6 The Earliest Putative Hominids

Transcription

1 The Earliest Putative Hominids Brigitte Senut Abstract Following the molecular studies, the hominid family has long been considered as emerging during the Pliocene. But today we have good evidence of hominids in the African Upper Miocene strata. However, reconstructing our earliest history is a difficult task as the Miocene data remain poorly known and fragmentary. Moreover, the tendency in anthropology to consider the modern chimpanzee as a good model for the last common ancestor of African apes and hominids has obscured our understanding of evolution because the apelike features are exclusively defined on the basis of a modern animal and not on those of Miocene hominoids. On the basis of detailed studies of Miocene apes and modern hominoids, it appears that bipedalism is probably the most reliable feature for defining hominids. Of the new hominoid taxa discovered in the Upper Miocene, only Orrorin tugenensis exhibits clear evidence of adaptation to bipedalism. At this stage, bipedalism in Sahelanthropus tchadensis and Ardipithecus kadabba still needs to be demonstrated. A common idea in hominoid evolution is that hominids emerged in dry, savannah like environments; but the data gained from the Upper Miocene levels in Baringo (Kenya) clearly demonstrate that the environment of the earliest hominids was more forested and humid than expected. Finally, first discoveries of modern looking apes have been made in 12.5Ma old strata at Ngorora (Kenya) and Ma old deposits at Kapsomin and Cheboit, indicating that the dichotomy between African apes and humans could be much older than generally thought..1 Introduction Identifying the earliest hominids remains a difficult task because the definition of the family varies widely from author to author. For some authors, the term hominid should be restricted to humans and their bipedal predecessors, whereas for others it should include all extant and fossil apes and humans; at its most extreme definition all African Great Apes should be included in the genus Homo # Springer-Verlag Berlin Heidelberg 2007

2 1520 The earliest putative hominids (Czelusniak and Goodman 1998), or in a slightly less extreme view, only chimpanzees and bonobos (with the exclusion of Gorilla) should be grouped with Ardipithecus, Australopithecus, and humans in this genus (Wildman et al. 2003). In the latter scenarios, the search for the oldest hominid leads to a strange situation where the quest becomes that of identifying the earliest ape rather than the earliest humans. This is definitely not what the theme of the research on the origins of humans is today. The only consensus today among scientists (molecularists and anatomists) in ape evolution is that Pongo, Pan, and Gorilla do not belong to the same taxonomic group, a view that was widely accepted in the last century; the family Pongidae is now restricted to Pongo (Greenfield 1979). Homo is closely related to African apes and may be closer to Pan than to Gorilla. Whatever systematic scheme is considered, the focus is on understanding the ancestors of humans after their split from African apes. This is why it is more appropriate to restrict the term Hominidae to humans and their fossil forerunners. The widespread confusion in the use of the term hominids is due to the fact that authors usually do not define their position. To understand the earliest hominids, we need to apply a geohistorical approach. The opposition between Asia and Africa in the history of our origins cannot be dismissed out of hand. However, today it seems clear from available field data that the development of the human lineage occurred in Africa. Finally, we must consider the fact that, for the last 30 years, the history of research into the dichotomy between apes and humans has been dominated by the controversial results obtained by paleontologists on the one hand and molecularists on the other. The debate has focused on two major aspects: chronology and the search for the closest relative. There was a heated debate in the 1970s concerning the molecular clock and its implications for hominid evolution versus paleontological evidence and geological time. But discrepancies in the time scales between various neontological studies have never been thoroughly debated, as was pointed out by Arnason et al. (2001). We have known for almost two centuries that the African apes are our closest relatives, but the research published in the last three decades has attempted to focus on the question in greater detail and this has led to another major issue: is the common chimpanzee the closest relative to man? Or is it the bonobo? Or is it the group of African apes as a whole? At this point it has become widely accepted, almost without debate, that the closest relative to man is the chimpanzee, frequently claimed to share 98% or more of its genetic material with humans (or even 99.4% for some authors such as Wildman et al. 2003). This acceptance has occurred despite the fact that the problem is not yet definitively solved (Marks 2002). It is within this complex framework that research on our oldest ancestors has taken place during the past three decades. In addition, preconceived ideas about our earliest relatives make it

3 The earliest putative hominids 1521 even more difficult to have a dispassionate discussion. A statement such as the common ancestor of human and chimpanzees was probably chimpanzee like, a knuckle walker with small thin enamelled teeth (Pilbeam 199) takes us back 200 years, being no different from the quest for the missing link. This widespread preconception is probably one of the reasons why most anthropologists have used modern chimpanzees as the basic comparative material when researching hominid origins. This brings us to another aspect of the problem related to the definition of the earliest hominid. Most anthropologists consider that apelike (i.e., chimpanzee like) features are primitive, and humanlike ones are derived. However, chimpanzees are not primitive; they are in fact highly derived in their locomotory and dietary adaptations and the use of their features as ancestral traits is a major error. Humans are also derived in their locomotion, but in a different way from chimpanzees. It is, therefore, not possible to define the polarity of these traits on the sole basis of some modern relict species; the Miocene apes were highly diverse and this diversity has to be considered when reconstructing phylogenies. The neontological approach, which has been in favor in some scientific circles, turns out to be a total failure when dealing with the definition of the earliest hominids. This approach leads to a search for magic traits, such as flat face, small canine, and thick enameled teeth, which are considered almost universally to be hominid features: for when only modern chimpanzees and humans are compared, these features seem to be obvious and clear. However, it is necessary to understand their meaning and emergence before using them as a reference. When Miocene hominoids are included in the study, these same features are found to occur in many of them, suggesting that a flat face, small canines, and thickenameled cheek teeth are plesiomorphic and that the elongated face of chimps, their large canines, and thin enameled cheek teeth are apomorphies of the chimpanzee clade rather than plesiomorphies of hominoids. Exclusion of the fossils in the comparisons of modern apes and humans erases the diversity of the past which is the raw material for understanding our evolution..2 The rise and fall of the Ramapithecus Kenyapithecus group During the 190s and 1970s, it was widely claimed that Kenyapithecus (sometimes considered to be an African relative of the Asian Ramapithecus) was a hominid, aged ca. 15 Ma. This idea (Leakey 191, 192; Simons 191; Simons and Pilbeam 195; Andrews 1971) was questioned by some morphologists (Genet Varcin 199; Greenfield 1978). The divergence between apes and humans was thus considered

4 1522 The earliest putative hominids by these authors to be very ancient (about 1 Ma or even close to 20 Ma). But in the 1970s, the development of molecular biology and the application of the molecular clock led to the notion that the dichotomy was considerably more recent, and ages of divergences for the African great apes and hominids of about 2 4 Ma were proposed (Wilson and Sarich 199). It was in this context, 30 years ago, that Lucy and the Afar australopithecines were discovered in 3 millionplus year old deposits (Johanson and Taieb 197). Considered at the time to be the earliest hominid, these fossils were later formalized as Australopithecus afarensis (Johanson et al. 1978). This major discovery was widely acclaimed: for the first time, we could examine a quasi complete fossil skeleton of an early time; the earliest stages of bipedalism (a key feature in the definition of hominids) could be seen, and we could get information on body proportions of the earliest members of our family Hominidae. Not least, Lucy was considered by many to occur in the range of dates estimated by the famous molecular clock, which at the time suggested that the dichotomy between apes and humans took place about 4 Ma (Wilson and Sarich 199). Subsequently, it was demonstrated that the molecular clock was not reliable as it did not run at a constant rate in mammals and in particular in primates (Britten 198; Pickford 1987; Stanyon 1989). In numerous papers, a large variety of dates was advanced for the dichotomy between apes and humans, depending on the calibration ages accepted in the studies and the type of protein used for the demonstration: these dates ranged from 2.5 up to 4 Ma. But the fossils seemed always to give an earlier date. The question of an early or a late divergence was addressed by Greenfield (1980): he had already proposed that Sivapithecus (¼Ramapithecus) brevirostris and Sivapithecus (¼Kenyapithecus) africanus were size variants of Sivapithecus, and he suggested a late divergence for the group of Homo, Pan, and Gorilla from the pongid stock. However, the age of this dichotomy that he published (10 5 Myr) was greater than the one proposed by geneticists. Following general acceptance of the molecular evidence that supported a divergence between chimpanzees and humans around 4 Ma, the matter of chronology was thus thought to be solved and neither Ramapithecus nor Kenyapithecus was subsequently considered by many authors to be hominid. By the end of the 1970s, the Kenyapithecus material had been restudied, especially in the light of sexual dimorphism in modern and fossil apes (Greenfield 1978, 1979; Pickford 198; Pickford and Chiarelli 198). It transpired that the group of Ramapithecines Kenyapithecines did not belong to Hominidae and as a result the Middle Miocene estimates for the dichotomy between apes and humans were abandoned. Eventually a meeting organized at the Vatican in 1982 led to a consensus between paleontologists and molecularists: 7 Ma was the date of the divergence adopted at this meeting.

5 The earliest putative hominids 1523 However, despite the fact that several isolated fossils of putative early hominid ancestors were already known at that time, such as the Lothagam mandible thought to be close to 7 Myr old (Patterson et al. 1970), the Lukeino lower molar (Pickford 1975), and the Kanapoi humerus (Patterson 19; Patterson and Howells 197), these materials were too fragmentary to be taken seriously by most paleoanthropologists and there was a tendency to avoid them in the phylogenies. Then Coppens (1983) reconsidered all the hominoids, some of which had been attributed to hominids. Taking into account environmental changes, chronology and geography, he formalized his East Side Story. Until the end of the twentieth century, australopithecines were considered to be direct ancestors of humans, even though some scholars pointed out that more modern forms existed during the same period, which implied that early Plio Pleistocene hominids were more diverse than expected and that australopithecines might have been a side branch of human evolution (see Senut 1992 for a review). But by the end of the twentieth century, it was widely accepted that the earliest hominid ancestor was to be found in the Early Pliocene..3 Bipedalism and its impact on the origins of Hominidae Among living primates, facultative bipedalism is frequent; but even if primates can sit with the back upright, stand on two feet, and walk bipedally for short distances, humans are the only ones that can move on two legs for long distances and extended periods of time. This difference is reflected in the skeletal characters of extant humans, often defined in comparison with chimpanzees. While a suite of features linked to femoral, pelvic, or sacral morphology appears to be soundly based, others are questionable. This is the case with the position of the foramen magnum. For the past 80 years, following Dart (1925), most scientists have considered that an anterior position of the foramen magnum indicates bipedality in hominids. Clark Le Gros (1950) used the anterior position of the occipital condyles to confirm the hominid nature of the australopithecines and proposed a condylar position index, but he noticed that in modern humans this position varied between dolichocephalous and brachycephalous individuals. Later (in 1972), the same author warned: It has been assumed that the condylar position index, by itself, is always correlated with the degree of postural erectness. The fallacy of this assumption is exposed by the fact that the index varies quite considerably even in modern H. sapiens. However, generic, specific, and/or populational studies remained limited before 190, despite the fact that Schultz (1955)

6 1524 The earliest putative hominids highlighted the variability of this feature. Since then, it has been shown that an anterior position of the foramen is not linked exclusively with bipedalism but could be related to the development of the brain (Biegert 193). Several authors demonstrated that its position relative to the cranial foramina was variable (Dean and Wood 1981, 1982; Schaeffer 1999; Granjean 2005). It is difficult to discriminate individuals on these isolated features as there is a great overlap between apes and humans. Different forms of bipedalism have existed in the past. Of these, the most debated concerns Oreopithecus bambolii, discovered in Late Miocene lignites of Tuscany (Hürzeler 1958; Schultz 190; Straus 193; Sarmiento 1983; Tardieu 1983; Senut 1989) and which was recently demonstrated to be bipedal (Köhler and Moyà Solà 1997; Rook et al. 1999). For the pedal features, these authors showed that this Miocene ape could move bipedally when on the ground, but with a stabilization morphology that differed from those of humans and australopithecines. Oreopithecus lived in an island environment where the absence of large predators and limited trophic resources played an important role in the evolution of mammals (Köhler and Moyà Solà 1997)..4 The case of Australopithecus afarensis (¼antiquus) At one time every single fossil older than A. afarensis from Afar in Ethiopia was considered to be the earliest human ancestor; and this ancestor was almost always interpreted as being in the direct line leading to the genus Homo and then to us. However, this approach ignored or underestimated the probable diversity of Pliocene hominids. In fact, in the late 1970s, several authors had already pointed out that there might be a taxonomic problem with the species Australopithecus afarensis: was it, as claimed, a single bipedal species? Did this species include two different taxa, one of which was a combination of a climber and a terrestrial biped and the other a more advanced species which was primarily a ground dwelling biped? (see a review of Australopithecus afarensis locomotor adaptations in Stern 2000 and Coppens and Senut 1991). The difficulty derived mainly from the fact that before the 1970s, scientists had built their phylogenetic trees almost exclusively on the basis of dental anatomy, whereas the incorporation of locomotor traits led to a modification of these phylogenies. The picture became more complex in subsequent years, with a crop of new species of australopithecines being created; several of these had specimens also included in other hypodigms. This was especially clear with Praeanthropus africanus, Australopithecus afarensis, and Australopithecus anamensis. The use of cladistic methods did not clear up the problem (Strait et al. 1997; Strait and Grine 1999, among others), and

7 The earliest putative hominids 1525 the phylogenetic approach became more and more confused, various scholars using the same species in different ways without defining them. As discoveries became more and more numerous, several genera were resurrected or created: Praeanthropus, Ardipithecus, Orrorin, Sahelanthropus, and Kenyanthropus. New specimens of a Pliocene hominid were found at Sterkfontein in South Africa (Clarke 1995). A major question remains today: is Australopithecus afarensis a direct ancestor or a side branch of our family? This question is still unanswered..5 The new challenge The majority of scenarios concerning the dichotomy of apes and humans, with the exception of the East Side Story of Coppens (1983), failed to take into account the environment. Coppens hypothesis was eco geographic in nature, the African Rift Valley constituting an ecological barrier between the apes in the west and early hominids in the east from about 7 to 8 Ma. But the most important elements of his hypothesis were chronological (the divergence took place between 8 and 7 Ma) and ecological (climatic change engendering modifications in regional vegetation patterns, etc.), whereas, despite its name, the geographic element was subsidiary in terms of the evolutionary scenario. As soon as we began to look for early and/or putative hominids in strata older than the Pliocene, we found them. In 2000, the discovery of early hominid remains (O. tugenensis) in the Upper Miocene strata of Kenya, and subsequent finds in Middle to Upper Miocene sediments of the same country, shed new light on the question of our divergence from the African apes. The Orrorin discovery was subsequently followed by finds in Ethiopia (Ardipithecus kadabba) and then Chad (Sahelanthropus tchadensis). The debate mainly focused on the C/P3 complex and on adaptations to bipedalism, and the status of these two species is still a matter of debate. But the main disagreement lies in the fact that in several studies comparisons were made basically with modern apes and later hominids, and very little with Miocene apes. As pointed out above, structures or features supposed to be hominid apomorphies might well be retained from older Miocene apes and some of the modern African ape features, usually considered to be primitive, might not be so..5.1 Ardipithecus ramidus In 1994, Australopithecus ramidus was published and in 1995 it was attributed to a new genus Ardipithecus. This hominoid from Aramis localities 1 7 in the Middle

8 152 The earliest putative hominids Awash (Afar Depression in Ethiopia) (White et al. 1994, 1995) was announced as the earliest known hominid. All the specimens, except the humerus (which was found above the Daam Aatu Basaltic Tuff) come from a level located between the Daam Aatu Basaltic Tuff and the Gaala Vitric Tuff complex. The tuff complex, situated at the base of the sections, has been dated at Myr and an age between 4.2 and 4.5 Ma can be estimated for the fossil hominid (WoldeGabriel et al. 1994). At the time of the discovery, these fossils were among the few supposed hominids older than 4 Ma. Recently, a few more specimens have been described from the Early Pliocene at As Duma in the Gona Western Margin (Ethiopia), the ages of which have been estimated at Ma (Semaw et al. 2005). According to its discoverers, the new genus was based on differences from Australopithecus: the reduced megadontia of the postcanine teeth, the greater width of the upper and lower incisors compared with postcanine teeth, a narrow and obliquely elongated lower dm1 with a large protoconid and a small, distally place metaconid without an anterior fovea, a small, low talonid with reduced cuspule development, absolutely and relatively thinner canine and molar enamel, lower P3 and upper P3 more strongly asymmetrical, with more dominant buccal cusps. With a canine that is not mesiodistally elongated, it is distinguishable from modern African apes. However, some of the cited features including the thin enamel in the molars, asymmetrical upper and lower third molars, and the size relationships between the canines and jugal teeth places Ardipithecus closer to the chimpanzee than to any of the oldest hominids known. The first deciduous molar shows resemblances to those of bonobos. But the morphology of the canine distances Ardipithecus from apes: it is more incisiform than in the latter group. Metric comparisons of the adult teeth were made with A. afarensis and underline the diminutive size of Ardipithecus. The upper canine/lower anterior premolar complex is typical of apes and was described as being morphologically and functionally only slightly removed from the presumed ancestral ape condition (White et al p 308). However, certain features taken as support for its hominid status occur in female apes which have a reduced canine/premolar complex compared to those of males. Its postcranial bones reveal several apelike features, but the proximal humerus is more humanlike in the shallowness of the bicipital groove. However, this character occurs not only in hominids but also in other primates, such as Pongo, which is a cautious climber (Senut 1981). The fragment of occipital preserved would suggest that the foramen magnum is placed anteriorly relative to the carotid foramen, but for the reasons given above we must be cautious with the interpretation of this feature. At the end of 1994, a skeleton was found in the Aramis strata, but it has not yet been published. More recently, Semaw et al. (2005) briefly described a proximal third of a pedal proximal phalanx from the deposits of As Duma. They write: The transversely

9 The earliest putative hominids 1527 broad oval proximal facet is oriented dorsally, a character diagnostic of bipedality, and a trait also seen in Ardipithecus kadabba. But, Rose (198) had already described the same feature in Sivapithecus from the Miocene of Pakistan. Given such weak evidence, it is difficult to accept bipedalism in Ardipithecus ramidus. On the basis of the fauna, the botanical and sedimentological indications, the environment of Ardipithecus ramidus at Aramis is a forested one (WoldeGabriel et al. 1994). In the Gona sites, the faunal association, carbon isotopes, and sedimentology suggest a moderate rainfall woodland and woodland/grassland (Semaw et al. 2005)..5.2 Orrorin tugenensis The discovery of Orrorin led to the elucidation of several aspects of early hominids (Senut et al. 2001). The specimens come from four sites: Cheboit, Kapsomin, Kapcheberek, and Aragai in the Lukeino Formation aged ca. Ma ( 5.8 Ma) (Bishop and Chapman 1970; Bishop and Pickford 1975; Chapman and Brook 1978; Kingston et al. 1994; Pickford and Senut 2001) (> Figure.1). The Lukeino Formation overlies the Kabarnet Trachyte dated by K/Ar, paleomagnetism, and biochronology at.1 Ma and is overlain by the Kaparaina Basalt, the age of which is estimated to be 5.7 Ma (Sawada et al. 2002). In the section, Cheboit and Aragai are the oldest sites, followed by Kapsomin and then Kapcheberek which lies in the upper level of the formation. Up to now, 20 specimens of Orrorin have been found consisting of the posterior part of a mandible in two pieces, a symphysis and several isolated teeth, as well as three femoral fragments, a partial humerus, a first phalanx, and a distal thumb phalanx. The genus is defined by its jugal teeth being smaller than those of australopithecines, an upper canine short with a shallow and narrow vertical mesial groove and a low apical height, a small triangular upper M3, a lower P4 with offset roots and oblique crown, small Homo like rectangular lower M2 and M3, thick enamel on the lower cheek teeth, a buccal notch well developed on the cheek teeth, no cingulum on the molars, a femur with a spherical head rotated anteriorly, the femoral neck elongated and oval in section, a medially salient lesser trochanter, a deep digital fossa, a humerus with a vertical brachioradialis crest, a curved proximal manual phalanx, and a dentition that is small relative to body size. Orrorin differs from Australopithecus in the morphology of the cheek teeth, which are smaller and less elongated mesiodistally. It differs from Ardipithecus by the greater thickness of enamel. It differs from both by the presence of a mesial groove on the upper canine. The upper and lower canines exhibit an apelike morphology, seen in female chimpanzees and Miocene apes; they are reduced in comparison with Pan. The apex of

10 1528 The earliest putative hominids. Figure.1 Remains attributed to Orrorin tugenensis in 2000 the upper canine is pointed and almost sectorial, and a poorly developed lingual wear facet is visible. The femora reveal that Orrorin was bipedal (Senut et al. 2001; Pickford et al. 2002; Galik et al. 2004). However, the other postcranial bones suggest that it could climb trees. The distal phalanx of the thumb exhibits features which are classically (but probably erroneously) associated with the manufacture of tools; these traits could be related to grasping abilities when climbing trees (Gommery and Senut, 200).

11 The earliest putative hominids 1529 At the time of its discovery, Orrorin was the first known bipedal hominid older than 5 Ma and indicated that the dichotomy between the African apes and the hominids had to be older than Ma and that the classic recent dates of divergences estimated by molecular biologists did not fit with the paleontological evidence. On the other hand, the locomotor and dental features suggest that Orrorin was different from Australopithecus afarensis. It was a microdont animal with small postcanine teeth and a rather large body size, whereas Australopithecus was a megadont hominid with large postcanine teeth and small body size. Modern humans are microdont. Orrorin did not live in an open environment but in a more forested one as suggested by the faunal remains, such as impalas, colobines, water chevrotain, arboreal civets, and floral remains, which contain large leaves with drip points (Pickford and Senut 2001; Senut and Pickford 2004; Senut 200) from which it is concluded that in its early stages, bipedalism was not related to dry environments (Senut 200). The humid conditions persisted in the Lower Pliocene (Pickford et al. 2004)..5.3 Ardipithecus kadabba Material discovered in Ethiopia (Haile Selassie 2001) from sediments aged between 5.2 and 5.7 Ma was identified as belonging to a subspecies of Ardipithecus ramidus, more recently raised to the specific rank Ardipithecus kadabba (Haile Selassie et al. 2004). The material was collected at five different sites: Digiba Dora, Asa Koma, Alayla, Saitune Dora, and Amba East, from the Asa Koma Member of the Adu Asa Formation. The first four are in the Asa Koma Member of the Adu Asa Formation, and the deposits which have yielded the hominids are securely dated at Myr by radiometric methods applied to underlying and overlying basalts. The Amba East material is slightly younger, being from the Kuseralee Member of the Sagantole Formation dated at Ma (Renne et al. 1999). The morphology of the upper canine crown with a more rounded outline differs from Orrorin; but it also differs from Ardipithecus ramidus in the crest pattern of the same tooth, as well as in the morphology of the lower premolar which is more asymmetric in outline, and by the presence of a small anterior fovea. Moreover, the lingual cusps are more salient and sharp in the lower M3 and the upper M3 bears four cusps. The species Ardipithecus kadabba differs from extant apes by its canines, which have a tendency to be incisiform as in A. ramidus, and by the presence of a clearly defined fovea on the lower P3, which is isolated from the mesial marginal ridge by a fold like buccal segment. The postcranial morphology (Haile Selassie 2001)

12 1530 The earliest putative hominids indicates several similarities to African apes and selected specimens from the Hadar, but the shape of the ulnar olecranon differs from that of hominids. A proximal pedal phalanx resembles the ones from Hadar, and on the basis of the dorsal orientation of the proximal facet of the bone, it supposedly belongs to a bipedal animal. However, the curvature seen in the Ardipithecus kadabba phalanx might be linked with arboreal adaptations as discussed by several authors (Stern and Susman 1983; Susman et al. 1984), and we must remain careful when assessing a locomotor complex on the basis of restricted material. Ardipithecus kadabba is associated with relatively wet and wooded environments as indicated by the fauna. As for the Amba East site, it seems slightly drier (WoldeGabriel et al. 2001)..5.4 Sahelanthropus tchadensis The discovery of Sahelanthropus in Chad was published in 2002 (Brunet et al. 2002; Vignaud et al. 2002). Announced as the earliest known hominid, this status has been the subject of debate (Wood 2002; Wolpoff et al. 2002). It was found at Toros Menalla (Chad) in deposits dated between and 7 Ma, maybe closer to 7 Ma, by comparison with the Lukeino Formation and Nawata Formation (Vignaud et al. 2002). The following diagnostic features of the species have been published: orthognathic face and weak subnasal prognathism, small ape sized braincase, long and narrow basicranium, small canines, robust supraorbital torus, absence of supratoral sulcus, marked postorbital constriction, small, posteriorly located sagittal crest and large nuchal crest, wide interorbital pillar, low crowned jugal teeth and enamel thickness between that of Pan and Australopithecus, and anterior position of the foramen magnum. It is considered different from all the living great apes because of the relatively small canines, the apical wear of the canines, and a probable non-honing C/P3 complex. The claimed hominid status is based on the small, apically worn canine and on the structure of the face. However, when these complexes are considered among all fossil and extant hominoids, it appears that they are more frequent than believed. The maxillofacial complex in extant apes varies according to sex just as it does in Miocene hominoids (Proconsul, Kenyapithecus, Ramapithecus). It was this combination of features that originally led to Ramapithecus being proposed as a hominid, whereas it is today thought to be the female of Sivapithecus. Bipedalism in Sahelanthropus has been inferred from the position of the foramen magnum, but again, for the reasons expressed above, this feature can be misleading. The cranial base and nuchal area of Sahelanthropus (with its strongly developed nuchal crest and the flatness of the occipital) seem more apelike to some authors (Wolpoff et al. 2002),

13 The earliest putative hominids 1531 suggesting a quadrupedal posture and locomotion despite the reconstruction proposed by Zollikofer et al. (2005), which fails to bring more evidence to the debate. The orientation of the plan of the foramen magnum falls within the range of variation of modern apes (Pickford 2005). Whatever Sahelanthropus is, its status as a hominid is still being debated (Wood 2002). Sahelanthropus was found in perilacustrine sandstones and the sedimentological context suggests a mosaic of environments between lake and desert, which have been compared with the Okavango delta.. An earlier dichotomy? During the past decade, several apelike fossils have been discovered in the Baringo District (> Figure.2): a lower molar in the 12.5 Ma Ngorora Formation and three fragmentary teeth from the Lukeino Formation found in the same strata as O. tugenensis...1 Ngorora In 1999, a lower molar was collected at Kabarsero, Ngorora Formation, Tugen Hills (Pickford and Senut 2005) 12.5 Ma (Bishop and Pickford 1975). This tooth, probably a lower M2 (Pickford and Senut 2005), is close in morphology to Dryopithecus (Begun 2002) and chimpanzees and distant from similarly aged Kenyapithecus and Otavipithecus (Conroy et al. 1992; Ward and Duren 2002). An upper molar had already been described from Ngorora (Bishop and Chapman 1970; Leakey 1970; Bishop and Pickford 1975), but it appears to be closer in morphology to Kenyapithecus (Ishida and Pickford 1998; Pickford and Ishida 1998; Senut 1998), and the thickness of the enamel and the more centralized. Figure.2 (a) Bar , right lower molar, stereo occlusal view; (b) Pan paniscus right m/2, occlusal view; (c) Pan troglodytes, right m/2, occlusal view; (d f) Dryopithecus brancoi lower molars from Europe, d¼trochtelfingen, e¼salmendingen, f¼ebingen; (g) Gorilla gorilla lower m/ 2, occlusal view; (h j) Bar , Kapsomin large ape, occlusal, lingual, and oblique views; (k) Gorilla gorilla, M2/, oblique view; (l) Australopithecus afarensis, upper M2/, occlusal view; (m) Gorilla gorilla upper M2/, occlusal view; (n) Pan troglodytes, upper M1/ M3/, occlusal view; (o) O. tugenensis upper molar row, occlusal view; (p) Bar , detail of dentineenamel junction at hypoconulid; (q) KNM LU 335, Orrorin tugenensis, left m/3, occlusal view; (r) Praeanthropus africanus cast of upper incisor from Laetoli, lingual view; (s) BAR , Kapsomin large ape, lingual view; (t) Gorilla gorilla upper central incisor, lingual view; (u) Praeanthropus africanus cast of upper incisor from Laetoli, distal view; (v) BAR , Kapsomin large ape, distal view; (w) Gorilla gorilla upper central incisor, distal view

14 1532 The Figure.2 (continued) earliest putative hominids

15 The earliest putative hominids 1533 cusps suggest that it belongs to a different hominoid from that of the lower molar. Two different kinds of hominoids would have coexisted at Kabarsero, a possibility which is also suggested in the Lower (Napak) and Middle (Moroto) Miocene sites of Uganda (Gommery et al. 1998, 2002). If the derived characters of the Ngorora tooth are homologous to those of chimpanzees, then it would indicate that chimps were already a separate lineage by the end of the Middle Miocene, a suggestion that accords with some interpretations of the molecular data (Arnason et al. 2001). The resemblances between the Ngorora tooth and Dryopithecus indicate that the latter genus may have originated in Africa and migrated toward Europe about 12.5 Ma...2 Kapsomin In 2002, half an upper molar of a large hominoid was found at Kapsomin, Lukeino Formation, aged 5.9 Ma (Pickford and Senut 2005). This tooth is larger than those of O. tugenensis and the crown morphology is different. The trigon is wide, the distal fovea broad, the main cusps high and less inflated, and there is a deep buccal slit. The dentine penetrance is also high. Most of these features occur in Gorilla and are different from Pan. In 2000, an upper central incisor was found in the same strata as Orrorin. Originally assigned to O. tugenensis, its morphology did not seem to fit with the early hominid. After a restudy of the specimen, it appears that it differs strongly from australopithecines and other hominids because of the lack of fossa on the lingual side of the tooth. Moreover, the crown is relatively low compared to root length, whereas in hominids the crown is higher with a scoop shaped profile. In contrast, in Gorilla incisors, the lingual fossa is missing and the crown is wedge shaped. In 2003, a lower molar was found at Cheboit, near the site of discovery of the first hominid tooth from the Lukeino Formation (Pickford 1975). The morphology of the tooth is compatible with the half upper molar from Kapsomin and the specimens probably belong to the same taxon. As for Ngorora and the Ugandan sites, two different hominoids would have coexisted at Kapsomin in the same strata, Ma..7 Conclusions The debate about our earliest origins is probably not closed and is fueled by the poverty of fossils in the time period between 12 and 4 Ma. This is why it is

16 1534 The earliest putative hominids necessary to continue excavation and prospecting in different areas of Africa in order to fill the gaps and extend our knowledge of variation. One of the most troubling aspects of the research done to date on the origins of hominids is related to the comparative samples. Most scientists still focus on modern hominoids as good reference for primitive morphologies. However, these animals are highly derived in their cranial and postcranial anatomy. As long as Miocene apes are not properly considered in these studies, we will remain trapped in the quest for a mythical missing link. Of all the features used to define hominids, probably the least controversial is bipedalism. We know that in the past there have been several types of bipedalism, but there is definitely a basic one that is known in australopithecines, Orrorin and Homo. In this group, adaptation to arboreality is variable: greater in some taxa, less in some others, and very little in Homo. There was probably a variety of early forms of hominids; the oldest widely accepted biped (supported by postcranial evidence) is Orrorin and we await further data on Ardipithecus and Sahelanthropus to clarify their status (> Figure.3). What the evidence from the Upper Miocene tells us is that we cannot continue to support an origin of the earliest. Figure.3 Proposed relationships between early hominids and late apes

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