Embed Size (px)
Citation preview
Marshall UniversityMarshall Digital Scholar
Biological Sciences Faculty Research Biological Sciences
Spring 3-2007
The Evolution of Zinjanthropus boiseiPaul J. ConstantinoBiological Sciences, [email protected]
Bernard A. WoodGeorge Washington University
Follow this and additional works at: http://mds.marshall.edu/bio_sciences_faculty
Part of the Biological and Physical Anthropology Commons, Biology Commons, PaleobiologyCommons, and the Paleontology Commons
This Article is brought to you for free and open access by the Biological Sciences at Marshall Digital Scholar. It has been accepted for inclusion inBiological Sciences Faculty Research by an authorized administrator of Marshall Digital Scholar. For more information, please [email protected], [email protected].
Recommended CitationConstantino, Paul J. and Wood, Bernard A., "The Evolution of Zinjanthropus boisei" (2007). Biological Sciences Faculty Research. 38.http://mds.marshall.edu/bio_sciences_faculty/38
The Evolution of Zinjanthropus boiseiPAUL CONSTANTINO AND BERNARD WOOD
Many people assume that OH 5, the type specimen of Paranthropus boisei,collected in 1959, was the first evidence of that taxon to be found, but OH 3,recovered in 1955, predated the discovery of OH 5 by four years. Thus, Para-nthropus boisei recently celebrated the equivalent of its fiftieth birthday. Thisreview marks that milestone by examining the way our understanding of thistaxon has changed during its fifty, or so, year history.
Several hominin taxa have beenestablished longer or have a larger fos-sil record, but Paranthropus boisei, the
hominin taxon that began life as Zin-janthropus boisei, is unusual for severalreasons. First, much of its skull mor-phology is apparently derived1–3 andhighly distinctive (Table 1). Second,most of its hypodigm comes from siteswith good stratigraphic and chrono-logical control and can be dated withrelative precision.4,5 Third, the fossilrecord of Paranthropus boisei isalmost exclusively cranial, consistingmostly of jaws and teeth. This meansthere are reasonably sized, relativelywell-dated samples for some morpho-logical regions like the mandible andthe mandibular dentition. Researcherscan thus trace the evolution of metri-cal and nonmetrical variables acrosshundreds of thousands of years.Finally, all these factors, together withthe fifty, or so, years that have elapsedsince its discovery, mean that it is pos-sible to use Paranthropus boisei as anexample of how our understanding ofa hominin taxon changes over time.For example, to what extent has theincrease in the size of the samplechanged our perception of the taxon?Have important sample parameterschanged significantly as the hypodigmhas increased in size? To what extentcan we disentangle the influence of anenlarged fossil record from the bene-fits that have accrued from advancesin analytical methods? Thus, thisreview not only summarizes what weknow of the evolutionary history ofParanthropus boisei, but also tracesthe evolution of our understanding ofits evolutionary history.
HISTORY OF DISCOVERY
The first evidence of a megadonthominin (that is, a hominin with verylarge postcanine tooth crowns relativeto its estimated body size) from EastAfrica was found at Olduvai Gorgein 1955 (Fig. 1).6,7 Labeled OH 3, for‘‘Olduvai Hominid 3,’’ it was a speci-men consisting of two teeth, a decidu-ous canine and a large deciduousmolar crown (Fig. 2). The huge size ofthe teeth made them unique amongEast African hominins known at thetime. The taxonomy of OH 3 thereforeremained uncertain until the 1959 re-covery of a well-preserved subadultcranium with similar teeth (OH 5)that was assigned to Zinjanthropusboisei (Fig. 3).8
No mandibles to match the OH 5cranium have been found at OlduvaiGorge, but the recovery in 1964 of awell-preserved, robust-bodied, adultmandible with megadont postcaninetooth crowns (Peninj 1) from a site onthe western shore of Tanzania’s LakeNatron seemed to provide evidence ofthe type of mandible that would becompatible with OH 5.9 Three yearslater, another hominin mandible withpostcanine megadontia was recovered
from the Omo Shungura Formation
in southern Ethiopia (Omo 18.18).10
Since 1967, many additional mandi-
bles and isolated teeth similar to these
megadont fossils have been collected
from these same sediments.11–14
Beginning in 1968, a series of P. boi-sei fossils was uncovered near whatwas then known as East Rudolf (nowcalled Koobi Fora) in northern Kenya.This series included the recovery in1969 of a well-preserved but edentu-lous adult cranium (KNM-ER 406)and the recovery in 1970 of an adulthemicranium preserving the majorityof the vault, the right side of the face,
ARTICLES
Paul Constantino is a doctoral candidatein hominid paleobiology at the GeorgeWashington University in Washington,DC. His interest in Paranthropus led tohis dissertation study on how fracture-re-sistant foods influence masticatory mor-phology and function in primates andbears. In addition to his laboratory-based morphology work, Paul studiesthe dietary ecology of baboons in south-ern Africa and giant pandas in centralChina. Hominid Paleobiology DoctoralProgram, Department of Anthropology,The George Washington University, 2110G Street NW, Washington, DC 20052.Phone: 202-994-7894, Fax: 202-994-6097, E-mail: [email protected]
Bernard Wood is University Professor ofHuman Origins at the George Washing-ton University. His main research inter-ests have been the alpha taxonomy andsystematics of the hominin fossil record,and he has always had a particular inter-est in Paranthropus boisei. His currentpreoccupation is how to make detaileddata about the hominin fossil recordmore widely available for the purposesof education and research.Center for the Advanced Study of HumanPaleobiology, Department of Anthropol-ogy, The George Washington University,2110 G Street NW, Washington, DC20052, USA, and Human Origins Pro-gram, National Museum of Natural His-tory, Smithsonian Institution, Washington,DC 20560, USA. E-mail: [email protected]
Key words: Paranthropus; Australopithecus; Oldu-
vai Gorge; Koobi Fora; cranial morphology
VVC 2007 Wiley-Liss, Inc.DOI 10.1002/evan.20130Published online in Wiley InterScience(www.interscience.wiley.com).
Evolutionary Anthropology 16:49–62 (2007)
and part of the right side of the cranialbase (KNM-ER 732) (Fig. 4). Severalmandibular specimens have also beenfound at Koobi Fora and elsewhere,so that numerically it is the best-sampled region of the P. boisei skele-ton (Fig. 5).1 About the same time thatmany of the Koobi Fora fossils werebeing discovered, the Chemoigut For-
mation at Chesowanja, Kenya alsoprovided evidence of P. boisei, mostnotably in the form of a craniumdiscovered in 1970 that preservedthe right side of the face and the ante-rior part of the cranial base (KNM-CH 1).15
The intensive prospecting in theOmo Shungura Formation and at
Koobi Fora in the late 1960s and early1970s resulted in the rate of discoveryof P. boisei fossils reaching its peak inthe second decade (1966–1975) of thetaxon’s history (Fig. 6). After thattime, cranial remains belonging to P.boisei continued to be recovered fromKoobi Fora and began to be found atWest Turkana.1,4,16–18 Two notewor-thy P. boisei-like specimens fromWestTurkana, a mandible (KNM-WT16005) and a cranium (KNM-WT17000), were recovered in sedimentsdating to ca. 2.5 Ma.16,19 Along withOmo 18.18 and others, these speci-mens have been suggested as possiblerepresentatives of a second megadonttaxon in East Africa, Paranthropusaethiopicus, which was geologicallyolder than P. boisei. They thereforehave particular relevance to thedebate about the origin and subse-quent evolution of megadont archaichominins. Additional evidence of P.boisei has come from sites elsewherein East Africa, most notably in 1993,when a well-preserved skull of P. boi-sei (KGA 10-525) was recovered inEthiopia at Konso (formerly calledKonso Gardula).20 This skull was notonly the geologically youngest knownspecimen of P. boisei, at 1.4 Ma, butalso increased the geographical rangeof the taxon. Moreover, this was thefirst time that cranial and mandibularevidence from the same individualhad been found in proximity, affirm-ing the presumed associationsbetween the ‘‘robust’’ crania and largejaws made by previous researchers.Also, in 1999, a P. boisei-like maxillawas recovered from Malema, Malawi,thus substantially expanding thesouthern extent of P. boisei’s range bymore than 1,000 km.21
FOSSIL EVIDENCE
Cranial
More than 111 craniodental speci-mens are now attributed to P. boiseisensu stricto; an additional 56 areassigned to P. aethiopicus. Only themost complete and well-preserved ofthese are reviewed here.Similarities between the type speci-
men (OH 5, Fig. 3) and the large,crested cranium from Koobi Fora(KNM-ER 406, Fig. 4) were noted at
Figure 1. Map of P. boisei sites in East Africa highlighting the change in its known geo-graphic range over the past five decades. The only new site discovered between 1975and 1985 was West Turkana; no new sites were discovered between 1985 and 1995. Thelast decade has seen a significant increase in the range of P. boisei due mainly to thediscovery of Malema in Malawi, but also Konso in Ethiopia. Adapted from Delson andcoworkers.99
50 Constantino and Wood ARTICLES
the time of the latter’s announce-ment.22 Most researchers have con-
cluded that the differences betweenthese two large, presumedmale craniaare best interpreted as evidence ofintraspecific and not interspecific var-iation.1 The morphology of two otherpartial crania from Koobi Fora(KNM-ER 13750 and 23000) and ofthe skull from Konso is also suffi-ciently similar to that of OH5 andKNM-ER 406 to suggest that all fivecrania belong to P. boisei. Someaspects of their morphology, such asthe topography of the ectocranialcrests and the face, vary within thepresumed male morph of P. boisei,while other regions, such as the cra-nial base, are relatively invari-ant.17,23,24
A calvarium (KNM-ER 407) and apartial hemicranium (KNM-ER 732)differ in both size and shape from thepresumed male P. boisei crania. In thecase of KNM-ER 407, the contrast inmorphology was considered to be sogreat that its initial taxonomic assess-ment concluded it was ‘‘either a grac-ile species of Australopithecus or else avery early representative of Homo. . ..’’22 In contrast it was suggestedthat KNM-ER 406 and 732 ‘‘representthe two sexes of the same species.’’25
Most researchers now agree with thisassessment, interpreting these craniaas smaller-bodied, presumably femalerepresentatives of P. boisei,1,26,27 thusproviding evidence of substantial cra-nial sexual dimorphism within thistaxon (Fig. 4). Another cranium re-covered from Koobi Fora (KNM-WT17400) has lost some of the diagnosticmorphology of the face, but whatremains of its osseous and dentalmorphology leaves little doubt thatthis specimen represents anotherexample of the small, presumablyfemale morph of P. boisei.
Postcranial
The only sure way for researchers toknow what the postcranial hypodigmof a hominin taxon looks like is to finddiagnostic craniodental remains to-gether with elements of the postcra-nial skeleton. Unfortunately, there isno compelling evidence of an associ-ated skeleton for P. boisei (but seeGrausz and coworkers28). Thus, theproblem researchers have faced atOlduvai Gorge, Koobi Fora, and else-where is how to tell which of the unas-sociated hominin postcranial fossilsshould be assigned to P. boisei and
TABLE 1. Some Characteristic and Distinctive Features of Paranthropus boisei
sensu stricto
Cranium– Orthognathic facial profile– Broad mid-face with anteriorly positioned and laterally flaring zygomatic
bones– High degree of postorbital constriction– Overlap of parietotemporal sutures with marked striae parietales– Polymorphic pattern of sagittal and nuchal cresting in presumed males– Anteriorly positioned, heart-shaped foramen magnumMandible– Deep and wide corpus with a rounded base– Substantial superior and inferior transverse tori at the symphysis– Tall and wide ramusDentition– Very small anterior teeth relative to the posterior teeth– Very large posterior teeth relative to skull size– Maxillary premolars having large crowns with a relatively large paracone;
2 or 3 roots– Maxillary molars, M1 < M2 ¼ M3; large crowns with high incidence of a
Carabelli’s cusp; 3 roots– Mandibular premolars, P4 crown base area is ca. 140% that of P3; talonid
area is positively allometric relative to total crown area; 2 plate-like roots– Mandibular molars-M1 < M2 < M3; expanded talonid; usually > 6 cusps;
usually at least one C6; unlikely to have a C7; 2 plate-like roots– ‘‘Hyper-thick’’ enamel with relatively little enamel decussation on
postcanine crowns
Figure 2. The first evidence of Paranthropusboisei. The deciduous right M2 of OH 3 inocclusal (A), alveolar (B), mesial (C), distal(D), buccal (E), and lingual (F) views. FromTobias.100
Figure 3. Early photo of OH 5 in lateral viewshortly after its reconstruction. The mandi-ble was created based on the known mor-phology of the cranium. Its size and shapewere later affirmed by the discovery of thePeninj mandible at Lake Natron, whichclosely resembles the one created for OH 5.Photo by Bob Campbell.
ARTICLES The Evolution of Zinjanthropus boisei 51
which should be assigned to the con-temporaneous speciesHomo habilis.The only unassociated hominin
postcranial fossil recovered at OlduvaiGorge to be explicitly assigned to P.boisei is a proximal femoral fragment(OH 20, Fig. 7).29 A detailed analysisof OH 20 suggested that it shares asuite of features with two proximalfemora attributed to P. robustus (SK
82 and 97). These features promptedDay29 to remark that ‘‘it would seemreasonable to allocate the new femo-ral fragment to Australopithecus cf.boisei’’ (Note that Australopithecusboisei is the same taxon as Paranthro-pus boisei. The reason for the contin-ued disagreement about whether toattribute these fossils to Australopithe-cus or Paranthropus will be discussedlater). At that time, no one knew whatan H. habilis femur looked like, so itseemed logical to link a P. robustus-like proximal femur with P. boisei, aswell as to link what were then inter-preted as the more modern human-like Olduvai Bed I and II postcranialspecimens (for example, OH 8 and 10)withH. habilis.
The discovery of a modern human-like ankle bone (the talus KNM-ER813) at Koobi Fora30 weakened thecase for assuming that the OH 8 footbelonged to H. habilis, since the OH 8talus more closely resembles a talusassigned to P. robustus (TM
1517).31,32 Wood31 argued that thelogic that had led to the interpretationof Olduvai foot fossils (OH 8 and 10)as modern human-like was flawed andsuggested that they have as muchclaim to be attributed to P. boisei asthey have toH. habilis.At approximately the same time
that these reassessments of the Oldu-
Figure 4. Right anterosuperior view of thepresumed male cranium KNM-ER 406 (A)and anterior view of the presumed femalecranium KNM-ER 732 (B).
Figure 5. Occlusal views of KNM-ER 729 (A)and KNM-ER 992 (B) casts. KNM-ER 729 hasbeen attributed to P. boisei. Easily visibleare its huge molar teeth, molarized premo-lars, and thick corpus. KNM-ER 992 is thetype specimen of Homo ergaster. Althoughits postcanine teeth are larger than those ofmodern humans, they are clearly muchsmaller than those of P. boisei.
Figure 6. The number of P. boisei speci-mens discovered each decade for thepast 50 years. The large number of speci-mens discovered between 1965 and 1975was mostly due to the beginning of fieldwork at Koobi Fora and the Omo.
Figure 7. The proximal left femur OH 20 inanterior (A) and posterior (B) views.
52 Constantino and Wood ARTICLES
vai hominin postcranial fossils weretaking place, Richard Leakey and histeam had begun to recover homininpostcranial remains from Koobi Fora.Most were femoral specimens; provi-sional comparisons suggested thatthey could be divided into those thatwere more like the femora of modernhumans and those that were ‘‘notunlike other femoral fragments thathave been collected elsewhere andassigned to Australopithecus.’’25 How-ever, the attributions of the moreprimitive specimens to Australopithe-cus and, by inference, to Australopi-thecus cf. boisei, depended on theuntested assumption that the femoraof H. habilis were recognizably moremodern human-like than were thefemora of P. boisei. The subsequentdiscovery of an H. habilis partial skel-eton (OH 62) challenged this assump-tion. The partial skeleton is poorlypreserved and its interpretation re-mains controversial. Nevertheless, itsfemoral morphology is evidently simi-lar enough to that of femora fromOlduvai and Koobi Fora that hadbeen assigned to Australopithecus andthence to P. boisei33 to make these lat-ter attributions suspect. Conse-quently, there is no current way of tell-ing to which taxon or taxa the‘‘Australopithecus-like’’ hominin post-cranial evidence from Olduvai andKoobi Fora belongs. For the timebeing, it would be prudent to regardthis fossil evidence as Hominini gen.et sp. indet.Attempts to identify the postcranial
skeleton of P. boisei at sites other thanOlduvai and Koobi Fora have been adhoc, and none has been particularlyconvincing. So where does that leaveus? In short, we are badly in need ofan associated skeleton that includescranial elements diagnostic of P. boi-sei. Finding archaic-looking femora isnot enough because at least one othersynchronic East African hominin, H.habilis, exhibits similar morphology.It may be that some of the homininpostcranial specimens assigned toH. habilis actually belong to P. boiseibut, for the time being, we have noway of telling. We suggest it is betterto accept that for various reasons nopostcranial remains can be confi-dently assigned to P. boisei than tocontinue with the present confusion.
SYSTEMATICS
Upon the discovery of OH 5, LouisLeakey8 drew attention to twenty dif-ferences between this cranium andcrania already attributed to Australo-pithecus and Paranthropus, which atthe time were only known from south-ern Africa. The following year Robin-son34 went through Leakey’s claimed‘‘major differences’’ and, to the for-mer’s satisfaction, refuted the vastmajority. Robinson suggested that thegenus name Zinjanthropus be aban-doned and proposed that OH 5 beincluded within the existing genusParanthropus.
How Many Species?
There are currently three maindebates about the taxonomy of P. boi-sei. The first focuses on whetherthere are sufficient differences
. . . we are badly in needof an associatedskeleton that includescranial elementsdiagnostic of P. boisei.
between P. boisei and P. aethiopicus tojustify retaining P. aethiopicus as aseparate species. The second askswhether recent discoveries haveblurred the distinction between P. boi-sei and the megadont taxon fromsouthern Africa, Paranthropus robus-tus. The third debate concernswhether the differences in size andshape subsumed within P. boisei areconsistent with a sexually dimorphicearly hominin taxon or whether theyare an indication that even P. boiseisensu stricto subsumes more than onetaxon.
If the hypodigm of P. boisei is re-stricted to the post-2.3 Ma fossil re-cord, then the name P. boisei sensustricto should be retained for the mainhypodigm and P. aethiopicus shouldbe used as the species name for theearlier fossil evidence. However, if theP. boisei hypodigm is judged to
include the pre-2.3 Ma fossils, amongthem Omo 18.18, L338y-6, and KNM-WT 17000, then P. aethiopicusbecomes a junior synonym of P. boiseisensu lato. The point at issue iswhether the differences betweenKNM-WT 17000 and the < 2.3 Ma cra-nia belonging to the P. boisei sensustricto hypodigm (for example, OH 5,KNM-ER 406) justify a specific dis-tinction for the West Turkana cra-nium and the early megadont jawsand teeth attributed to P. aethiopi-cus.10 Two studies have looked at thisproblem in detail. Suwa35 concludedthat there are differences in mandibu-lar premolar cusp morphologybetween the pre-2.3 Ma and the post-2.3 Ma megadont fossil evidence, withthe later material having larger andmore elaborate talonids. Wood,Wood, and Konigsberg23 found thatseveral features of the mandible andthe mandibular dentition (other thanthe premolar morphology referred toby Suwa35) also change at ca. 2.3 Ma.These authors supported the interpre-tation that the early stage of the Para-nthropus lineage in East Africa shouldbe recognized as a different species.The main differences between the twoEast African Paranthropus species arethe greater facial prognathism, largerincisors, flatter cranial base, smallermandibular corpus, and shorter post-canine tooth row of P. aethiopicus.23
Tobias36 cogently made the case fordistinguishing between P. boisei andP. robustus and, until recently, theenlargement of the two hypodigmshad not materially altered that assess-ment. However, the discovery of amegadont hominin skull (KGA 10-525) at Konso prompted Suwa andcoworkers20 to suggest that someaspects of its morphology are com-mon to both P. boisei and P. robustus.This, together with the recovery ofadditional cranial material fromKoobi Fora (for example, KNM-ER23000)17 and the publication of thedetailed analysis of a cranium fromthe Omo (Omo 323–896)14 promptedat least one commentator to suggestthat Paranthropus taxonomy shouldbe reassessed.37 In addition, the re-covery of a large, ‘‘P. boisei size’’ molarfrom Gondolin38 suggests that itwould be worthwhile to considerwhether the recent discoveries in
ARTICLES The Evolution of Zinjanthropus boisei 53
southern Africa at this site and at Dri-molen39 may have closed the morpho-logical gap between P. robustus and P.boisei. However, recent studiesaddressing these issues have found nosupport for taxonomic revision basedon the current evidence. Wood andLieberman24 concluded that ‘‘theKonso specimens fit within the popu-lation parameters of P. boisei pre-dicted by the ‘pre-Konso’ hypodigm.When Constantino and Wood40 com-pared the regional hypodigms of Par-anthropus before and after addition ofthe new material from Drimolen andGondolin, they found that the numberof significant metrical differences be-tween the postcanine dentition fromEast and southern Africa increasedrather than decreased.As for whether the P. boisei hypo-
digm samples more than one hominintaxon, it has been suggested that thedegree of size variation in the mandib-ular hypodigm of P. boisei is excep-tional.41,42 However, much of this ‘‘ex-cessive’’ variation can be explained bypost mortem cracks that fill with ma-trix and artificially inflate the size ofthe mandibular corpus of larger indi-viduals, while erosion of surface bonehas reduced the size of the corpus ofsome of the smaller individuals in thehypodigm.1,43 Apart from these ex-trinsic causes of differences in overallsize, the size and shape of the mandib-ular corpus of P. boisei is remarkablystable through geological time23 (see
Fig. 2E), with both small and largemandibles in the sample retainingtheir characteristically robust corpusand rounded base.1,23
Is Paranthropus Monophyletic?
Regardless of whether one or twoParanthropus species are recognizedin East Africa, dental metrical evi-dence still indicates that P. boisei isdistinct from P. robustus.40 But didthe East and southern African mega-dont taxa evolve from a recent com-mon ancestor exclusive to themselvesand thus form a monophyletic group,or did the various regional Paranthro-pus taxa evolve independently (Fig. 8)?
In 1988 Wood44 reviewed fifteenhominin cladistic studies, all of whichconcluded that the two regional var-iants of Paranthropus are sister taxa.An independent review published inthe same year also found that oneof the few reliable parts of the homi-nin cladogram is the Paranthropusclade.45 The major cladistic study byStrait, Grine, and Moniz46 also foundthat the most parsimonious clado-grams support Paranthropus mono-phyly. As part of their comprehensivemorphological analysis of the cranialremains of Au. afarensis, Kimbel, Rak,and Johanson3 also found consistentsupport for a ‘‘robust’’ australopith clade.
Given the near unanimity of theconclusions of these studies, what rea-sons are there to continue to scruti-
nize the hypothesis of ‘‘robust’’ mono-phyly? First, the average confidenceinterval for hominin cladistic analysesof ca. 0.65 means that approximately35% of the characters used in theanalyses must have been independ-ently acquired; that is, they are homo-plasies. If these homoplasies are con-centrated in one anatomical regionsuch as the skull, and if that regionhas a major influence on the shape ofthe cladograms, then an analysis ofthe preserved morphology may notresult in an accurate reconstruction ofevolutionary relationships. Second,many of the characters that link Para-nthropus taxa are related to the masti-catory system. For example, whenWood and Chamberlain47 organizedcharacters according to anatomicalregion, they found that support for aParanthropus clade relied heavily oncharacters from the face, palate, andmandible. These regions all reflectmasticatory adaptations and are thuslikely to be functionally integrated.Therefore, the characters derivedfrom those regions are potentially‘‘non-independent’’ and if so, shouldnot be coded as individual charactersin a cladistic analysis. Skelton andMcHenry48 reached a comparableconclusion. Evidence from othergroups of mammals (see, for example,Maglio49 and Vrba50,51) also suggeststhat the masticatory system might bethe equivalent of a ‘‘homoplasyghetto.’’ It should be noted, however,
Figure 8. Adaptations of two proposed phylogenies for Plio-Pleistocene hominin evolution with the ‘‘robust’’ australopiths highlighted inbold. The phylogeny by Skelton and McHenry48 shows the ‘‘robust’’ australopiths as a polyphyletic group descended from two differentancestors, with many of the morphological features that are shared between Au. (P.) aethiopicus and the Au. (P.)boisei/Au. P. robustus
clade having evolved through parallel or convergent evolution. The phylogeny by Strait, Grine, and Moniz46 shows the ‘‘robust’’ austral-
opiths as monophyletic (all evolving from the same recent common ancestor). The length of the lines is arbitrary and not meant to be
reflective of time. In the phylogeny by Strait, Grine, and Moniz,46 ‘‘Au. afarensis’’ is in quotes because the authors designated a newtaxon name for members of this group. ‘‘Au. afarensis’’ is retained here for clarity of comparison with the Skelton and McHenry phylog-eny. Also for ease of comparison, additional taxa such as Kenyanthropus platyops and Au. garhi are not included.
54 Constantino and Wood ARTICLES
that even when Strait, Grine, andMoniz46 excluded masticatory charac-ters from one of their cladistic analy-ses they still found strong support fora Paranthropus clade.A third argument for questioning
Paranthropus monophyly is that astudy that used Patterson’s52 similar-ity and ontogenetic criteria to test thehypothesis of Paranthropus mono-phyly44 with respect to mandibularmolar cusp morphology and mandib-ular premolar root form producedmixed results in terms of supportingor falsifying the hypothesis. In a fur-ther examination of Paranthropuspostcanine cusp morphology, Suwa,Wood, and White53 noted that ‘‘theindividual cups involved in the talonidexpansion are not always the same,’’with the hypoconid and the entoconidcontributing more to talonid expan-sion in P. boisei and P. robustus, res-pectively. This suggests that the de-rived dental morphology in the twoParanthropus taxa may not have thesame developmental basis.The question of Paranthropus mo-
nophyly is therefore unresolved.Future research will have to deter-mine whether the shared skull mor-phology of East and southern AfricanParanthropus is due to common an-cestry or convergent evolution. If oneis sanguine that hard-tissue morphol-ogy is capable of recovering phyloge-netic relationships established on thebasis of independent genetic evidence,then Paranthropus monophyly mustbe the hypothesis of choice. But if oneis more skeptical about its ability todo so, then what others interpret asoverwhelming evidence for Paranthro-pus monophyly looks less compelling.This has taxonomic implications sincethe genus name Paranthropus is onlyappropriate if these taxa form a mo-nophyletic group. Otherwise, theycannot be included in their own sepa-rate genus and should be included asmembers of the genus Australopithe-cus. Because the majority of phyloge-netic analyses currently support Para-nthropus monophyly, we suggest thatuntil the evidence demonstrates oth-erwise, the genus name Paranthropusshould be used to recognize the strongpossibility that megadont taxa in bothregions form an adaptively distinctiveand monophyletic group.
What about the evolutionary rela-
tionships between Paranthropus and
nonrobust taxa? A recent attempt to
use morphological evidence to reeval-
uate the phylogenetic relationships of
Au. afarensis has revealed several sim-
ilarities in cranial morphology
between that taxon and P. boisei sensulato,3 but failed to support a direct
phyletic link between these hominins.
Interestingly, another hominin with
postcanine megadontia, Australopi-thecus garhi, has been recovered from
ca. 2.5 Ma sediments in the Middle
Awash of Ethiopia.54 While it does not
seem to be a member of the Para-nthropus clade based on other aspects
of its craniofacial morphology, it is
too early to know how it is related to
other hominins. Finally, most
researchers accept that the derived
morphology shared between Para-nthropus and Homo, such as cranial
base flexion, either evolved independ-
ently in the two lineages or was inher-
ited from an as-yet undiscovered
recent common ancestor of the Para-nthropus and Homo clades. The dis-
tinctness of other aspects of their
morphology leaves little doubt that H.habilis and P. boisei are at least sepa-
rate species, probably belonging to dif-
ferent genera. Thus, the existing fossil
evidence suggests that the genus Para-nthropus went extinct without contrib-
uting to the evolution of later hominins.
CONTEXT
Geographical andTemporal Range
Paranthropus boisei sensu lato (P.boisei sensu stricto plus P. aethiopicus)is currently known from eight sites inEast Africa and spans a geological agerange of ca. 2.6–1.4 Ma (Figs. 1 and 9).With the exception of the Omo, nomajor East African sites are known tohave fossiliferous deposits dated tobetween ca. 1.4 and 1.0 Ma or between3.0 and 2.5 Ma. Therefore, it could beargued that there is a gap of half a mil-lion years on each side of the temporalrange of P. boisei sensu lato. We donot know how far into those gaps Par-anthropus fossils extend, but the appa-rent absence of Paranthropus fossilsin the older Omo sediments suggests
that the currently accepted temporalrange of ca. 1.2 Ma is likely to be closeto the true temporal range.
Paleohabitat
There have been various interpreta-
tions of the habitat preferences of Par-
anthropus in East Africa. Shipmanand Harris55 concluded that P. boiseisensu lato probably preferred closedand wet habitats, while Reed56 sug-gested that these hominins lived inmore open environments such as eda-phic grasslands. Some P. boisei sitesnot included in these analyses, suchas Peninj and Chesowanja, do nothave detailed paleoenvironmentaldata available for the relevant strati-graphic levels, but habitats have beenreconstructed at the more recentlydiscovered sites of Konso and Mal-ema. The nine Konso specimens areassociated with a ‘‘predominantly drygrassland fauna’’20 close to a paleo-lake,57 with no P. boisei fossils comingfrom the more mesic (moderatelywet) localities. The faunal assemblagefound with the P. boisei maxillaryfragment21 at Malema is sparse andhighly biased, but it is dominated byopen-habitat mammals includingalcelaphines, antilopines, Hipparion,and the pig Notochoerus scotti, sug-gesting that P. boisei was preserved ina relatively open environment at thatsite as well. The results of earlierwork58 also indicate the proximity of alarge paleolake at Malema. Thus, atboth Konso and Malema, the evidencesupports the assertion that P. boiseifavored open habitats near permanentwater, as advocated by Reed.56
BEHAVIOR
Given the lack of postcranial bonesthat can be confidently attributed to P.boisei, there is not much that can besaid of this taxon’s dexterity, posture,or locomotion except that data on therelative position of the foramen mag-num67,68 indicate that the habitualposture of P. boisei was similar to thatof modern humans. This section willtherefore focus on the evidence wehave regarding diet and the functionof the masticatory system, followed bya brief discussion of attempts to infersocial structure frommorphology.
ARTICLES The Evolution of Zinjanthropus boisei 55
Diet
There has not been much successin determining the diet of P. boisei.This is somewhat surprising consid-
ering the predominance of cranial,gnathic, and dental evidence in itshypodigm, the likely role diet playedin the evolution of its derived masti-catory morphology, and the potential
for diet to provide informationregarding the divergence betweenParanthropus and early Homo. Wewill review what has been done tounderstand P. boisei’s diet in terms
Figure 9. Stratigraphic location of the P. boisei hypodigm. Shaded areas indicate levels where P. boisei fossils have been found. The spe-cific positions of key specimens mentioned in the text are shown. The oldest known specimens of P. aethiopicus are from the Omo andare dated to ca. 2.6 Ma, while the oldest fossils of P. boisei sensu stricto are from Malema and are approximately 2.3 Ma, based on fau-nal correlations with the Omo. The specimens from Konso are the youngest known for P. boisei, at ca. 1.4 M.
56 Constantino and Wood ARTICLES
of dental morphology, masticatorybiomechanics, dental microwear,and chemical analyses of bones andteeth.
Dental morphology
The small incisors of P. boisei appear toindicate a diet that did not require a sig-
nificant amount of incisal preparation
such as one consisting of leaves or ber-
ries.69 Therefore, if P. boisei was eating
fruit, then the fruit either lacked thick
husks or fleshy pulp or was small
enough to need little preparation before
mastication with the postcanine teeth.
However, the possibility that foods were
being prepared outside of the mouth
must be considered (see Box 1).
The very large, bunodont postca-nine tooth crowns of P. boisei mayhave been an adaptation to dispersehigh occlusal loads or simply toincrease the surface area over whichfood could be processed at any onetime. Lucas, Corlett, and Luke,70
showed that the ratio of the area ofM1 to M3 (both upper and lower) inprimates was inversely related to theamount of leaves consumed and sug-gested that the low M1:M3 ratio ofParanthropus indicates that they were‘‘probably consuming small mouth-fuls of leaves and seeds.’’ However, thelow shearing crests71 and roundedcusps of these teeth suggest that a diethigh in fibrous leaves or grasses wasunlikely. Nevertheless, it is still possi-ble that seeds and plant undergroundstorage organs such as tubers, bulbs,
roots, and rhizomes made up a signifi-cant proportion of P. boisei’s diet.72,73
All post-4 Ma hominins have rela-tively thick enamel but, as with post-canine crown area, P. boisei was evenmore derived along this morphoclinethan were other hominins; its enamelhas been described as ‘‘hyper-thick’’74
(p. 33). The functional role of thickenamel is still unclear, but it has beensuggested that it is part of a strategyto resist wear and/or withstand highocclusal loads caused by abrasive orhard foods. Gantt and Rafter75 sug-gested that the hyper-thick enamel ofP. boisei was linked with ‘‘increasedcrushing and grinding and adaptationto savanna habitat.’’ While few woulddisagree with this statement, there isstill no consensus as to what it was thatP. boiseiwas ‘‘crushing and grinding.’’
Masticatory biomechanics
The cranial attachments for the mass-eter muscles are more anteriorly posi-tioned in P. boisei than they are inother early hominins76 and, to judgefrom the size of the ectocranial crests,zygomatic bones, and other muscleattachment areas, P. boisei probablyhad larger masticatory muscles aswell (Fig. 10).77 However, it is unclearwhether these larger masticatorymuscles would have resulted in higher
When the OH 5 cranium was discov-ered at FLK I, it was assumed to bethe manufacturer of the stone toolsfound on the ‘‘living floor.’’8 How-ever, the career of P. boisei as themaker of the Oldowan stone toolsended just five years later, whenLouis Leakey was forced to considerthe implications of the subsequentdiscovery of Homo habilis fossils inassociation with the Oldowan cul-ture at three other localities at Oldu-vai. He concluded that ‘‘while it ispossible that Zinjanthropus andHomo habilis both made stone tools,it is probable that the latter was themore advanced tool maker and thatthe Zinjanthropus skull represents anintruder (or a victim) on a Homohabilis living site.’’59 This conclusionwas reached not because any evi-dence suggested that P. boisei couldnot be the toolmaker, but because H.habilis, with its larger brain andapparently modern human-like handbones, seemed a more likely tool-maker than did P. boisei.Since 1964, virtually all research-
ers have come to agree that H.habilis made stone tools. Most ofthese researchers have relegated P.
boisei to the sidelines of culturalevolution. However, a few haveentertained the possibility thatmembers of more than one homininlineage may have had the ability tomanufacture simple stone tools.60–64 The truth is that there is no directevidence linking any of these earlyhominin species with stone tools.No hand bones can be confidentlyassigned to either P. aethiopicus orP. boisei, so we do not know whetherthese taxa were dexterous enough tomake or use stone tools. Hand bonestentatively attributed to P. robustusin southern Africa reportedly indi-cate that these hominins were capa-ble of a human-like precision grip.65
Both stone and bone tools have beenfound in loose association with P.
robustus at Swartkrans61 and Sterk-
fontein.66 However, even if these an-
atomical and archeological associa-
tions prove to be sound, it is unclear
what the implications would be for
P. boisei. Thus far, there is no firm
evidence that P. boisei made and
used stone tools, but there is also no
firm evidence that members of this
taxon were incapable of doing so.
BOX 1: Was Paranthropus boisei a maker anduser of stone tools?
Figure 10. KNM-ER 406 (A) and KNM-ER3733 (B) in superior view. The large and lat-erally flaring zygomatic arches of KNM-ER406 can be seen clearly. Coupled with theshorter anteroposterior length of the cra-nium, this gives P. boisei a much more cir-cular cranial circumference when viewedfrom this angle. Also apparent in this pho-tograph are the high degree of postorbitalconstriction and sagittal crest develop-ment in P. boisei, both related to its smallerrelative brain size. One can also see evi-dence of the convergence in facialorthognathy between P. boisei and Homo.
ARTICLES The Evolution of Zinjanthropus boisei 57
occlusal forces. As Demes and Creel78
have pointed out (and as Walker79
pointed out earlier for P. robustus), P.boisei would have been able to gener-ate exceptionally high bite forces rela-tive to those of other hominins, butthe occlusal forces at the molarswould not have been exceptional ifthey were distributed over the entireocclusal surface. Only if P. boisei wasfeeding on limited numbers of smallobjects at any one time would increasedforce on any single object result.Since, under certain circumstances,
P. boisei could generate significantlyhigher bite forces than could otherhominins, it is not surprising that theyalso appear to have had the ability towithstand high bite forces. Hylander80
has suggested that the thick mandibu-lar symphysis and the deep, thickmandibular corpus of P. boisei, whichis approximately three times largerthan would be expected in a general-ized hominoid of the same bodymass,81 allowed these creatures toresist high stresses caused by masti-cating very hard or tough food items.
Dental microwear
Thus far, no study of P. boisei dentalmicrowear has been reported in theliterature. This is due, at least in part,to the fact that most P. boisei fossilsare found on the surface, and surfacespecimens typically exhibit a substan-tial proportion of nondiet-relatedmicrowear due to erosion, weather-ing, and trampling.82 Although theanalysis of dental microwear has pro-ven to be a valuable technique forunderstanding diet in the megadonthominins from southern Africa,83,84 itis unclear what these results say, ifanything, about the diet of P. boisei.
Chemical analysis
The chemical analysis of bones andteeth is another method that has sig-nificantly increased our understand-ing of hominin diet but, as with dentalmicrowear analysis, it has not yetbeen used in an in-depth study of thediet of P. boisei. One of the only chem-ical studies that included P. boisei wasby Boaz and Hampel,85 who found
that P. boisei had lower Sr:Ca ratiosthan did early Homo. This is broadlyconsistent with later analyses of P.robustus from Swartkrans86 and sug-gests that Paranthropus may havebeen consuming more meat than didthe earliest members of our own ge-nus. However, the results of the Boazand Hampel study need to be inter-preted with caution due to the smallsamples used for earlyHomo.
Social Structure
Plavcan87 has been at the forefront
of efforts to predict the social struc-
ture of extinct taxa through compari-
sons of sexual dimorphism in body
size and canine crown size. Unfortu-
nately, we currently lack reliable ways
of determining the sex of most early
hominins but, as mentioned earlier,
the pattern of craniodental size
dimorphism apparent in P. boisei sug-
gests the presence of distinctive male
and female morphs. These morphs
are somewhat unusual, however, in
that they both possess relatively small
canines, despite their evident cranio-
dental and inferred body size differen-
ces. Therefore, even if we assume that
the larger specimens are males and
the smaller specimens are females,
there are no modern higher primate
analogues that show a comparable
pattern of within-species variation.Inferences could be made about
the social structure of P. boisei byatomizing its morphology and thencomparing the predictions from eachof the components (canine crownheight, canine crown buccolingualwidth, body size, and so on), butPlavcan87 suggested that the relation-ships among these variables in livinghigher primates are ‘‘not strongenough to make detailed inferencesabout mating systems or behavior onthe basis of dimorphism alone.’’ In alater paper, Plavcan88 cautionsagainst assuming that any livinghominoid is a suitable analogue forearly hominins with respect to pre-dicting social structure.
LIFE HISTORY
The stages through which an indi-
vidual passes during its lifetime are
collectively termed its life history.
Knowledge of the pattern and timing
of an organism’s life history can reveal
information about its strategies for
survival and reproduction. Unfortu-
nately, little is known about the life
history of P. boisei. Here we discuss
why neither life-history variables
(ones directly related to life history)
nor life-history-related variables (ones
indirectly related to life history) arecurrently able to tell us much aboutlife history in this taxon.
Life-History Variables
Age at weaning is an indicator ofrelative offspring dependence andmaternal investment. Because lacta-tion suppresses ovulation in greatapes and humans, it is also a determi-nant of interbirth interval. Among liv-ing primates, weaning appears tocoincide with M1 eruption,89 butwithin the hominin clade some evi-dence suggests that weaning may pre-date M1 emergence.90 This is certainlythe case for modern human groupswho wean infants at about the age of2.5 years, whereas the first permanentmandibular molar does not eruptuntil children are approximately 6years old. Determination of age atweaning in fossil hominins has thusbeen based on an assessment of thedegree and timing of the deciduousdental attrition associated with die-tary supplementation. Aiello, Mont-gomery, and Dean91 showed thatspecimens of P. boisei and P. robustusjudged to be between 2.5 and 3.5 yearsof age exhibit high levels of deciduousdental attrition compared to specimensof Au. afarensis.However, these authorsacknowledged that this difference couldbe related to either an earlier age atweaning or to differences in diet.
Life-History-Related Variables
Body size
There are strong correlations betweenbody size and life-history variablessuch as gestation length, weaning age,age at first reproduction, interbirthinterval, and maximum life spanacross subfamilies of primates.92
Researchers who have used cranial
58 Constantino and Wood ARTICLES
variables as proxies for body mass93,94
have concluded that the estimatedbody mass of P. boisei is similar tothat of archaic hominin taxa in the ge-nus Australopithecus. Thus, differen-ces in body mass cannot be used toaccount for any differences in predic-tions about the life history of P. boiseiand other archaic hominins.
Brain size
Brain mass has also been shown to behighly correlated with many life-his-tory variables.92 Brain mass can be
derived from brain volume, and brainvolume can be derived from endocra-nial volume if allowance is made forthe space occupied by the endocranialvasculature and the intracranial extra-cerebral cerebrospinal fluid. Themean of the ten endocranial volumesin the P. boisei sample is 481 cm3, witha range of 400–545 cm3. This rangesubstantially overlaps with that ofextant nonhominin higher primatesand that of archaic hominins, includ-ing H. habilis sensu stricto.95 Likebody size, therefore, brain size is notvery useful in elucidating life-history
differences between P. boisei andclosely related taxa.
Dental ontogeny
In some respects, such as incisorcrown formation and eruptionsequence, dental development in P.boisei resembles that of modernhumans, while in others, such as therate of root formation, it resemblesthat of chimpanzees. In still otherrespects, dental development in P. boi-sei is unique (for example, enamel for-
Figure 11. The effect of additional specimens on three P. boisei dentognathic variables including (A) P4 buccolingual breadth, (B) M3
buccolingual breadth, and (C) mandibular corpus area (h � w) at M1. Variables were chosen based on the number of available fossilspecimens. For the three variables selected, the median values stabilize after approximately 7 to 15 specimens have been assessed.The dark horizontal line across each box is the median value; the box itself represents the interquartile range (middle 50%); the lines(whiskers) show the complete range (excluding outliers). [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]
ARTICLES The Evolution of Zinjanthropus boisei 59
mation in the postcanine teeth). The
premolar and molar crowns of P. boi-sei take the same time, or less, to form
than do those of modern humans and
chimps, despite the fact that P. boisei
crowns are approximately twice the
size of human and chimp crowns.
This is due to a combination of more
enamel secretion per day by amelo-
blasts and a faster rate of ameloblast
activation.96 We need more informa-
tion before we can determine whether
these differences are due to selection
operating on life history, on diet, or
on a combination of the two.
TRACKING MORPHOLOGICALVARIABLES OVER TIME
Most contributions to the paleoan-thropological literature either focuson the latest tranche of fossil discov-eries or look in depth at the fossil evi-dence from a single site or from a par-ticular region or body part. Relativelyfew studies focus attention on theaccumulated hypodigm of a singleearly hominin taxon.3,97
Mandibular and dental remains areparticularly well represented in thehypodigm of P. boisei and for someparameters the sample sizes (N > 20)are respectable, at least by paleonto-logical standards. For some variables,therefore, it is possible to investigatehow much the sample parameters ofP. boisei have changed as the samplesizes have increased. We track the pa-rameters of three such variables (Fig.11). These variables have been chosenat random to the extent that they hap-pen to be the ones represented by thelargest number of specimens. The pa-rameters of all three variables areremarkably consistent, and other vari-ables with smaller hypodigms showcomparable patterns. The two largestsamples are for M3 buccolingualbreadth and mandibular corpus areaat M1. There is very little change in thesample parameters once the hypo-digm reaches N ¼ ca. 10. These datacontradict the notion that paleoan-thropological samples are generallytoo small to support claims of mor-phological distinctiveness. RichardSmith has provided a chastening dem-onstration that this is the case for verysmall samples,98 but our post-hocinvestigation of one early hominin
taxon should encourage field re-searchers and funding agencies torecognize that even relatively modest-sized samples can provide useful in-formation about the original popula-tion from which the fossil sample wasdrawn. Larger samples are still impor-tant, however. As this review has high-lighted, larger samples of P. boisei fos-sils have increased our understandingabout morphological character com-binations, the geographic and tempo-ral range of the taxon, and variationin nonmetrical traits such as thepatterns of ectocranial cresting.
The premolar and molarcrowns of P. boisei takethe same time, or less, toform than do those ofmodern humans andchimps, despite the factthat P. boisei crowns areapproximately twice thesize of human andchimp crowns. This isdue to a combination ofmore enamel secretionper day by ameloblastsand a faster rate ofameloblast activation.
CONCLUSIONS AND PROSPECTS
Half a century of collection and
analysis has vindicated some of the
initial assessments of the taxonomy of
P. boisei by Leakey8 and Tobias.36 For
example, two judgments of Leakey8
appear to have been supported by the
new evidence. First, only Robinson34
has seriously doubted the wisdom of
establishing a new taxon for the P.boisei hypodigm. Second, although
support for recognizing P. boisei
and its ilk at the level of a separate
‘‘sub-family Australopithecinae’’8 has
waned, few would demur from the
judgment that P. boisei belongs to the
same general grade of archaic homi-nins as do taxa presently included inthe genera Australopithecus and Keny-anthropus, albeit as the most derivedmember of that grade grouping. Twojudgments about the phylogeneticrelationships of P. boisei have faredless well. First, the enlargement of thehypodigm has effectively falsifiedLouis Leakey’s claim that OH 5‘‘differs from both Australopithecusand Paranthropus much more thanthese two genera differ from eachother.’’8 Because phylogenetic analy-ses seldom, if ever, put H. habilissensu stricto and P. boisei in the sameclade, Phillip Tobias’36 suggestion thatit is ‘‘unlikely’’ that P. boisei and H.habilis ‘‘were genetically isolated’’ (p.244) can be refuted.This review highlights how much
remains to be learned about mostaspects of P. boisei’s paleobiology,including its diet, life history, tool use,temporal and geographical range, phy-logenetic relationships, and even whatit looked like from the neck down. Sohow can we improve our understand-ing of the paleobiology of P. boisei?The first priority is to find at least one,and preferably several, taxonomicallyunambiguous associated skeletons.This would help researchers work outwhich limbs go with which heads atOlduvai and Koobi Fora. The secondpriority is to extract more informationabout the functional morphology of P.boisei’s masticatory system, and thusabout its diet, from the fossil record.Third, we need to clarify the evolution-ary relationships between P. boisei andthe other ‘‘robust’’ taxa. Fourth on thelist would be a way of teasing out whataspects of dental growth and develop-ment are diet-related and what aspectscarry a signal about life history. Finally,and perhaps the trickiest of all, is thetask of finding ways of establishingwhether, and to what extent, P. boiseiwas a cultural animal. Did its culturalrepertoire go beyond that of a modernchimpanzee? If so, how did its culturediffer from that of the other less mega-dont archaic hominins?The rate of discovery is on the
decline for P. boisei fossils (Fig. 6),probably due mainly to changes inresearch priorities within paleoanthro-pology. Nevertheless, there is much tolearn about this intriguing taxon, and
60 Constantino and Wood ARTICLES
we need both additional fossils andnew analytical methods and strategiesin order to move forward.
ACKNOWLEDGMENTS
PC is supported by an NSF IGERTgrant. BW is grateful to Richard Lea-key for giving him the opportunity toget in at the ‘‘ground floor’’ in terms ofthe fossil evidence for P. boisei. Thatopportunity is still greatly appreci-ated. BW thanks the Henry LuceFoundation, the George WashingtonUniversity, and the National ScienceFoundation for their generous sup-port. We thank Chris Campisano forproviding the geological ages of P. boi-sei specimens and for creating Figure9, as well as Elizabeth Harmon, Fer-nando Ramirez-Rozzi, Gen Suwa, FredGrine, Peter Ungar, and Alan Walkerfor information and advice. Finally, wethank John Fleagle for his persistence.
REFERENCES
1 Wood BA. 1991. Koobi Fora research project,vol. 4. Hominid cranial remains. Koobi ForaResearch Project, series ed. Leakey RE. Oxford:Clarendon Press.
2 Strait DS, Grine FE. 2004. Inferring hominoidand early hominid phylogeny using cranioden-tal characters: the role of fossil taxa. J HumEvol 47:399–452.
3 Kimbel WH, Rak Y, Johanson DC. 2004. Theskull of Australopithecus afarensis. Oxford:Oxford University Press.
4 Feibel CS, Brown FH, McDougall I. 1989.Stratigraphic context of fossil hominids fromthe Omo group deposits: Northern TurkanaBasin, Kenya and Ethiopia. Am J Phys Anthro-pol 78:595–622.
5 McDougall I, Brown FH. 2006. Precise40Ar/39Ar geochronology for the upper KoobiFora Formation, Turkana Basin, northernKenya. J Geol Soc London 163:205–220.
6 Leakey LSB. 1958. A giant child among thegiant animals of Olduvai? A huge fossil milkmolar which suggests that Chellean Man inTanganyika may have been gigantic. The Illus-trated London News 232:1104–1105.
7 Leakey LSB. 1958. Recent discoveries at Old-uvai Gorge, Tanganyika. Nature 181:1099–1103.
8 Leakey LSB. 1959. A new fossil skull fromOlduvai. Nature 184:491–493.
9 Leakey LSB, Leakey MD. 1964. Recent discov-eries of fossil hominids in Tanganyika, at Oldu-vai and near Lake Natron. Nature 202:5–7.
10 Arambourg C, Coppens Y. 1968. Decouverted’un australopithecien nouveau dans les Gise-ments de L’Omo (Ethiopie). S Afr J Sci 64:58–59.
11 Coppens Y. 1978. Evolution of the hominidsand of their environment during the Plio-Pleis-tocene in the lower Omo Valley, Ethiopia. In:Bishop WW, editor. Geological background tofossil man. Edinburgh: Scottish AcademicPress. p 499–506.
12 Coppens Y. 1980. The differences betweenAustralopithecus and Homo; preliminary con-
clusions from the Omo research expedition’sstudies, ed. Konigsson LK. Oxford, Pergamon.
13 Coppens Y, Sakka M. 1983. Un nouveau craned’australopitheque. Evolutive Morphogenese duCranie et Anthropogenese. Paris, CNRS. p 185–194.
14 Alemseged ZY, Coppens Y, Geraads D. 2002.Hominid cranium from Omo: description andtaxonomy of Omo-323-1976-896. Am J PhysAnthropol 117:103–112.
15 Gowlett JAJ, Harris JWK, Walton D, WoodBA. 1981. Early archaeological sites, hominidremains and traces of fire from Chesowanja,Kenya. Nature 294:125–129.
16 Leakey REF, Walker A. 1988. New Australo-pithecus boisei specimens from East and West LakeTurkana, Kenya. Am J Phys Anthropol 76:1–24.
17 Brown B, Walker A, Ward CV, Leakey RE.1993. New Australopithecus boisei calvaria fromEast Lake Turkana, Kenya. Am J Phys Anthro-pol 91:137–159.
18 Prat S, Brugal J-P, Roche H, Texier P-J.2003. Nouvelles decouvertes de dents d’homi-nides dans le membre Kaitio de la formation deNachukui (1, 65-1, 9 Ma), Ouest du lac Turkana(Kenya). CR Palevol 2:685–693.
19 Walker AC, Leakey RE, Harris JM, BrownFH. 1986. 2.5 Myr Australopithecus boisei fromwest of Lake Turkana, Kenya. Nature 322:517–522.
20 Suwa G, et al. 1997. The first skull of Aus-tralopithecus boisei. Nature 389:489–492.
21 Kullmer O, Sandrock O, Abel R, Schrenk F,Bromage TG, Juwayeyi YM. 1999. The first Par-anthropus from the Malawi Rift. J Hum Evol37:121–127.
22 Leakey REF. 1970. New hominid remainsand early artefacts from North Kenya. Nature226:223–224.
23 Wood BA, Wood CW, Konigsberg LW. 1994.Paranthropus boisei: an example of evolutionarystasis? Am J Phys Anthropol 95:117–136.
24 Wood B, Lieberman DE. 2001. Craniodentalvariation in Paranthropus boisei: a developmen-tal and functional perspective. Am J PhysAnthropol 116:13–25.
25 Leakey REF. 1971. Further evidence ofLower Pleistocene hominids from East Rudolf,North Kenya. Nature 231:241–245.
26 Robinson JT. 1972. The bearing of EastRudolf fossils on early hominid systematics.Nature 240:239–240.
27 Wood BA, Li Y, Willoughby C. 1991. Intra-specific variation and sexual dimorphism incranial and dental variables among higher pri-mates and their bearing on the hominid fossilrecord. J Anat 174:185–205.
28 Grausz HM, Leakey RE, Walker AC, WardCV. 1988. Associated cranial and postcranialbones of Australopithecus boisei. In: Grine FE,editor. Evolutionary history of the ‘‘robust’’ Aus-tralopithecines. New York: Aldine de Gruyter.p 127–132.
29 Day MH. 1969. Femoral fragment of a ro-bust australopithecine from the Olduvai Gorge,Tanzania. Nature 221:230–233.
30 Wood BA. 1974. Evidence on the locomotorpattern of Homo from Early Pleistocene ofKenya. Nature 251:135–136.
31 Wood BA. 1974. Olduvai Bed I post-cranialfossils: a reassessment. J Hum Evol 3:373–378.
32 Gebo DL, Schwartz GT. 2006. Foot bonesfrom Omo: implications for hominin evolution.Am J Phys Anthropol 129:499–511.
33 Johanson DC, et al. 1987. New partial skele-ton of Homo habilis from Olduvai gorge, Tanza-nia. Nature 327:205–209.
34 Robinson JT. 1960. The affinities of the newOlduvai australopithecine. Nature 186:456–458.
35 Suwa G. 1988. Evolution of the ‘‘robust’’australopithecines in the Omo succession: evi-dence from mandibular premolar morphology.In: Grine FE, editor. Evolutionary history of the‘‘robust’’ australopithecines. New York: Aldinede Gruyter. p 199–222.
36 Tobias PV. 1967. Olduvai Gorge, vol. 2. Thecranium and maxillary dentition of Australopi-thecus (Zinjanthropus) boisei. Cambridge: Cam-bridge University Press.
37 Delson E. 1997. One skull does not a speciesmake. Nature 389:445–446.
38 Menter CG, Kuykendall KL, Keyser AW,Conroy GC. 1999. First record of hominid teethfrom the Plio-Pleistocene site of Gondolin,South Africa. J Hum Evol 37:299–307.
39 Keyser AW, Menter CG, Moggi-Cecchi J,Pickering TR, Berger LR. 2000. Drimolen: anew hominid-bearing site in Gauteng, SouthAfrica. S Afr J Sci 96:193–197.
40 Constantino P, Wood B. 2004. Paranthropuspaleobiology. Miscelanea en homenaje a Emi-liano Aguirre. Madrid: Museo Arqueolocico Re-gional. p 136–151.
41 Dean MC. 1988. Growth of teeth and devel-opment of dentition in Paranthropus. In: GrineFE, editor. Evolutionary History of the ‘‘Ro-bust’’ Australopithecines. New York, Aldine deGruyter. p 43–53.
42 Groves CP. 1989. A theory of human andprimate evolution. Oxford: Clarendon Press.
43 Silverman N, Richmond B, Wood B. 2001.Testing the taxonomic integrity of Paranthropusboisei sensu stricto. Am J Phys Anthropol115:167–178.
44 Wood BA. 1988. Are ‘‘robust’’ australopithe-cines a monophyletic group? In: Grine FE, edi-tor. Evolutionary history of the ‘‘robust’’ Aus-tralopithecines. New York: Aldine de Gruyter.p 269–284.
45 Corruccini RS. 1994. How certain are homi-noid phylogenies? The role of confidence intervalsin cladistics. In: Corruccini RS, Ciochon RL, edi-tors. Integrative paths to the past: paleoanthropo-logical advances in honor of F. Clark Howell.Englewood Cliffs: Prentice Hall. p 167–183.
46 Strait DS, Grine FE, Moniz MA. 1997. Areappraisal of early hominid phylogeny. J HumEvol 32:17–82.
47 Wood BA, Chamberlain AT. 1986. Australo-pithecus: grade or clade? In: Wood B, Martin L,Andrews P, editors. Major topics in primateand human evolution. Cambridge: CambridgeUniversity Press. p 220–248.
48 Skelton RR, McHenry HM. 1992. Evolution-ary relationships among early hominids. J HumEvol 23:309–349.
49 Maglio VJ. 1975. Origin and evolution of theElephantidae. Trans Am Philos Soc 63:1–149.
50 Vrba ES. 1979. Phylogenetic analysis andclassification of fossil and recent Alcelaphini(Mammalia: Bovidae). Biol J Linnaean Soc11:207–228.
51 Vrba ES. 1984. Evolutionary pattern andprocess in the sister-group Alcelaphini-Aepycer-otini (Mammalia: Bovidae). In: Eldredge N,Stanley SM, editors. Living fossils. New York:Springer-Verlag. p 62–79.
52 Patterson C. 1982. Morphological charactersand homology. In: Joysey KA, Friday AE, edi-tors. Problems of phylogenetic reconstruction.London: Academic Press. p 21–74.
53 Suwa G, Wood BA, White TD. 1994. Furtheranalysis of mandibular molar crown and cusp
ARTICLES The Evolution of Zinjanthropus boisei 61
areas in Pliocene and Early Pleistocene homi-nids. Am J Phys Anthropol 93:407–426.
54 Asfaw B, White T, Lovejoy O, Latimer B,Simpson S, Suwa G. 1999. Australopithecusgarhi: a new species of early hominid fromEthiopia. Science 284:629–635.
55 Shipman P, Harris JM. 1988. Habitat prefer-ence and paleoecology of Australopithecus boi-sei in eastern Africa. In: Grine FE, editor. Evo-lutionary history of the ‘‘robust’’ Australopithe-cines. New York: Aldine de Gruyter. p 343–381.
56 Reed KE. 1997. Early hominid evolutionand ecological change through the African Plio-Pleistocene. J Hum Evol 32:289–322.
57 Nagaoka S, Katoh S, Wolde Gabriel G, SatoH, NaKaya H, Beyene Y, Suwa G. 2005. Lith-ostratigraphy and sedimentary environmentsof the hominid-bearing Pliocene-PleistoceneKonso Formation in the southern Main Ethio-pian Rift, Ethiopia. Palaeogeogr Palaeocl 216:333–357.
58 Schrenk F, Bromage TG, Gorthner A, San-drock O. 1995. Paleoecology of the Malawi Rift:vertebrate and invertebrate faunal contexts ofthe Chiwondo Beds, northern Malawi. J HumEvol 28:59–70.
59 Leakey LSB, Tobias PV, Napier JR. 1964. Anew species of the genus Homo from OlduvaiGorge. Nature 202:7–9.
60 Isaac GL. 1984. The archaeology of humanorigins: studies of the Lower Pleistocene in EastAfrica 1971–1981. Advances in World Archaeol3:1–87.
61 Brain CK, Churcher CS, Clark JD, Grine FE,Shipman P, Susman RL, Turner A, Watson V.1988. New evidence of early hominids, theirculture and environment from the Swartkranscave, South Africa. S Afr J Sci 84:828–835.
62 Clark JD. 1990. The earliest cultural eviden-ces of hominids in southern and south centralAfrica. In: Sperber G, editor. New York: Wiley-Liss. p 1–15.
63 Susman RL. 1991. Who made the Oldowantools? Fossil evidence for tool behavior in Plio-Pleis-tocene hominids. J Anthropol Res 47:129–151.
64 Wood BA. 1997. The oldest whodunnit inthe world. Nature 385:292–293.
65 Susman RL. 1988. Hand of Paranthropusrobustus from Member 1, Swartkrans: fossil evi-dence for tool behaviour. Science 240:781–784.
66 Kuman K, Clarke RJ. 2000. Stratigraphy, ar-tifact industries and hominid associations forSterkfontein, Member 5. J HumEvol 38:827–847.
67 Dean MC, Wood BA. 1981. Metrical analysisof the basicranium of extant hominoids and Aus-tralopithecus. Am J Phys Anthropol 54:63–71.
68 Dean MC, Wood BA. 1982. Basicranial anat-omy of Plio-Pleistocene hominids from East andSouth Africa. Am J Phys Anthropol 59:157–174.
69 Hylander WL. 1975. Incisor size and diet inanthropoids with special reference to Cercopi-thecidae. Science 189:1095–1098.
70 Lucas PW, Corlett RT, Luke DA. 1986. Post-canine tooth size and diet in anthropoid prima-tes. Z Morphol Anthropol 76:253–276.
71 Kay RF. 1975. The functional adaptations ofprimate molar teeth. Am J Phys Anthropol43:195–216.
72 Hatley T, Kappelman J. 1980. Bears, pigs,and Plio-Pleistocene hominids: a case for theexploitation of belowground food resources.Hum Ecol 8:371–387.
73 Laden G, Wrangham R. 2005. The rise of thehominids as an adaptive shift in fallback foods:plant underground storage organs (USOs) andaustralopith origins. J Hum Evol 49:482–498.
74 Grine FE, Martin LB. 1988. Enamel thick-ness and development in Australopithecus andParanthropus. In: Grine FE, editor. Evolution-ary history of the ‘‘robust’’ australopithecines.New York: Aldine de Gruyter. p 3–42.
75 Gantt DG, Rafter JA. 1998. Evolutionary andfunctional significance of hominoid toothenamel. Connect Tissue Res 39:195–206.
76 Rak Y. 1988. On variation in the masticatorysystem of Australopithecus boisei. In: Grine FE,editor. Evolutionary history of the ‘‘robust’’ Aus-tralopithecines. New York: Aldine de Gruyter.p 193–198.
77 Tobias PV. 1963. Cranial capacity of Zinjan-thropus and other australopithecines. Nature197:743–746.
78 Demes B, Creel N. 1988. Bite force, diet, andcranial morphology of fossil hominids. J HumEvol 17:657–670.
79 Walker AC. 1981. Diet and teeth: dietaryhypotheses and human evolution. Philos TransR Soc Lond B 292:57–64.
80 Hylander WL. 1988. Implications of in vivoexperiments for interpreting the functional sig-nificance of ‘‘robust’’ australopithecine jaws. In:Grine FE, editor. Evolutionary history of the‘‘robust’’ Australopithecines. New York: Aldinede Gruyter. p 55–83.
81 WoodBA, Aiello LC. 1998. Taxonomic and func-tional implications of mandibular scaling in earlyhominins. Am J Phys Anthropol 105: 523–538.
82 Walker A, personal communication. 2006.
83 Grine FE. 1981. Trophic differences betweengracile and robust Australopithecus: a scanningelectron microscope analysis of occlusal events.S Afr J Sci 77:203–230.
84 Scott RS, Ungar PS, Bergstrom TS, BrownCA, Grine FE, Teaford MF, Walker A. 2005.Dental microwear texture analysis showswithin-species diet variability in fossil homi-nins. Nature 436:693–695.
85 Boaz NT, Hampel J. 1978. Strontium con-tent of fossil tooth enamel and diet of earlyhominids. J Paleontol 52:928–933.
86 Sillen A, Hall G, Armstrong R. 1995. Stron-tium calcium ratios (Sr/Ca) and strontium iso-topic ratios (87Sr/86Sr) of Australopithecus
robustus and Homo sp. in Swartkrans. J HumEvol 28:277–285.
87 Plavcan JM. 2000. Inferring social behaviorfrom animal dimorphism in the fossil record. JHum Evol 39:327–344.
88 Plavcan JM. 2003. Scaling relationshipsbetween craniofacial sexual dimorphism andbody mass dimorphism in primates: implica-tions for the fossil record. Am J Phys Anthropol120:38–60.
89 Smith BH. 1991. Age of weaning approxi-mate age of emergence of the first permanentmolar in non-human primates. Am J Phys An-thropol (suppl):163–164.
90 Dean MC. 2000. Progress in understandinghominoid dental development. J Anat 197:77–101.
91 Aiello LC, Montgomery C, Dean C. 1991.The natural history of deciduous tooth attritionin hominoids. J Hum Evol 21:397–412.
92 Harvey PH, Clutton-Brock TH. 1985. Lifehistory variation in primates. Evolution 39:559–581.
93 Aiello L, Wood B. 1994. Cranial variables aspredictors of hominine body mass. Am J PhysAnthropol 95:409–426.
94 Kappelman J. 1996. The evolution of bodymass and relative brain size in fossil hominids.J Hum Evol 30:243–276.
95 de Sousa A, Wood B. 2007. The homininfossil record and the emergence of themodern human central nervous system. In:Kaas JH, editor. The evolution of primatenervous systems. Oxford: Elsevier. p 291–336.
96 Beynon A, Wood B. 1987. Patterns and ratesof enamel growth in the molar teeth of earlyhominids. Nature 326:493–496.
97 Weidenreich F. 1935. The Sinanthropus pop-ulation of Choukoutien (locality) with a prelimi-nary report on new discoveries. Bull Geo SocChina 14:427–466.
98 Smith RJ. 2005. Species recognition in pale-oanthropology: implications of small samplesizes. In: Lieberman DE, Smith RJ, Kelley J,editors. Interpreting the past: essays on human,primate, and mammal evolution in honor ofDavid Pilbeam. Boston: Brill Academic Publish-ers. p 207–219.
99 Delson E, Tattersall I, Van Couvering JA,Brooks AS, editors. 2000. Encyclopedia ofhuman evolution and prehistory, 2nd ed. NewYork: Garland Publishing.
100 Tobias PV. 1991. Olduvai Gorge, vol. 4. Theskulls, endocasts and teeth of Homo habilis.Cambridge: Cambridge University Press.
VVC 2007 Wiley-Liss, Inc.
62 Constantino and Wood ARTICLES
