4.18 the hominin fossil record, emergence of the modern cns

4.18 The Hominin Fossil Record and theEmergence of the Modern Human CentralNervous System

A de Sousa and B Wood, The George WashingtonUniversity, Washington, DC, USA

ª 2007 Elsevier Inc. All rights reserved.

4.18.1 Introduction 2924.18.2 How can Fossil Evidence Be Used to Reconstruct the Recent Evolution of

the Modern Human CNS? 2924.18.2.1 Fossil Evidence Relevant for Reconstructing the Size and Shape of the Brain 2924.18.2.2 Data Interpretation 2944.18.2.3 Brain Size Measures and Estimates 2944.18.2.4 Comparing Different Types of Measurements and Estimates 2974.18.2.5 Indices for Estimating and Comparing the Relative Sizes of Brains 2974.18.2.6 Major Lines of Fossil Evidence for CNS Evolution, Plus Other Endocranial Morphology 299

4.18.3 The Hominin Fossil Record 3024.18.3.1 Defining Hominins 3024.18.3.2 Terminology 3024.18.3.3 Organizing the Hominin Fossil Record 3034.18.3.4 Review of Individual Hominin Fossil Taxa 304

4.18.4 Review of Hominin Taxa 3054.18.4.1 Possible and Probable Primitive Hominins 3054.18.4.2 Archaic Hominins 3074.18.4.3 Megadont Archaic Hominins 3114.18.4.4 Transitional Homo 3144.18.4.5 Premodern Homo 3164.18.4.6 Anatomically Modern Homo 322

4.18.5 Trends in Hominin CNS Evolution 3244.18.5.1 Primitive Brain Morphology 3244.18.5.2 Modern Human or Hominin Lineage 3244.18.5.3 Brain Evolution in Other Lineages 329

Glossary

anatomically modernhuman

Hominin fossil evidence thatcannot be distinguishedfrom the skeletal remains ofcontemporary modernhumans.

brain specific mass The average density of thebrain.

brain tissue volume The volume of the brainitself (i.e., brain volumeminus the volume of theCSF within the ventricles ofthe brain and the volume ofany meninges and cranialnerves that may adhere tothe brain).

brain volume Usually defined as the sumof the volume of the wholebrain (including the ventri-cles) plus the leptomeninges

(i.e., the arachnoid and piamater).

clade (Gk.clados¼ Branch)

A grouping of taxa that con-tains no more and no lessthan all the descendants ofthe group’s most recentcommon ancestor.

encephalization (syn.cephalization,cephalisation)

The process by which, for agiven taxon, relative brainsize becomes larger thanpredicted from the generalscaling relationship betweenbrain size and body size.

encephalization quotient(EQ)

The ratio of the observedbrain size over the expectedbrain size, based on a gen-eral scaling relationship.

endocranial cast A natural or artificial castthat uses the walls, roof,and floor of the cranial cav-ity as a mold.

292 The Hominin Fossil Record and the Emergence of the Modern Human CNS

endocranial volume (syn.cranial capacity, endocra-nial capacity)

The volume of the endocra-nial cavity. This is the sumof brain volume plus thevolumes of the meninges,the extracerebral CSF (i.e.,the CSF outside the ventri-cles), the intracranial (butextracerebral) vessels, andthe cranial nerves withinthe cranial cavity.

hominin (L.homin¼Man)

Vernacular for a species (oran individual specimenbelonging to a taxon) withinthe tribe Hominini (e.g.,Paranthropus boisei is ahominin taxon and KNM-ER 1470 is a hominin fossilcranium).

meningeal vessels The meningeal arteries andveins that supply blood to,and drain most of the bloodfrom, the neurocranium andthe dura mater.

petalia The greater anterior, poster-ior, or lateral protrusion ofone cerebral lobe relative tothe other.

suture (L. sutura ¼ ASeam)

Fibrous joint between twobones of the cranial vault.The fibrous tissue in thesejoints gradually disappearsas the bones fuse together.

virtual endocast 3-D digital cast of the neu-rocranial cavity, createdusing 2-D computed tomo-graphy slices.

4.18.1 Introduction

This article focuses on what the fossil evidence forhuman evolution can tell us about the evolution ofthe modern human central nervous system (CNS).Its scope is the hominin clade, which extends in timefrom the hypothetical common ancestor of chim-panzees and modern humans, via the appearanceof the first hominins (c. 8–5 Mya), to the emergencea little over 190 kya ago of anatomically modernhumans. We use the term ‘hominin’ for modernhumans and all extinct species that are more closelyrelated to modern humans than to any other livingtaxon, and the term ‘panin’ for living chimpanzeesand all extinct species that are more closely relatedto chimpanzees than to any other living taxon.

The first section reviews the ways in which thefossil and archeological records can be used to helpreconstruct the CNS of extinct hominin taxa. Thesecond section reviews the relationships of modern

humans, and outlines the organization of the homi-nin fossil record. The third section reviews each ofthe fossil hominin species. It uses a relatively spe-ciose hominin taxonomy, but it also indicates howthe same fossil evidence would be arranged if it weregrouped into a smaller number of more inclusivetaxa. Brief descriptions of each taxon are provided.There are two reasons why this section concentrateson the craniodental evidence. The first relates to therelative durability of the hard tissues of the head andneck of higher primates. Because they are generallyhard and dense, they tend to preserve in larger num-bers than do the bones of the limbs and trunk. Thismeans that most species are defined on the basis of aset of distinctive craniodental traits. The secondreason is that because, in this article, we focus onhow the quality and scope of the fossil evidence foreach taxon can contribute to our knowledge aboutthe recent evolutionary history of the modernhuman CNS, this inevitably means emphasizingthe cranial evidence. The fourth section of the articlesummarizes trends in the evolution of the homininCNS. It summarizes the differences between theCNSs of modern humans and chimpanzees, andmakes predictions about the CNS of the commonancestor of chimpanzees and modern humans. Itaddresses, among others, the following questions:

1. When did hominin brain size begin to increasebeyond the levels we see in contemporary nonhu-man higher primates?

2. At what stages in hominin evolution do we seegrade shifts in brain morphology?

3. Were changes in brain size and shape restricted toour own genus, or did they occur in other hominingenera?

4.18.2 How can Fossil Evidence Be Usedto Reconstruct the Recent Evolution ofthe Modern Human CNS?

4.18.2.1 Fossil Evidence Relevant forReconstructing the Size and Shape of the Brain

The biggest obstacle to understanding the evolutionof the human CNS is that the CNS is not preservedin the hominin fossil record. However, inferencescan be made about the size and shape of the CNSfrom natural endocasts, from the fossilized mor-phology of the neurocranium, the cranial base, andthe axial skeleton. Endocasts and neurocranial fos-sils convey information about the size, shape,external convolutional morphology, and blood sup-ply of the brain. Cranial base morphology containsinformation about the brainstem, and the cranial

The Hominin Fossil Record and the Emergence of the Modern Human CNS 293

nerves and blood vessels that perforate it. Finally,the neural canal conveys information about thespinal cord which extends in adult modern humansfrom the atlas (C1) to the first (usually) or secondlumbar vertebras. Across primate species, the cross-sectional area of the vertebral canal provides anindication of spinal cord dimensions – particularlyin its most rostral aspect, but less so more caudallywhere a greater proportion of the canal is devoted tospinal nerves (MacLarnon, 1995).

Although endocasts look remarkably brain-like,an endocast is not a fossil brain, but rather a cast ofthe neurocranial cavity. A natural endocast isformed during fossilization as the cranial cavityfills with fine sediments that enter through the var-ious foramina and fissures that perforate the floor ofthe cranial cavity. Similarly, a synthetic endocast ismade by stopping these perforations and then liningthe inner surface of the endocranial cavity withquick-drying latex. Once dry, the thin layer of flex-ible latex can be peeled off the endocranial surfaceand removed through the foramen magnum. It isalso possible to create a three-dimensional (3-D)digital cast of the neurocranial cavity, called a vir-tual endocast, and this has become the method ofchoice for investigating delicate and/or fragmentaryfossils (e.g., Falk et al., 2005; Zollikofer et al.,2005). Endocasts potentially preserve details of theconvolutional morphology of the surface of the cer-ebral and cerebellar hemispheres that are imprintedthrough the three layers of meninges (from outsidein: the dura, arachnoid, and pia mater). In addition,endocasts preserve the imprints of blood vessels andskeletal sutures.

Convolutional details are not always well pre-served. The differential imprinting of convolutionaldetail may be due to taphonomy, the relative size ofthe brain, and the effects of ontogeny. In general,natural endocasts produce more details than syn-thetic endocasts. Falk (1980a) proposed twoexplanations for this: (1) natural endocasts maybegin to form before the dura mater has fully disin-tegrated, so that any details present on it, but absenton the endocranial surface of the inner table of theneurocranium, are preserved; and (2) synthetic endo-casts are often produced from crania that have beenreconstructed from fragments, and the process ofreconstruction can introduce morphological noise.The relatively small-brained Australopithecus endo-casts are usually more detailed than endocasts madefrom crania assigned to larger-brained later Homotaxa. It is noteworthy that, for various groups ofmammals, those with the largest brains within thatgroup tend to produce the least-detailed endocasts,although this pattern does not hold true for absolute

brain size across major groups (Radinsky, 1972,p. 176). This is related to the fact that endocranialvolume increases more rapidly than brain sizeincreases within primates (Martin, 1990, pp. 365,392). The intensity of gyral impressions is also relatedto ontogeny. In modern humans there are few or noimpressions on the endocranial aspect of the cranialvault before 1 year (Du Boulay, 1956). Gyral impres-sions are probably most marked during adolescence,and with increasing age basal markings become moreprominent whereas vault impressions become fainter(Connolly, 1950, p. 291).

The convolutional details of endocasts are notor-iously difficult to interpret (Symington, 1916;Holloway, 1966). A feature might be the impressionof a sulcus, or a blood vessel, or a skeletal suture, orit might be an artifact, and observers might offergenuinely different interpretations of what the samefeature represents (Connolly, 1950; Falk, 1980a).For example, over the last three decades, Hollowayand Falk have been providing often conflictinginterpretations of the same endocasts. Only a hand-ful of researchers study the details of endocastmorphology, and both Falk and Holloway havecalled on other paleoanthropologists to join thedebate (Falk, 1987; Holloway et al., 2004a).

Not all researchers are convinced that the detailedmorphology of endocasts has functional relevance.Many paleoneurologists take it for granted that sulcidelimit functional or somatotopic cortical areas (seeRadinsky, 1972, and references therein). However,it has become clear that the primate brain exhibits asubstantial amount of intraspecific variability insulcal anatomy and cytoarchitectural boundaries(Geyer et al., 2001; Rademacher et al., 2001). Insome cases, the relationship between sulcal land-marks and functional areas is maintained within aspecies (Holloway et al., 2003), but in others itvaries within species (Sherwood et al., 2003). Itmight not be possible to make detailed interpreta-tions of brain function from endocasts alone.

Information about fossil hominin brain evolutionis not limited to the hard-tissue fossil record.Natural endocasts are a form of trace fossil thatrecord, often in unusual detail, the endocranial mor-phology of an individual. Archeologists also claimthat artifacts reveal information about the evolutionof the hominin CNS. Tools, art, and other artifactsfound in association with hominin remains providedirect evidence of the capacity of a species for spe-cific behaviors, something that fossils cannot reveal.

The combination of paleontological and archeo-logical evidence provides more insight into the brainfunction of fossil hominins than either of these twolines of evidence could generate on their own.


4.18.2.2 Data Interpretation

In a specimen of an extant taxon, the size and shapeof the brain can be estimated from either the brainitself or, indirectly, from cranial measurements. In afossil specimen, measurements are taken from eitheran endocast (natural or synthetic) or from a fossilneurocranium. In general, the same measurementmethods are used for endocasts and whole brains,and similar methods are applied to extant and fossilneurocrania. However, there are several reasonswhy data taken from contemporary taxa and datataken from fossil specimens might not be compar-able and suggestions have been made to correct forthe discrepancies.

First, it is important to appreciate that the volumeof an endocast is the volume of the neurocranialcavity (i.e., endocranial capacity or endocranialvolume). Endocranial volume includes not only thevolume of the brain, but also the space occupied bymeninges, extracerebral cerebrospinal fluid (CSF),and cranial nerves.

Second, all fossils, including endocasts and cra-nial fossils, are imperfect representations of the hardtissues they represent. Problems include incomplete-ness and plastic deformation. Incomplete fossilsrequire that assumptions are made about the sizeand shape of the missing parts, and deformationmay be difficult to detect when the form of theundeformed brain is unknown. Matrix can fill andwiden cracks, expanding the size of the fossilbeyond the size of the original bone. Virtual meth-ods have recently been developed to correct for suchdeformation.

Third, even well-preserved fossils present sam-pling problems that affect interspecificcomparisons. For example, we do not know thechronological age of individual fossils, yet if theindividual is immature it may be necessary to esti-mate the size of the equivalent adult. However,ontogenetic age is difficult to estimate even in extantanimals, let alone in a fossil species for which wewill never have a satisfactory reference sample. Inaddition, sexual dimorphism may introduce sub-stantial variation in brain volume within a species.In hominin species with a sparse fossil record, over-representation of a particular sex might give aninaccurate impression of the species’ true meanand range of brain size.

4.18.2.3 Brain Size Measures and Estimates

The brain sizes of fossils can be obtained from avariety of methods that vary in their accuracy andprecision. For example, de Miguel and Henneberg(2001) reviewed the brain size estimates for OH 5

cited in the literature and found that for this rela-tively complete Paranthropus boisei fossil cranium15 different endocranial volume estimates are givenranging from 500 to 750 cm3. Holloway (1983b)has devised a useful system for indicating the relia-bility of endocranial volume measurements whichuses a letter code for the method used and a numbercode for the reliability of the measurement.

4.18.2.3.1 Measurements of the volume of a brainor of a solid endocast by water displacement Thepreferred way to determine the volume of a brain oran endocast, natural or artificial, is by water displa-cement according to Archimedes’ principle. Forextant species this is done using postmortem brains,but how well does this method measure brain size?For postmortem samples, one or more of the follow-ing confounding factors needs to be taken intoaccount: time from death to measurement, timefrom death to fixation, fixation method and pre-paration prior to measurement, whether theleptomeninges and CSF are included, adequacy ofdissection, and shrinkage. For example, whatStephan and others (Stephan et al., 1970, 1988;Stephan, 1981) call brain weight includes meninges,hypophysis, and any nerves still attached to thebrain (Heiko Frahm, personal communication).Similarly, the largest brain mass data sets for mod-ern humans (Dekaban and Sadowsky, 1978) andchimpanzees (Herndon et al., 1999) include lepto-meninges and CSF in the brain mass estimates.Jerison (1973) estimates that the effect of includingor excluding variables such as these can cause mea-surements to differ by as much as 20%.

Holloway et al. (2004a, 2004b) found that weigh-ing the water displaced by an endocast was a moreconsistent method than measuring its volume.Volumes measured using artificial endocasts mightbe underestimates of the true volume because endo-casts are likely to have undergone shrinkage(Gingerich and Martin, 1981; Broadfield et al.,2001).

4.18.2.3.2 Measurements of the volume of theendocranial cavity4.18.2.3.2.(i) Packing methods Packing methodsinvolve filling the cranial cavity with small particlessuch as mustard seed, sintered glass beads, orshotgun pellets, and then determining the volumeof the packing material. Different types of fillers canproduce slightly different endocranial volume esti-mates (Miller, 1991). For fossil crania, packingmethods are sometimes preferred over water displa-cement of a latex endocast because the problem ofendocast shrinkage is avoided. However, because of


variation in techniques for settling the packingmaterial, these methods almost certainly underesti-mate the true endocranial volume (Gould, 1978,1996).

4.18.2.3.2.(ii) Filling methods Filling methodsare like packing methods, but involve a fluid ratherthan a solid. Uspenskii (1954) describes a method inwhich a rubber balloon is put into the cranial cavityand then filled with water. Similar values (meandifference 1.67 cm3) were obtained with thismethod and with water displacement, but packingwith millet seed resulted in smaller (mean difference65.4 cm3) values than those obtained using the bal-loon method (Uspenskii, 1954).

4.18.2.3.3 Estimating volumes from slices4.18.2.3.3.(i) Cavalieri’s principle Using Cavalieri’sprinciple, it is possible to produce an unbiasedestimate of total brain volume from measurementsof the cross-sectional area of a sample of brainsections (Stephan, 1981, p. 3; Gundersen and Jensen,1987). Cavalieri’s principle can be used to determinebrain volume from actual and virtual brains. Serialsections of brains mounted onto slides undergoshrinkage as a result of fixation and embedding, sovolume measurements determined from slide-mounted sections need to be corrected accordingly.In early papers, the effect of shrinkage was over-looked. Stephan (1981) advised researchers togenerate an individual conversion factor (Cind) for abrain with known mass and known volume:

Cind ¼Volume of fresh brain

Serial section volume:

Stephan (1981, p. 4) list conversion factors forspecific types of fixation, ranging from 1.54 to2.4. Aside from mismeasurement due to shrink-age, the only disadvantage with using sections asopposed to water displacement is that the formerestimates volume, rather than measuring it.However, what the estimate loses in precision itmay gain in accuracy, since imaging makes itpossible to be sure that only brain tissue isincluded.

4.18.2.3.3.(ii) In vivo MRI Magnetic resonanceimaging (MRI) has recently begun to be applied tocomparative samples of living hominoid species inorder to obtain volumes of both entire brains andparticular brain regions (e.g., Rilling and Insel,1999; Semendeferi and Damasio, 2000; Sherwoodet al., 2004). Comparison of MRI volumes withvolumes obtained by water displacement haveestablished that as few as 5–6 MRI slices per brain

are enough to yield reliable estimates of mean brainvolume, with a coefficient of error (CE) of approxi-mately 5% (Mayhew and Olsen, 1991). The CEdecreases as the number of slices increases (e.g., for28 slices, CE < 1%).

There are several advantages to using in vivo MRIvolumes over autopsy brain volumes. In vivo MRIbrain volumes avoid biases inherent to usingautopsy brains; for example, autopsy brain samplesoverrepresent aged individuals. In vivo MRIvolumes are not affected by changes in brain volumedue to the elapsed time between death and measure-ment or fixation. Peters et al. (1998) compared theresults of cross-sectional studies in which humanbrain volumes were obtained either in vivo by MRI(or nuclear magnetic resonance, NMR) or fromautopsy brains. They found large discrepanciesbetween the means of the different samples (evenin cases in which the same method was used), butthey did not identify the way in which the autopsyand MRI volumes differed.

4.18.2.3.3.(iii) Postmortem MRI Peters et al.(2000) compared estimates of brain volumeobtained from MRI and from water displacementin autopsy specimens. They found that providedthin MRI slices (1–1.25 mm) were used, MRIvolumes did not differ significantly from water dis-placement volumes. However, MRI volumes werefound to be overestimates when thicker slices(5 mm) were used.

4.18.2.3.3.(iv) CT slices and virtual endocasts Awidely applicable and noninvasive way in which toaccurately estimate fossil endocranial volumes is byusing two-dimensional (2-D) computed tomogra-phy (CT) slices. It is possible to use these slices toobtain an endocranial volume in two ways whichyield similar results: (1) either directly usingCavalieri’s principle, or (2) through the constructionof virtual endocasts (e.g., Conroy et al., 1998).Increasingly popular, a 3-D virtual endocast is a3-D model of the fossil constructed from the 2-DCT slices (Zollikofer et al., 1998; Tobias, 2001;Zollikofer, 2002). For matrix-filled skulls, thresh-olding to distinguish between local object densitiesis the method used to separate the walls of the fossilneurocranium from the matrix at their interface(Conroy and Vannier, 1985; Conroy et al., 1990;Zollikofer et al., 1998). Fragmentary specimens arecompleted using mirror-imaged parts from theopposite side (e.g., Conroy et al., 2000a), or scaledparts from another specimen (e.g., Zollikofer et al.,1998). Once the virtual cranium has been created(e.g., Zollikofer et al., 2005), it is possible to create a


virtual endocast. If there is uncertainty about thedimensions, several potential endocrania are createdto establish a range of endocranial volumes, fromwhich a most likely endocranial volume can bedetermined (Conroy et al., 2000b). The virtualendocast technique was tested on 10 Homo sapienscrania whose endocranial volumes were measuredusing a mustard seed filler; it was found that thedifference between the measured and virtual endo-cast volumes was around 2% (Conroy et al., 1998).

4.18.2.3.4 Measuring incomplete endocasts4.18.2.3.4.(i) Partial endocast method Tobias(1964, 1971, p. 64) introduced a method for esti-mating endocranial volume. The method, which hasbecome known as the partial endocast method,involves taking a complete endocast with knownendocranial volume, reducing it to the anatomy pre-served in the fossil of interest, and then determiningwhat proportion of the complete endocast is repre-sented by the reduced endocast. This provides aconversion factor to estimate complete endocranialvolume for the specimen for which there is only apartial endocast. This method was originally used todetermine the volume of OH 7, the type specimen ofH. habilis, and its large endocranial capacity (esti-mated by the partial endocast method to be 675–680 cm3; Tobias, 1964), was one of the reasonsgiven for including the new taxon in the genusHomo (Leakey et al., 1964). This spawned a debaterevolving around the reliability and taxonomicimplications of the original estimate, in which alter-native methods to determine endocranial volumesfrom partial endocasts were suggested (Pilbeam,1969; Wolpoff, 1969, 1981; Holloway, 1983d;Vaisnys et al., 1984).

4.18.2.3.4.(ii) Reconstructed endocast methodSynthetic and natural endocasts are typically recon-structed using plasticene to fill in missing areas. Ifonly small parts of bilateral structures are missingon one side the necessary reconstruction does notrequire much guesswork. Holloway (1973, 1975)distinguishes between minimal plasticene recon-struction (method A) and extensive plasticenereconstruction involving close to half the total endo-cast (method B). Endocast reconstruction should bere-evaluated as additional fossils are discovered, andnew, improved, methods should be applied to exist-ing endocasts, not just to newly discovered evidence.Holloway’s method involves making one endocastreconstruction based on comparisons with speci-mens belonging to the same hypodigm, or tomembers of different fossil hominin hypodigms(e.g., P. robustus and P. boisei) with brains that

are similar in size and shape. Reconstructionsmade independently by different researchers providea test of reliability. For example, the differencesbetween the endocranial volumes of Holloway’s(914 cm3) and Broadfield’s (921 cm3) reconstruc-tions of the Sambungmacan 3 calvaria are minimal(Broadfield et al., 2001).

4.18.2.3.5 Extrapolations from ecto- and endocraniallinear metrics Several formulas have been suggestedto estimate brain volume from linear dimensions ofthe endocranial cavity of crania, or endocasts.MacKinnon et al. (1956) compared linear measure-ments of the cranial cavity taken from radiographicimages to mustard seed endocranial capacities for 52modern human crania. They devised the followingformula, which predicts endocranial volume with anerror of 0.62% (0.87 cc in a 1400 cc cranium):

V ¼ 0:51½1=2ðLHW � LBWÞ�;

where L is endocast length from frontal pole tooccipital pole, W is maximum width (usually takenat the level of the superior aspect of the temporal), Bis the distance from bregma to basion, and H is thedistance from vertex to the deepest portion of thecerebellar lobes.

Holloway (1973, p. 450) applied this formula toendocasts, but he replaced the value of 0.51 with f, avariable determined for each taxon:

V ¼ f ½1=2ðLHW þ LBWÞ�:

It is not advisable to calculate endocranial volumefrom external head or cranial measurements.Simmons (1942) found that crania with similarexternal perimeter measurements had differentinternal capacities, and Wickett et al. (1994) foundthat head perimeter measurements were not signifi-cantly correlated with total brain size. Booksteinet al. (1999) found that some of the factors respon-sible for the differences between the external and theinternal cranial form were independent, so theinability of external head dimensions to accuratelypredict endocranial volume is not surprising.Further, there are particular problems with applyingformulas designed for modern humans on fossilhominins. Formulas that have been developed toestimate modern human endocranial volume, suchas those of Welcker (1885), Pearson (1926), andManouvrier (1898), do not provide accurate estima-tions of the cranial capacity of fossils (Olivier andTissier, 1975). Olivier and Tissier (1975) developedformulas specifically designed for archanthropiansand paleoanthropians, but the fact that members ofthe taxon H. heidelbergensis fall into both


categories suggests that the reliability of thisapproach is dependent on having a satisfactorytaxonomy.

4.18.2.4 Comparing Different Types ofMeasurements and Estimates

Brain size can be measured as a volume or as aweight (or mass). European authors tend to useweight whereas American authors tend use mass,but in most cases these terms are used inter-changeably. For consistency we will refer tomasses in grams (g) and volumes in cubic centi-meters (cm3).

4.18.2.4.1 Brain tissue mass from brainmass Measurements reported as brain mass fromautopsy brains typically include the leptomeninges(i.e., the arachnoid and pia mater) as well as what-ever CSF remains in the ventricles (Peters et al.,1998). Volumes taken from MRI or stained sectionsmeasure brain tissue volume from which the volumeof the meninges and the CSF are excluded (Peterset al., 1998). This is comparable to the net brainvolume calculated by adding up brain volumes forvarious brain components (e.g., Stephan, 1981). Inmodern humans, the meninges and CSF are esti-mated to contribute an additional 183 g for malesand 132 g for females (Peters et al., 1998). Thus, formale modern humans:

Brain tissue mass ðgÞ ¼ ½Brain mass ðgÞ� � 183;

and for female modern humans:

Brain tissue mass ðgÞ ¼ ½Brain mass ðgÞ� � 132:

4.18.2.4.2 Brain mass from brain volume For asample of 78 adult human brains, the brain tissuewas found to have an average specific mass of1.032 g cm�3 (Zilles, 1972). Thus,

Brain mass ðgÞ ¼ ½Brain volume ðcm3Þ� � 1:032:

The specific mass of the brain has also been deter-mined by comparing rodent brain weights withvolumes to give an average specific mass of1.036 g cm�3 (Stephan, 1960). Thus,

Brain mass ðgÞ ¼ ½Brain volume ðcm3Þ� � 1:036:

This suggests that brain mass is c. 3% larger thanbrain volume (but see Jerison’s argument below).

4.18.2.4.3 Brain volume from endocranialvolume Brain volume and endocranial volume(¼ cranial capacity) are not identical. Endocranialvolume is larger as it also includes meninges, CSF,

and cranial nerves. Few data are available for actualbrain volume and endocranial volume from thesame specimen because it is difficult to remove thebrain from the brain case without causing damageto either. Novel imaging techniques could improveour understanding of this relationship, although inpractice different techniques are used to visualizesoft (MRI) and hard (CT) tissues.

Pickering (1930) found a correlation betweennonfixed brain volume as determined by water dis-placement and endocranial volume measured withmustard seed in a sample of 29 modern humans,using the following conversion formula(r2¼ 0.805):

Brain volume ¼ ðEndocranial volumeÞ � 0:8598:

In other words, approximately 14% of the endocra-nial volume does not represent brain volume.

4.18.2.4.4 Brain mass from endocranialvolume Count (1947) suggested a value of0.876 g cm�3 for brain mass/endocranial volume,so that:

Endocranial volume ðcm3Þ¼ ½Brain mass ðgÞ� � 1:14;

Brain mass ðgÞ¼ ½Endocranial volume ðcm3Þ� � 1:14:

Ruff et al. (1997) used an equation that acknowl-edged the allometric nature of the relationshipbetween endocranial volume and brain mass (seeMartin, 1990). Ruff et al. derived brain mass fromendocranial volume using a regression based onbrain masses from Stephan et al. (1970) and cranialcapacities from Martin (1990) for 27 primate spe-cies (r2¼ 0.995):

Brain mass ðgÞ¼ 1:476� ½Endocranial volume ðcm3Þ�0:976:

Jerison (1973, p. 30) does not recommend con-verting endocranial volumes into brain volumes orbrain masses. Apparently, the specific gravity of themammalian brain ranges from 0.9 to 1.1; for exam-ple, brain mass (in g) is approximately 5% largerthan endocranial volume in insectivores (Bauchotand Stephan, 1967), whereas brain mass (in g) isapproximately 3% smaller than endocranial volumein a cat (Jerison, 1973).

4.18.2.5 Indices for Estimating and Comparingthe Relative Sizes of Brains

The relationship of brain size to body size, analyzedby Snell (1891), was the basis of Dubois’ index of


cephalization (Dubois, 1897), which related brainsize to (1) body size and somatic functions, and (2)the encephalization of psychic functions. Jerisonand Martin have further investigated the relation-ship between brain size and body size, and havemade contributions to the most widely used measureof relative brain size, the encephalization quotient.

4.18.2.5.1 Encephalization quotient Some research-ers (e.g., Jerison, 1973; Martin, 1990) do not considerabsolute brain size to be an appropriate way to com-pare the mental capacities of different species. Nor isit useful to compare the brain/body ratio, because thisratio decreases with increasing body size. The solu-tion has been to plot log brain mass on log body mass,from which is derived the allometric formula:

E ¼ kPb;

where E is brain size, P is body size, k is the allo-metric coefficient, and � is the allometric exponent.It has been suggested that different taxonomicgroups tend to have a similar value for � (reflectinga consistent functional relationship), but differentvalues for k (reflecting different grades; Martin,1981). This is usually expressed as the log-trans-formed linear equation:

logE ¼ logkþ bðlogPÞ:

The key variable � is typically referred to as thescaling coefficient.

For all mammals, Jerison (1961, 1973) observedthat the relationship between brain size and bodysize was described by the equation

Brain mass ¼ 0:12� ðBody massÞ2=3:

Jerison developed Dubois’ proposal for an equa-tion to quantify encephalization (Dubois, 1897),and derived what he referred to as the encephaliza-tion quotient (EQ):

EQ ¼ ðBrain massÞ=½0:12� ðBody massÞ2=3�:

Encephalization occurs when there is a departurefrom the general relationship between brain size andbody size. Encephalization occurs in mammals andbirds, but is rare in other vertebrates.Encephalization is explained by Jerison’s (1973)additive theory of brain size: E ¼ Ev þ Ec, where Eis brain size, Ev is brain size determined by bodysize, and Ec is associated with improved adaptivecapabilities. According to his theory, if Ec¼ 0, thenthe brain is of a size sufficient for somatic mainte-nance. If one assumes there is a relationship betweenbrain size and neuron number, and if Ec > 1, thenthe brain has extra neurons designated to deal with

extracorporeal pressures. The presence of extra neu-rons is referred to as encephalization.

A scaling coefficient value of 2/3 (or 0.66) wassuggested for several sets of mammals (Snell, 1891;Jerison, 1955, 1961, 1973; Gould, 1975), but a laterstudy suggested that a scaling coefficient of 3/4 (or0.75) is more appropriate (Martin, 1981). Based onthis, Ruff et al. (1997) used the following equationto generate EQ in hominins:

EQ ¼ Brain mass=½11:22� ðBody massÞ3=4�:

A scaling coefficient of approximately 3/4 (i.e.,0.78) was also described for a comprehensive sam-ple of primates (Bauchot and Stephan, 1969),although subsets of primates have a wider range ofvalues. The scaling coefficient of nonhuman homi-noids (i.e., the apes) is much lower (e.g., EQ ¼ 0.58;Bauchot and Stephan, 1969).

4.18.2.5.2 Other standards for brain sizecomparison Although brain size is most often con-sidered in relation to body mass, other standards forcomparing brain size have been used. Some authorssuggest that the scaling relationship between brainmass and body mass is a surrogate measure for someunderlying variable (e.g., Harvey and Krebs, 1990).CNS or CNS-related standards of comparison aresometimes preferred because they vary less intraspe-cifically, and measure brain versus nervous systeminformation flow. All standards have advantagesand disadvantages.

Krompecher and Lipak (1966) were the first tosuggest scaling brain size against the mass ofanother CNS structure (the spinal cord); subse-quently, Passingham (1975) scaled brain mass to aCNS-related structure (the foramen magnum). Thelatter method has the advantage that it uses a hard-tissue structure that is occasionally preserved in thehominin fossil record. The absolute size of the spinalcord gives an indication of total neuronal input andoutput to the brain. In fact, an index of brain size tononbrain CNS size provides a direct measure ofJerison’s extra neurons. On the other hand, it hasbeen suggested that body mass is better for use inscaling relationships precisely because, unlike theCNS or CNS-related structures, it is independentof brain mass (Stephan et al., 1988). Radinsky(1967) suggested that foramen magnum area was agood estimate of body size, although it is less vari-able within a species than is body mass. However,others have suggested that foramen magnum area islinked more closely with brain size than with overallbody size (Jerison, 1973; Gould, 1975; Martin,1981). In fact, the relationship of the size of a


given CNS or CNS-related structure to body mass isvariable. For example, the relationship betweenbody size and foramen magnum/medulla size maybe strongly influenced by specializations such asadaptation to water (Stephan and Dieterlen, 1982;Stephan and Kuhn, 1982).

Finally, it has been suggested that CNS structuresmake better standards because they vary less withina species than body mass does (Radinsky, 1967).One reason why body mass varies so much is thatit comprises several components, including musclemass and adipose tissue, which are themselves vari-able (Pitts and Bullard, 1968). Muscle tissue, whichis well innervated, and other components of fat-freemass scale more closely to CNS mass than does themass of the less well-innervated adipose tissue(Schoenemann, 2004). This finding has implicationsfor certain questions about the scaling of brain sizeto body size. For example, the difference betweenmale and female brain mass might be partiallyexplained by the fact that male body mass containsproportionally more muscle (Manouvrier, 1903;Ankney, 1992; Gould, 1996). Along these lines,when scaled to fat-free mass, it has been suggestedthat the very muscular Neanderthals would havemuch smaller relative brain size than would modernhumans (Schoenemann, 2004).

4.18.2.5.3 Measure of brain organization: A/Sratio Scaling brain size to other appropriate partsof the CNS gives a direct indication of the size of thebrain in relation to the amount of input and output.Hebb (1949) advocated replacing brain/body sizecomparisons with an A/S (association cortex/pri-mary sensory cortex) ratio, since the primarysensory areas are related to input from an animal’ssurroundings, whereas association areas areinvolved in higher-level cognitive processing. Thisprocedure is also advocated by Holloway, who dis-cussed in detail the problems associated with basingintelligence on brain/body size relationships(Holloway, 1968, 1979; Holloway and Post, 1982).

4.18.2.6 Major Lines of Fossil Evidence for CNSEvolution, Plus Other Endocranial Morphology

Particular attention is paid to fossil anatomy thatcan be used to make inferences about the functionalanatomy of the CNS. In addition, non-CNS relatedaspects of endocranial morphology are included.

4.18.2.6.1 CNS-related fossil evidence The cate-gories described below are the major lines ofevidence that can be used to infer CNS evolutionfrom the hominin fossil record. Their comparative

contexts are data from extant primates from theendocranium and brain, and from the vertebral col-umn and spinal cord. There is a dearth of data aboutthe CNS of extant hominoids, so most inferencesshould be treated as preliminary. The extant homi-noid data tend to be based on very small samples(e.g., one or two individuals per species, and oftenthe same individuals are used in several studies), and,with respect to the cerebral cortex, rely on grossmorphological landmarks as proxies for functionalregions (see The Development and EvolutionaryExpansion of the Cerebral Cortex in Primates).

4.18.2.6.1.(i) Absolute and relative brainsize Sample mean EQs are calculated using theformula of Ruff et al. (1997), which is based onMartin (1981), and using the calculation for esti-mating brain mass from endocranial volume of Ruffet al. (1997), based on Martin (1990). A list ofendocranial volumes used here is available fromthe authors upon request; mean body mass estimatesare from Skinner and Wood (in press). For moreinformation, see Section 4.18.2.5.1.

4.18.2.6.1.(ii) Left occipital right frontal (LORF)petalia This asymmetrical pattern, with a widerand more posteriorly protruding left occipital pole,and a wider right frontal lobe, is typical of modernhumans, and is statistically significantly related toright-handedness; that is, left-handed and ambidex-trous people are more likely to be symmetrical orhave the opposite pattern (Le May, 1976). Althoughpetalias are also common in great apes (Le May,1976; Le May et al., 1982), they are less frequentthan in humans and rarely involve both the frontaland the occipital lobes (Holloway and de Lacoste-Lareymondie, 1982).

4.18.2.6.1.(iii) Orbital surface of frontal lobe Theorbital surface of the frontal lobe is blunt andexpanded in modern humans. In contrast, it is beakedand pointed in African apes. This region correspondsto cytoarchitectural area 10, which is involved in plan-ning future actions, abstract thinking, and undertakinginitiatives (Semendeferi et al., 2001). A regression ofnonhuman primate area-10 volumes against brainvolumes shows that humans have a larger thanexpected area-10 volume, but the residual (6%) isless striking than for other regions (Holloway, 2002).

4.18.2.6.1.(iv) Fronto-orbital sulcus The fronto-orbital (or orbitofrontal) sulcus typically incisesthe orbitolateral border of the frontal lobe ofAfrican apes, but is rarely present on modernhuman brains (Falk, 1980b). Due to the opercular


expansion of the frontal lobe in humans, this sulcushas probably been shifted so far posteriorly that itnow comprises the anterior limiting sulcus of theinsula, giving modern human brains a distinctlyshaped lateral edge of the frontal lobe (Connolly,1950, p. 330). The human frontal lobe (Semendeferiet al., 1997; Semendeferi and Damasio, 2000) andits cortex (Semendeferi et al., 2002) have volumesexpected for an ape of similar brain size. It has beensuggested that the human prefrontal cortex is largerthan expected for a primate with a similar sizedbrain (Deacon, 1997), and that it has a higher thanexpected white/gray matter ratio (Schoenemannet al., 2005), but these inferences are not reliable(Semendeferi et al., 2002; Sherwood et al., 2005).Note, however, that even if the frontal lobe didnot become relatively larger, it is still possible forthe prefrontal cortex to become relatively largerwithin it.

4.18.2.6.1.(v) Broca’s cap region Broca’s cap asseen on endocasts represents portions of Brodmannareas 47 and 45 (Broadfield et al., 2001). Broca’scap overlaps with (but does not exactly correspondto) Broca’s language area. Broca’s area correspondsto the Brodmann cytoarchitectural areas 45 and 44(respectively, ‘pars triangularis’ and ‘pars opercu-laris’ of the inferior frontal gyrus) (Aboitiz andGarcia, 1997). In the majority of modern humans,the left hemisphere is dominant for language (seeThe Evolution of Language Systems in the HumanBrain), and Broca’s region on the left hemisphere isasymmetrically enlarged in comparison to the con-tralateral areas 45 and 44 (Amunts et al., 1999).Although an enlarged Broca’s cap is a characteristicof modern humans, it does occur, albeit more rarely,in apes (Holloway, 1996). Questions persist aboutwhether the African ape Broca’s area homologueexhibits modern humanlike asymmetry (Holloway,1996; Cantalupo and Hopkins, 2001; Sherwoodet al., 2003). Investigators have drawn attention tomodern humanlike Broca’s cap asymmetry in fossilhominin endocasts, in particular to those specimensin which the left side is larger than its homologue onthe right. They also describe overall size and con-volutional detail, particularly in fossils where onlyone hemisphere is present. Because an asymmetry inwhich the left Broca’s area is larger than the right(L > R) is related to right-handedness is a charac-teristic of most modern humans, attention is drawnto cases in which Broca’s area L > R asymmetriesare found along with LORF L > R asymmetries.

4.18.2.6.1.(vi) Temporal poles Modern humanendocasts have anteriorly expanded, laterally

pointed temporal poles (Falk et al., 2005), in con-trast to African apes, which have rounded temporalpoles. In modern humans, the anterior lateral tem-poral pole, particularly in the left hemisphere, isinvolved in human face recognition and naming(Damasio et al., 1996; Grabowski et al., 2001).The corresponding monkey area, TG, also functionsin visual learning and recognition (Horel et al.,1984; Nakamura and Kubota, 1995).

4.18.2.6.1.(vii) Lunate sulcus4.18.2.6.1.(vii).(a) Primary visual cortex reductionThe lunate sulcus (LS) is within the secondary visualarea, close to the anterior border of the primaryvisual cortex. Modern humans have a more poster-iorly located primary visual cortex than do the greatapes. Most modern human brains lack an LS, butwhen present it is situated more posteriorly than itis in the great apes. A regression of occipital lobevolumes against mean brain volumes from smallsamples of diverse primate species suggests that mod-ern humans have substantially less (�121%) primaryvisual cortex than expected for a nonhuman primateof similar brain size (Holloway, 1992). Althoughchimpanzees typically have a relatively larger pri-mary visual cortex than do modern humans, aminority of chimpanzees show repositioning of theLS to a more modern humanlike posterior position(Holloway et al., 2003). Holloway et al. (2003) usedthis point to argue that the hypothetical panin–homi-nin common ancestor must also have had within itspopulation individuals with reduced primary visualcortices, so you would expect this condition in earlyhominins such as Australopithecus afarensis. The LSmay be unique among the cortical sulci visible onendocasts in that it might provide informationabout the proportion of cortex allocated to distinctfunctional categories, and provides an estimate of theaforementioned ratio of association to sensory cortex(Holloway, 1966, 1968).

4.18.2.6.1.(vii).(b) Parietal expansion The poster-ior location of the LS indicates relative reduction ofthe primary visual cortex and relative expansion ofthe posterior parietal association cortex. The poster-ior parietal lobe is concerned with several aspects ofsensory processing and sensorimotor integration(Lynch, 1980; Hyvarinen, 1981). The superior par-ietal lobule subcomponent is involved in visuomotortasks, including finger movements (Shibata andIoannides, 2001). The inferior parietal lobule sub-component is involved in language and calculationabilities, and it is greatly expanded in humans com-pared to monkeys (Simon et al., 2002). Derivedmodern human behaviors involving the posterior


parietal lobe include enhanced social behavior,including communication, tool-making, and tooluse (Holloway et al., 2004a). Bruner et al. (2003)suggested that the unique globular shape of the neu-rocranium of H. sapiens is related to an additionalexpansion of the parietal lobe in modern humans.Bruner (2004) associated the manufacture of moresophisticated tools and refined language ability withthis difference.

4.18.2.6.1.(viii) Posterior cranial fossa A cerebel-lar quotient (CQ ¼ actual/predicted value) wasobtained when recent modern human cerebellarvolume (determined from posterior cranial fossavolume) was regressed against brain volume (deter-mined from endocranial capacity) minus cerebellarvolume (Weaver, 2001, 2005). Extant hominoidbrain data suggest that the modern human cerebel-lum is smaller than would be expected for an ape ofsimilar brain size (Rilling and Insel, 1998;Semendeferi and Damasio, 2000). The differencebetween modern human and great ape relative cer-ebellar volumes is statistically significant, althoughless dramatic when considered along with the rangeof inferred relative cerebellar volumes found withinthe hominin fossil record (Weaver, 2005). The cer-ebellum of modern humans is relatively larger thanthat of some earlier hominins, perhaps because itssize is linked to the complexity of cognitive func-tions (Weaver, 2005).

4.18.2.6.1.(ix) Thoracic vertebral canal Differencesin thoracic vertebral canal size between humans andnonhuman primates have been related to uniqueaspects of breathing in human speech (MacLarnon,1993). The thoracic part of the vertebral canal and thespinal cord segments which it encases (in modernhumans, T2–S2) are enlarged in modern humans com-pared with nonhuman primates. It is inferred that thisdifference is due to an increase in the size of theanterior horns of the spinal cord and of nerves stem-ming from the segments which innervate the mid orlower trunk region. Some of these nerves innervateintercostal muscles and a set of abdominal musclesthat are responsible for the fine control of breathingin modern human speech (Campbell, 1968, 1974;Gould and Okamura, 1974). Modern human speechinvolves long, punctuated, and modulated utterances(Draper et al., 1959; Campbell, 1968; Hixon andWeismer, 1995), which require respiratory controlmechanisms far beyond those necessary for nonhu-man primate vocalizations. For example, it appearsthat in modern human speech the exhalatory portionof the breathing cycle is extended (Borden and Harris,1984); this is in contrast to primate vocalizations,

which drop in pitch during their duration(MacLarnon and Hewitt, 1999, 2004). MacLarnonand Hewitt (1999) explored several alternate hypoth-eses for increased thoracic vertebral canal size inhumans, including postural control for bipedalism,endurance running, and parturition, but found thatnone were congruent with the fossil and neurologicalevidence.

4.18.2.6.2 Other endocranial morphology Endo-casts preserve information about cranial venoussinuses and meningeal arteries. These may havetaxonomic significance, although there is no evi-dence that their morphology is related to brainfunction (Holloway et al., 2004a).

4.18.2.6.2.(i) Cranial venous sinuses Modernhumans, apes and most hominins have a dominanttransverse-sigmoid cranial venous sinus system. Incontrast, a subgroup of hominin taxa have a domi-nant occipital/marginal (O/M) sinus system; that is,the occipital and marginal sinus complex isenlarged, and the transverse and sigmoid sinus com-plex is reduced (Falk and Conroy, 1983). Thefunctional relevance of variations in the cranialvenous sinus system is not clear. The radiatorhypothesis (see Constraints on Brain Size: TheRadiator Hypothesis) interprets the cranial blooddrainage specializations of hominin taxa as an epi-genetic adaptation to bipedalism (Falk, 1986,1990). These specializations include an enlargedO/M sinus system, multiple hypoglossal canals,and augmented emissary vein foramina. Africanapes have none of these anatomical features, exceptmultiple hypoglossal canals. Within the homininclade, different combinations of these traits occur.Both Au. afarensis and Paranthropus (P. boisei andP. robustus) have high frequencies of an enlargedO/M sinus system, and the latter has high frequen-cies of posterior condyloid foramina and multiplehypoglossal canals, but low frequencies of mastoidand parietal foramina. There is a trend in the homi-nin clade toward the modern human condition (e.g.,an increase in the number of mastoid and parietalforamina in H. erectus and later Homo), and adecrease in the frequencies of an O/M venous sinussystem (in Au. africanus and Homo). Multiple hypo-glossal canals are found in Pan and generally withinthe hominin clade. Braga and Boesch (1997a) inves-tigated the incidence of these venous channels inAfrican apes and hominins. They did not find sta-tistically significant differences betweenParanthropus and African apes with respect tothe frequency of condylar canals, nor did theyfind statistically significant differences between


Paranthropus, Australopithecus, and African apeswith respect to the frequency of divided hypoglossalcanals, mastoid canals, and parietal and occipitalforamina. Further, they suggest that, if differencesdid exist, these would probably be due to differencesin brain size between African apes and hominins.The statistical arguments are set out in subsequentpapers (Braga and Boesch, 1997b; Falk and Gage,1997).

4.18.2.6.2.(ii) Meningeal arteries Descriptions ofmeningeal vessels are confused by the fact thatseveral descriptive systems have been used to cate-gorize the patterns of these vessels, and homologiesbetween the vascular systems of different species areuncertain (see Falk, 1993; Grimaud-Herve, 1997;Holloway et al., 2004a). Meningeal vessels aremeningeal arteries and veins that supply blood tothe neurocranium and also to the dura mater(Holloway et al., 2004a). Of the three componentsof the meningeal arterial system (anterior, middle,and cerebellar), the middle has undergone thegreatest change in hominin evolution (Falk,1993; Grimaud-Herve, 1994; Holloway et al.,2004a). In modern humans, the middle meningealartery is divided into an anterior (bregmatic) branchwhich primarily supplies the frontal region, and aposterior (lambdatic) branch which primarily sup-plies the parietal region (Netter, 1997). In addition,there is an obelic (middle) branch, which varies inits relationship to the other two branches, andwhich serves as the basis for Adachi’s (1928) sim-plistic classification of human meningeal arteryconfigurations. This system has influenced paleoan-thropologists, but it is not applicable to nonhumantaxa because it assumes that meningeal arteriesenter the middle cranial fossa through its floor,which is the case for nearly all modern humans. Inthe great apes some or all of the meningeal arteriesmay enter through the back of the orbit (Falk,1993).

4.18.3 The Hominin Fossil Record

4.18.3.1 Defining Hominins

Molecular biology has revolutionized our knowl-edge of the relationships within the great ape cladeof the Tree of Life. Relationships between organ-isms can now be pursued at the level of the genomeinstead of having to rely on morphology (traditionalhard- and/or soft-tissue anatomy, or the morphol-ogy of proteins) for information about relatedness.Comparisons of the DNA of organisms have beenmade using two methods. In DNA hybridization, all

the DNA is compared, but at a relatively crude level.In DNA sequencing, the base sequences of compar-able sections of DNA are determined and thencompared. The results of hybridization (e.g.,Caccone and Powell, 1989) and sequencing studiesof both nuclear and mtDNA (e.g., Bailey et al.,1992; Horai et al., 1992; Gagneux and Varki,2001; Wildman et al., 2002, 2003) are virtuallyunanimous in suggesting that modern humans andthe African apes are more closely related to eachother than any of them is to the orangutan. Theyalso suggest that modern humans and modern chim-panzees, i.e., commom chimpanzees and bonobos,both (belonging to the genus Pan) are more closelyrelated to each other than either is to the gorilla(Miyamoto et al., 1987; Sibley and Ahlquist, 1987;Goodman et al., 1990, 1998; Goodman, 1999;Salem et al., 2003; Wildman et al., 2003; Ruvolo,2004; but see Ruano et al., 1992; Deinard and Kidd,1999; Barbulescu et al., 2001). Phylogenetic analy-sis of genome-wide gene expression profiles of theanterior cingulate cortex (ACC) also supports theserelationships (Uddin et al., 2004).

Thus, if we accept that the hominin twig of theTree of Life may extend back in time toc. 8 Mya, and that the earliest unambiguoushominin is probably Au. anamensis (see below),then between 8 and 4 Mya we would expect tofind primitive hominin and primitive panin taxa,and close to 8 Mya we should expect to seeevidence of the common ancestor of panins andhominins. Not all of these primitive taxa, be theyhominins, panins, or members of another clade,are direct ancestors of modern humans and chim-panzees. Some will belong to extinct panin andhominin subclades and it is also possible therewere major clades for which we have no livingrepresentative.

4.18.3.2 Terminology

Paleoanthropologists have differed, and still do dif-fer, in the way they classify the higher primates. Wehave tried to avoid using technical terms, but someare necessary in order to understand the implica-tions of the different classifications. Linneantaxonomic categories immediately above the levelof the genus (i.e., the family, the subfamily, and thetribe) have vernacular equivalents that end in ‘id’,‘ine’, and ‘in’, respectively. In the past, H. sapienshas been considered to be distinct enough to beplaced in its own family, the Hominidae, with theother great apes grouped together in a separatefamily, the Pongidae. Thus, modern humans andtheir close fossil relatives were referred to as


‘hominids’, and the other great apes and their closefossil relatives were referred to as ‘pongids’(Table 1).

However, this scheme is inconsistent with theoverwhelming evidence that modern humans andchimpanzees are more closely related to each otherthan either is to the gorilla or to the orangutan.Some researchers advocate combining modernhumans and chimps in the same genus (e.g.,Wildman et al., 2003), which, according to therules of zoological nomenclature, must be Homo.We adopt a less radical solution. The taxonomy weprefer lumps all the great apes including humansinto a single family, the Hominidae (Table 1), andrecognizes three subfamilies within the Hominidae:

Table 1 A traditional taxonomy and a modern taxonomy that

take account of the molecular and genetic evidence that chim-

panzees are more closely related to modern humans than they

are to gorillas. Extinct taxa are given in bold type

Traditional taxonomy

Superfamily Hominoidea (hominoids)

Family Hylobatidae (hylobatids)

Genus Hylobates

Family Pongidae (pongids)

Genus Pongo

Genus Gorilla

Genus Pan

Family Hominidae (hominids)

Subfamily Australopithecinae (australopithecines)

Genus Ardipithecus

Genus Australopithecus

Genus Kenyanthropus

Genus Orrorin

Genus Paranthropus

Genus Sahelanthropus

Subfamily Homininae (hominines)

Genus Homo

Modern taxonomy

Superfamily Hominoidea (hominoids)

Family Hylobatidae (hylobatids)

Genus Hylobates

Family Hominidae (hominids)

Subfamily Ponginae

Genus Pongo (pongines)

Subfamily Gorillinae

Genus Gorilla (gorillines)

Subfamily Homininae (hominines)

Tribe Panini

Genus Pan (panins)

Tribe Hominini (hominins)

Subtribe Australopithecina (australopiths)

Genus Ardipithecus

Genus Australopithecus

Genus Kenyanthropus

Genus Orrorin

Genus Paranthropus

Genus Sahelanthropus

Subtribe Hominina (hominans)

Genus Homo

Ponginae for the orangutans, Gorillinae for the gor-illas, and Homininae for modern humans andchimpanzees. The latter subfamily is broken downinto two tribes: Panini (or panins) for chimpanzees,and Hominini (or hominins) for modern humans.The latter is further broken down into two sub-tribes: one, Australopithecina, which includes onlyextinct hominin genera; and the other, Hominina,for the genus Homo, which includes the only livinghominin taxon, H. sapiens. Thus, modern humansare hominids (family), hominines (subfamily), andthen hominins (tribe). Modern humans and all thefossil taxa judged to be more closely related to mod-ern humans than to chimpanzees are calledhominins; the chimpanzee equivalent is panin. Weuse ‘australopith’ when we refer to taxa belongingto the subtribe Australopithecina.

4.18.3.3 Organizing the Hominin Fossil Record

The classification of the hominin fossil evidence is acontroversial topic. Some researchers favor recog-nizing relatively few taxa, whereas others think thatmore species and genera are needed to accommo-date the observed morphological diversity. We use arelatively speciose (or splitting) taxonomy, but wealso provide an example of a less-speciose (or lump-ing) taxonomy so that readers can appreciate howthe evidence for human evolution would look ifinterpreted in a different way. The taxa included inthe two taxonomies are listed in Table 2. Some ofthe taxon names are used in different senses in thespeciose and less-speciose taxonomies. When werefer in the text to the hypodigm (the fossil evidencereferred to that taxon) of one of these taxa in thespeciose taxonomy we generally use the less-inclu-sive interpretation of the taxon, sensu stricto (s.s.).To save space we omit the sensu stricto if we are notmaking a particular distinction between members ofthe taxon sensu lato and members of the taxon sensustricto (e.g., Au. afarensis means Au. afarensis, s.s.).When we refer to the same taxon in the more inclu-sive taxonomy (i.e., the hypodigm is larger), theLinnean binomial is followed by sensu lato (e.g.,Au. afarensis sensu lato or Au. afarensis s.l.). Thisindicates that we are using the taxon name in a‘looser’ sense. Table 2 demonstrates how theless-speciose taxonomy maps onto the more-speciose one.

The temporal spans of the taxa in the speciosetaxonomy are illustrated in Figure 1. The age ofthe first and last appearances of any taxon in thefossil record (called the first-appearance datum, orFAD, and last-appearance datum or LAD) almostcertainly underestimate the temporal range of the

Table 2 Speciose (splitter) and less-speciose (lumper) hominin taxonomies and skeletal representation of the taxa in the speciose

taxonomy

Speciose taxonomy Age (Mya) Type specimen Crania Dentition Axial Upper limb Lower limb

S. tchadensis 7.0–6.0 TM 266-01-060-1 X X

O. tugenensis 6.0 BAR 1000’00 X X X

Ar. kadabba 5.8–5.2 ALA-VP-2/10 X X X X

Ar. ramidus s.s. 4.5–4.4 ARA-VP-6/1 X X X ff

Au. anamensis 4.2–3.9 KNM-KP 29281 ff X X X

Au. afarensis s.s. 3.9–3.0 LH 4 X X X X X

K. platyops 3.5–3.3 KNM-WT 40000 X X

Au. bahrelghazali 3.5–3.0 KT 12/H1 X

Au. africanus 3.0–2.4 Taung 1 X X X X X

Au. garhi 2.5 BOU-VP-12/130 X X ? ?

P. aethiopicus 2.5–2.3 Omo 18.18 X X

P. boisei s.s. 2.3–1.3 OH 5 X X ? ?

P. robustus 2.0–1.5 TM 1517 X X X X

H. habilis s.s. 2.4–1.6 OH 7 X X X X X

H. rudolfensis 1.8–1.6 KNM-ER 1470 X X ?

H. ergaster 1.9–1.5 KNM-ER 992 X X X X X

H. erectus s.s. 1.8–0.2 Trinil 2 X X ? ? X

H. antecessor 0.7–0.5 ATD6-5 X X

H. heidelbergensis 0.6–0.1 Mauer 1 X X X

H. neanderthalensis 0.2–0.03 Neanderthal 1 X X X X X

H. sapiens s.s. 0.19–present None designated X X X X X

H. floresiensis 0.090–0.012 Liang Bua 1 X X X X X

Less-speciose taxonomy Age (Mya) Taxa included from long taxonomy

Ar. ramidus s.l. 7.0–4.4 Ar. ramidus s.s., Ar. kadabba, S. tchadensis, O. tugenensis

Au. afarensis s.l. 4.5–3.0 Au. afarensis s.s., Au. anamensis, Au. bahrelghazali, K. platyops

Au. africanus 3.0–2.4 Au. africanus

P. boisei s.l. 2.5–1.3 P. boisei s.s., P. aethiopicus, Au. garhi

P. robustus 2.0–1.5 P. robustus

H. habilis s.l. 2.4–1.6 H. habilis s.s., H. rudolfensis

H. erectus s.l. 1.9–0.2 H. erectus s.s., H. ergaster

H. sapiens s.l. 0.7–present H. sapiens s.s., H. antecessor, H. heidelbergensis, H. neanderthalensis

H. floresiensis 0.090–0.012 H. floresiensis

Skeletal representation key: X, present; ff, fragmentary specimens; ?, taxonomic affiliation of fossil specimen(s) uncertain.


taxa. Nonetheless, FADs and LADs provide anapproximate temporal sequence for the hominintaxa. The heights of the columns of those taxawith good, well-dated, fossil records (e.g., Au. afar-ensis and P. boisei) are a reasonable estimate of thetemporal range of those taxa, but the heights ofother columns marked with an asterisk (e.g.,S. tchadensis and Au. bahrelghazali) reflect uncer-tainties about the age of the taxon because either thesample size is too small, or because the estimates oftemporal range are not reliable.

For various reasons it is very unlikely that we havea complete record of hominin taxonomic diversity,particularly in the pre-4-Mya phase of hominin evo-lution. This is because intensive explorations ofsediments of this age have been conducted for lessthan a decade, and because these investigations havebeen restricted in their geographical scope. Thus, thefossil evidence we are working with in the early phase

of hominin evolution is almost certainly incomplete.More taxa are likely to be identified. We should bearthis in mind when formulating and testing hypothesesabout any aspect of hominin evolution, especially theevolution of bipedalism. We have not used lines toconnect the taxa because the constraints of existingknowledge suggest that there are only two relativelywell-supported subclades within the hominin clade,one for Paranthropus taxa, and the other for post-H. ergaster taxa belonging to the Homo clade.Without more well-supported subclades it is prob-ably unwise to try to identify specific taxa asancestors or descendants of other taxa.

4.18.3.4 Review of Individual Hominin Fossil Taxa

Each hominin taxon is placed in one of six informalgrades (Huxley, 1958) based on a combination ofbrain and postcanine tooth size and on inferred

K. platyops *4

3

2

1

0

Ar. ramidusAu.anamensis *

Au. afarensis

Au.bahrelghazali * Au. africanus *

P. aethiopicus *

P. robustusP. boisei

H. habilis

H. rudolfensis

H. ergaster

H. erectus

H. antecessor *

Au. garhi *

6

5

7

8

O. tugenensis *

H. heidelbergensis *

H. neanderthalensis

H. sapiens

S. tchadensis *

Ar. kadabba *

Mya

H. floresiensis *

Anatomically modern Homo

Premodern Homo

Megadont archaic hominins

Archaic hominins

Possible and probable early hominins

Transitional hominins

Figure 1 Speciose hominin taxonomy.


locomotor mode. The six grades are: possible andprobable primitive hominins (PH); archaic hominins(AH); megadont archaic hominins (MAH); transi-tional hominins (TH); premodern Homo (PMH);and anatomically modern Homo (AMH)(Figure 1). Several taxon samples are too small todo other than make an informed guess about thegrade of the taxon. Within each grouping, the taxaare listed in order of their first appearance in thefossil record.

Unless homoplasy (shared morphology not derivedfrom the most recent common ancestor) is morecommon than we anticipate, there is little doubtthat recent hominin taxa (i.e., post-H. ergaster taxain group PMH) are more closely related to modernhumans than to chimpanzees. These taxa all haveabsolutely and relatively large brains, they were obli-gate bipeds, and they have small canines, slenderjaws, and small chewing teeth. However, the closerwe get to the split between hominins and panins themore difficult it is to find features we can be surefossil hominins possessed and fossil panins, or taxa inany other closely related clade, did not. In theearly stages of hominin evolution it may be eitherthe lack of panin features or relatively subtle differ-ences in the size and shape of the canines, or in thedetailed morphology of the limbs, that mark outhominins.

We are conscious that many readers might beunfamiliar with the details of the hominin fossil

record, so we provide basic information about themorphology of each taxon. The formal way to cite ataxon name is to give the Linnean binomial,followed by the name(s) of the authors and thedate of the paper that introduced the taxon.Conventionally, this citation is not placed in par-entheses. However, when a taxon has been movedfrom its initial genus, the original reference is placedwithin parentheses followed by the revising refer-ence: for example, Homo erectus (Dubois, 1892)Weidenreich, 1940. Further details about mostof the taxa and a more extensive bibliography canbe found in Wood and Richmond (2000). Recentrelevant reviews of most of these taxa can be foundin Hartwig (2002) and Wood and Constantino(2004).

4.18.4 Review of Hominin Taxa

4.18.4.1 Possible and Probable PrimitiveHominins

This category includes one species, Ardipithecusramidus, which is almost certainly a member of thehominin clade, one species, Sahelanthropus tcha-densis, which is a possible hominin, and twospecies, Ardipithecus kadabba and Orrorin tugen-ensis, which may be hominins.

Taxon name. Sahelanthropus tchadensis Brunetet al., 2002.


Temporal range. c. 7–6 Mya.Initial discovery. TM 266-01-060-1 – an adult

cranium; Toros-Menalla, Chad, 2001 (Brunetet al., 2002).

Type specimen. As above.Source(s) of the evidence. Toros-Menalla, Chad,

Central Africa.Nature of the evidence. A distorted cranium,

although an attempt to correct the distortion hasbeen made in a virtual reconstruction (Zollikoferet al., 2005), plus several mandibles and someteeth.

Characteristics and inferred behavior. Cranial: Achimp-sized animal displaying a novel combinationof primitive and derived features. Much about thebase and vault of the cranium is chimp-like, but therelatively anterior placement of the foramen mag-num, the presence of a supraorbital torus, the lackof a muzzle, the small, apically worn canines, thelow, rounded molar cusps, the relatively thick toothenamel, and the relatively thick mandibular corpus(Brunet et al., 2002) suggest that S. tchadensis doesnot belong in the Pan clade. Postcranial: No evi-dence. Conclusion: It is either a primitive hominin,the common ancestor of hominins and panins, or itbelongs to a separate clade of hominin-like apes.

CNS-related fossil evidence. The endocranialvolume is estimated to be between 350 and370 cm3, the smallest of any adult hominin, andwithin the range of extant chimpanzees.

Taxon name. Orrorin tugenensis Senut et al.,2001.

Temporal range. c. 6.0 Mya.Initial discovery. KNM LU 335– left mandibular

molar tooth crown; Tugen Hills, Baringo, Kenya,1974 (Pickford, 1975).

Type specimen. BAR 1000’00 – fragmentarymandible; Tugen Hills, Baringo, Kenya, 2000(Senut et al., 2001).

Source(s) of the evidence. The relevant remainscome from four localities in the Lukeino Formation,Tugen Hills, Kenya.

Nature of the evidence. The 13 specimens includethree femoral fragments.

Characteristics and inferred behavior. Cranial:The discoverers admit that much of the critical den-tal morphology is ‘‘ape-like’’ (Senut et al., 2001,p. 6). Postcranial: The femoral morphology hasbeen interpreted (Pickford et al., 2002; Galik et al.,2004) as suggesting that O. tugenensis is an obligatebiped, but some researchers interpret the radio-graphs and CT scans of the femoral neck asindicating a mix of bipedal and nonbipedal locomo-tion. Conclusion: O. tugenensis could prove to be a

hominin, but it is more likely that it belongs toanother part of the adaptive radiation that includedthe common ancestor of panins and hominins.

CNS-related fossil evidence. None.

Taxon name. Ardipithecus kadabba Haile-Selassie et al., 2004.

Temporal range. 5.8–5.2 Mya.Initial discovery. ALA-VP-2/10 – partial mand-

ible; Alayla, Western Margin, Middle Awash,Ethiopia, 1997.

Type specimen. As above.Source(s) of the evidence. Middle Awash and

Gona, Ethiopia.Nature of the evidence. Mandible, teeth, and

postcranial evidence.Characteristics and inferred behavior. Cranial:

The upper canine and lower first premolar morphol-ogy is less ape-like than that of O. tugenensis, butmore ape-like than that of Ar. ramidus. Theresearchers who found it suggest that it closelyapproaches the extant and fossil ape condition(Haile-Selassie et al., 2004, p. 1505); they also sug-gest that the morphology of the canine–premolarcomplex of S. tchadensis, O. tugenensis, andAr. kadabba is so similar that they may belong toone genus, or even one species (Haile-Selassie et al.,2004). Postcranial: Ar. kadabba has been suggestedto be a biped on the basis that the shape of theproximal articular surface of the fourth proximalphalanx of the foot resembles that of Au. afarensis,but similar morphology may also be found in thequadrupedal African apes. Conclusion: Ar. kadabbais probably a member of an extinct clade closelyrelated to hominins and panins.


Taxon name. Ardipithecus ramidus (White et al.,1994) White et al., 1995.

Temporal range. c. 4.5–4.4 Mya.Initial discovery. ARA-VP-1/1 – right M3;

Aramis, Middle Awash, Ethiopia, 1993 (Whiteet al., 1994). (NB: if a mandible, KNM-LT 329,from Lothagam, Kenya, proves to belong to thehypodigm, then this would be the initial discovery.)

Type specimen. ARA-VP-6/1 – associated upperand lower dentition; Aramis, Middle Awash,Ethiopia, 1993 (White et al., 1994).

Source(s) of the evidence. A site called Aramisin the Middle Awash region of Ethiopia. A secondsuite of fossils, including a mandible, teeth, andpostcranial bones, recovered in 1997 from fivelocalities in the Middle Awash, that range in agefrom >5.7 to 5.2 Mya were initially allocated tothis taxon (Haile-Selassie, 2001), but they were


subsequently transferred to Ar. kadabba (seeabove).

Nature of the evidence. The published evidenceconsists of isolated teeth, a piece of the base of thecranium, and fragments of mandibles and longbones. A fragmented associated skeleton has beenfound and is being prepared and reconstructed.

Characteristics and inferred behavior. Cranial:The remains attributed to Ar. ramidus share somefeatures in common with living species of Pan,others that are shared with the African apes in gen-eral, and, crucially, several dental and cranialfeatures are shared only with later hominins suchas Au. afarensis. Its chewing teeth are relativelysmall, and the thin enamel covering on the teethsuggests that the diet of Ar. ramidus may havebeen closer to that of the chimpanzee than to thatof modern humans. Postcranial: Judging from thesize of the shoulder joint, Ar. ramidus weighedabout 40 kg. The position of the foramen magnumsuggests that the posture and gait of Ar. ramiduswas respectively more upright and bipedal than isthe case in the living apes. Conclusions: The disco-verers initially allocated the new species toAustralopithecus (White et al., 1994), but they sub-sequently assigned it to a new genus, Ardipithecus(White et al., 1995). Of the hominin taxa in thiscategory, Ar. ramidus, is the most likely to be anearly hominin.

CNS-related fossil evidence. A crushed craniumhas been reported, but no details have beenpublished.

4.18.4.2 Archaic Hominins

This group, which includes all the remaining homi-nin taxa not conventionally included in Homo andParanthropus, subsumes two genera, Australo-pithecus and Kenyanthropus. As it is used in thisand many other taxonomies, Australopithecus isalmost certainly not a single clade, but untilresearchers can generate a reliable phylogeny thereis little point in revising its generic terminology.

Taxon name. Australopithecus anamensis Leakeyet al., 1995.

Approximate time range. c. 4.2–3.9 Mya.Initial discovery. KNM-KP 271 – left distalhumerus; Kanapoi, Kenya, 1965 (Patterson andHowells, 1967).

Type specimen. KNM-KP 29281 – an adultmandible with complete dentition and a temporalfragment that probably belongs to the same indivi-dual; Kanapoi, Kenya, 1994.

Source(s) of the evidence. Allia Bay and Kanapoi,Kenya.

Nature of the evidence. The evidence consists ofjaws, teeth, and postcranial elements from the upperand lower limbs.

Characteristics and inferred behavior. Cranial:The main differences between Au. anamensis andAu. afarensis relate to details of the dentition. Insome respects the teeth of Au. anamensis are moreprimitive than those of Au. afarensis (e.g., theasymmetry of the premolar crowns, and the rela-tively simple crowns of the deciduous firstmandibular molars), but in others (e.g., the lowcross-sectional profiles, and bulging sides of themolar crowns) they show similarities toParanthropus (see below). Postcranial: The upperlimb remains are australopith-like, but a tibiaattributed to Au. anamensis has features asso-ciated with obligate bipedality.


Taxon name. Australopithecus afarensisJohanson et al., 1978.

Approximate time range. c. 4–3 Mya.Initial discovery. AL 128-1 – left proximal femur

fragment; Hadar Formation, Afar, Ethiopia, 1973(Johanson and Taieb, 1976).

Type specimen. LH 4 – adult mandible; Laetoli,Tanzania, 1974.

Source(s) of the evidence. Laetoli, Tanzania;White Sands, Hadar, Maka, Belohdelie and Fejej,Ethiopia; Allia Bay, West Turkana, and Tabarin,Kenya.

Nature of the evidence. Au. afarensis is the ear-liest hominin to have a comprehensive fossil recordincluding a well-preserved skull, several crania,many lower jaws, and sufficient limb bones to beable to estimate stature and body mass. The collec-tion includes a specimen, AL-288, that preservesjust less than half of the skeleton of an adult female.

Characteristics and inferred behavior. Cranial:It has incisors that are much smaller than those ofextant chimpanzees, but the premolars and molarsof Au. afarensis are relatively larger than those ofthe chimpanzee. Postcranial: The hind limbs of AL-288 are substantially shorter than those of a mod-ern human of similar stature. The range of bodymass estimates is from 25 to >50 kg. The upperlimb, especially the hand, retains morphology thatmost likely reflects a significant element of arboreallocomotion. The size of the footprints, the length ofthe stride, and stature estimates based on the lengthof the limb bones suggest that the standing heightof adult individuals in this early hominin specieswas between 1.0 and 1.5 m. Direct evidence of the


locomotion of either Au. afarensis or another syn-chronic hominin comes from the 3.6 Mya homininfootprint trails at Site G in the Laetolil Formation,at Laetoli, Tanzania. If we assume that the skeletalevidence from Hadar and the trace fossil evidencefrom Laetoli represents one taxon, and if we weighthe primitive and derived characteristics observed inthe Hadar pedal remains and in the Laetoli foot-prints, the form and function of the Au. afarensislocomotor system was not modern humanlike.

CNS-related fossil evidence. Endocranial:Au. afarensis is represented by at least 15 speci-mens that preserve endocranial anatomy and somefor which endocranial volume can be estimated.The estimated mean adult endocranial volume is446 cm3 (n ¼ 5; range 387–550). The range isinterpreted as reflecting a substantial degree ofsexual dimorphism. The average of the two largestcrania (probable males) is 125 cm3 greater thanthat for the three smallest crania (probablefemales). These values are larger than the averageendocranial volume of a chimpanzee, and if theestimates of the body size of Au. afarensis areapproximately correct then relative to estimatedbody mass the brain of Au. afarensis is substan-tially larger than that of Pan. The sample meanEQ for Au. afarensis is 2.5. Holloway has longargued that the primary visual cortex is relativelyreduced in size in Au. afarensis, as is apparent intwo specimens, AL 162-28 (Holloway, 1983a;Holloway and Kimbel, 1986) and AL 288-1(Holloway et al., 2004a). However, he allowsthat another specimen (AL 333-45) may have aproportionately larger, more ape-like, primaryvisual cortex. Other evidence presented byHolloway et al. for brain organization inAu. afarensis is ambiguous. There may be evidenceof a slight left occipital petalia in one specimen (AL333-45), but a juvenile specimen (AL 333-105)retains the ape pattern of an inferior frontal orbitalsulcus (Holloway et al., 2004a). On the other hand,Falk (1985b) argues that Au. afarensis (particularlyAL 162-28) has an entirely ape-like sulcal patternwith no evidence of a relatively reduced primaryvisual cortex, and with an ape-like condition of acerebellum projecting posteriorly beyond the occipi-tal lobe, a suggestion Holloway and Kimbel (1986)and Holloway et al. (2004a) dismiss as a misinter-pretation due to the way the fossil was oriented.Vertebral canal: This species is represented by foursets of vertebras. The most complete set of verte-bras includes 15 vertebral elements belonging to AL288-1, of which the thoracic vertebras have beenused to make inferences about the spinal cord. Au.afarensis retains small (relative to modern human)

thoracic vertebral canals in cross-sectional area,suggesting a small thoracic spinal cord, and byinference a lack of fine control of breathing forspeech, and thus the lack of a complex vocal lan-guage ability (MacLarnon and Hewitt, 1999).Behavioral interpretations: Both Holloway andFalk recognize that the brain of Au. afarensisshows some degree of reorganization toward themodern human condition. However, a point ofcontention between these authors has been the rela-tive location of the LS, and the coincident reductionof the primary visual cortex and expansion of theparietal association cortex cortex. Some Au. afar-ensis brains have a posteriorly placed LS, but somechimpanzee brains also have a posteriorly placed LS(Figure 2b) (Holloway et al., 2003). Holloway et al.(2003) argue that the hypothetical panin–hominincommon ancestor must also have had within itspopulation individuals with reduced primary visualcortices, so you would expect this condition in earlyhominins such as Au. afarensis.

Other endocranial morphology. Cranial venoussinuses: Eight Au. afarensis from Hadar (AL 333-45, Al 333-105, AL 333-114, AL 333-116, AL 162-28, AL 444-2, AL 288-1, and AL 439-1) have anenlarged, and thus presumably dominant, occipitalmarginal sinus system (Kimbel et al., 2004; Falket al., 1995). However, LH 21, and probably AL224-9 and AL 427-1b, lack an enlarged occipitalmarginal sinus system. Meningeal vessels: Present,but not diagnostic.

Taxon name. Kenyanthropus platyops Leakeyet al., 2001.

Approximate time range. c. 3.5–3.3 Mya.Initial discovery. KNM-WT 38350 – left maxilla

fragment; Lomekwi, West Turkana, Kenya, 1998(Leakey et al., 2001).

Type specimen. KNM-WT 40000 – a relativelycomplete cranium but it is criss-crossed by matrix-filled cracks; Lomekwi, West Turkana, Kenya, 1999(Leakey et al., 2001).

Source(s) of the evidence. West Turkana, andperhaps Allia Bay, Kenya.

Nature of the evidence. The initial report lists thetype cranium and the paratype maxilla plus 34 spe-cimens – including three mandible fragments, amaxilla fragment, and isolated teeth – some ofwhich may also belong to the hypodigm, but atthis stage the researchers are reserving their judg-ment about the taxonomy of many of these remains(Leakey et al., 2001). Some of them have onlyrecently been referred to Au. afarensis (Brownet al., 2001).

Parallel sulcus(a) (b)

(d)

Lunate sulcus

(c)

(e)Snd

mmv

si

oci

L

lb

pf

Lunate sulcus

Occipital pole(OP)

Temporal lobe

Cerebellum

Reconstruction(Plasticene)

Lunate sulcus

Midsugittalplane (Approx.)

Figure 2 a, Left lateral view of a typical chimpanzee brain cast showing relatively anterior position of the LS (Holloway et al.,

2004b). b, Left lateral view of unusual chimpanzee brain with the LS in a more posterior position (� indicates lateral calcarine fissure)

(Holloway et al., 2003). c, Right lateral view of a natural endocast and sketch of juvenile Au. africanus (Taung) (Dart, 1925). d, Left

oblique view of Au. africanus (Stw 505) partially reconstructed endocast showing the location of the LS (Holloway et al., 2004b).

e, Left lateral view of virtual endocast and sketch of H. floresiensis (LB1) showing the location of the LS (Falk et al., 2005). Images are

not shown to the same scale. a and d, Reproduced from Holloway, R. L., Clarke, R. J., and Tobias, P. V. 2004b. Posterior lunate

sulcus in Australopithecus africanus: Was Dart right? C. R. Palevol. 3, 287–293, Elsevier. b, Reproduced from Morphology and

histology of chimpanzee primary visual striate cortex indicate that brain reorganization predated brain expansion in early hominid

evolution, Anat. Rec.; Holloway, R. L., Broadfield, D. C., and Yuan, M. S.; Copyright ª 2003, Wiley-Liss. Reprinted with permission of

Wiley-Liss, Inc., a subsidiary of John Wiley & Sons, Inc. c, Reproduced from Dart, R. A. 1925. Australopithecus africanus: The man-

ape of South Africa. Nature 115, 195–199, with permission from Nature Publishing Group. e, Reprinted with permission from Falk, D.,

Hildebolt, C., Smith, K., et al. 2005. The brain of LB1, Homo floresiensis. Science 308, 242–245. Copyright 2005 AAAS.


Characteristics and inferred behavior. Cranial:The main reasons why Leakey et al. (2001) didnot assign this material to Au. afarensis are itsreduced subnasal prognathism, anteriorly situatedzygomatic root, flat and vertically orientatedmalar region, relatively small but thick-enameledmolars, and the unusually small M1 compared tothe size of the P4 and M3. Some of the morphol-ogy of the new genus, including the shape of theface, is Paranthropus-like, yet it lacks the postca-nine megadontia that characterizes Paranthropus.Postcranial: No evidence. Conclusion: The authorsnote that the face of the new material resemblesthat of H. rudolfensis (see below), but they rightly

point out that the postcanine teeth of the latterare substantially larger than those of KNM-WT40000. K. platyops apparently displays a hithertounique combination of facial and dental morphol-ogy. Some researchers contend that KNM-WT40000 is an Au. afarensis cranium that is distortedby the matrix-filled cracks.

CNS-related fossil evidence. No estimate of endo-cranial volume is given, although it is apparentlyaustralopith-like in size.

Taxon name. Australopithecus bahrelghazaliBrunet et al., 1996.

Approximate time range. c. 3.5–3.0 Mya.


Initial discovery. KT 12/H1 – anterior portion ofan adult mandible; Koro Toro, Chad, 1995 (Brunetet al., 1996).

Type specimen. As above.Source(s) of the evidence. Koro Toro, Chad.Nature of the evidence. Published evidence is

restricted to a fragment of the mandible and anisolated tooth.

Characteristics and inferred behavior. Cranial: Itsdiscoverers claim that its thicker enamel distin-guishes the Chad remains from Ar. ramidus, andthat its smaller mandibular symphysis and morecomplex mandibular premolar roots distinguish itfrom Au. afarensis. Otherwise, there is too littleevidence to infer any behavior. Postcranial: No evi-dence. Conclusion: This taxon may be a regionalvariant of Au. afarensis.


Taxon name. Australopithecus africanus (Dart,1925).

Approximate time range. c. 3.0�–2.4 Mya. �NB: itremains to be seen whether the associated skeletonStw 573 from Member 2 (Clarke and Tobias, 1995;Clarke, 1998, 1999, 2002) and the 12 hominin fos-sils recovered from the Jacovec Cavern since 1995(Partridge et al., 2003) belong to the Au. africanushypodigm. Samples of quartz grains from Member 2and the Jacovec Cavern have recently been dated toc. 4.2–4.0 Mya using ratios of the 26Al and 10Beradionuclides (Partridge et al., 2003).

Initial discovery. Taung 1 – a juvenile skull withpartial endocast; Taung (formerly Taungs), now inSouth Africa, 1924.

Type specimen. As above.Source(s) of the evidence. Most of the evidence

comes from two caves, Sterkfontein andMakapansgat, with other evidence coming fromcaves at Taung and Gladysvale.

Nature of the evidence. This is one of the best, ifnot the best, fossil record of an early hominin taxon.The cranium, mandible, and dentition are wellsampled. The postcranium and particularly theaxial skeleton is less well represented in the sample,but there is at least one specimen of each of the longbones. However, many of the fossils have beencrushed and deformed by rocks falling onto thebones before they were fully fossilized.

Characteristics and inferred behavior. Cranial:Au. africanus had relatively large chewing teethand apart from the reduced canines the skull isrelatively ape-like. Postcranial: Overall, the post-cranial remains of Au. africanus suggest that thishominin could engage in both arboreal andbipedal locomotion. The Sterkfontein evidence

suggests that males and females of Au. africanusdiffered substantially in body size, but probablynot to the degree they did in Au. afarensis (seeabove). Conclusion: This is a hominin with amixed locomotor mode, part climbing and partbipedal walking.

CNS-related fossil evidence. Endocranial:Au. africanus is represented by at least 15 specimensrepresenting the neurocranium, many of which arenatural endocasts. Au. africanus endocasts areunique among hominin endocasts in that they pre-serve a great deal of convolutional detail (Falk,1987). This species has the most studied (anddebated) endocast morphology of any fossil homi-nin species. The estimated mean adult endocranialvolume for Au. africanus is 460 (n¼ 9; range 428–515). The sample mean EQ for Au. africanus is 2.8.An early claim for reorganization of the cerebralcortex, in the form of a relatively reduced primaryvisual cortex and relatively expanded parietal–occi-pital association areas, was made by Dart (1925) onthe basis of a humanlike posteriorly located LS onthe Taung child endocast (Figure 2c). This observa-tion is the focus of a long-standing debate over theidentification and location of the LS, including sup-port for Dart’s view (Holloway, 1975), one authorarguing for a very posterior position (Schepers,1946), others arguing for an anterior position(Keith, 1931; Le Gros Clark et al., 1936; Falk,1980b, 1985a), and some noting that it is impossibleto know the position with certainty (Le Gros Clark,1947; Holloway, 1985; Tobias, 1991). The debateover the location of the Taung LS developed into alarger debate between Falk and Holloway aboutwhether brain reorganization preceded brain sizeincrease. On the one hand, Holloway (Holloway,1975, 1983a, 1984, 1985, 1988b) and Hollowayet al. (2004a, 2004b) maintain that Taung andother Au. africanus specimens demonstrate aspectsof humanlike brain organization. Holloway doesnot maintain that a particular line clearly representsthe LS, but states that for Taung there is no goodevidence for a LS in a typical anterior pongid posi-tion (Holloway et al., 2004a, p. 97). In addition,Holloway et al. claim that two other specimens (Stw505 and Sterfontein Type 3) also show a relativereduction in primary visual cortex size, based onthe position of the LS (see Figure 2d) (Hollowayet al., 2004a, p. 97). In addition, they find evidenceof a humanlike brain morphology associated withright-handedness. Two specimens (Sts 5 andSterfontein type 2) have Broca’s cap regions whichdemonstrate a trend toward a modern humanlikepattern, and one of these (Sts 5) displays a slightLORF petalia (Holloway et al., 2004a). On the


other hand, Falk (1980b, 1983b, 1985a) maintainsand defends her interpretation of a more anterior,ape-like, position for the LS in Taung and other Au.africanus individuals. In addition, Falk points toother ape-like features of Au. africanus endocasts,most significantly the fronto-orbital sulcus. Falk(1980b) claims that Taung is ape-like in the positionand size of the fronto-orbital sulcus at the lateraledge of frontal lobe (but see Holloway, 1981b). Fiveother Au. africanus endocasts (Sts 60, Type 2, Type3, Sts 58, Sts 1017) are considered to have similarape-like sulcal patterns, although based on muchless evidence (Falk, 1980b). However, Falk et al.(2000) have pointed to derived, modern humanlikeaspects of Au. africanus brain morphology that dif-ferentiate this species from Paranthropus. Theorbital surface of the frontal lobe is blunt andexpanded in Au. africanus (Sts 5, Stw 505, and seealso the more fragmentary Type 2 and Sts 60) just asin H. sapiens (Falk et al., 2000). Anteriorlyexpanded, laterally pointed temporal poles alsocharacterize Au. africanus and H. sapiens to theexclusion of Paranthropus (Falk et al., 2000).Vertebral canal: One set of 15 vertebras (Sts 14)and two individual vertebras (Sts 65, Sts 73) havebeen referred to this species. Au. africanus thoracicvertebral canals have a small cross-sectional arearelative to those of modern humans. Behavioralinterpretations: In the original description of thetype specimen, Dart argued that Au. africanusdemonstrates humanlike brain reorganization onthe basis of the position of the LS. Although Falkdoes not concede the position of the LS, Falk et al.(2000) do agree that in other respects the Au. afri-canus brain has been reorganized relative to Africanape brains. There are several examples showing anearly start to a trend toward modern humanlikecortical reorganization (Falk et al., 2000). Theenlarged orbital surfaces of the frontal lobes inAu. africanus are thought to indicate an expansionof area 10 prior to brain size increase. The anteriorlateral regions of the temporal poles, which show amodern humanlike expansion in Au. africanus, areinvolved in visual learning and recognition. In addi-tion, Au. africanus (Sts 5) is more modernhumanlike than ape-like in the size and shape of itsolfactory bulbs (Falk et al., 2000). In modernhumans, olfactory bulbs are less than half the sizeof those of the apes. Furthermore, the fraction offunctioning olfactory receptor genes is reduced inmodern humans relative to apes (Gilad et al.,2003a), a finding that corroborates behavioraldata that suggest modern humans do not rely ontheir sense of smell as much as apes do. Reductionof olfactory bulb size, and corresponding changes in

the dependence on smell (Gilad et al., 2003b), mayhave arisen early in hominin evolution. Falk et al.(2000) point to shared morphology in Au. africanusand H. sapiens to the exclusion of Paranthropus asevidence of an Au. africanus–Homo lineage, but thisis a highly contested proposal (e.g., Johanson andWhite, 1979). In spite of evidence for brain reorga-nization, there is no very strong evidence for brainmorphology that can be related to language capa-city. Moreover, the small vertebral canals in thethoracic region suggest a lack of fine breathing con-trol, and thus the lack of complex vocal languageability. This conclusion is similar to that forAu. afarensis.

Other endocranial morphology. Cranial venoussinuses: Most researchers who have studied thecranial venous sinuses of Au. africanus suggestthat it retains a symplesiomorphic dominant trans-verse sigmoid sinus and lacks an enlarged O/Msinus (e.g., Sts 5, Sts 19, Sts 26, MLD 1 and MLD37/38) (Tobias and Falk, 1988; Conroy et al.,1990; Falk et al., 1995). Two exceptions areTaung and Stw 187a, which have evidence for adominant O/M sinus system (Tobias and Falk,1988; Kimbel et al., 2004). Falk et al. (1995)argue that this unusual feature contributes to theuncertainty of Taung’s taxonomic affinity.Holloway et al. (2004a) suggest that MLD 1 hasan O/M sinus drainage system. Meningeal vessels:Saban (1983) drew distinctions betweenAustralopithecus (i.e., Au. africanus) andParanthropus (P. boisei and P. robustus) withrespect to the configuration of meningeal vessels,but this interpretation has since been rejected(Falk, 1993; White and Falk, 1999). Saban(1983) showed that two Au. africanus specimens(Sts 60, Taung) have middle meningeal vesselsthat bifurcate into simple anterior and posteriorbranches, with no middle branch, in contrast toParanthropus in which a middle branch is present.

4.18.4.3 Megadont Archaic Hominins

This group includes hominin taxa included in thegenus Paranthropus and one other taxon, Au. garhi.The genus Paranthropus was reintroduced whencladistic analyses suggested that three of the fourspecies in this grade formed a clade. Two genera,Zinjanthropus and Paraustralopithecus, are sub-sumed within the genus Paranthropus.

Taxon name. Paranthropus aethiopicus(Arambourg and Coppens, 1968) Chamberlain andWood, 1985.

Approximate time range. c. 2.5–2.3 Mya.


Initial discovery. Omo 18.18 (or 18.1967.18) – anedentulous adult mandible; Shungura Formation,Omo Region, Ethiopia, 1967.

Type specimen. As above.Source(s) of the evidence. Shungura Formation,

Omo region, Ethiopia; West Turkana, Kenya.Nature of the evidence. The hypodigm includes a

well-preserved cranium from West Turkana (KNM-WT 17000), several mandibles (e.g., KNM-WT16005), and isolated teeth from the ShunguraFormation. No postcranial fossils have beenassigned to this taxon.

Characteristics and inferred behavior. Cranial:Similar to P. boisei (see below) except that the faceis more prognathic, the cranial base is less flexed,the incisors are larger, and the postcanine teeth arenot so large or morphologically specialized. Whenthis taxon was introduced in 1968 it was the onlymegadont hominin in this time range. With the dis-covery of Au. garhi (see below) it is apparent thatrobust mandibles with similar length premolar andmolar tooth rows are being associated with what areclaimed to be two distinct forms of cranialmorphology.

CNS-related fossil evidence. Endocranial: Onealmost complete cranium is the only source of infor-mation about the CNS of P. aethiopicus. Theestimated endocranial volume is 410 cm3 (Walkeret al., 1986). Holloway et al. (2004a) describe a slightLORF petalial pattern, but no claims of humanlikebrain organization have been made. Falk et al. (2000)suggest that this specimen retains aspects of ape-likebrain morphology not found in Au. africanus. Theolfactory bulb of P. aethiopicus is ape-like in size andshape, in contrast to Au. africanus (Falk et al., 2000).P. aethiopicus has an ape-like beak-shaped orbitalsurface of the frontal lobe, in contrast to Au. africa-nus and Homo. The P. aethiopicus temporal lobe isape-like in both size and shape and contrasts with themorphology seen in Au. africanus and Homo, but itshares this trait with other Paranthropus taxa (Falket al., 2000). Holloway (1988a) suggests that thecerebellum of this specimen is chimpanzee-like inthat it is posteriorly protruding and laterally flaring,in contrast to the more modern humanlike tucked-under cerebellum of P. robustus (SK 1585) andP. boisei (OH 5). The ape-like morphology andsmall brain size are consistent with the conclusionthat this species was more ape-like than humanlike interms of its cognition.

Other endocranial morphology. Cranial venoussinuses: The lack of transverse sigmoid sinusgrooves in KNM-WT 17000 is taken (by default)as evidence for an enlarged O/M sinus system inP. aethiopicus (Brown et al., 1993).

Taxon name. Paranthropus boisei (Leakey, 1959)Robinson, 1960.

Approximate time range. c. 2.3–1.3 Mya.Initial discovery. OH 3 – deciduous mandibular

canine and molar; Olduvai Gorge, Tanzania, 1955(Leakey, 1958).

Type specimen. OH 5 – adolescent cranium;Olduvai Gorge, Tanzania, 1959 (Leakey, 1959).

Source(s) of the evidence. Olduvai and Peninj,Tanzania; Omo Shungura Formation and Konso,Ethiopia; Koobi Fora, Chesowanja, and WestTurkana, Kenya; Melema, Malawi.

Nature of the evidence. P. boisei has a compre-hensive craniodental fossil record. There are severalskulls (the one from Konso being remarkably com-plete and well preserved), several well-preservedcrania, and many mandibles and isolated teeth.There is evidence of both large and small-bodiedindividuals, and the range of the size difference sug-gests a substantial degree of sexual dimorphism.There are no postcranial remains that can, withcertainty, be assigned to P. boisei.

Characteristics and inferred behavior. Cranial:P. boisei is the only hominin to combine a massive,wide, flat, and face, massive premolars and molars,and small anterior teeth. The face of P. boisei islarger and wider than that of P. robustus, yet theirbrain volumes are similar. The mandible of P. boiseihas a larger and wider body or corpus than anyother hominin (see P. aethiopicus above). Thetooth crowns apparently grow at a faster rate thanhas been recorded for any other early hominin. Thefossil record of P. boisei extends across about 1 My,during which there is little evidence of any substan-tial change in the size or shape of the components ofthe cranium, mandible, and dentition (Wood et al.,1994). Postcranial: There is, unfortunately, nopostcranial evidence that can with certainty beattributed to P. boisei.

CNS-related fossil evidence. Endocranial: TheP. boisei neurocranium is represented by 11 speci-mens: OH 5 (Olduvai Gorge); Omo L-338Y-6 andOmo-323-1976-896 (Omo Shungura Formation);KGA-10-525 (Konso); KNM-ER 23000, KNM-ER406, KNM-ER 407, and KNM-ER 732 (KoobiFora); KNM-CH 304 (Chesowanja); and KNM-WT 13750 and KNM-WT 17400 (West Turkana).The mean adult endocranial volume for P. boisei is488 cm3 (n¼ 10; range 400–545 cm3). The samplemean EQ for P. boisei is 2.5. Four or five P. boisei(KGA-10-525, KNM-ER 23000, KNM-WT 13750,OH 5, and possibly Omo L338Y-6) endocasts haveslight LORF petalial patterns (Holloway et al.,2004a). For all other P. boisei endocasts, either itis not possible to determine whether a petalia exists,


or this information has not been reported. For onespecimen (KNM-WT 17400) the Broca’s cap regionis larger on the left side than on the right side, but itis not clear whether or not this is due to distortion(Holloway et al., 2004a). Three P. boisei have con-volutional details in the occipital region, suggestinga reduction in the relative size of the primary visualcortex size (KGA-10-525, KNM-ER 23000, OmoL338Y-6). For all other P. boisei, it is either notpossible to determine the key occipital landmarks,or this information has not been reported. The tem-poral lobe of KNM-WT 17400 is ape-like in its sizeand shape. This contrasts with morphology seen inAu. africanus and H. sapiens, but it shares thismorphology with other Paranthropus taxa (Falket al., 2000). Three P. boisei endocasts (KNM-ER2300, KNM-WT 17400, and OH 5) have a pointedrostral frontal lobe. They share this morphologywith P. aethiopicus and the great apes, and it con-trasts with the condition in Au. africanus andmodern humans (Falk et al., 2000). Vertebralcanal: No evidence. Behavioral interpretations:There is more and better evidence for a more mod-ern humanlike pattern of brain organization inP. boisei than in Au. afarensis. This may indicatethat not only did Paranthropus brain size expandover time (Elton et al., 2001), but some brain reor-ganization may have occurred in this lineage.Certainly, the impact of brain size on brain mor-phology (e.g., Jerison, 1975) could be a contributingfactor to this trend.

Other endocranial morphology. Cranial venoussinuses: The cranial venous sinus system of P. boiseihas been given much attention. Tobias (1967) firstnoted that OH 5 had an enlarged occipital marginalsinus system, a trait it shares with most other scorableP. boisei specimens: that is, KNM-CH 304 (Gowlettet al., 1981), KNM-ER 23000 (Brown et al., 1993),KNM-ER 407 (Day, 1976), and KNM-ER 732(Leakey et al., 1972). A probable exception to thisis Omo L-338Y-6, because several authors (Rak andHowell, 1978; Holloway, 1981a; Kimbel, 1984;Holloway et al., 2002) have failed to confirm thepresence of an enlarged O/M sinus system in thisspecimen (cf. Falk et al., 1995). The fossil KGA-10-525 lacks an O/M sinus system (Suwa et al., 1997;Holloway et al., 2004a), although it has been sug-gested that transverse sinus grooves are also missing(Suwa et al., 1997; White and Falk, 1999; cf.Holloway et al., 2004a). Meningeal vessels: Saban(1983) found that P. boisei (KNM-ER 407), likeP. robustus, has three major branches of the middlemeningeal vessels: anterior, middle, and posterior.However, Saban found only simple anterior and pos-terior branches for Omo 338y-6, now considered to

belong to P. boisei, but originally thought to be annon-megadont australopith (Walker and Leakey,1988; White and Falk, 1999).

Taxon name. Paranthropus robustus Broom,1938.

Approximate time range. c. 2.0–1.5 Mya.Initial discovery. TM 1517 – an adult, presum-

ably male, cranium and associated skeleton; Phase IIBreccia, now Member 3, Kromdraai B, SouthAfrica, 1938.

Type specimen. As above.Source(s) of the evidence. Kromdraai,

Swartkrans, Gondolin, Drimolen, and Cooper’scaves, all situated in, or near to, the BlauuwbankValley, near Johannesburg, South Africa.

Nature of the evidence. The fossil record is similarto but less numerous than that of Au. africanus. Thedentition is well represented, some of the cranialremains are well preserved, but many of the mand-ibles are crushed and/or distorted. The postcranialskeleton is not well represented. Research atDrimolen was only initiated in 1992, yet alreadymore than 80 hominin specimens have been recov-ered and it promises to be a rich source of evidenceabout P. robustus.

Characteristics and inferred behavior. Cranial: Thebrain, face, and chewing teeth of P. robustus are largerthan those of Au. africanus, yet the incisor teeth aresmaller. Postcranial: It has been suggested that thethumb of P. robustus would have been capable ofthe type of grip necessary for stone tool manufacture,but this claim is not accepted by all researchers. Thefoot retains some arboreal capability, and the pelvicmorphology suggests a relatively inefficient system formass transfer, but the finger curvature is reduced, andit has more modern humanlike limb proportions andfoot morphology, evidence that P. robustus was amore committed biped than, say, Au. afarensis, orH. habilis (see below).

CNS-related fossil evidence. Endocranial: TheP. robustus neurocranium is represented by at leastsix specimens: four from Swartkrans (SK 1585, SK46, SK 54, and SK 859), one from Kromdraai (TM1517), and one from Drimolen (DNH 7). The meanadult endocranial volume is 533 (n¼ 4; range450–650). The sample mean EQ for P. robustus is3.1. The evidence for modern humanlike aspects ofbrain morphology is much weaker than for P. boisei,in spite of the larger brain size of P. robustus. Two orthree specimens (SK 1585, SK 859, and possibly SK54) have slight left occipital petalias, but there is noindication of whether they also have right frontalpetalias (Holloway et al., 2004a). It is not possibleto tell whether the primary visual cortex is reduced in


SK 1585, SK 54, and SK 859, since for each of theseendocasts the location of the LS and the interparietalsulcus cannot be determined with certainty(Holloway, 1975; Holloway et al., 2004a). OneP. robustus individual (SK 1585) has a beak-shapedfrontal lobe and a rounded temporal lobe – ape-liketraits shared with other Paranthropus, in contrast tothe morphology of Au. africanus and Homo (Falket al., 2000). Vertebral canal: There are a handful ofvertebras associated with this species, none of whichare thoracic vertebras, although there is one near-complete axis (SK 854).

Other endocranial morphology. Cranial venoussinuses: All three P. robustus specimens with therelevant anatomy preserved demonstrate anenlarged O/M sinus system. These are SK 1585, SK46, and SK 859 (Tobias, 1967; Holloway, 1972;Kimbel, 1984). Meningeal vessels: Saban (1983)found that one P. robustus endocast (SK 1585) hadthree major branches of the middle meningeal ves-sels: anterior, middle, and posterior.

Taxon name. Australopithecus garhi Asfaw et al.,1999.

Approximate time range. c. 2.5 Mya.Initial discovery. GAM-VP-1/1 – left side of man-

dibular corpus; Gamedah, Middle Awash, Ethiopia,1990.

Type specimen. BOU�-VP-12/130 – a cranium;Bouri, Middle Awash, Ethiopia, 1997 (�the prefixARA was erroneously used in the text of Asfawet al., 1999).

Source(s) of the evidence. Bouri, Middle Awash,Ethiopia.

Nature of the evidence. A cranium and two par-tial mandibles.

Characteristics and inferred behavior. Cranial:Au. garhi combines a primitive cranium with large-crowned postcanine teeth. However, unlikeParanthropus (see above), the incisors and caninesare large and the enamel lacks the extreme thicknessseen in the latter taxon. Postcranial: A partial skeletoncombining a long femur with a relatively long forearmwas found nearby, but is not associated with the typecranium of Au. garhi (Asfaw et al., 1999); these fossilshave not been formally assigned to Au. garhi.

CNS-related fossil evidence. The single cranialspecimen has an endocranial volume of 450 cm3,based on water displacement of a plaster model ofthe reconstructed endocast (reliability A1–A2).Holloway et al. (2004a) described the endocastmorphology, but there was no evidence of a modernhumanlike brain reorganization.

Other endocranial morphology. Meningeal ves-sels are present, but are not diagnostic.

4.18.4.4 Transitional Homo

This group contains two hominin taxa (H. habiliss.s. and H. rudolfensis) that are conventionallyincluded within Homo, but which some research-ers (e.g., Wood and Collard, 1999) have suggestedmight not belong in the Homo clade. Until we havethe means to generate sound phylogenetic hypoth-eses about these and other early hominin taxa, it isnot clear what their alternative generic attributionshould be. Thus, for the purposes of this review,these two taxa are retained within Homo, but arereferred to as transitional hominins.

Taxon name. Homo habilis Leakey et al., 1964.Approximate time range. c. 2.4–1.6 Mya.

Initial discovery. OH 4 – fragmented mandible;Olduvai Gorge, Tanzania, 1959.

Type specimen. OH 7 – partial skull cap and handbones; Olduvai Gorge, Tanzania, 1960.

Source(s) of the evidence. Olduvai Gorge,Tanzania; Koobi Fora, and perhaps Chemeron,Kenya; Omo (Shungura), and Hadar, Ethiopia,East Africa; perhaps also Sterkfontein, Swartkrans,Cooper’s and Drimolen, South Africa.

Nature of the evidence. Mostly cranial and dentalevidence with only a few postcranial bones that canbe confidently assigned to H. habilis.

Characteristics and inferred behavior. Cranial:All the crania are wider at the base than acrossthe vault, but the face is broadest in its upperpart. The jaws and teeth are absolutely small, butwhen related to estimated body mass they are lar-ger than in other later premodern Homo taxa.Postcranial: The curved proximal phalanges andwell-developed muscle markings on the phalangesof OH 7 also indicate the hand was used for morepowerful grasping (such as would be needed forarboreal activities) than is the case in any otherspecies of Homo. Conclusion: The jaws and teethof H. habilis are absolutely small, but they arerelatively large. Also, postcranial evidence suggeststhat H. habilis was capable of traveling arboreallyand bipedally.

CNS-related fossil evidence. Endocranial: TheCNS-related fossil evidence for H. habilis com-prises six crania, two from Koobi Fora (KNM-ER1813 and KNM-ER 1805), and four from OlduvaiGorge (OH 7, OH 13, OH 16, and OH 24). Brainsare larger in H. habilis than in Australopithecusand Paranthropus, with a mean adult endocranialvolume of 609 cm3 (n ¼ 6; range 509–687 cm3).The sample average EQ for H. habilis is 3.7.Most of the inferences about derived modernhumanlike morphology in this species are contro-versial, mainly due to poor preservation of the


relevant structures. Falk (1983a) has cast doubt onthe allocation of KNM-ER 1805 to H. habilis onthe grounds that it displays ape-like frontal orbitalsulci at the lateral borders of the frontal lobes. Theevidence for the petalial pattern in H. habilis isweak. Holloway et al. (2004a) claim that a singlespecimen, KNM-ER 1805, has a slight LORF peta-lial pattern, but the observation of frontal petaliais not reliable because of postmortem deformation(Begun and Walker, 1993; Holloway et al.,2004a). Tobias (1987) makes a case for languageability in H. habilis, but this is controversial asmuch of the derived anatomy he describes forH. habilis is not confirmed by other authors, whoclaim the fossils are too fragmented and distortedto justify these interpretations (Begun and Walker,1993; Holloway et al., 2004a). Tobias (1987) sug-gests that OH 24, and probably OH 16 (but thereis bone missing), have right frontal petalias.According to Tobias, the morphology of the frag-mented of the frontal regions of the OH 7 and OH16 endocasts is suggestive of a modern humanlikeBroca’s area, but Holloway et al. (2004a) see toofew convolutional details to confirm this. Thesupramarginal angular gyri of the inferior parietalregion – corresponding to Brodmann areas 40 and39, respectively – are well developed in all fourOlduvai H. habilis specimens (i.e, OH 7, 16, 13,and 24) (Tobias, 1987). Tobias states that thesegyri are included in Wernicke’s area (although heallows that the area’s definition is controversial).In fact, the inferior parietal lobule is probably notpart of Wernicke’s language comprehension area,which is restricted to the left superior temporalcortex posterior to the primary auditory cortex(i.e., posterior part of Brodmann area 22) (Wiseet al., 2001). However, as previously mentioned,the inferior parietal lobule is greatly expanded inhumans compared to monkeys, a difference thathas been correlated with the development of lan-guage and calculation abilities (Simon et al.,2002). Tobias (1987) mentions that in three H.habilis specimens (OH 24, OH 13, and OH 7) thesuperior parietal lobule is well developed, a char-acteristic also of Au. africanus (Dart, 1925;Schepers, 1946). Because the development isgreater on the left size, he calls the asymmetryparietopetalia, but note that none of these speci-mens has the typical modern humanlike LORFpetalial pattern. Holloway et al. (2004a) do notconfirm these asymmetries, and instead they notethat OH 7 and OH 24 are distorted and that thismakes the identification of parietal petalias ques-tionable, and that in OH 13 inferences about aparietal petalia depend on the way the specimen

is orientated. Holloway et al. (2004a) do not referto the placement of the LS or to the size of theoccipital lobe in H. habilis. However, Begun andWalker (1993) suggest that the occipital lobe intwo H. habilis specimens (KNM-ER 1813 andKNM-ER 1805) is smaller and less projectingthan in KNM-ER 1470, a cranium referred toH. rudolfensis. Vertebral canal: Unfortunately,no H. habilis thoracic vertebras are available toinvestigate potentially language-related aspects ofspinal cord anatomy in this taxon. Behavioralinterpretations: There is no evidence of modernhumanlike Broca’s cap morphology in H. habilis,nor is there any evidence for any reduction in thesize of the primary visual cortex. In summary, theoriginal suggestion that H. habilis is the earliesthominin with the cognitive capacity for languageis no longer supported.

Other endocranial morphology. Cranial venoussinuses: Three specimens (KNM-ER 1813, KNM-ER 1805, and OH 16) demonstrate the usual mod-ern humanlike dominant transverse-sigmoid sinussystem. Meningeal vessels: H. habilis endocasts forwhich the morphology is available (KNM-ER 1805,KNM-ER 1813, OH 7) have evidence of three majorbranches of the middle meningeal artery (Tobias,1991; Holloway et al., 2004a).

Taxon name. Homo rudolfensis (Alexeev, 1986)sensu Wood, 1992.

Approximate time range. c. 1.8–1.6 Mya.Initial discovery. KNM-ER 819 – mandible frag-

ment; Koobi Fora, Kenya, 1971.Type specimen. Lectotype: KNM-ER 1470 – cra-

nium; Koobi Fora, Kenya, 1972 (Leakey, 1973).Source(s) of the evidence. Koobi Fora, and perhapsChemeron, Kenya; Uraha, Malawi.

Nature of the evidence. Several incomplete cra-nia, two relatively well-preserved mandibles, andseveral isolated teeth.

Characteristics and inferred behavior. Cranial:H. rudolfensis and H. habilis show different mixturesof primitive and derived, or specialized, cranial fea-tures. For example, although the absolute size of thebrain case is greater in H. rudolfensis, its face is widestin its mid-part, whereas the face of H. habilis is widestsuperiorly. The more primitive face of H. rudolfensisis combined with a robust mandible and mandibularpostcanine teeth with larger, broader crowns andmore complex premolar root systems than thoseof H. habilis. The mandible and postcanine teeth ofH. rudolfensis are larger than one would predict for ageneralized hominoid of the same estimated bodymass, suggesting that its dietary niche made mechan-ical demands comparable to those of the archaic


hominins. Postcranial: No postcranial remains canyet be reliably linked with H. rudolfensis.

CNS-related fossil evidence. Endocranial – CNS-related data are preserved in three cranial speci-mens (KNM-ER 1470, KNM-ER 1590, andKNM-ER 3732). H. rudolfensis mean adult endo-cranial volume is 776 (n ¼ 3; range 750–825),although when it is related to admittedly crudeestimates of body mass (EQ ¼ 3.2) the brain ofH. rudolfensis is not substantially larger than thatof Paranthropus, and is smaller than that of H.habilis. KNM-ER 1470 has a modern humanlikeBroca’s region which is expanded on the left side(Tobias, 1975; Falk, 1983a; Begun and Walker,1993; Holloway et al., 2004a), a feature thatKNM-ER 3732 probably shares, although distor-tion obscures the interpretation of the morphologyof this region. The clearly delimited, modernhumanlike Broca’s cap is taken by Holloway(1983c) to be suggestive of both language capacityand right-handedness, although he cautions thatchimpanzees may also have well-developedBroca’s caps. KNM-ER 1470 has a clear, modernhumanlike LORF petalial pattern. Unlike H. habi-lis (KNM-ER 1805), KNM-ER 1470 lacks anape-like fronto-orbital sulcus on the surface of thefrontal lobe (Falk, 1983a). Holloway et al. (2004a)found no evidence of an LS or occipital lobe reduc-tion in H. rudolfensis. However, Begun and Walker(1993) mention that the occipital lobe in theH. rudolfensis specimen KNM-ER 1470 is largerand more projecting than in two H. habilis speci-mens (KNM-ER 1813 and KNM-ER 1805).Vertebral canal: No vertebras are known for thistaxon. Behavioral interpretations: H. rudolfensis(in particular, KNM-ER 1470) represents the old-est undisputed evidence of modern humanlikebrain anatomy and it possesses features suggestiveof language ability and right-handedness (Falk,1983a; Holloway et al., 2004a). In support ofthese interpretations, Toth (1985) has inferredthat contemporaneous stone tools were producedby predominately right-handed hominins.Interestingly, there is much more evidence ofmodern humanlike CNS-related anatomy inH. rudolfensis than in H. habilis. Also noteworthy,the debate over particular convolutional detailslessens with the appearance of Homo. This is inpart due to the fact that the endocranial convolu-tions of Homo are less obvious than those ofarchaic hominins. Falk (1980a, 1980b) notes thatfrontal convolutions should be the focus of endo-cast studies as these are more visible. This visibilitycontrasts with the relatively poor preservation ofthe LS in premodern Homo (Falk, 1991).

Other endocranial morphology. Cranial venoussinuses: H. rudolfensis does not show any evidenceof an enlarged O/M sinus system. Meningeal vessels:One specimen (KNM-ER 1470) has separate ante-rior, middle, and posterior branches of its middlemeningeal artery (Holloway et al., 2004a).

4.18.4.5 Premodern Homo

The species in this category are all usually assignedto the Homo clade. However, at least one species,H. ergaster, has a brain size that overlaps with thatof archaic and transitional hominins.

Taxon name. Homo ergaster Groves and Mazak,1975.

Approximate time range. c. 1.9–1.5 Mya.Initial discovery. KNM-ER 730 – corpus of an

adult mandible with worn teeth; Koobi Fora,Kenya, 1970.

Type specimen. KNM-ER 992 – well-preservedadult mandible; Koobi Fora, Kenya, 1971.Source(s) of the evidence. Koobi Fora, WestTurkana, Kenya; Dmanisi, Republic of Georgia.

Nature of the evidence. Cranial, mandibular, anddental evidence, including a remarkably completeassociated skeleton of a juvenile male individualfrom Nariokotome, West Turkana.

Characteristics and inferred behavior. Cranial:Two sets of features are claimed to distinguishH. ergaster from H. erectus. The first comprisesfeatures for which H. ergaster is more primitivethan H. erectus, with the most compelling evi-dence coming from details of the mandibularpremolars. The second set comprises featuresof the vault and base of the cranium for whichH. ergaster is less specialized, or derived, thanH. erectus. The small chewing teeth of H. ergasterimply that it was either eating different foodthan the australopiths, or that it was preparingthe same food extraorally. This could haveinvolved the use of stone tools, or cooking, or acombination of the two. Postcranial: Postcranialsimilarities to modern humans suggest these homi-nins were habitual bipeds. Conclusion: Overall,H. ergaster is the first hominin to combine mod-ern human-sized chewing teeth with a postcranialskeleton (e.g., long legs, large femoral head, etc.)apparently committed to long-range bipedalism,and to lack morphological features associatedwith locomotor and postural behaviors related toarboreality.

CNS-related fossil evidence. Endocranial:Relevant fossil evidence for H. ergaster comprisesthree well-preserved crania from Africa (KoobiFora, and West Turkana), and four crania from


Dmanisi in the Republic of Georgia. The adult meanendocranial volume of the six H. ergaster specimensis 762 cm3, with an average of 851 cm3 for the threeAfrican specimens, and a much lower average of675 cm3 for the three Dmanisi specimens with pub-lished endocranial volume estimates. The sampleaverage EQ for H. ergaster is 2.8. When theDmanisi specimens (for which no body mass hasbeen estimated) are excluded, the EQ for the threeAfrican specimens of H. ergaster is 3.1.Convolutional details are known only for the threeAfrican specimens. Two specimens have modernhumanlike LORF petalial patterns (KNM-WT15000, KNM-ER 3883), whereas the third speci-men (KNM-ER 3733) has a less pronouncedasymmetry (Begun and Walker, 1993; Hollowayet al., 2004a). All three specimens seem to have amodern humanlike asymmetry of the Broca’s capregion, with the evidence for this pattern beingclearest in KNM-ER 15000, whereas in the othertwo East African specimens the morphology in thatarea is uncertain (Begun and Walker, 1993;Holloway et al., 2004a). Occipital convolutionaldetails are not preserved in any H. ergaster cranialspecimen. Vertebral canal: The juvenile WestTurkana (KNM-WT 15000) skeleton also includesa vertebral column. H. ergaster resembles earlierhominins and nonhuman primates in having rela-tively smaller thoracic vertebral canals than recenthumans, suggesting that this hominin did not yetshow the expanded canal that has been associatedwith more precise control of the muscles associatedwith speech (see entry for H. neanderthalensis for adiscussion). Behavioral interpretations: Hollowayet al. (2004a) interpret the cranial findings as clearevidence of right-handedness and language ability.In contrast, evidence from the vertebral canal sug-gests humanlike increased control of breathing;thus, speech most likely did not yet exist in thesehominins. Great apes (Patterson, 1978; Gardneret al., 1989; Shapiro and Galdikas, 1999) andhuman infants (Bonvillian et al., 1983, 1997;Bonvillian and Patterson, 1999) lack the capacityfor vocal language production, but they are able tocommunicate with hand signals. A study of a deafsign-language user found that Broca’s region main-tains its function in nonvocal language (Corinaet al., 1999; Corina and McBurney, 2001).Language-related cerebral anatomy might haveexisted as part of a complex of preadaptations tolanguage, along with a series of cranial modifica-tions seen in H. ergaster and H. erectus (MacLarnonand Hewitt, 2004). These data suggest thatincreased nonvocal language ability preceded vocallanguage.

Other endocranial morphology. Cranial venoussinuses: There is no indication of enlarged O/Msinus system for this taxon. Meningeal vessels: Theanterior branch of the middle meningeal artery isespecially well developed in H. ergaster crania suchas KNM-WT 15000 (Begun and Walker, 1993), andKNM-ER 3883 (Holloway et al., 2004a). Anteriorbranches are characteristically more developed onendocasts of later African fossil Homo, includingmodern humans (Grimaud-Herve, 1994; Hollowayet al., 2004a).

Taxon name. Homo floresiensis Brown et al.,2004.

Approximate time range. c. <90–12 kya.Initial fossil discovery. LB1 – partial adult skele-

ton; Liang Bua, Flores Indonesia, 2003 (Brownet al., 2004).

Type specimen. As above.Sources of the evidence. Liang Bua, Indonesia.Nature of the evidence. LB1 partial adult skeleton

plus cranial and postcranial evidence of a total of atleast nine individuals (Morwood et al., 2005).Characteristics and inferred behavior. Cranial:Cranial morphology suggests a dwarfed H. erectus.Similar to Au. afarensis in stature and endocranialvolume. Postcranial: Femur and pelvic morpholo-gies show affinities to H. habilis and Au. afarensis.Possibly associated with oldowan-like stone arti-facts. Charred bones hint at control of fire.

CNS-related fossil evidence. Endocranium: Theendocranial volume estimate of LB 1 is 417 cm3.The H. floresiensis EQ, assuming a body mass of26 kg, is 3.1; this is within the Australopithecusrange. For comparison, if one assumes the low-endbody mass estimate of 16 kg, the EQ is 4.5, andassuming the given the high-end body mass estimateof 36 kg, the EQ is a mere 2.4 – the smallest of anyfossil hominin. All inferences about H. floresiensisbrain morphology were made by Falk et al. (2005),based on observations of both the LB1 fossil neuro-cranium and a virtual endocast. In endocranialshape, LB1 resembles classic Asian H. erectus. LB1has a LORF petalial pattern. Details are not given,although the Broca’s cap region is consistent withmodern humanlike morphology (Falk et al., 2005).The endocast lacks ape-like fronto-orbital sulci;these are also absent in H. rudolfensis, but they areretained in other (smaller-brained) early homininssuch as H. habilis and Au. africanus (Falk, 1980b,1983a). The LS is posterior to the lambdoid suture,in a derived position which suggests relative reduc-tion of the primary visual cortex at the expense ofenlargement of posterior parietal association areas(Figure 2e). There are a few features in which the


H. floresiensis brain differs from the classicH. erectus brain. First, it is inferred that prefrontalcortex in the region of area 10 is expanded andmuch more convoluted than in H. erectus orAu. africanus (Falk et al., 2005). This aspect ofH. floresiensis is significant because the prefrontalcortex is the region of the human brain that hasmost clearly increased in relative degree of gyrifi-cation (Zilles et al., 1988; Rilling and Insel, 1998).Second, LB1 has extremely wide temporal lobes.Interestingly, the temporal lobe is predicted to haveundergone more change in the modern human line-age than has any other brain component(Semendeferi and Damasio, 2000), and it is largerin modern humans than predicted for a nonhumanprimate of similar brain size (Rilling and Seligman,2002). Third, the LB1 occipital lobe does not hangover the cerebellum. An occipital lobe thatoverhangs the cerebellum is a derived feature ofH. erectus (Falk et al., 2005). Vertebral canal: Nodescription available. Behavioral interpretations:H. floresiensis is a dwarfed hominin species inwhich the size reduction was more pronounced inthe brain than the body. In spite of its small abso-lute and relative brain size, the H. floresiensis brainis at least as modern humanlike in its morphologyas is the brain of H. erectus. Compared to classicH. erectus, H. floresiensis is more modern human-like in having a well-developed temporal lobe andincreased gyrification of the prefrontal region.Might the specialized brain morphology of H. flor-esiensis relate to the fact that this species has beenassociated with unusually sophisticated artifacts?At present, it is impossible to know. Many cogni-tive functions of the prefrontal and temporalregions (e.g., processing of auditory information,language production, higher-order processing ofvisual information, planning, and memory) arepredicted to be emphasized in a species that isassociated with stone tools. However, these areasare probably not the ones most involved in the actof stone toolmaking (see Stout et al., 2000). Analternative hypothesis is that in this species thetemporal lobe and prefrontal cortex did notbecome relatively larger; rather, other structures(e.g., primary visual cortex) became relativelysmaller more quickly. Domesticated mammalshave relatively smaller brains and sensory struc-tures than do their wild counterparts, with thesize of the primary visual cortex and eyes beingthe most reduced – a pattern that is also found inthe fossil dwarfed bovid Myotragus (Kohler andMoya-Sola, 2004).

Other endocranial morphology. Cranial venoussinuses: Present, but not diagnostic. Meningeal

vessels: The configuration suggests that vessels thatoriginate in the orbit contribute to the supply of themeninges overlying the temporal lobe; this feature iscommon in apes and found in some H. erectus (Falk,1993; Falk et al., 2005).

Taxon name. Homo erectus (Dubois, 1892)Weidenreich, 1940.

Approximate time range. c. 1.8 Mya to< 200 kya.

Initial discovery. Kedung Brubus 1 – mandiblefragment; Kedung Brubus, Java (now Indonesia),1890.

Type specimen. Trinil 2 – adult calotte; Trinil,Ngawi, Java (now Indonesia), 1891.

Source(s) of the evidence. Sites in Indonesia (e.g.,Trinil, Sangiran, Sambungmachan), China (e.g.,Zhoukoudian, Lantian), Africa (e.g., OlduvaiGorge, Melka Kunture), and possibly India(Hathnora).

Nature of the evidence. Mainly cranial with somepostcranial evidence, but little or no evidence of thehand or foot.

Characteristics and inferred behavior. Cranial:The crania belonging to H. erectus have a lowvault, a substantial, more-or-less continuous torusabove the orbits, and the occipital region is sharplyangulated. The inner and outer tables of the cranialvault are thickened. The body of the mandible is lessrobust than that of the australopiths and in thisrespect it resembles H. sapiens, except that the sym-physeal region lacks the well-marked chin that is afeature of later Homo and modern humans. Thetooth crowns are generally larger, and the premolarroots of many specimens are more complicated thanthose of modern humans. All the dental and cranialevidence points to a modern humanlike diet forH. erectus. Postcranial: The cortical bone of thepostcranial skeleton is thicker than that in modernhumans. The limb bones are modern humanlike intheir proportions and have robust shafts, but theshafts of the long bones of the lower limb are flat-tened from front to back (femur) and from side toside (tibia) relative to those of modern humans.There is no fossil evidence relevant to assessing thedexterity of H. erectus, but if H. erectus manufac-tured Acheulean artifacts then dexterity would beimplicit. The postcranial elements are consistentwith a habitually upright posture and obligate,long-range bipedalism.

CNS-related fossil evidence. Endocranial: At least43 crania or cranial fragments preserve informationabout the CNS of H. erectus. The mean endocranialvolume of H. erectus is 991 cm3 (n ¼ 36; range727–1260). The EQ for H. erectus is 3.9, and


H.erectus shows aspects of modern humanlike brainorganization similar to those described for H. erga-ster. This taxon shows surprisingly little variabilityin endocast morphology. Holloway (1980),Broadfield et al. (2001), and Holloway et al.(2004a) drew attention to the very clear pattern ofLORF petalial patterns and modern humanlikeasymmetry of the Broca’s cap region. There issome suggestion of a right-hander’s petalial config-uration from all sites with scored fossils (i.e.,Olduvai, Ngandong, Sambungmacan, Sangiran,Trinil, Zhoukoudian) (Holloway et al., 2004a).The asymmetries range from slight to strong, andin many specimens the evidence exists for both theleft occipital and the right frontal (Ngandong 1, 6,17, 14; Sangiran 2, 17; Trinil 2, Zhoukoudian III E,III L), although in other specimens there are missingdata or there is distortion in either the left occipitalor right frontal regions (Ngandong 13; OH 9, 12;Sangiran 4, 10, 12; Zhoukoudian I L; Hollowayet al., 2004a). However, Begun and Walker (1993)took a different position with respect to the existenceof petalias in the Zhoukodian specimens that theyexamined. They state that no frontal petalias areevident for Zhoukoudian I L, II, III E, and III L, andno occipital petalias are evident for Zhoukoudian IIand III E, although they do allow that occipital peta-lias are evident for Zhoukoudian I L and III L.Holloway et al. (2004a) do not describe the morphol-ogy of Zhoukoudian II. Most authors agree that thefrontal lobe of H. erectus is derived toward the mod-ern humanlike condition. Convolutional details ofthe frontal lobe are more modern humanlike thanape-like for Sangiran 2 (Ariens Kappers andBouman, 1939; Weidenreich, 1943; Connolly,1950). Broca’s region is more modern humanlike inH. erectus than in earlier hominins. This was firstmentioned by Dubois (1897), who noted that thetype specimen (Trinil 2) had a fairly well-developedthird (¼inferior) frontal convolution, the gyrus asso-ciated with Broca’s area. In fact, the Broca’s capregion is enlarged, and/or there is an asymmetry inwhich the left side is larger and better defined orprotrudes more laterally in all scorable specimens(i.e., Ngandong 6 and 14, Sambungmacan 3,Sangiran 2, 3, 10 and 17, Trinil 2, andZhoukoudian III E) (Holloway, 1980; Grimaud-Herve, 1994; Holloway et al., 2004a). Hollowayet al. (2004a) infer that H. erectus was capable ofrudimentary language and was predominantly right-handed. In the occipital lobe, the LS has been identi-fied in a few specimens (Sangiran 10, OH 12, Trinil2) and in all it is in a posterior position. A possibleexception is Sangiran 2 in which the identification ofthe LS is uncertain, and the sulcus referred to may

actually be a lateral calcarine sulcus in a position thatwould be unusual in modern humans. The two fossilsfrom Olduvai (OH 9 and OH 12) resemble the Asianspecimens in aspects of brain morphology. OH 9 hasa strong left occipital petalia like other H. erectus andH. ergaster (due to missing data, whether or not therewas a right frontal petalia cannot be determined).OH 12 has a posterior LS like other H. erectus (con-volutional details in this region are not preserved inany H. ergaster specimen). However, whereas OH 9is in the upper 50% of H. erectus endocranialvolume, OH 12 has the smallest H. erectus endocra-nial volume and fits better with H. ergaster. Thedevelopment of three cranial features (the tympanicplate, the bregmatic area of the cranial vault, andthe subarcuate fossa) and a comparison of adultH. erectus endocranial volumes with that of theMojokerto child, reveal an ape-like pattern of brainontogeny for this specimen (Coqueugniot et al.,2004).

Other endocranial morphology. Cranial venoussinuses: Three specimens (Zhoukoudian II, III E,and III L) have dominant transverse-sigmoid sinussystems, and one specimen (Trinil 2) has an O/Msinus system on the left and an enlarged transversesinus on the right (Falk, 1986). Meningeal vessels:Weidenreich (1938) used a modern human-basedsystem of classification in his description of theZhoukoudian fossils which overlooked similaritiesbetween the H. erectus meningeal patterns and thatof the apes; but he did note that H. erectus wasprimitive in having fewer ramifications than modernhumans. In Falk’s re-evaluation of Weidenreich’sdescription of the meningeal vessels (Falk, 1993),she concludes that they are ape-like to the extentthat there is a high frequency of the meningealarteries originating from the orbit rather than thefloor. In comparison to modern humans, in AsianH. erectus specimens the obelic branch of the middlemeningeal artery is more developed, and may havecontributions from both the anterior and the poster-ior branches. Grimaud-Herve describes threeregional patterns. First, it is common for the obelicbranch to arise independently as a third majorbranch in Zhoukoudian endocasts (e.g.,Zhoukoudian I L, III E). Second, the obelic branchbifurcates near the origin of middle branch in Trinil2 and several Sangiran endocasts (e.g., Sangiran 17).Third, in most Ngandong endocasts, the obelicbranch derives from the anterior branch but alsohas a contribution from the posterior branch; theanterior branch is often better developed than theposterior (e.g., Ngandong 3, 7). In the NorthAfrican H. erectus Ternifine 4, a very ramified obe-lic branch stems from the anterior branch of the


middle meningeal artery (Saban, 1984; Hollowayet al., 2004a). The developed anterior branch issaid to be typical of African specimens of latertaxa, but, as mentioned above, the developed obelicbranch is also typical of H. erectus. The principalvessel of the anterior branch has posterior ramifica-tions that run parallel to it in H. erectus, in contrastto their more oblique orientation in modern humans(Grimaud-Herve, 1994; see The Evolution ofParallel Visual Pathways in the Brains of Primates).

Taxon name. Homo antecessor Bermudez deCastro et al., 1997.

Approximate time range. c. 700–500 kya.Initial discovery. ATD6-1 – left mandibular

canine; Level 6, Gran Dolina, Spain, 1994.Type specimen. ATD6-5 – mandible and asso-

ciated teeth; Level 6, Gran Dolina, Spain, 1994.Source(s) of the evidence. Gran Dolina, Atapuerca,Spain.

Nature of the evidence. The partial cranium of ajuvenile, parts of mandibles and maxillae, and iso-lated teeth.

Characteristics and inferred behavior. Cranial:Researchers who found the remains claim the com-bination of a modern humanlike facial morphologywith large and relatively primitive tooth crowns androots is not seen in H. heidelbergensis (see below).The Gran Dolina remains also show no sign of anyderived H. neanderthalensis traits. Its discovererssuggest H. antecessor is the last common ancestorof Neanderthals and H. sapiens.

CNS-related fossil evidence. The only H. antecessorcranium (ATD-15) has an estimated endocranialvolume of 1000 cm3 (Bermudez de Castro et al., 1997).

Taxon name. Homo heidelbergensis Schoetensack,1908.

Approximate time range. c. 600–100 kya.Initial discovery. Mauer 1 – adult mandible;

Mauer, Heidelberg, Germany, 1907.Type specimen. As above.Source(s) of the evidence. Sites in Europe (e.g.,

Mauer, Petralona); Near East (e.g., Zuttiyeh);Africa (e.g., Kabwe, Bodo); and China (e.g., Dali,Jinniushan, Xujiayao, Yunxian). Researchers whosee distinctions between the African and non-African components of the hypodigm refer to theformer as H. rhodesiensis.

Nature of the evidence. Many crania but rela-tively little mandibular and postcranial evidence.

Characteristics and inferred behavior. Cranial:What sets this material apart from H. sapiens andH. neanderthalensis (see below) is the morphologyof the cranium and the robusticity of the postcranial

skeleton. Some brain cases are as large as those ofmodern humans, but they are always more robustlybuilt with a thickened occipital region, an evenlyprojecting face with large separate ridges above theorbits, unlike the more continuous brow ridge ofH. erectus. Compared with H. erectus (see above),the parietals are expanded, the occipital is morerounded and the frontal bone is broader. The craniaof H. heidelbergensis lack the specialized features ofH. neanderthalensis such as the anteriorly project-ing midface and the distinctive swelling of theoccipital region. H. heidelbergensis is the earliesthominin to have a brain as large as anatomicallymodern H. sapiens. Postcranial: the postcranial ske-leton of H. heidelbergensis suggests that its robustlong bones and large lower limb joints were wellsuited to long-distance bipedal walking.

CNS-related fossil evidence. Endocranial: H. hei-delbergensis is represented by at least 22 cranialfossils that preserve evidence of the CNS. The meanadult endocranial volume for H. heidelbergensis is1242 cm3 (n¼ 21; range 880–1450 cm3). There isan increase in mean endocranial volume comparedto H. erectus and H. ergaster. The EQ for H. heidel-bergensis is 4.2. For all the specimens, the LS is in themodern humanlike posterior position, according toHolloway et al. (2004a). Broken Hill 1 was describedby Smith (1928) to have an ape-like LS, but Hollowayet al. (2004a) disagree with this interpretation.Holloway et al. (2004a) describe LORF petalial pat-terns in most specimens, and very pronouncedasymmetrical Broca’s regions in some specimens.This is most pronounced in Arago, which has veryprotruding Broca’s caps on both sides. Unfortunately,several specimens are missing entire frontal lobes, andthere is no specimen for which all the relevant lan-guage/handedness morphology is preserved.

Other endocranial morphology. Cranial venoussinuses: Arago, Broken Hill, and Sale lack an O/Msinus system, although Guomde has an O/M sinussystem (on both sides) and Swanscombe has an O/Msinus system on the right, not on the left (Falk, 1986).Meningeal vessels: The anterior branch of the middlemeningeal artery is especially developed in AfricanH. heidelbergensis. The anterior branch has a fewanastomoses in Sale, and more numerous anastomosesin Broken Hill 1. In some European H. heidelbergensis(e.g., Swanscombe, Ehringsdorf 9), the anteriorbranch is more prominent and is the source of theobelic branch (Falk, 1986). In contrast, in oneEuropean H. heidelbergensis the posterior ramus isjust as prominent as the anterior ramus (Falk, 1986).

Taxon name. Homo neanderthalensis King,1864.


Approximate time range. c. >400 or 200–30 kya.Initial discovery. Engis 1 – a child’s cranium;

Engis, Belgium, 1829.Type specimen. Neanderthal 1 – adult calotte and

partial skeleton; Feldhofer Cave, Mettmann,Germany, 1856.

Source(s) of the evidence. Fossil evidence forH. neanderthalensis has been found throughoutEurope, with the exception of Scandinavia, as wellas in the Near East, the Levant and Western Asia.Taxonomic note: The scope of the hypodigm ofH. neanderthalensis depends on how inclusively thetaxon is defined. For some researchers the taxon isrestricted to fossils from Europe and the Near Eastthat used to be referred to as classic Neanderthals.Others interpret the taxon more inclusively andinclude within the hypodigm fossil evidence that isgenerally earlier and less derived (e.g., Steinheim,Swanscombe and Atapuerca (Sima de los Huesos)).

Nature of the evidence. Many specimens are bur-ials and so all anatomical regions are represented inthe fossil record.

Characteristics and inferred behavior. Cranial:The distinctive features of the cranium of H. nean-derthalensis include thick, double-arched browridges, a face that projects anteriorly in the midline,a large nose, laterally projecting and rounded par-ietal bones, and a rounded, posteriorly projectingoccipital bone (i.e., an occipital bun). The size andwear on the incisors suggest that the Neanderthalsregularly used their anterior teeth as tools, either forfood preparation or to grip hide or similar material.Postcranial: Neanderthals were stout with a broadrib cage, a long clavicle, a wide pelvis, and limbbones that are generally robust with well-developedmuscle insertions. The distal extremities tend to beshort compared to most H. sapiens, butNeanderthals were evidently obligate bipeds. Thegenerally well-marked muscle attachments and therelative thickness of long bone shafts point to astrenuous lifestyle.

CNS-related fossil evidence. Endocranial: There areat least 27 neurocranial fossils preserving evidence ofthe H. neanderthalensis CNS. The mean adult endo-cranial volume for H. neanderthalensis is 1404 cm3

(n¼ 27; range 1172–1740 cm3). The EQ for H. nean-derthalensis is 4.7, smaller than that of H. sapiens.Neanderthals were often considered to have largercranial capacities than H. sapiens, but this hasrecently been reconsidered in light of new estimates(Holloway et al., 2004a, pp. 301, 304–305).Holloway et al. (2004a) suggest that Neanderthalshave an overall modern humanlike brain shape,although there is occipital bunning in many speci-mens. Similarities with modern human brain shape

include broad, round, vertical prefrontal lobes, andwide, full parietal lobes. In contrast, Bruner et al.(2003) argue that brain shape in Neanderthals followsarchaic (i.e., H. erectus and H. heidelbergensis) allo-metric trends for brain size expansion. In contrast,they suggest that modern humans show a differentpattern of brain growth that emphasizes expansion ofthe parietal lobes. Distinct petalias are the norm forNeanderthals. Many have very strong petalias,although not all specimens display the LORF pattern.One of the crania with an atypical petalia (LaFerrassie 1) also has a larger Broca’s area on theright than on the left, and in another (La Chapelle-aux-Saints), a usual LORF petalial pattern is com-bined with a right dominant Broca’s area. However,most have a modern humanlike pattern of Broca’sarea asymmetry.

Holloway et al. (2004a) suggest that, in all theNeanderthals they looked at, the LS is posterior tothe lambdoid suture, as it is in modern humans.They are most certain about the position of the LSin Monte Circeo I, where it is far posterior to thelambdoid suture. They are uncertain about theidentification of, or make indirect inferencesabout, the location of the LS in Le Ferrassie 1,La Quina 5, Neanderthal, Spy I, and Spy II. In LaChapelle-aux-Saints, Boule and Anthony (1911)had originally suggested the LS was anterior tothe lambdoid suture. This was disputed(Symington, 1916; Le Gros Clark et al., 1936),and Holloway et al. (2004a) point out thatBoule and Anthony (1911) misidentified the LS,and that the real LS is posterior to the lambdoidsuture. Holloway et al. did not look at theKrapina endocasts in detail, but they suggest thatthe Krapina specimens have more derived andmodern features than Western EuropeanNeanderthals. Holloway et al. (2004a, p. 235)consider that, in terms of their CNS morphology,H. sapiens and H. neanderthalensis should only beseparated at the subspecific level. Vertebral canal:At least four (Kebara, La Chapelle-aux-Saints,Shanidar 2, Shanidar 3) sets of Neanderthal fossilvertebras provide information about the size ofthe vertebral canal that transmits the spinal cord.Neanderthals resemble modern humans (and aredifferent from all earlier hominins) in havingenlarged thoracic vertebral canals relative tononhuman primates. Increased muscular controlassociated with speech may explain the increasein spinal cord size in the Late Pleistocene homi-nins (MacLarnon and Hewitt, 1999, 2004).

Behavioral interpretations. H. neanderthalensisis modern humanlike in terms of its endocranialvolume, inferred spinal cord dimensions, and

Au. afarensisAu. africanusH. ergasterH. neanderthalensisH. sapiens

R

2 = 0.8571

1.5

2

2.5

3

3.83.63.43.232.82.62.42.2

R

2 = 0.7646

1.5

2

2.5

3

5.45.254.84.64.44.24

log 1

0 m

inim

um th

orac

icca

nal C

SA

(m

m2 )

log10 endocranial volume (cm3)

log 1

0 m

inim

um th

orac

icca

nal C

SA

(m

m2 )

log10 body mass (g)(b)(a)

Figure 3 Log–log plots of minimum thoracic vertebral canal cross-sectional area (CSA) versus endocranial volume (a) and body

mass (b) for fossil hominin specimens. Fossil hominin endocranial volume sources are available from the authors, by request.

Thoracic CSA and body mass data are from MacLarnon and Hewitt (1999) and references therein.


brain organization. This, taken together withanatomy consistent with spoken language, andarcheological evidence of complex, possibly sym-bolic burial behavior, suggests that Neanderthalsshared with their early modern human contem-poraries many characteristics of modern humancognition. However, no Neanderthal remains areassociated with artifacts that can unequivocallybe interpreted as art, which would serve as undis-puted evidence of symbolic behavior. In contrast,contemporaneous early modern humans are asso-ciated with art throughout Europe by the time ofNeanderthals last appearance c. 28 kya, suggest-ing that these two hominin taxa differed in termsof culture and cognition (Klein, 1999). Theincrease in thoracic vertebral canal cross-sectional area from early to late hominins mightbe explained by the corresponding increase inendocranial volume. The only Neanderthal forwhich both measures are available, La Chapelle-aux-Saints, has the largest minimum thoracic ver-tebral cross-sectional area of any primatespecimen listed (253 mm2 at T6) and a very largeendocranial volume (1625 cm3) (MacLarnon andHewitt, 1999, 2004, p. 188). MacLarnon andHewitt’s conclusions are based on hominin valuescompared with a thoracic vertebral canal to bodysize scaling relationship for extant primates. Butdifferent taxa have different brain mass to bodymass scaling relationships (Holloway and Post,1982), and the relationship between brain sizeand spinal cord size is even more variable withinlarge taxonomic groups (MacLarnon, 1995). Awithin-hominin spinal cord to brain size scalingrelationship (or CNS scaling law) could accountfor the observed variation in spinal cord size (seeFigure 3a). Further, the pivotal specimen for theargument of MacLarnon and Hewitt is a single

H. ergaster specimen – a juvenile for which thegrowth trajectory is uncertain (see Coqueugniotet al., 2004, and references therein) and for whichthe small vertebral canal may be pathological(Ohman et al., 2002). This specimen sits on theregression line, and most hominin fossils plotabove it (see MacLarnon and Hewitt, 1999;Figure 3b). A best-fit line for thoracic vertebralcanal cross-sectional area against body mass forthe fossil hominin specimens is much steeper thanthat for all primates (Figure 3b). Therefore,Neanderthals and modern humans have thoracicvertebral canal cross-sectional areas that fallwithin the range predicted for a hominin of simi-lar brain size and body mass, although H. ergasterhas a smaller thoracic vertebral canal cross-sec-tional area than expected for its body mass.

Other endocranial morphology. Cranial venoussinuses: There is no evidence of an O/M sinus systemin any Neanderthal specimen (Falk, 1986).Meningeal vessels: In some Neanderthal crania (LeMoustier, Neanderthal, La-Chapelle-aux-Saints),the posterior branch of the middle meningeal arteryis as prominent as the anterior branch (Hollowayet al., 2004a). In other Neanderthals (Gibraltar 1and 2, Teshik Tash 1, Engis 2, La Ferrassie 1, LaQuina H 5), the anterior branch is more prominent,and is the source of the obelic branch, as is commonin modern humans. Both configurations found inNeanderthals were also found in EuropeanH. heidelbergensis (Holloway et al., 2004a).

4.18.4.6 Anatomically Modern Homo

This category includes all those specimens that lackthe autapomorphies of premodern Homo taxa,or which cannot be distinguished from livingH. sapiens.


Taxon name. Homo sapiens Linnaeus, 1758.Approximate time range. c. 190 kya to the present

day.Initial fossil discovery. With hindsight, the first

recorded evidence to be recovered was the Red Ladyof Paviland, found in Wales in 1822–23.

Type specimen. Linnaeus did not designate a typespecimen.

Source(s) of the evidence. Fossil evidence ofH. sapiens has been recovered from sites on all con-tinents except the Antarctic. The earliest absolutelydated remains are from Omo Kibish (McDougallet al., 2005) and Herto (White et al., 2003) inEthiopia. Taxonomic note: Researchers who wishto make a taxonomic distinction between fossilssuch as Florisbad, Omo 2, and Laetoli 18, and sub-recent and living modern humans refer the Africansubset to H. (Africanthropus) helmei (Dreyer, 1935).

Nature of the evidence. Many are burials so thefossil evidence is good, but in some regions of theworld (e.g., West Africa) remains are few and farbetween.

Characteristics and inferred behavior. Cranial:The earliest evidence of anatomically modernhuman cranial morphology in the fossil recordcomes from sites in Africa and the Near East. It isalso in Africa that there is evidence for a likelymorphological precursor of anatomically modernhuman morphology. This takes the form of craniathat are generally more robust and archaic-lookingthan those of anatomically modern humans yetwhich are not archaic enough to justify their alloca-tion to H. heidelbergensis or derived enough to beH. neanderthalensis (see above). Specimens in thiscategory include Jebel Irhoud from North Africa,Omo 2 and Laetoli 18 from East Africa, andFlorisbad and Cave of Hearths in southern Africa.There is undoubtedly a gradation in morphologythat makes it difficult to set the boundary betweenanatomically modern humans and H. heidelbergen-sis, but unless at least one other taxon (e.g.,H. neanderthalensis) is recognized the variation inthe later Homo fossil record is too great to be accom-modated in a single taxon. Postcranial: There arerelatively few early H. sapiens postcranial fossils.

CNS-related fossil evidence. Endocranial: Earlymodern H. sapiens have a mean endocranial volumeof 1463 cm3 (n¼ 79, range 1090–1880 cm3). TheEQ for early H. sapiens is 5.3. The mean brain massand EQ are within the range of recent modernhuman values. However, the extreme fossil endo-cranial volumes (when converted to brain masses,1133–1799 g) fall outside of the range for a sample(n > 227) of recent modern humans aged 20–30years (1239–1526 g).

Fossil modern humans are essentially modernhumanlike in shape and endocranial volume. TheJebel Irhoud crania (Jebel Irhoud 1 and 2) are alsoconsidered to be H. sapiens but are said to beNeanderthal-like in overall shape; for example, JebelIrhoud 2 has some occipital bunning, and theJebel Irhoud 1 cranium is low and broad. The twoJebel Irhoud endocrania show evidence of modernhumanlike brain morphology, including a LORFpetalial pattern, an asymmetrically enlarged leftBroca’s area, and a reduced primary visual cortex,plus taxonomic indicators not related to the CNS(mentioned below). As is the case of recent modernhumans, the manifestation of the LORF petalia pat-tern is variable. Cro-Magnon III, Dolni Vestonice 3 –and probably also Combe Capelle, and Brno 3 – havetypical LORF petalias. Predmosti 10 has one of themost extreme cases of the right-hander’s LORF peta-lial pattern, but there is no clear evidence of thispattern from the other specimens from the site(Predmosti 3, 4, and 9). Brno II has a reversed, left-hander’s pattern of right-occipital and left-frontalpetalias. Jebel Irhoud 1 and 2 provide the only evi-dence of asymmetrically enlarged left Broca’s capregions. The right side of Cro-Magnon III Broca’sarea is enlarged but the left is not preserved. Fossiland modern H. sapiens neurocrania are uniquelyglobular in shape (Lieberman et al., 2002), apparentlyhaving overcome constraints which cause H. nean-derthalensis and archaic (i.e., H. erectus andH. heidelbergensis) neurocranial shape to plot alongthe same allometric trajectory (Bruner et al., 2003).Expanded temporal and possibly frontal lobes inmodern humans possibly contribute to this morpho-logical change (Lieberman et al., 2002). Morerecently, it has been suggested that volumetricallyexpanded parietal lobes have consequences for overallbrain shape which contribute to the characteristicglobularity of the human brain (Bruner et al., 2003).In comparison to the brains of earlier Homo, themodern human brain is shaped such that the anteriorand posterior ends seem to approach each other frombelow. This is related to a decrease in relative endo-cranial length, a relative shortening of the frontal andoccipital poles, and displacement of the cerebellum toa more inferior position (Bruner, 2004). Weaver(2005) suggests that relative cerebellum size differsbetween fossil modern humans and recent modernhumans. The Early to Middle Pleistocene group(Au. africanus, P. boisei, H. habilis, H. rudolfensis,and H. erectus, H. heidelbergensis) does not differsignificantly from recent modern humans or fromthe great apes with respect to CQ values (Weaver,2005). However, the very low CQ values of theLate Pleistocene group (H. neanderthalensis and


H. sapiens) are significantly different from those ofthe Early to Middle Pleistocene group, the greatapes, and from recent humans (Weaver, 2005).The shift toward larger CQ values in recenthumans is said to be due to expansion of relativecerebellar size during a time of stasis in encephali-zation. Weaver suggests the cerebellum becameexpanded in recent humans to better manage thecomplex cognitive functions. However, this inter-pretation assumes that the Late Pleistocene grouprepresents the condition directly ancestral to recenthumans. The group with the lowest CQ values areLate Pleistocene hominins, which are all European,and the lowest value in the entire sample is fromthe Swanscombe specimen (CQ¼ 0.60). Thedecrease to the CQ values characteristic of theEuropean Middle–Late Pleistocene group may bedue to shared ancestry or geographical conver-gence, and it may not necessarily indicate thecondition which precedes that of recent humans.

Other endocranial morphology. Cranial venoussinuses: Jebel Irhoud 1 and 2, Kanjera 1, andPredmost II and X have evident dominant transversesinuses and no O/M system (Holloway et al., 2004a).Brno III has an enlarged O/M sinus on the right (itsleft side is strongly deformed), and Predmost IV hasevidence of an O/M sinus system on the right but noton the left. Skhul I has an O/M system on both sides.Meningeal vessels: The number of ramifications andanastomoses is increased from the ape-like level seenin H. erectus (Weidenreich, 1943, p. 13) to the char-acteristic modern human condition (Saban, 1984;Grimaud-Herve, 1994). The principal vessel of theanterior ramus has posterior ramifications whichrun parallel to it in H. erectus, but which becomemore oblique inferoposteriorly relative to the morerounded occipital of recent humans (Grimaud-Herve,1994). In modern humans, the anterior and obelicbranches are more developed, and the posteriorbranch is less developed – a pattern also seen inKNM-WT 15000. The anterior branch of the middlemeningeal artery is well developed in fossil AfricanH. sapiens, with numerous anastomoses in JebelIrhoud (1 and 2) and Omo 2. In some fossilEuropean H. sapiens, the obelic branch takes originfrom both the anterior and posterior branches(Predmost 3, Predmost 4 left side, Dolni Vestonice1, 2).

4.18.5 Trends in Hominin CNS Evolution

4.18.5.1 Primitive Brain Morphology

In order to determine whether a morphological fea-ture is primitive or derived within the hominin

clade, it is necessary to consider the brain morphol-ogy of the most recent hypothetical commonancestor of modern humans and living chimpanzees.The principle of parsimony suggests the panin–hominin ancestor possessed all shared derived fea-tures of extant humans and chimpanzees, but itwould lack those features acquired solely alongeither the panin or the hominin lineages. It is diffi-cult to reconstruct the panin–hominin ancestor withcertainty with respect to well-represented regions ofthe hard tissue fossil record, and it is particularlydifficult to do so for CNS-related morphology forwhich the extant and fossil evidence is both sparserand more difficult to interpret. For simplicity, wewill assume that the chimpanzee brain is equivalentmorphologically to the primitive hominin brain.There is no significant evidence for derived chim-panzee brain morphology which is not also sharedwith modern humans, although chimpanzees arelikely to have evolved CNS autoapomorphiesrelated to species-specific behaviors, which may bebrought to light by future hominoid comparativeneuroanatomical studies.

4.18.5.2 Modern Human or Hominin Lineage

4.18.5.2.1 Earliest appearance of derived modernhuman morphology The data suggest that,whereas fully modern human brain morphologyonly occurs in recent humans, some aspects of mod-ern human brain morphology are present in earlierforms (see Table 3).

The aspect of modern human brain morphologythat may have appeared earliest is the reduction ofthe primary visual cortex, as evidenced by the posi-tion of the LS. A posterior LS has been reported forsome Au. afarensis specimens, but at the least thisfeature is variable within the taxon. Given the smallsample it is difficult to tell whether the Au. afarensisbrain really is derived in the direction of the modernhuman brain, or whether it expresses variabilitysimilar to that seen in chimpanzees. In contrast,there are several aspects of endocast anatomyderived in the direction of modern humanlikebrain reorganization in Au. africanus, which hasbetter evidence for a reduced primary visual cortex.In addition, Au. africanus shows evidence of: (1) asomewhat expanded, blunt orbitofrontal cortex,(2) anteriorly expanded, laterally pointed temporalpoles, (3) an incipient LORF petalial pattern, and(4) a modern humanlike Broca’s cap region.Although these features are not as pronounced asin modern humans, they can be interpreted as beingderived in the direction of modern humans. TheLORF petalial pattern and Broca’s cap region

Table 3 Aspects of endocranial morphology and/or inferred CNS morphology

Taxon

FAD

(Mya)

Mean

endocranial

volume

(cm3) EQ

LORF

petalial

patterna

Fronto-

orbital

sulcusb

Orbital

surface of the

frontal lobec

Broca’s

cap

regiondNeurocranial

globularitye

Temporal

pole

morphologyf

Lunate

sulcus

positiong

Relative

size of

cerebellum

(CQ)h

Thoracic

vertebral

canal i

Pan troglodytes (M) 1.6

Pan troglodytes (F) 1.9 P P P P P P P 1.2 P

Recent H. sapiens (M) 5.1

Recent H. sapiens (F) 5.4 M M M M M M M 1 M

S. tchadensis 7 365 – – – – – – – – –

O. tugenensis 6 – – – – – – – – –

Ar. kadabba 5.8 – – – – – – – – –

Ar. ramidus 4.5 – – – – – – – – –

Au. anamensis 4.2 – – – – – – – – –

Au. afarensis 3.9 446 2.5 I – – P – – P/M – P

K. platyops 3.5 – – – – – – – – –

Au. bahrelghazali 3.5 – – – – – – – – –

Au. africanus 3 460 2.8 m P m m – m M 0.8 P

Au. garhi 2.5 450 – – – – – – – – –

P. aethiopicus 2.5 410 m – P – – P – – –

P. boisei s.s. 2.3 488 2.5 m – P – – P M 1 –

P. robustus 2 533 3.1 I – P – – P M – –

H. habilis s.s. 2.4 609 3.7 P P – I – – – 1 –

H. rudolfensis 1.8 776 3.2 M M – M – – – 0.9 –

H. ergaster 1.9 763 2.8 M – – I – – – 0.9 P

H. erectus s.s. 1.8 991 3.9 M – – M P – M 0.9 –

H. antecessor 0.7 – – – – – – – – –

H. heidelbergensis 0.6 1242 4.2 M – – M P – M 0.8 –

H. neanderthalensis 0.2 1404 4.7 M – – M P – M 0.7 M

H. sapiens s.s. 0.19 1463 5.3 M – – M M – M 0.7 M

H. floresiensis 0.090 417 3.1 M M M I – M – –

aLORF (left occipital right frontal) petalial pattern (P) infrequent, rarely involves both frontal and occipital lobes; (M) usual.bFronto-orbital sulcus (P) present; (M) absent.cOrbitofrontal region (P) beak-shaped; (M) blunt and expanded.dAsymmetrical Broca’s area (P) not asymmetrically enlarged; (M) L>R asymmetry.eEndocast shape (P) archaic; (M) globular, suggests expanded parietal.fTemporal pole morphology (P) rounded; (M) anteriorly expanded, laterally pointed.gLunate sulcus position (P) anterior (some variability); (M) more posterior.hTaxon mean EQ (encephalization quotient) values, calculated from specimen CQ (cerebellar quotient) values (LSR-05 in Weaver, 2001).iThoracic vertebral canal cross-sectional area (P) size expected for a primate of similar body mass; (M) larger than expected for a primate of similar body mass.

–, No relevant evidence; I, insufficient evidence; M, modern humanlike morphology either described or inferred; m, incipient modern human morphology either described or inferred; P, Pan-

like morphology either described or inferred.

Pan-like (P) and modern humanlike (M) morphology (please refer to text for a more detailed explanation).


become even more modern in H. rudolfensis, theearliest taxon for which there is evidence forhumanlike brain organization (there are insufficientdata for the other three aforementioned featuresuntil later Homo). In addition, H. rudolfensis isthe earliest taxon not to have an orbitofrontal sul-cus. Interestingly, there is no good evidence for amodern humanlike LORF petalial pattern and aBroca’s cap region in H. habilis; indeed, there isevidence of an African ape-like orbitofrontral sul-cus. Where data exist, H. erectus and H. ergasterendocasts tend to share the modern humanlikefeatures that are found in H. rudolfensis. H. nean-derthalensis is the earliest taxon known to have anexpanded thoracic vertebral canal. A globular braindue to parietal lobe expansion has been proposed asan autoapomorphy of modern humans (Bruneret al., 2003). An increase in relative cerebellumsize from fossil to recent anatomically modernhumans might be a final refinement within thisspecies.

4.18.5.2.2 Earliest appearance of increase in abso-lute and relative brain size Modern human meanbrain mass for adults 21–39 years old is 1450 g formales, and 1290 g for females (Figure 4, Table 4)(Dekaban and Sadowsky, 1978). The chimpanzeemean brain weight for adolescents and young adults(7–30 years) is 406 g for males and 368 g for females

250

350

450

550

650

750

850

950

1050

1150

1250

1350

1450

1550

1650

1750

4.003.002.001.000.00

FAD (Mya)

Bra

in m

ass

(g)

Figure 4 Chimpanzee and recent modern human male and femal

showing ranges within two standard deviations. Fossil hominin bra

showing range within two standard deviations from the mean. FAD

(Herndon et al., 1999). In both species, average brainmass decreases in older individuals; for example,Dekaban and Sadowsky (1978) reported a 7.4%decrease (approximately 100 g) in modern humanbrain mass between 20–30 years and 70–80 years.In fact, the mean endocranial volumes from a moretypical modern human autopsy data set (average age65 years) are dramatically different (male¼ 1308 g,female¼ 1179 g) (Zilles, 1972). Sex is also an impor-tant consideration in brain size comparisons becausemale and female samples of hominoid taxa have sig-nificantly different brain sizes. It is not possible toknow the sex of fossil specimens, and statisticalmethods of sexing are not possible for the smallearly hominin cranial samples. Therefore, fossiltaxa are not assigned to sex, but are compared aswhole taxon samples to samples of both sexes ofextant taxa. Previously, absolute brain size has beenused to determine a cerebral Rubicon criterion forinclusion in the genus Homo, variably set between600 and 800 cm3 (Leakey et al., 1964). Currently,absolute brain size is thought to lack biological sig-nificance, since it does not give an indication ofdegree of encephalization, or the number of extraneurons (Jerison, 1973; Martin, 1990). However,aspects of brain morphology such as brain compo-nent volumes and degree of gyrification scale toabsolute brain size (Zilles et al., 1988, 1989;Semendeferi and Damasio, 2000; Semendeferi et al.,

7.006.005.00

Chimpanzee mean (M)

Chimpanzee mean (F)

S. tchadensis

Au. garhi

P. aethiopicus

H. antecessor

Au. afarensis

Au. africanus

P. boisei

P. robustus

H. habilis

H. erectus

H. ergaster

H. heidelbergensis

H. floresiensis

Modern human mean (M)

Modern human mean (F)

H. rudolfensis

H. neanderthalensis

H. sapiens

e brain mass means are plotted, with y-axis bars and dashed lines

in mass individual specimen values are plotted with y-axis bars

, first-appearance datum. For more information, see Table 4.

Table 4 Absolute and relative brain sizes for fossil and extant panin and hominin taxa

TaxonaFAD

(Mya)

Number in

sample

Mean

endocranial

volume

Minimun

endocranial

volume

Maximum

endocranial

volume

Mean

brain

massbMinimum

brain mass

Maximum

brain mass

Brain

mass

SD

Mean

body

mass EQc

Pan troglodytes (M) 17 406 347 530 39 58 1.6

Pan troglodytes (F) 17 368 308 458 37 43 1.9

Recent H. sapiens (M) 351 1450 1343 1526 20 70 5.1

Recent H. sapiens (F) 201 1290 1239 1366 30 57 5.4

S. tchadensis 7 1 365 363

Au. afarensis 3.9 5 446 387 550 442 385 542 69 38 2.5

Au. afarensis (M?) 2 521 492 550 514 486 542 40 45 2.6

Au. afarensis (F?) 3 396 387 400 393 385 397 7 29 2.7

Au. africanus 3 9 460 428 515 455 424 508 33 34 2.8

Au. garhi 2.5 1 450 446

P. aethiopicus 2.5 1 410 407

P. boisei 2.3 10 488 400 545 483 397 537 43 41 2.5

P. robustus 2 4 533 450 650 525 446 638 82 36 3.1

H. habilis 2.4 6 609 509 687 599 503 674 60 33 3.7

H. rudolfensis 1.8 3 776 750 825 758 734 805 41 55 3.2

H. ergaster 1.9 6 763 600 900 746 590 877 111 64 2.8

H. ergaster (Africa) 3 851 804 900 830 785 877 46 64 3.1

H. ergaster (Dmanisi) 3 675 600 775 662 590 758 86

H. erectus 1.8 36 991 727 1260 963 712 1218 134 58 3.9

H. antecessor 0.7 1 1000 972

H. heidelbergensis 0.6 21 1242 880 1450 1200 858 1397 131 71 4.2

H. neanderthalensis 0.2 27 1404 1172 1740 1353 1135 1669 153 72 4.7

H. sapiens 0.19 79 1463 1090 1880 1408 1057 1799 124 64 5.3

H. floresiensis 0.090 1 417 414 26 3.1

aSources: Chimpanzee brain and body mass data for individuals 7–30 years from Herndon et al. (1999). Recent modern human brain and body mass data for adults 21–39 years (except

minimum and maximum brain mass, which are for 20–30 years) from Dekaban and Sadowsky (1978). In both data sets, brain mass is taken from fresh autopsy specimens and includes brain

tissue as well as leptomeninges and CSF. Fossil hominin endocranial volume raw data and sources are available from the authors, by request.bFossil endocranial volumes were converted into brain masses after Ruff et al. (1997).cEQ (encephalization quotient) values after Martin (1981), and Ruff et al. (1997). Extant taxon EQ values are means of individual EQ values. Fossil taxon sample mean EQ values are obtained

from each taxon’s mean brain mass and mean body mass estimates (SD, standard deviation). EQ values obtained by either method are very similar and have been used interchangeably (e.g.,

Ruff et al., 1997).


2002; Weaver, 2005), an important considerationwhen investigating the evolution of the brain of mod-ern humans.

The smallest adult hominin brain belongs to thesingle cranial specimen of Sahelanthropus, the ear-liest possible hominin, and its endocranial volumefalls slightly below the female chimpanzee mean.Single specimens of P. aethiopicus, Au. garhi, andH. floresiensis plot around the male chimpanzeemean. The Au. afarensis sample is not significantlydifferent from the combined sex sample of chimpan-zees (p¼ 0.093), nor from the male chimpanzeesample (p ¼ 0.456), although it is significantly lar-ger than the female chimpanzee sample (p ¼ 0.011)(all statistical comparisons are derived from aKruskal–Wallis test of significance). The Au. africa-nus sample is significantly different from thecombined sex sample (p< 0.001), and the male(p¼ 0.001) and female (p< 0.001) subsamples ofchimpanzees. However, this does not suggest thatthe brain size of Au. africanus is significantlyincreased relative to chimpanzees and that ofAu. afarensis is not; these two groups do not differsignificantly from each other (p ¼ 0.385). Althoughthe Au. africanus mean value (455 g) is only slightlylarger than that for Au. afarensis (442 g), the rangefor Au. africanus is much smaller than that for thesexual dimorphic Au. afarensis (but see Reno et al.,2005 for an alternative interpretation that suggestsonly modest levels of sexual dimorphism inAu. afarensis). Au. afarensis attains higher indivi-dual brain mass estimates than Au. africanus.

Early hominin fossil crania for which endocranialvolume and body mass have been reliably estimatedare extremely rare, making it impossible to do com-parative statistical tests of EQs. However, given thatearly fossil hominins (e.g., Australopithecus andParanthropus) have smaller estimated body massesthan chimpanzees (mean body mass 58 kg for males,43 kg for females; Herndon et al., 1999), any signifi-cant increase in relation to chimpanzee brain volumecan be assumed to be an increase in both absoluteand relative brain size (Table 4). Thus, the increasefrom the brain size of a chimpanzee-like hypotheticalcommon ancestor to brains the size of those belong-ing to Au. afarensis and Au. africanus is evidence ofan increase in relative brain size. This finding isfurther evidenced by the EQ values of Au. afarensis(2.5) and Au. africanus (2.8), which are well abovethose for chimpanzees (male EQ¼ 1.7, femaleEQ¼ 1.9), overlapping with those of Paranthropus(P. boisei EQ¼ 2.5; P. robustus EQ¼ 3.1), andapproximating that of H. ergaster (2.8).

By the appearance of H. rudolfensis and H. habi-lis, both absolute and relative brain size have clearly

departed from the Pan-like condition. H. habilis isthe smallest-brained hominin for which all the speci-men values fall outside of two standard deviationsof the male chimpanzee mean. H. habilis andH. rudolfensis are significantly different in brainmass (p ¼ 0.02), and the entire range of H. rudol-fensis values plot above the range of H. habilisvalues. However, when the brain mass data areseen in the light of body mass data, H. habilis(EQ ¼ 3.7) is more encephalized than H. rudolfensis(EQ ¼ 3.2). Relative brain mass in both H. habilisand H. rudolfensis is greater than that inAustralopithecus and Paranthropus, and itapproaches the values for H. erectus (EQ ¼ 3.9).

In summary, although encephalization in thehominin lineage might have begun as early asAu. afarensis, it was evident in Au. africanus (inparallel to the encephalization of Paranthropus,see Section 4.18.5.3) and definitely by the time ofthe appearance of H. habilis and H. rudolfensis.

4.18.5.2.3 Appearance of derived modern humanCNS morphology in relation to brain size Althoughthere are hints of a trend toward a modern humanlikerelative brain size and brain morphology in Au. afar-ensis, there is a lot of variability in the size andmorphology of this taxon. Given small samples, onecannot be certain whether or not this variation isdifferent from the variation seen in chimpanzees.Further, the functional and adaptive significance ofthese features in the early taxa is questionable.Modern humanlike endocranial anatomy in Au. afar-ensis might be a pre-adaptation which only acquires itsmodern functions in Au. africanus, H. rudolfensis, orin even later hominins.

Most aspects of modern humanlike endocastmorphology make an appearance in Au. africa-nus, but they do not yet show the fully modernform. The reason for their occurrence in thistaxon is uncertain, but might be influenced bybrain size increase, and it is quite possibly relatedto exceptional preservation of brain morphologyin this taxon. The appearance of several aspectsof modern brain morphology in Au. africanuscomplement the fact that this taxon is the firstto have a brain size significantly different fromchimpanzees. However, as a whole, the Au. afri-canus brain still differs considerably from themodern human brain, and any similarities arenot considered sufficient to suggest a modernhumanlike cognitive capacity or behavior forAu. africanus.

This is in contrast to the more modern humanlikebrain morphology of H. rudolfensis which is gener-ally taken as evidence of more modern humanlike


cognitive capacities. Most notably, these featuresare suggestive of language ability and right-handed-ness, coincident with the first stone tools whichapparently were made by right-handed hominins.This is associated with the earliest brain massesoutside of what is expected for a chimpanzee, andan EQ higher than that of earlier taxa. However,H. habilis has a higher EQ than H. rudolfensis,and this later appearing hominin also has brainmass values outside of what is expected for achimpanzee. It is not yet possible to tell whetherthe more modern humanlike brain morphology ofH. rudolfensis, compared to H. habilis, is, or isnot, size-related.

4.18.5.3 Brain Evolution in Other Lineages

The P. boisei mean value (483 g) for estimated brainmass is larger than the value for P. aethiopicus(407 g) and somewhat larger than the means forAu. africanus (455 g) and Au. afarensis (442 g).Further, the majority of the P. boisei specimens falloutside of two standard deviations of the male chim-panzee mean. Therefore, it is inferred that P. boiseihas increased its absolute brain size relative to theprimitive condition. The P. boisei sample mean isnot significantly different (p ¼ 0.357) from that ofthe later occurring P. robustus sample, even thoughthe latter attains a much higher maximum value(638 g) and has a much higher mean (565 g).P. boisei and P. robustus have EQs that are higherthan those for male and female chimpanzees.However, the P. boisei EQ is smaller than that ofAu. africanus and is similar to the Au. afarensisvalue. Given the lack of postcranial evidence, onecannot be certain that EQ has increased fromP. aethiopicus to later Paranthropus taxa. Thesedata are, however, consistent with the suggestionof a temporal trend for brain size increase withinthe Paranthropus lineage (Elton et al., 2001).

There is little evidence to suggest modernhumanlike reorganization of the Paranthropusbrain. In particular, slight LORF petalial patternsare found in P. aethiopicus and P. boisei, and aposteriorly positioned LS has been identified inP. boisei. The evidence does not suggest that theParanthropus brain becomes increasingly modernhumanlike over time, as is the case for Homo.Further, Paranthropus retains ape-like beak-shapedorbital surface of frontal lobe and rounded temporalpoles, differentiating it from Au. afarensis andH. sapiens. The modern humanlike endocranial fea-tures seen in Paranthropus most likely reflect ashared ancestry with the modern human lineage.Similarly, brain size increase in Paranthropus is

probably the continuation of a trend beginning in acommon ancestor of Paranthropus and modernhumans.

There is presumed to be a decrease in absoluteand relative brain size in H. floresiensis (Brownet al., 2004), but this trend might also apply toother fossil hominin taxa. H. floresiensis had a tinybrain (414 g), with an EQ (3.0) much lower thanthat of its presumed closest fossil relative, H. erec-tus. Interestingly, its EQ is higher than the one listedhere for H. ergaster (2.8, includes Dmanisi) and onlyslightly lower than the EQ for African H. ergaster(3.1). Body mass estimates obtained from Dmanisipostcranial remains will refine the H. ergaster EQ.Given that H. ergaster is thought to have expandedoutside of Africa, evidence from the relative brainsize alone suggests that it, rather than H. erectus,may be the sister taxon of H. floresiensis. If so, thiswould indicate that EQ did not actually decrease inH. floresiensis, thereby solving one of the majorpuzzles of this taxon (Brown et al., 2004). It isnoted that H. floresiensis possesses much morphol-ogy that is derived from the primitive ape-likecondition. Several of these features are thought tobe found in the most recent H. floresiensis–modernhuman common ancestor (which may also be themost recent H. erectus–modern human commonancestor).

Brain size increase and the appearance of someaspects of modern humanlike brain morphologyoccur in at least two hominin lineages. BothParanthropus and Homo have absolutely and rela-tively larger brains than Australopithecus.However, only in Homo does brain size increaseoccur in parallel with the acquisition of modernhumanlike brain morphology. Interestingly, H. flor-esiensis provides striking evidence that, even withinHomo, estimated brain mass and inferred brainmorphology can become disassociated.

Acknowledgments

We thank the Henry Luce Foundation, the GWAcademic Excellence Initiative, the NSF IGERTProgram, and NSF DIG No. 01-113 for support.

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Zollikofer, C. P. E. 2002. A computational approach to paleoan-thropology. Evol. Anthropol. Suppl. 1, 64–67.

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Zollikofer, C. P. E., Ponce de Leon, M. S., Lieberman, D. E., et al.2005. Virtual cranial reconstruction of Sahelanthropus tcha-densis. Nature 434, 755–759.

Further Reading

Allman, J. M. 2000. Evolving Brains. Scientific American

Library.

Bruner, E. 2003. Fossil traces of the human thought:Paleoneurology and the evolution of the genus Homo. Riv.Antropol. 81, 29–56.

Falk, D. 2004. Hominin brain evolution: New century, new

directions. Coll. Antropol. 2, 59–64.Wood, B. 2005. Human Evolution: A Very Short Introduction.

Oxford University Press.

4.18 the hominin fossil record, emergence of the modern cns

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