1 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 MANUSCRIPT: Title: The Fossil Records of Early African Homo Byline: Kes Schroer and Chrisandra Kufeldt Introduction: Molecular and paleontological evidence suggests that modern humans first originated in Africa as early as 250,000 years ago. However, fossil remains in Eurasia dating to at least 1.8 mya (million years ago) suggest that some of our ancient relatives had already migrated out of Africa by the time modern humans emerged. Thus, the peopling of the world does not begin with modern humans. Rather, the fossil record suggests a long history of previous occupations in Africa and Eurasia. In this review, we discuss the nearest fossil relatives of modern humans. The fossil species we review include the early members of the genus Homo, a group within the broader category of “hominins” (all primate species more closely related to modern humans than to any other living taxon). Early Homo likely shared its environment with non-Homo hominins such as Paranthropus, a taxon with a suite of morphological features distinct from the derived characteristics of the genus Homo. When we speak of derived traits in Homo, we mean traits shared with modern humans. In contrast, primitive traits are morphological features shared by all hominins and therefore not unique to Homo. Both primitive and derived traits are combined to define the morphology of a fossil taxon. “Taxon” (pl. taxa) refers to a hierarchical category and although taxon is often equated with species, this is not necessarily correct. “Homo” is a genuslevel taxon while our species, Homo sapiens, is a species-level taxon. Because it is difficult to establish speciation events for certain in the fossil record, we prefer to use the term taxon and begin by reviewing the definition of the taxon Homo. Definition: What is Homo? In 1940, Franz Weidenreich proposed the inclusion of several hominin fossils in the genus Homo on the basis of their morphological similarities with two well-established taxa of Homo known at the time, H. sapiens and Homo neanderthalensis (Neanderthals). These additional specimens were classified as Homo erectus. The addition of a new taxon to the genus Homo necessitated an improved definition of the genus Homo. In 1950, Ernst Mayr proposed that Homo was a genus of modern human-like creatures whose members showed morphological evidence of increased brain size and bipedal locomotion. However, this definition was unsatisfactory, for it would have included specimens belonging to, Australopithecus, a different hominin genus established in 1925. Wilfrid Le Gros Clark expanded upon Mayr’s definition and provided four critera for inclusion into the genus Homo: a minimum endocranial volume of 750 cc (cubic centimeters), evidence of tool use, evidence of a precision grip, and evidence of spoken language. Additionally, he suggested that derived morphological traits of Homo included a cranium with less robust muscular markings, a flatter (more orthognathic) face, a rounded dental arcade with no evidence of a premolar-canine honing complex, smaller teeth, and adaptations for bipedalism. 2 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 This description of Homo has undergone many revisions and interpretations, especially in light of the discoveries of many more hominin fossils since the 1950s. Some of the modifications to this definition are discussed in the text that follows, but it is important to note that researchers today have the benefit of more fossils and more rigorous phylogenetic methods to assess the evolutionary relationships of modern humans and fossil hominins. One prominent cladisticsbased definition describes the crania of members of Homo as possessing, relative to Australopithecus, a thicker cranial vault, greater cranial vault height, reduced postorbital constriction, increased contribution of the occipital bone to the cranial sagittal arc length; an anteriorly-situated foramen magnum, reduced prognathism, narrow tooth crowns especially in the premolars, and reduction in the length of the molar row (Chamberlain and Wood, 1987). Another phylogenetic study found only four derived features common to all members of the genus Homo – a larger brain, the absence of a nasal sill, reduced temporal lines, and fewer air cells in the temporal squama (Strait et al., 1997). Though there are discrepancies between analyses, definitions of Homo are becoming more specific and quantifiable. In both historic and modern approaches to defining the genus Homo, there is a wellrecognized distinction between the earliest forms of Homo that still share many traits with Australopithecus and intermediate forms of Homo that appear more like H. sapiens but have not yet reached complete anatomic modernity. We refer to these groups as transitional Homo and pre-modern Homo, respectively, and discuss the significance, morphology, and key fossils of the taxa within these groups below. Historical Background: Transitional Homo – Homo habilis Significance From 1960-1963, a series of fragmentary fossils were found in Olduvai Gorge, Tanzania that seemed to belong to a new Homo taxon. Despite some morphological similarity to younger Homo remains, these fragments (OH 4, a mandibular fragment, and OH 6, cranial fragments and an upper molar), were considered too incomplete to determine a new species. Instead, the announcement was made after the discovery of OH 7, an associated find of fragmentary parietal bones, a badly damaged juvenile mandible but with the tooth crowns in good condition, an isolated upper molar, and hand bones. The discoverers of OH 7 noted derived traits shared between this specimen and members of the genus Homo, but the endocranial volume of OH 7 was unusually small for Homo. The discoverers of OH 7 combined its announcement with a revision to the criteria for membership in Homo that reduced the requisite endocranial volume to only 600 cc and thus within the upper range of Australopithecus. This decision was met with objection by other researchers. Since OH 7 was found in the same stratigraphic level as primitive (i.e., Oldowan) stone tools, it was dubbed Homo habilis, the Handy Man. In addition to proposing a new species of Homo, the announcement of H. habilis changed our understanding of the depth of the evolutionary history of the genus Homo. The stratigraphic level of OH 7 dates to 1.8 mya, a million years earlier than the previously known emergence date of Homo. Morphology 3 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130 131 132 133 134 135 136 137 Some researchers argue that H. habilis marks the first evidence for derived features such as encephalization (Tobias, 1966; 1971), a more modern human-like cranium and face (Bromage, 1989), and reduction in the size of the tooth and jaw size (Vandebroek, 1969). H. habilis appears especially distinct from Australopithecus in the shape of its cranial base (Wood, 1996). Until the discovery of potential tools at Dikika dating to 3.39 mya, H. habilis was also considered the oldest tool-making hominin. H. habilis has some modern human-like features of its hand bones that suggest the ability to craft tools. The trapezium, the wrist bone that articulates with the thumb, has a broad articular surface that would have allowed for a wide range of medial rotation, and H. habilis has broad apical tufts on the distal phalanges that suggest robust finger tips (Napier, 1962; Tocheri et al., 2008). However, some researchers consider the morphology of H. habilis too primitive for inclusion in the genus Homo. With an average of 680 cc among specimens, the cranium of H. habilis is only slightly larger than Australopithecus, and the crown areas of the cheek teeth are not notably reduced. Even the bones of the hand appear less modern human-like than originally believed. The phalanges are curved and robust, with fibrotendinous marks suggesting frequent climbing. Some aspects of the wrist, including broad lunate and scaphoid articular surfaces, also appear primitive. Whether or not H. habilis possessed the precision grip that defines modern human hands cannot be reliably determined from the current evidence. Whether or not emerging Homo possessed the striding gait of modern humans is also a matter of debate. Although the foot of H. habilis (OH 8) possesses some adaptations for supporting the body during bipedal walking, its morphology does not suggest a propulsive role for the big toe. The foot overall retains ape-like morphology consistent with climbing, and the femur has a knee-joint not well adapted for modern bipedalism. It is possible that H. habilis shared a form of bipedalism with Australopithecus that was unlike the gait of H. erectus and later H. sapiens. Recently, some researchers have re-opened the proposal that the OH 8 foot may not belong to early Homo, but to Paranthropus boisei (Gebo and Schwartz, 2006). Notable fossils In addition to the type specimen OH 7, Olduvai has yielded many fragmentary remains of H. habilis. Notable specimens include OH 8, dating to 1.76 mya. The fossils comprising OH 8 are a well preserved left foot (see above), some dental fragments, and the adult hand bones originally grouped with OH 7. The foot is likely adult and therefore not part of the juvenile OH 7. However, some researchers argue that the foot is juvenile, in which case it could belong to the same individual as OH 7, and the remains of a tibia and fibula (OH 35) may also belong to the same individual (Susman and Stern, 1982). However, this unlikely as the discrepancies in joint surfaces and the respective stratigraphic and spatial locations of OH 7, OH 8, and OH 35 are not consistent with them belonging to the same individual. Other discoveries of H. habilis at Olduvai include two fragmentary juvenile skulls (OH 13 and OH 16) a fragmented and distorted cranium (OH 24), and a partial skeleton (OH 62). The skulls of OH 13 and OH 16 date to 1.7 mya, and the OH 24 and OH 62 date to at least 100,000 years earlier. The OH 24 cranium includes derived cranial traits distinct from Australopithecus such as reduced postorbital constriction, an inverted V-shape formed by the lamboidal suture, 4 138 139 140 141 142 143 144 145 146 147 148 149 150 151 152 153 154 155 156 157 158 159 160 161 162 163 164 165 166 167 168 169 170 171 172 173 174 175 176 177 178 179 180 181 182 and a more modern human-like mandible. The cranial capacity, however, is small even compared to the juvenile OH 7. The OH 62 partial skeleton allows for a poor estimate of body proportions in H. habilis, and the forelimb to hindlimb proportions are suggested to be more ape-like than those of Australopithecus. Although these differences in limb proportions may be the result of intraspecific variation, they may also be evidence that H. habilis did not share the locomotor style of later hominins. Beginning in the 1970s, transitional Homo remains were also recovered from the site of Koobi Fora, Kenya (Figure 1). KNM-ER 1813 is a nearly complete cranium with a cranial capacity of only 510 cc. It dates to 1.88-1.90 mya, although earlier dates have been proposed (Gathogo and Brown, 2006). The incomplete skull KNM-ER 1805, which is possibly older than 1.87 mya, is similar to KNM-ER 1813 and both specimens are often designated as examples of H. habilis. However, some researchers argue that some unusual features of the cranium and teeth of KNM-ER 1805 preclude it from belonging to early Homo. A recent discovery at Koobi Fora, the KNM-ER 42703 maxilla, dates to 1.44 mya, and expands the temporal range of H. habilis to much later than previously thought. Also found at Koobi Fora is KNM-ER 3735, a partial skeleton with evidence of the cranium, the upper limb and its girdle, the sacrum, and the lower limb dating to 1.88-1.9 mya. The postcranial evidence of KNM-ER 3735 is more similar to Australopithecus than OH 62; the scapula and radius are especially ape-like. The geographical range of H. habilis expands beyond the boundaries of the principal sites of Olduvai and Koobi Fora. A fragmentary cranium, L 894-1, dating to 1.8 mya, that comes from the Shungura Formation, Omo, Ethiopia is comparable to OH 13 and OH 24. A maxilla from Hadar, Ethiopia (AL 666-1) extends the earliest known date of appearance for H. habilis to 2.3 mya. A temporal bone KNM-BC 1 from the Tugen Hills, Kenya dates to 2.4 mya and has also been referred to transitional Homo. One African specimen outside of eastern Africa has been likened to H. habilis though never formally included in its hypodigm. STW 53 is a well-preserved cranium from Sterkfontein, South Africa that dates to at least 2.0-1.5 mya. Examination of the bony labyrinth of STW 53 suggests that it is not similar to later Homo and may have relied on less bipedal locomotion than Australopithecus (Spoor et al., 1994). Cladistics analyses that treat this specimen as its own taxonomic unit suggest it is a sister-taxon to a H. habilis/H. erectus/H. sapiens clade (Smith and Grine, 2008). Transitional Homo – Homo rudolfensis Significance Several of the transitional Homo fossils found at Koobi Fora, Kenya in the 1970s were referred to transitional Homo and later subsumed within the H. habilis hypodigm (i.e., KNM-ER 1813). Others, however, exhibited more robust features than the Olduvai sample of transitional Homo (i.e., KNM-ER 1470). Aleexev (1986) argued that KNM-ER 1470, a cranium dating to 1.88-1.95 mya, was distinct enough to constitute a new species and recommended the name Pithecanthropus rudolfensis. Groves (1989) later transferred this taxon to Homo since the genus name Pithecanthropus was no longer used. 5 183 184 185 186 187 188 189 190 191 192 193 194 195 196 197 198 199 200 201 202 203 204 205 206 207 208 209 210 211 212 213 214 215 216 217 218 219 220 221 222 223 224 225 226 227 There remains considerable debate over the Koobi Fora sample of H. rudolfensis and whether it represents a taxon distinct from H. habilis. Some authors argue that the variation within a combined H. habilis/H. rudolfensis sample reflects a high degree of sexual dimorphism or anagenetic change rather than evidence of speciation. However, if the specimens belonging to H. rudolfensis are incorporated in the H. habilis hypodigm, the resulting interspecific variation is greater than seen in several extant ape species and the pattern of variation is different from that seen in any great ape or in modern humans. Additionally, KNM-ER 1813 shares with H. habilis buccolingually narrow premolars and molars while KNM-ER 1470 does not. It is likely that two transitional Homo taxa are sampled at Koobi Fora. Morphology The suite of derived and primitive traits in the crania of H. habilis and H. rudolfensis are distinct. H. rudolfensis retains several primitive traits, including a thin-walled cranium with marked postorbital constriction and an inflated mastoid region, deep zygomatics, and larger postcanine teeth with more complex premolar and molar crowns and roots. The face of H. rudolfensis is also wider at the midface rather than the upper face as in H. habilis. However, H. rudolfensis also has more some features more derived than H. habilis, including a more orthognathic face. At 800 cc, its endocranial volume is larger than H. habilis and larger than its contemporary KNM-ER 1813, which has a cranial capacity of only 510 cc. However, when the effects of body size are taken in account, the endocranial volume of KNM-ER 1470 and H. habilis are not significantly different. Notable fossils There are several craniodental discoveries at Koobi Fora referred to H. rudolfensis but none as complete as the lectotype, KNM-ER 1470. There are no postcranial remains unequivocally referred to H. rudolfensis; the site at which potential H. rudolfensis postcrania have been found is also where cranial evidence of P. boisei, H. habilis, and H. ergaster has been found. Two femora, KNM-ER 1472 and KNM-ER 1481, may belong to H. rudolfensis. A mandible found in 2.5-2.3 mya sediments of Uraha, Malawi (HCRP-UR 501) has also been referred to H. rudolfensis. If this designation holds true, it greatly expands the geographic and temporal range of this taxon. Pre-modern Homo: Homo ergaster/Homo erectus Significance In the early 1890s, a hominin fossil found on the island of Java was classified as a new hominin called originally Anthropopithecus erectus and later Pithcanthropus erectus. This discovery, the Trinil calotte, demonstrated a smaller brain size and more primitive features than the two species of Homo (H. sapiens and H. neanderthalensis) known at the time of its discovery. The calotte was also much older than these taxa, dated originally to 500,000 years old and later closer to between 700,000 and 1 mya. Similar finds were subsequently discovered at the site of Sangiran, also on Java and at what is now called Zhoukoudian, in China. The overall 6 228 229 230 231 232 233 234 235 236 237 238 239 240 241 242 243 244 245 246 247 248 249 250 251 252 253 254 255 256 257 258 259 260 261 262 263 264 265 266 267 268 269 270 271 272 273 similarity of the cranial morphology of these Asian specimens to modern Homo eventually led to their inclusion within the genus as Homo erectus. Fossils of similar morphology were later found in Koobi Fora and dated to around 1.5 mya, 0.5 mya older than the Trinil calotte. Although the Koobi Fora specimens shared some of the derived features of H. erectus, they were less well-defined. For example, H. ergaster generally had thinner cranial vaults, less sagittal keeling, and larger and more complex premolars. Groves and Mazak (1975) argued that these early African specimens do not share the morphology of Asian H. erectus and they provided a new species name, Homo ergaster, for the East African sample. However, some researchers argue that the East African sample is an early form of H. erectus that does not require a separate name and they refer to this taxon as “early African Homo erectus” (Kramer, 1993). Morphology Homo ergaster is, in general, more modern-human like than transitional Homo. The mandible of H. ergaster is reduced in size compared to transitional Homo as is the dentition of H. ergaster. However, the endocranial volume of H. ergaster is still relatively small, and when body size is taken into account, the endocranial volume is not significantly larger than Australopithecus. Homo ergaster is the earliest hominin to demonstrate a modern body form. H. ergaster is also larger than hominins of the past, with an especially significant increase in the height of females. The lower limbs of H. ergaster and its modern thoracic shape suggest bipedal locomotion, with no evidence of climbing adaptations. Cross-sectional measures of the femoral and humeral shafts demonstrate a modern human-like strength in the forelimbs and hindlimbs, and the pelvis is similar to modern humans. Additionally, the semicircular canal structure of the inner ear is similar to modern humans and suggests upright posture (Spoor et al., 1994). It is probable that H. ergaster was capable of long-distance walking and transport, and possibly adapted to endurance running. Archaeological evidence from H. ergaster localities suggests that raw materials for stone tools were being carried over long distances (Anton, 2003). Notable fossils The KNM-ER 992 mandible that dates to 1.5 mya is the type specimen of H. ergaster. The first well-preserved cranium of H. ergaster to be recovered is KNM-ER 3733, which dates to 1.78-1.65 mya; it has an endocranial volume of about 848 cc. This is similar to the endocranial volume estimates for KNM-ER 3883, an H. ergaster calvaria that dates to 100,000 years later. The 1.55 mya cranium without a face, KNM-ER 42700, is referred to H. ergaster but it has an estimated adult body size more similar to transitional Homo. This relatively large range of body size suggests that H. ergaster may have retained a high degree of sexual dimorphism. Among the postcranial remains known for H. ergaster, two notable discoveries are KNM-ER 803, a partial skeleton dating to 1.5 mya, and KNM-ER 3228, a 1.9 million year old pelvic bone. These fossils provide evidence that H. ergaster shared a similar walking pattern with modern humans. Perhaps the most significant fossil remains of H. ergaster are those of KNM-WT 15000 (Turkana Boy), a well-preserved skeleton of an 8-12 year-old boy dating to 1.55 mya. Found in 1984, KNM-WT 15000 took four seasons to excavate and is one of the most complete skeletons 7 274 275 276 277 278 279 280 281 282 283 284 285 286 287 288 289 290 291 292 293 294 295 296 297 298 299 300 301 302 303 304 305 306 307 308 309 310 311 312 313 314 315 316 317 318 319 in the early human fossil record. The discovery demonstrates conclusively that H. ergaster possessed modern limb proportions and a modern body shape. The teeth of KNM-WT 15000 provide for some life history reconstruction, and it has been determined that H. ergaster shares a similar dental development pattern with transitional Homo (Dean and Smith, 2009). This suggests that modern life history patterns originated late in human evolution. Turkana Boy also has a cranial capacity of 909 cc, which is still small relative to later Homo. All specimens formally referred to H. ergaster come from Kenya, but other H. ergaster/H. erectus-like remains have been found in Ethiopia, Tanzania, and South Africa. At Konso, Ethiopia, the left side of mandibular corpus with preserved postcanines was found in association with Acheulean tools. This specimen, KGA 10-1, dates to 1.4 mya and has strong similarities to KNM-ER 992. At Olduvai, several specimens have been formally referred to early African H. erectus. The OH 9 partial calvaria has a well-preserved supraorbital region and dates to 1.5-1.2 mya. The OH 12 skull, which comprises a fragmentary calvaria plus part of the mandible, is more recent (c. 0.78 mya) yet its endocranial volume of 727 cc is substantially smaller than that of OH 9. Among the hominin remains at Swartkrans, SK 15, SK 45, and SK 847 have been referred to early H. erectus. SK 15 is a distorted mandibular corpus dating to 1.5-1.0 mya, and SK 45 is a fragment of the right mandible dating to 2.0-1.5 mya. SK 847 is known as the “Composite Cranium” and also dates to 2.0-1.5 mya. In 1969, 20 years after their discovery, Ron Clarke realized that the fossils SK 80, SK 846, and SK 847 belonged to the same individual. Today, SK 847 is composed of the left side of the face and cranial base. Some authors argue its affiliation is with H. erectus, but others refer all three of these specimens to transitional Homo (Strait et al., 1997). Key Issues: Phylogenetic relationships Phylogenetic analyses demonstrate that H. habilis is not consistently grouped more frequently with Homo than with Australopithecus, and some argue for its removal from the hypodigm of Homo. Still other researchers maintain that there exists phylogenetic support for a clade of Homo that includes H. habilis, with H. habilis as the possible sister-taxon of H. ergaster. Regardless of whether or not H. habilis belongs in the genus Homo, it is unlikely to prove an ancestor of later hominins such as H. ergaster because some remains of H. ergaster are found in the same fossil localities and date to the same era as H. habilis. Homo habilis and H. rudolfensis overlap significantly both temporally and geographically, and their potential sister-taxa relationship is often debated. Like H. habilis, H. rudolfensis does not group consistently with Homo, and it is possible this taxon represents a member of Australopithecus. However, Homo rudolfensis may also represent a better candidate for the ancestor of H. ergaster/H. erectus than H. habilis based on its cranial shape (GonzalezJose et al., 2008). This ancestral relationship, however, is unlikely since H. rudolfensis and H. ergaster also overlap considerably in time and place. H. ergaster’s inclusion in the genus Homo is well established, but its relationships to other Homo taxa are debatable (Figure 2). Homo ergaster overlapped significantly in time and place with members of transitional Homo, suggesting they do not have an ancestor-descendant relationship. Similarly, the earliest known emergence dates of H. ergaster in Africa and 8 320 321 322 323 324 325 326 327 328 329 330 331 332 333 334 335 336 337 338 339 340 341 342 343 344 345 346 347 348 349 350 351 352 353 354 355 356 357 358 359 360 361 362 363 364 H. erectus in Asia are close, and it is hard to reconstruct an ancestor-descendant relationship between these two taxa if these earliest known dates of emergence are correct. Although traditionally described as “early African Homo erectus,” H. ergaster may be a sister-taxon of H. erectus or both taxa may be descendants of an earlier taxon. Dispersal from Africa Paleoenvironment Transitional Homo and H. ergaster are known from 1.9 mya and older geological sediments in east and southern Africa. Around 2 mya, Africa experienced great climate change, especially increasing aridity. Olduvai fossil plants from the same stratigraphic level as OH 7 imply the emergence of more grasslands during this time, and high C4 isotopic signals suggest the same (Cerling, 1991). High C4 signals have also been found in the lacustrine sediments around Koobi Fora (Cerling et al., 1988) and in southern Africa (Hopley et al., 2007). Grazing bovids appear to become more prevalent in East Africa around 2.4 mya, also suggesting the emergence of more grassland. Current environmental reconstructions suggest that transitional Homo and H. ergaster evolved during a time of increasing complexity and heterogeneity in the landscape, which was likely composed of a mixture of closed forests and open grasslands. While the fossil and archeological records of transitional Homo do not yet support long-distance travel, it is reasonably certain that H. ergaster made use of a wider range of landscapes than previous hominins. Certainly the presence of H. erectus in east Asia implies that hominins must have left Africa sometime before 1.3 mya ago. Out-of-Africa and the Multiregional Hypothesis Historically, there are two theories concerning the dispersal of hominins beyond Africa. The “Out of Africa” hypothesis argues that the genetic changes giving rise to modern humans evolved only once in an African population, then dispersed to Asia and Europe and subsequently the rest of the world. This theory has since been divided into Out of Africa I (the dispersal of H. ergaster/H. erectus) and Out of Africa II (the dispersal of H. sapiens). Genetic evidence demonstrates that the most parsimonious origin for modern DNA variation is Africa, lending support for this theory. The alternative hypothesis, the “Multiregional Hypothesis,” argues that gene flow between hominin populations gave rise to modern humans. Neanderthal DNA is more similar to non-African populations of modern Homo, suggesting some interbreeding between Homo populations. The debate between Out-of-Africa and the Multiregional Hypothesis is ongoing; new morphological and molecular data promise to provide some resolution in the coming years (Figure 3). Early fossil evidence of Homo outside of Africa While this review has focused on the fossil records of transitional Homo and H. ergaster/H. erectus, there are several sites outside of Africa that show evidence of these hominins or very similar taxa. Morphological analyses of these fossils provide an especially rich source of information for assessing the migration patterns of pre-modern hominins and the 9 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382 383 384 385 386 387 388 389 390 391 392 393 394 395 396 397 398 399 400 401 402 403 404 405 406 407 408 409 evolutionary origin of H. sapiens. These fossils deserve their own review, and we include here only a few highlights found in the Republic of Georgia and China. At the site of Dmanisi in the Republic of Georgia, a Homo mandible dating from 1.851.78 mya has been referred to the H. ergaster/H. erectus hypodigm. This mandible shares with Homo its small size, relative gracility, and symphyseal shape, but the mandible is also smaller than the earliest Homo currently known and includes a diminutive P4, M2, and M3. The premolars are especially narrow, similar to OH 13, a representative of H. habilis. The discovery of several skulls at Dmanisi sharing a unique combination of transitional Homo and pre-modern Homo traits has led some researchers to propose a new taxon, Homo georgicus, for this population, and at least one phylogenetic analysis suggests the cranial shape is similar to H. ergaster samples (Rosas et al., 1998). The postcrania of the Dmanisi fossils are a mosaic of primitive and derived traits, combining a small estimated body size and an encephalization coefficient within the range of H. habilis. There is no evidence of the humeral torsion seen in later Homo and the glenoid cavity is cranially oriented as in apes, suggesting the retention of adaptations for climbing. The clavicle, however, is modern like H. ergaster/H. erectus. The Dmanisi hominins also appear to have modern body proportions, including relatively long lower limbs. Longgupo Cave, a 1.96-1.78 million year old site in the Sichuan Province of China, is the site of another mosaic hominin referred to both H. ergaster and H. habilis. The Longgupo Cave remains include a fragmentary left mandible and right upper later incisor, originally referred to H. erectus. The same authors, however, note affinities with H. habilis and H. ergaster. The mandibular corpus of Longgupo Cave hominin is small for this taxon and the cusp morphology more primitive, leading some authors to identify it as an ancient ape (Etler et al., 2001). The P4 is especially distinct from the hypodigm of Asian H. erectus, having different talonid and root morphologies. Like other transitional Homo remains, the Longgupo Cave hominin was found in association with two items that may represent Oldowan tools. A second fossil site from China dating to the same era as Longgupo Cave is Yuanmou Cave in southwest China. The incisors of a hominin found in this cave strongly resemble the incisors of H. ergaster and have similarities to H. habilis. The Yuanmou Cave hominin was also found in association with stone tools. Conclusion: We are the last surviving species of a diverse hominin lineage. Previous members of our genus, Homo, were likely the earliest hominins to spread beyond Africa, having expanded beyond that continent by at least 1.8 mya. The diversity of transitional and pre-modern Homo forms is a testimony to the adaptive radiation of hominins to occupy new landscapes and ecological niches in a changing world 2 million years ago. The evolutionary and cognitive abilities that have enabled modern humans to occupy many different environments have their origins millions of years prior to the emergence of H. sapiens. Ongoing analysis of our fossil relatives H. habilis, H. rudolfensis, and H. ergaster will improve our understanding of these abilities and help us reconstruct the phylogenetic history of our lineage. Like the many modern human populations we observe today, these fossils of early Homo provide us with a view of the great antiquity of human migration, adaptation, and diversity. 10 410 411 412 413 414 415 416 417 418 419 420 421 422 423 424 425 426 427 428 429 430 431 432 433 434 435 436 437 438 439 440 441 442 443 444 445 446 447 448 449 450 451 452 453 454 455 References: ANTON, S. 2003. 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Revised stratigraphy of Area 123, Koobi Fora, Kenya, and new age estimates of its fossil mammals, including hominins. J. Hum. Evol. 51:471-9. GEBO, D.L. & G.T. SCHWARTZ. 2006. Foot bones from Omo: implications for hominid evolution. Am. J. Phys. Anthrop. 129:499-511. GONZALEZ-JOSE, R., I. ESCAPA, W.A. NEVES, R. CUNEO & H.M. PUCCIARELLI. 2008. Cladistic analysis of continuous modularized traits provides phylogenetic signals in Homo evolution. Nature 453:775-9. GROVES, C.P. 1989. A theory of human and primate evolution. Oxford: Clarendon. HOPLEY, P.J., J.D. MARSHALL, G.P. WEEDON, A.G. LATHAM, A.I.R. HERRIES & K.L. KUYKENDALL. 2007. Orbital forcing and the spread of C4 grasses in the late Neogene: stable isotope evidence from South African speleothems. J. Hum. Evol. 53: 620-34. JORDE, L.B., W.S. WATKINS, M.J. BAMSHAD, M.E. DIXON, C.E. RICKER, M.T. SEIELSTAD & M.A. BATZER. 2000. The distribution of human genetic diversity: a comparison of mitochondrial, autosomal, and y-chromosome data. 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Homoplasy and early Homo: an analysis of the evolutionary relationships of H. habilis sensu stricto and H. rudolfensis. J. Hum. Evol. 30: 97-120. MAYR, E. 1950. Taxonomic categories of fossil hominids. Cold Spring Harbor Symp. Quant. Biol. 25: 109-18. RIGHTMIRE, P. 1993. Variation among early Homo crania from Olduvai Gorge and the Koobi Fora Region. Am. J. Phys. Anthropol. 90: 1-33. ROBINSON, J.T. 1965. Homo ‘habilis’ and the australopithecines. Nature. 205:121-24. STRAIT, D.S. & F.E. GRINE. 2004. Inferring hominoid and early hominid phylogeny using craniodental characters: the role of fossil taxa. J. Hum. Evol. 47: 399-452. STRINGER, C. 1986. The credibility of Homo habilis, in B.A. Wood, L. Martin & P. Andrews (ed.) Major topics in primate and human evolution. Cambridge: Cambridge Univ. Press. STRINGER, C. 2002. Modern human origins: progress and prospects. Philos. Trans. R. Soc. 357: 563-79. WOLPOFF, M.H., X.Z. WU & A. THORNE. 1984. Modern Homo sapiens origins: A general theory of hominid evolution involving the fossil evidence from East Asia, in F.H. Smith & F. Spencer (ed.) The origin of modern humans. New York: Alan R. Liss. WOLPOFF, M.H., J.D. HAWKS & R. CASPARI. 2000. Multiregional, not multiple origins. Am. J. Phys. Anthropol. 112:129-36. WOOD, B.A. 1991. Koobi Fora research project. vol. 4 hominid cranial remains. Oxford: Clarendon. WOOD, B.A. 1992. Origin and evolution of the genus Homo. Nature. 355. WOOD, B.A. 1999. Plio-Pleistocene hominins from the Baringo Region, Kenya, in P. Andrews & P. Banham (ed.) Late Cenezoic Environments and Human Evolution: A Tribute to Bill Bishop. 13 548 549 550 551 552 553 554 555 556 557 558 559 560 561 562 563 564 565 566 567 568 569 570 571 572 573 574 575 576 577 578 579 580 581 582 London: Geol. Soc. WOOD, B.A., & J. BAKER. 2011. Evolution in the genus Homo. Annu. Rev. Evol. Syst. 42: 4769. FIGURE CAPTIONS: Figure 1. Fossil localities of transitional and pre-modern Homo in East and South Africa. Triangles denote discoveries of Homo habilis remains, squares denote discoveries of Homo rudolfensis remains, and circles denote discoveries of Homo ergaster remains. Question marks indicate that the affinities of specimens to specific taxa are uncertain. Note that most of the African continent remains unexplored. Figure 2. Proposed phylogenies and representative crania of Homo taxa. 2A. Four hypotheses of the taxonomic and phylogenetic relationships of transitional and pre-modern Homo remains (there may be others). 1) An anagenetic hypothesis suggesting that Homo ergaster is an early form of Homo erectus, descended from Homo habilis, and gives rise to modern humans. This phylogeny also shows Homo habilis and Homo rudolfensis as sister-taxa. 2) A second anagenetic hypothesis, in which Homo ergaster is instead descended from Homo rudolfensis. 3) A conservative hypothesis that places specimens referred to Homo rudolfensis within Homo habilis and specimens referred to Homo ergaster within Homo erectus. This phylogeny also indicates a direct descendant relationship between transitional Homo, pre-modern Homo, and modern humans. D) A hypothesis arguing that transitional Homo and Homo erectus are sister taxa, descended from a currently unknown ancestor. In this hypothesis, transitional Homo has no direct contribution to the evolutionary history of later Homo and modern humans. 2B: Cranial comparisons of (left to right) Homo habilis, Homo rudolfensis, Homo ergaster, and Homo sapiens in portrait (top row) and profile (bottom row) views. Casts represent Koobi Fora specimens in the collection of the National Museums of Kenya and a modern human. Figure 3. Possible scenarios of the origin of modern humans from early Homo. A) The Out-ofAfrica Hypothesis, in which modern humans evolve from an Homo ergaster/Homo erectus population in Africa, disperse throughout the world, and replace existing archaic hominin populations. B) The Multiregional Hypothesis, in which early Homo populations regularly encounter and interbreed with each other, eventually giving rise to regional but regularly interbreeding populations of modern humans.