAS Member, a level some- what higher in the deposits, dates to about 100,000 years and is anatomi- cally modern, as are the other cranial fragments from this site.15,43 Regarding the postcranial speci- mens, the conditions in the Klasies remains can be matched with recent population samples from Southern Africa.44,45 Some features, such as the relatively low coronoid height of the ulna, could alternatively be retained archaic features reflecting the mosaic pattern of evolution in the postcranial skeleton.45,46 But it is also possible that such postcranial conditions sim- ply belong to the range of variation of these early modern humans.47 This Figure 3. Early archaic Homo sapiens specimens from Bodo, Ethiopia, and Saldanha, latter view finds support in the fact South Africa. that the Omo 1 ulna has the most ‘‘modern’’ ratio of coronoid to olecra- non height of any of the African Mid- 38 195,000 6 5,000 years B.P. are the strong mid-sagittal keeling dle Stone Age specimens. Moreover, Whereas the Omo 1 specimen is fully and the angulated occipital bone the Skhul/Qafzeh humans display anatomically modern (Fig. 7) and, (Fig. 7). Although the two presum- greater coronoid development than according to the most recent dating ably rather contemporaneous Omo do the MSA South African ulnae.47 evidence, the oldest known modern crania illustrate the mosaic-like tran- Another important , the Omo 2 cranium shows a sitional pattern, recently discovered specimen is the Border Cave 1 par- mosaic of modern and archaic fea- cranial remains from Herto in the tial cranium from South Africa, tures. It exhibits a robust yet basi- Middle Awash (Ethiopia), dated by which, if it came from layer 4BS, is cally modern supraorbital morphol- Ar/Ar to 154,000–160,000 years B.P., about 90,000 years B.P. or, if it came ogy. Although this region is very adds further relevant evidence to the from 5BS, is somewhat older.48 This 39,40 fragmentary, it is clearly visible that process of modernization. The reconstructed specimen is basically the superciliary arch protrudes rela- large, robust Herto cranium BOU- anatomically modern, with a high, tive to the more flattened lateral seg- VP-16/1 (Fig. 7) exhibits a basically curved frontal bone. The supraorbital ment. Among the archaic conditions modern supraorbital morphology morphology is only slightly thickened ARTICLES The Origin of Modern Anatomy 27

simultaneously all over the conti- nent. Based on the current evidence, it seems likely that the earliest tran- sition to anatomically modern humans occurred in Eastern Africa. However, future dating and new dis- coveries may change this impression. Indeed, a mode of continuous evolu- tion without speciation events has been supported by a recent compre- hensive analysis of the Middle Pleis- tocene hominins showing clear tem- poral trends from early archaic up to modern Homo sapiens in many metrical and nonmetrical cranial features.50 These include, for exam- ple, major dimensions of the frontal, parietal, and occipital bones, as well as nonmetrical traits of the supraor- bitals, parietal expansion, temporal squama and mastoid region, occipi- tal shape, and facial features. Many of these changes certainly correlate with increasing rounding of the vault or a reduction and retraction of the face. However, since these changes can be observed in a mosaic-like pattern over some hun- dreds of thousands of years, it does not appear very likely that the origin of the anatomically modern shape was the result of just a few ev- olutionary adjustments within a short period associated with a speci- ation event as Lieberman, McBrat- ney, and Krovitz21 suggested. In her comment on such an interpretation, Brooks (cited by Balter51) empha- sized that ‘‘we don’t see any sudden leaps’’ in the emergence of modern Figure 4. Early archaic Homo sapiens specimens from Ndutu, Tanzania, and Kabwe, Zambia. humans. Instead, she sees a gradual process of both physical and behav- ioral change. Also commenting on Lieberman’s results, Aiello (cited by and anteriorly protrusive. Although it years ago are possible for these mod- Balter51) raised the question of is not clearly divided into medial and ern specimens. Current research lateral portions,12,49 its strongly might contribute to further clarifying whether these innovations in skull reduced condition differs from the the age of these diagnostic and rele- anatomy really add up to make tori present in the late archaics. vant remains. humans a truly different species; Northwestern Africa is also a that is, a separate group that could potential region for an early presence not breed with Neandertals or other extinct humans. Her answer was, of modern humans. However, much MODE OF MODERNIZATION depends here on the unclear dating ‘‘Nobody’s cracked this question yet evidence for the and the Considering the morphological and (p. 1222).’’ In my view, Lieberman, associated anatomically modern chronological evidence together, McBratney, and Krovitz’s21 interpre- human remains such as those from there is good documentation of tation that anatomical moderniza- Dar-es-Soltane, Te´mara, and Zouhra a continuous evolutionary change in tion can be boiled down to just a Cave (Morocco).37 Ages between Africa. This does not mean that few autapomorphies or genetic 40,000 and even more than 100,000 the modernization process occurred changes will be difficult to accom- 28 Bra¨ uer ARTICLES

(p. 208).53 Finally, three further p-demes around Klasies, Dar-es-Sol- tane, and possibly Singa are distin- guished as representing early mod- ern humans. However, current disagreements exist regarding the taxonomic level on which the major groups or entities should be distin- guished and consequently, about the resulting phylogenetic scenarios. Therefore, some current alternative views are discussed here.

HOMO HELMEI According to Foley,54 the three major groups should be classified as , Homo helmei, and Homo sapiens. Although this indicates a separation on the ‘‘species’’ level, he concedes that the

. . . the Middle Pleistocene fossil record from Africa can be morphologically subdivided into three grades or groups of an evolving species, Homo sapiens.

derived descendent taxa of Homo heidelbergensis are problematic Figure 5. Late archaic Homo sapiens specimens from Ileret, Kenya, and Florisbad, South because of the continuity that can be Africa. found between them and Homo hei- delbergensis: ‘‘These seem to be spe- modate within the current fossil evi- gested here. Howell53 recognized an cies in the sense that Simpson meant dence. early p-deme represented by Kabwe —lineages with independent trajecto- As suggested in the previous sec- and associated specimens like Salda- ries—but both the details of the fos- tion, the Middle Pleistocene fossil re- nha, Ndutu, Bodo, Baringo/Kap- sil record and the scale of the pro- cord from Africa can be morphologi- thurin, and Eyasi (here assigned as cess seem to rule out any punctuated cally subdivided into three grades or early archaic Homo sapiens). The events. Indeed, continuity between groups of an evolving species, Homo specimens from Jebel Irhoud and them, rather than discontinuity, is sapiens. The recognition of three Florisbad are seen as major repre- the reason for the persistent problem groups is well founded and widely sentatives of two later p-demes, the of delimiting the taxonomic units in accepted, as the discussion at the latter including specimens such as the later stages of Stony Brook Symposium and Work- Laetoli Hominid 18, Eliye Springs, and gives rise to the question of shop revealed. Also, Howell’s52,53 Ileret/ER 3884, and Omo 2. Regard- whether the species concept, which suggestion of paleo-demes, spatially ing this p-deme, ‘‘all the specimens lies at the heart of macroevolution- and temporally bounded entities exhibit substantially derived aspects ary theory, is sufficiently fine-tuned below the species level, is basically in of cranial morphology vis-a` -vis to cope with evolution at this scale. agreement with the sequence sug- antecedent African p-demes :::.’’ The lineages of later human evolu- ARTICLES The Origin of Modern Anatomy 29

Jebel Irhoud make unparsimonious ancestors for the , since not only do they post-date the appearance of clade characters in Europe, but they appear to lack Neanderthal morpho- logical characteristics that might be expected in a common ancestor (p. 567).’’ Another problem of Foley and Lahr’s proposal is that they also included technological aspects in their species definition. Stringer18 criticized their use of Mode 3 tech- nology as an ancestral ‘‘taxonomic’’ characteristic not only ‘‘because tech- nologies might transfer between dis- tinct populations or even different species :::, but also because the time and place of origin of prepared core techniques are currently unknown.’’ Similar criticism comes from McBrearty and Brooks.27 They regard it ‘‘a curious departure from normal taxonomic practice [that] Lahr and Foley (1998: 157) have included certain European fossils in H. helmei on the basis of their ages (isotopic stages 6, 7 and 8) and pre- sumed associated (‘‘mode 3’’).’’27 Moreover, McBrearty and Brooks27 regard Homo helmei in gen- eral as a problematic taxon with no formal diagnosis. In contrast to Foley and Lahr, they merely used the name Homo helmei or Homo sapiens for their morphologically intermedi- ate ‘‘Group 2’’ of African fossils, which is equivalent to ‘‘late archaic Homo sapiens.’’ In summary, it appears obvious that the species Figure 6. Late archaic Homo sapiens specimens from Laetoli, Tanzania, and Jebel Irhoud, Homo helmei sensu Foley and Lahr Morocco. hardly helps to clarify the issue.57 In view of the generally agreed transi- tional character of this derived pre- tion seem to show simultaneously tle justification in distinguishing this modern group,55 it is much more continuously evolving lineages and transitional55 or late archaic group appropriate to include this morph very distinctive derived endpoints, ::: as a distinct species, Homo helmei. within the species Homo sapiens as a They certainly highlight the prob- Yet there are more problems with late archaic group, an intermediate lems of reconciling terminology with regard to Foley and Lahr’s56 use of stage,36 or a somehow labeled process (p. 9–10).’’54 This statement Homo helmei, because they also in- chrono-subspecies. indicates that a distinction of three cluded European fossils in their species would, in fact, be an artificial hypodigm. Stringer18 clearly ad- HOMO HEIDELBERGENSIS division of a continuously evolving dressed the problems:11 ‘‘First, Nean- lineage in Africa. Stringer,18 as well, derthal characteristics were already Problems also exist with regard to recognizes here a gradual mosaic- evolving in Europe prior to the hypo- a possible species Homo heidelbergen- like evolution to modern humans in thesized appearance of ‘‘H. helmei,’’ sis in Africa. The oldest, most rele- Africa, using the term ‘‘archaic Homo e.g., in the Swanscombe specimen, vant African specimen that some sapiens’’ for the late archaic speci- dated to ca. 400 kyr. Second, African have assigned to this taxon is the mens. In fact, there appears to be lit- specimens such as Florisbad and Bodo hominin. However, Adefris,58 30 Bra¨ uer ARTICLES

Figure 7. Late archaic transitional and early modern specimens from Ethiopia: a) Omo 2; b) Omo 1; c) and d) Herto BOU-VP-16/1 (cour- tesy of T. White). based on her detailed anatomical more derived morphology of the hardly be plausible, for example, to study of this cranium, arrived in post-erectus species. But the major classify Omo 2 or Florisbad together 1992 at the conclusion that it should contrast (Fig. 8) is that Rightmire’s with Bodo (and the possible Homo be classified as an ‘‘archaic Homo scenario suggests two further, largely erectus from Ceprano, Italy61)as sapiens.’’ Only a short time later, sympatric speciations, one in Europe Homo heidelbergensis and Omo 1 as Rightmire25 regarded it more reason- from Homo heidelbergensis to Homo Homo sapiens, as indicated by Right- able to refer to Bodo as a Homo hei- neanderthalensis at ca. 300,000 years mire.60 Assigning the two Omo speci- delbergensis, together with Mauer, ago and another in Africa from mens to two different species would Arago, Petralona, Kabwe, Ndutu, and Homo heidelbergensis to Homo sapi- inadequately exaggerate the differen- others. Rightmire59 suggested a spe- ens at ca. 150,000 or 200,000 years ces. If they are indeed so close in ciation event between Homo erectus ago.59,60 age, Trinkaus62 would rather see a and Homo heidelbergensis in Africa As outlined, however, the evidence reflection of considerable intrapopu- at around 800,000 to 700,000 years from Africa rather shows a continu- lational variation. ago. This speciation refers to the ous gradual process of anatomical For Rightmire’s view on Homo hei- same event that I recognize between modernization without any clear delbergensis, however, it is also essen- Homo erectus and (archaic) Homo subdivisions on the species level, tial whether a speciation can be sapiens,15,16 since Rightmire25 also especially at the transition to ana- assumed in Europe. Yet here, as supports a single polytypic species tomically moderns. In view of the well, there is little support for a con- Homo erectus in Asia and Africa. many shared derived features of late clusive speciation event along the Thus, I agree with Rightmire on the archaics and early moderns, it can pre-Neandertal/Neandertal lineage. ARTICLES The Origin of Modern Anatomy 31

anatomical modernization process in Africa. Thus, Rightmire’s view of Homo heidelbergensis and two subse- quent speciation events is, in my view, hardly supported by the fossil evidence. In addition, Homo heidelbergensis sensu Rightmire is just one of quite a number of different definitions of this ‘‘species.’’ Stringer18 favors a similar widespread species but excludes African late archaic Homo sapiens from his hypodigm. Lahr and Foley68 exclude late archaic Africans as well, but classify these hominins together with some pre-Neandertals as Homo helmei. In view of the previ- ously noted problems with Homo hel- mei, such a definition of Homo heidel- bergensis appears highly problem- atic.57 Manzi,66 on the other hand, disagrees with such a single wide- spread species in Africa, Europe, and parts of East Asia, because it ‘‘may obscure the occurrence of separate lin- eages at a macro-regional scale and different patterns of adaptations and evolution.’’ Therefore, he and other researchers, including Bermu¨ dez de Castro and coworkers69 favor a sepa- rate morph, , for African Homo heidelbergensis sensu Rightmire and regard Homo heidelber- gensis as a chronospecies or, ‘‘more reasonably,’’ a chrono-subspecies of 66 Figure 8. Suggested scenario of Homo erectus and Homo sapiens evolution. *s ¼ specia- the anagenetic Neandertal lineage. 27 tion event. [Color figure can be viewed in the online issue, which is available at www. McBrearty and Brooks also interscience.wiley.com.] rejected the name Homo heidelber- gensis for Africa but, in contrast to Manzi, used the term Homo rhode- In fact, there is wide agreement that cess resulted from an increase in the siensis only for African specimens ‘‘the development of the Neandertal frequency of derived Neandertal con- equivalent to early archaic Homo morphology results from an accretion ditions in the pre-Neandertal/Nean- sapiens, thus excluding the late phenomenon beginning in the mid- dertal lineage (see also Stringer18) archaics.27 White and colleagues,39 dle of the Middle Pleistocene, around or, as Klein65 put it, the European although using the species name for 450,000 or a bit before (p. 301).’’63 lineage is ‘‘marked by the progressive early archaics as well, put it in quo- ‘‘Considering the mosaic of accumulation of Neandertal fea- tation marks (‘Homo rhodesiensis’). the accretion phenomenon, tracing tures.’’ Manzi also speaks of an ana- Hublin63 even doubted the appropri- clear divisions along the pre-Nean- genetic sequence, ‘‘which could be ateness of Homo heidelbergensis for dertals/Neandertals lineage is quite more reasonably considered a se- Europe: ‘‘If, in Europe, a taxon ana- artificial (p. 302).’’63 Most recent U- quence of chrono-subspecies.’’66 In tomically distinguishable from Homo series dates using inductively addition Condemi67 suggested an ev- erectus sensu lato was present before coupled plasma multicollector mass olutionary lineage that can be di- the development of the Neandertal spectometry (ICP-MS) yielded an age vided into early pre-Neandertals, late lineage, its hypodigm should be re- of about 600,000 years B.P. for the pre-Neandertals, and proto-Neander- stricted to the populations anterior pre-Neandertals from Atapuerca tals. In fact, over hundreds of thou- to the development of the first Nean- Sima de los Huesos,64 indicating that sands of years, this Neandertaliza- dertal apomorphies. In this case, the the Neandertalization process might tion process might have occurred term Homo heidelbergensis itself, have already started in the early Mid- without a speciation event in parallel with the Mauer mandible as a type dle Pleistocene. The accretion pro- with and largely isolated from the specimen, would be inappropriate. 32 Bra¨ uer ARTICLES

Considering its fragmentary nature, between the suggested ancestor of shared mtDNA ancestry with the this specimen is at least to be , , and Neandertals, premodern humans regarded as an insertae sedis,ifitis Homo erectus could not be supported were certainly able to interbreed not one of the first representatives of by many studies during the 1990s or with them and produce viable, fer- Homo neanderthalensis (p. 302).’’ Tat- more recent ones.60,74–81 There also tile, offspring, as hamadryas and tersall and Schwartz70 used the spe- is no evidence of a separate species anubis do.’’ Moreover, cies name in a broad sense but, at Homo antecessor in Africa, although according to Jolly83 ‘‘the other mes- the same time, emphasized that such a species is assumed to have sage from catarrhine hybridization is Homo heidelbergensis only serves as a originated there more than 1 million that recognizably distinct species useful umbrella for a diversity of fos- years ago.69 According to Tattersall that originated <2 million or even sils not necessarily belonging to one and Schwartz,82 it is, in fact, difficult <4 million years previously cannot species. The obviously great diversity to demonstrate, on the basis of the be assumed to be incapable of in using the name Homo heidelber- small sample of Gran Dolina homi- exchanging genes. Such exchange gensis reveals that it is hardly a well- nins, that this material represents may have results ranging from minor defined taxon proving that speciation the common ancestor of both parallelism to the formation of new, events occurred within the Neander- the Neandertal and modern human hybrid species (p. 663).’’ tal or modern human lineages. lineages. Based on the evidence from living , it appears plausible to regard European pre-Neandertals/ CLUES FROM EXTANT PRIMATES HOMO ANTECESSOR Neandertals and the African Middle If the diverse alternatives should Pleistocene lineage from Bodo to In addition to these different not just express personal tastes or modern humans as belonging to one views, another hypothesis suggests polytypic species, Homo sapiens, that the last common ancestor of the as it is widely agreed to do with Neandertal and modern lineages is regard to Homo erectus as well represented by a new species, Homo 75,76,78–81 69,71 The obviously great (Fig. 8). In such a scenario, antecessor. This species was sug- it still remains unclear whether the gested on the basis of the hominin diversity in using the post-erectus archaic group in China remains from the ca. 800,000-- name Homo (Jinniushan, Dali, Maba) also old TD6 level of Gran Dolina, Ata- heidelbergensis reveals resulted from a dispersal of archaic puerca (). Mainly, the modern- Homo sapiens, had regional Homo looking face and primitive aspects of that it is hardly a well- erectus ancestors, or is even a kind the dentition led to the suggestion defined taxon proving of hybrid population. ‘‘Speciation that it is ancestral to the later Afro- remains the special case, the less fre- European hominins and originated that speciation events quent and more elusive phenom- from Homo ergaster. However, the occurred within the enon, often arising by default’’ (p. material is very fragmentary. Indeed, 164).1 it might appear more likely that this Neandertal or modern material represents a late Homo erec- human lineages. tus or a transitional form between DNA AND ADMIXTURE Homo erectus and subsequent ar- chaic Homo sapiens or ‘‘Homo heidel- Studies of mitochondrial DNA bergensis.’’18,60 from several Neandertals have indi- The progressive traits of the face, views of groupings and splittings, cated that the Neandertal and mod- including the canine fossa, could be but are meant to approach the spe- ern lineages might have separated at due to subadult status, since the cies problem, comparisons with liv- about 500,000 years ago (between fossa is less developed in the adult ing taxa might be useful. Studies on 300,000 and 700,000 years ago).85–87 Gran Dolina specimen. This feature extant primates led Jolly83 to con- Most recent analyses of Neandertal in general shows great variation clude that Neandertals, Afro-Arabian nuclear DNA have supported these among Middle Pleistocene hominins ‘‘premodern’’ populations, and mod- estimates. The study of one million from Africa and Europe. Also, no ern humans are, roughly speaking, base pairs of Neandertal nuclear Neandertal features can be detected biological subspecies, comparable to DNA and comparison with the in the Gran Dolina material. Instead, interfertile allopatric taxa or phyloge- human and many dental features appear to show netic species of baboons. Based on suggest a divergence time of about great similarities to those of the research in contemporary zones of 500,000 years ago.88 Another study roughly contemporaneous late Homo hybridization such as the Awash of about 65,000 base pairs of Nean- erectus from Tighenif, .72 The anubis-hamadryas hybrid zone, dertal nuclear DNA places the most ATD6-96 partial mandible exhibits Jolly84 concluded ‘‘that unless an recent common ancestor at roughly close affinities to Chinese Homo erec- undocumented, radical genetic event 700,000 years ago and the split tus.73 Moreover, the distinction occurred in the 600 ka since they between human and Neandertal pop- ARTICLES The Origin of Modern Anatomy 33 ulations at ca. 370,000 years ago.89,90 modern gene flow exists62,95,96 has basis’’ and that Homo ergaster is ‘‘the Because the taxonomic significance led to more clarity. Re-examination best example of a taxon arising out of the genetic differences is ambigu- of proposed morphological indica- of cladistics.’’ Yet, as shown, there is, ous, the separate evolutionary line- tions of admixture have shown that in fact, a lot of confusion about ages during the Middle Pleistocene many of these suggestions are equiv- Homo heidelbergensis, which can can hardly prove that two differ- ocal or problematic.16,18,97–100 The hardly be regarded a reliable or well- ent biological species emerged. relatively scarce evidence of possible defined species.104 Intensive research Stringer18 argues that the DNA data admixture in the fossil record, for has also revealed that the original available ‘‘can be used to support a example in some early modern assumptions used in the mid-1980s placing of Neanderthals and recent remains from ,62,98,99,101 can for splitting Homo erectus into Homo humans in either the same or differ- be seen to agree with the current ergaster and Homo erectus are not ent species, given the recency of molecular evidence pointing to a tenable. All of the suggested East common ancestry.’’ The discussion small rate of possible Neandertal- Asian Homo erectus autapomorphies among molecular biologists and pale- modern gene flow. According to Lie- occur in the African specimens as oanthropologists has focused instead berman,119 the question of gene flow well, and morphometric analyses on whether or not there is evidence is relevant to the species question: ‘‘If were not able to distinguish between of admixture in the DNA or in the one can find good evidence that so-called Homo ergaster fossils like morphology of the fossils and humans and Neandertals interbred KNM-ER 3733 and KNM-ER 3883 whether the evidence indicates that and that modern humans have some and East Asian specimens.59,74–81,105 any Neandertal contribution to the Neandertal autapomorphies, then, by In fact, for several reasons ‘‘the ma- early modern gene pool was signifi- all means, let’s include Neandertals jority of researchers do not regard cant or minor. in our species’’ (p. 665). In fact, there the H. ergaster hypodigm as worthy An analysis of ancient mtDNA of of a separate species.’’104 Instead, it five Neandertals and five early mod- appears more plausible that ‘‘geo- erns yielded DNA sequences in all graphic subdivision of early H. erec- Neandertals that were similar to In fact, there is no tus into separate species lineages is each other but absent from the five biologically misleading, artificially early modern humans, as well as evidence from extant inflating early Pleistocene species from recent humans.91,92 Using a primates, current DNA diversity.’’80 simple model of a constant human results, or the fossils that This has most recently been under- effective population size, contribu- scored by a study of Homo erectus tion of Neandertal mtDNA to early would exclude features that also considered body modern Europeans larger than 25% Neandertals from having and brain size.81 Anto´ n and co- was statistically excluded. Under a workers81 arrived at the conclusion more realistic scenario of an expan- interbred with modern that ‘‘cranial characters, particularly sion of the population during and af- Homo sapiens. those related to vault thickness and ter the colonization of Europe, a development of the supraorbital smaller Neandertal contribution can torus and many of those related to be excluded, but such estimates differentiating African from Asian depend on when and how the expan- H. erectus, scale with brain size in sion occurred.91 Assuming a late sur- is no evidence from extant primates, H. erectus yielding little support for a vival, with Neandertals contributing current DNA results, or the fossils differentiation between H. erectus for 10,000 years (40,000–30,000 years that would exclude Neandertals from and H. ergaster.’’ Anto´n106 rather ago) and a rapid growth model, the having interbred with modern Homo finds ‘‘the most useful approach to Neandertal admixture would be very sapiens. In spite of the Neandertal- the of H. erectus to be that small.93 According to another com- modern differences in genes and proposed by Jolly,84 who recognized plex demographic simulation of morphology, there is no unequivocal both the complexity of species boun- Neandertal-modern interaction and evidence to classify these closely daries in living organisms and that replacement, the maximum genetic related taxa into two different the fossil record is magnitudes too 102,103 contribution appears to be only species. incomplete to test alternative inter- about 0.1%.94 Certainly, further pretations (if indeed it ever could). sequencing of the Neandertal nuclear Jolly84 suggested avoiding arguments CLADISTICS AND PITFALLS DNA will provide more clarity on the over definitionally induced differen- level of possible Neandertal-modern The major reason for the many ces in favor of recognizing geograph- gene flow. attempts over the last two decades to ically replacing allotaxa. Such a Over many years the continuous split taxa into new morphs or species move recognizes the likelihood that debate, between supporters of the is the application of cladistics in morphological differences may arise Multiregional Evolution and Out-of- . Foley,54 for among allotaxa, but allows for Africa models about whether evi- example, emphasized that Homo hei- hybridization between them. This dence for significant Neandertal- delbergensis has a ‘‘strong cladistic aptly reflects the situation in H. erec- 34 Bra¨ uer ARTICLES tus sensu lato, in which evident re- also be different from one individual recent example of the fact that, just gional variation exists in cranial to another within the same popula- by looking for unique derived traits, morphology and yet in which a total tion as documented by the Middle one can arrive at a view that morphological pattern is shared Pleistocene sites of Arago and Ata- excludes clearly anatomically mod- across regions’’ (p. 154). According puerca SH (p. 301).’’ Species defini- ern humans from being Homo sapi- to Jolly,84 most allotaxa are subspe- tions and phylogenies are often ens. Regarding such cladistic defini- cies by the biological species con- based on selected features or ana- tions, Foley,115 however, reminds us cept, so there is little reason to tomical regions, but evolutionary that variability and polymorphisms in assume a different mode for the spe- changes are likely to differ from one both ancestral and descendent taxa cies Homo sapiens sensu lato. Cer- anatomical area to another. Further- often make such autapomorphies tainly, the cladistic approach has more, as demonstrated earlier with hard to demonstrate (see also the useful elements for analyzing phylog- Homo heidelbergensis and Homo hel- criticism by Stringer116). In fact, a eny, but it reveals little about when mei, the operational taxonomic units look into a recent human skeletal speciation occurred because charac- are largely arbitrarily defined, so that collection reveals that there is obvi- ters normally change within a spe- exclusion or inclusion of specimens ously great variability in mor- cies. There are no direct relation- will to different results. phology, with many specimens lack- ships between change of morphologi- It is often difficult to determine ing an inverted-T-shape. This clearly cal features and speciation107 or, as the autapomorphic status of mor- shows that the feature is too nar- Grubb1 put it: ‘‘Cladogenetic events phological features, as has been rowly defined and thus problematic may need to accumulate before it is shown with regard to the suggested for taxonomic classifications (see possible to achieve speciation, the Homo erectus autapomorphies76 and also Pearson19). less frequent and often less tangible as is likely the case with regard to a Moreover, according to Foley115 ‘‘it phenomenon (p. 163).’’ recent definition of Homo sapiens by is unlikely that the species concept When using cladistics, however, Schwartz and Tattersall.49,113,114 itself will be the most useful tool for one has to be aware of various prob- These authors suggested ‘‘nine fea- unraveling what is in effect ::: a lems and pitfalls,76,108–111 which are tures of the skull that do appear very small-scale event, especially in likely to make results based on fossil among hominoids to be autapomor- its later stages (the last half million material less clear than many sup- phic for Homo sapiens (p. 599).’’49 years).’’ In view of all these prob- porters of this approach appear to These anatomical details include, for lems, it should come as no surprise believe. Only a few of these problems example, extreme lateral placement that there are large disagreements can be addressed here. For example, of the styloid process; a narrow, high regarding the definitions used the assessment of features as present occipital plane of the occipital bone; for Homo ergaster, Homo heidelber- or absent might in many cases be an a bipartite brow (glabellar butterfly); gensis, Homo rhodesiensis, Homo hel- inadequate simplification of the and the inverted-T-shaped chin. mei, Homo neanderthalensis, and extant variation and might lead to Based on these details, Schwartz and even Homo sapiens. Thus, how to inadequate character states and even Tattersall49 concluded that many define species and how many species to the assessment of a feature as specimens that have in the past been or morphs should be assumed absent when, in fact, it is clearly identified as modern Homo sapiens appears to be largely subjective. In present as, for example, the frontal should now be distinguished from contrast to the various attempts to keel on KNM-ER 3733 or Homo sapiens. These hominins split Middle Pleistocene hominins Bodo.66,76,112 Also, the traits used are include, for example, most but not into several species, Wolpoff and col- often functionally interrelated and all Klasies specimens, Omo 1, some leagues117,118 proposed an extremely cannot be regarded as independent but not all of the Qafzeh specimens, opposite view by even including features. Used in a cladistic analysis, Skhul, and even the undated, possi- Homo erectus in the species Homo such nonindependent characters will bly post-Pleistocene Boskop and Fish sapiens. A major reason for such a produce a numerical bias that influ- Hoek crania from South Africa. In wide definition is seen by these ences conclusions about the most the mandible of some Qafzeh speci- authors in a mix of erectus and sapi- parsimonious set of evolutionary mens, much as in Skhul, ‘‘there is a ens characteristics in many of the relationships among taxa and which teardrop-shaped bulge low down on Middle Pleistocene specimens from traits one interprets as homoplasy the external symphysis, but no keel’’ Africa, Europe, and Asia. However, and synapomorphies. (p. 600)’’,49 which would exclude the presence of plesiomorphic erectus Intraspecific polymorphism is also them from being Homo sapiens.In features in a specimen does not nec- widely ignored. Hublin63 illustrated contrast, Lieberman’s analyses, pre- essarily exclude it from belonging to this problem by stating that ‘‘the sented at the Stony Brook Workshop a different, more derived species. mosaic of derived and primitive fea- in 2004, based on relatively complete tures may be different in two con- cranial vaults and faces and using CONCLUSIONS temporaneous specimens. But this different autapomorphies, found that does not mean that we have two dif- Omo 1 and Skhul 5 fall within mod- As demonstrated in the present pa- ferent contemporary taxa in Europe. ern Homo sapiens. Schwartz and Tat- per, both the African and European As a matter of fact, the mosaic can tersall’s typological approach is a fossil records represent long continu- ARTICLES The Origin of Modern Anatomy 35 ous lineages through most of the it appears plausible here, as well, not nium. I thank Eszter Schoell and Middle Pleistocene; these lineages to split Homo sapiens into further Frederik Jessen for their support cannot consistently or reasonably be species. The variety of alternative with the final version of the manu- subdivided into different species. It scenarios discussed here can hardly script, as well as Maximilian von is likely that the lineages diverged be regarded as having convincingly Harling, Angelika Kroll, and Her- some time after the speciation of demonstrated that more than one mann Mu¨ ller for helping with the fig- Homo sapiens from Homo erectus in species was involved in this process, ures. Finally, I am most grateful to Africa about 700,000 or 800,000 even if this might be unsatisfactory Richard Klein for his useful com- years ago, and thus are closely for some splitters. This is a major ments on an earlier version of this related. This makes it reasonable to reason why the use of archaic Homo paper as well as to John Fleagle and assume that the African Middle Pleis- sapiens120 still appears adequate and three reviewers for their helpful sug- tocene lineage represents the species plausible. Archaic Homo sapiens is gestions. not a ‘‘wastebasket’’ for diverse Mid- dle Pleistocene hominin specimens, REFERENCES as some like to believe. Such a desig- 1 nation could then also be used for Grubb P. 1999. Evolutionary processes implicit in distribution patterns of modern Afri- This makes it reasonable Homo heidelbergensis in its predomi- can . In: Bromage TG, Schrenk F, edi- nant sense, since it includes most of tors. African biogeography, climate change, and to assume that the human evolution. New York: Oxford University the same phenetically diverse speci- Press. p 150–164. African Middle mens from Africa, Europe, and 2 Leakey REF, Butzer K, Day MH. 1969. Early Pleistocene lineage China. 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