4.18 The Hominin Fossil Record, Emergence of The Modern CNS

4.
18 The Hominin Fossil Record and the Emergence of the Modern Human Central Nervous System
A de Sousa and B Wood, The George Washington University, Washington, DC, USA
2007 Elsevier Inc. All rights reserved.
4.18.1 Introduction 4.18.2 How can Fossil Evidence Be Used to Reconstruct the Recent Evolution of the Modern Human CNS? 4.18.2.1 Fossil Evidence Relevant for Reconstructing the Size and Shape of the Brain 4.18.2.2 Data Interpretation 4.18.2.3 Brain Size Measures and Estimates 4.18.2.4 Comparing Different Types of Measurements and Estimates 4.18.2.5 Indices for Estimating and Comparing the Relative Sizes of Brains 4.18.2.6 Major Lines of Fossil Evidence for CNS Evolution, Plus Other Endocranial Morphology 4.18.3 The Hominin Fossil Record 4.18.3.1 Defining Hominins 4.18.3.2 Terminology 4.18.3.3 Organizing the Hominin Fossil Record 4.18.3.4 Review of Individual Hominin Fossil Taxa 4.18.4 Review of Hominin Taxa 4.18.4.1 Possible and Probable Primitive Hominins 4.18.4.2 Archaic Hominins 4.18.4.3 Megadont Archaic Hominins 4.18.4.4 Transitional Homo 4.18.4.5 Premodern Homo 4.18.4.6 Anatomically Modern Homo 4.18.5 Trends in Hominin CNS Evolution 4.18.5.1 Primitive Brain Morphology 4.18.5.2 Modern Human or Hominin Lineage 4.18.5.3 Brain Evolution in Other Lineages
292 292 292 294 294 297 297 299 302 302 302 303 304 305 305 307 311 314 316 322 324 324 324 329
Glossary
anatomically modern human Hominin fossil evidence that cannot be distinguished from the skeletal remains of contemporary modern humans. The average density of the brain. The volume of the brain itself (i.e., brain volume minus the volume of the CSF within the ventricles of the brain and the volume of any meninges and cranial nerves that may adhere to the brain). Usually defined as the sum of the volume of the whole brain (including the ventricles) plus the leptomeninges clade (Gk. clados Branch)
brain specific mass brain tissue volume
encephalization (syn. cephalization, ce phalisation)
encephalization quotient (EQ)
brain volume
endocranial cast
(i.e., the arachnoid and pia mater). A grouping of taxa that contains no more and no less than all the descendants of the groups most recent common ancestor. The process by which, for a given taxon, relative brain size becomes larger than predicted from the general scaling relationship between brain size and body size. The ratio of the observed brain size over the expected brain size, based on a general scaling relationship. A natural or artificial cast that uses the walls, roof, and floor of the cranial cavity as a mold.
292 The Hominin Fossil Record and the Emergence of the Modern Human CNS endocranial volume (syn. cranial capacity, endocranial capacity) The volume of the endocranial cavity. This is the sum of brain volume plus the volumes of the meninges, the extracerebral CSF (i.e., the CSF outside the ventricles), the intracranial (but extracerebral) vessels, and the cranial nerves within the cranial cavity. Vernacular for a species (or an individual specimen belonging to a taxon) within the tribe Hominini (e.g., Paranthropus boisei is a hominin taxon and KNMER 1470 is a hominin fossil cranium). The meningeal arteries and veins that supply blood to, and drain most of the blood from, the neurocranium and the dura mater. The greater anterior, posterior, or lateral protrusion of one cerebral lobe relative to the other. Fibrous joint between two bones of the cranial vault. The fibrous tissue in these joints gradually disappears as the bones fuse together. 3-D digital cast of the neurocranial cavity, created using 2-D computed tomography slices.
hominin (L. homin Man)
meningeal vessels
petalia
suture (L. sutura A Seam)
humans, and outlines the organization of the hominin fossil record. The third section reviews each of the fossil hominin species. It uses a relatively speciose hominin taxonomy, but it also indicates how the same fossil evidence would be arranged if it were grouped into a smaller number of more inclusive taxa. Brief descriptions of each taxon are provided. There are two reasons why this section concentrates on the craniodental evidence. The first relates to the relative durability of the hard tissues of the head and neck of higher primates. Because they are generally hard and dense, they tend to preserve in larger numbers than do the bones of the limbs and trunk. This means that most species are defined on the basis of a set of distinctive craniodental traits. The second reason is that because, in this article, we focus on how the quality and scope of the fossil evidence for each taxon can contribute to our knowledge about the recent evolutionary history of the modern human CNS, this inevitably means emphasizing the cranial evidence. The fourth section of the article summarizes trends in the evolution of the hominin CNS. It summarizes the differences between the CNSs of modern humans and chimpanzees, and makes predictions about the CNS of the common ancestor of chimpanzees and modern humans. It addresses, among others, the following questions: 1. When did hominin brain size begin to increase beyond the levels we see in contemporary nonhuman higher primates? 2. At what stages in hominin evolution do we see grade shifts in brain morphology? 3. Were changes in brain size and shape restricted to our own genus, or did they occur in other hominin genera?
virtual endocast
4.18.1 Introduction
This article focuses on what the fossil evidence for human evolution can tell us about the evolution of the modern human central nervous system (CNS). Its scope is the hominin clade, which extends in time from the hypothetical common ancestor of chimpanzees and modern humans, via the appearance of the first hominins (c. 85 Mya), to the emergence a little over 190 kya ago of anatomically modern humans. We use the term hominin for modern humans and all extinct species that are more closely related to modern humans than to any other living taxon, and the term panin for living chimpanzees and all extinct species that are more closely related to chimpanzees than to any other living taxon. The first section reviews the ways in which the fossil and archeological records can be used to help reconstruct the CNS of extinct hominin taxa. The second section reviews the relationships of modern
4.18.2 How can Fossil Evidence Be Used to Reconstruct the Recent Evolution of the Modern Human CNS?
4.18.2.1 Fossil Evidence Relevant for Reconstructing the Size and Shape of the Brain
The biggest obstacle to understanding the evolution of the human CNS is that the CNS is not preserved in the hominin fossil record. However, inferences can be made about the size and shape of the CNS from natural endocasts, from the fossilized morphology of the neurocranium, the cranial base, and the axial skeleton. Endocasts and neurocranial fossils convey information about the size, shape, external convolutional morphology, and blood supply of the brain. Cranial base morphology contains information about the brainstem, and the cranial
The Hominin Fossil Record and the Emergence of the Modern Human CNS
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nerves and blood vessels that perforate it. Finally, the neural canal conveys information about the spinal cord which extends in adult modern humans from the atlas (C1) to the first (usually) or second lumbar vertebras. Across primate species, the crosssectional area of the vertebral canal provides an indication of spinal cord dimensions particularly in its most rostral aspect, but less so more caudally where a greater proportion of the canal is devoted to spinal nerves (MacLarnon, 1995). Although endocasts look remarkably brain-like, an endocast is not a fossil brain, but rather a cast of the neurocranial cavity. A natural endocast is formed during fossilization as the cranial cavity fills with fine sediments that enter through the various foramina and fissures that perforate the floor of the cranial cavity. Similarly, a synthetic endocast is made by stopping these perforations and then lining the inner surface of the endocranial cavity with quick-drying latex. Once dry, the thin layer of flexible latex can be peeled off the endocranial surface and removed through the foramen magnum. It is also possible to create a three-dimensional (3-D) digital cast of the neurocranial cavity, called a virtual endocast, and this has become the method of choice for investigating delicate and/or fragmentary fossils (e.g., Falk et al., 2005; Zollikofer et al., 2005). Endocasts potentially preserve details of the convolutional morphology of the surface of the cerebral and cerebellar hemispheres that are imprinted through the three layers of meninges (from outside in: the dura, arachnoid, and pia mater). In addition, endocasts preserve the imprints of blood vessels and skeletal sutures. Convolutional details are not always well preserved. The differential imprinting of convolutional detail may be due to taphonomy, the relative size of the brain, and the effects of ontogeny. In general, natural endocasts produce more details than synthetic endocasts. Falk (1980a) proposed two explanations for this: (1) natural endocasts may begin to form before the dura mater has fully disintegrated, so that any details present on it, but absent on the endocranial surface of the inner table of the neurocranium, are preserved; and (2) synthetic endocasts are often produced from crania that have been reconstructed from fragments, and the process of reconstruction can introduce morphological noise. The relatively small-brained Australopithecus endocasts are usually more detailed than endocasts made from crania assigned to larger-brained later Homo taxa. It is noteworthy that, for various groups of mammals, those with the largest brains within that group 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 endocranial volume increases more rapidly than brain size increases within primates (Martin, 1990, pp. 365, 392). The intensity of gyral impressions is also related to ontogeny. In modern humans there are few or no impressions on the endocranial aspect of the cranial vault before 1 year (Du Boulay, 1956). Gyral impressions are probably most marked during adolescence, and with increasing age basal markings become more prominent whereas vault impressions become fainter (Connolly, 1950, p. 291). The convolutional details of endocasts are notoriously difficult to interpret (Symington, 1916; Holloway, 1966). A feature might be the impression of a sulcus, or a blood vessel, or a skeletal suture, or it might be an artifact, and observers might offer genuinely different interpretations of what the same feature represents (Connolly, 1950; Falk, 1980a). For example, over the last three decades, Holloway and Falk have been providing often conflicting interpretations of the same endocasts. Only a handful of researchers study the details of endocast morphology, and both Falk and Holloway have called on other paleoanthropologists to join the debate (Falk, 1987; Holloway et al., 2004a). Not all researchers are convinced that the detailed morphology of endocasts has functional relevance. Many paleoneurologists take it for granted that sulci delimit functional or somatotopic cortical areas (see Radinsky, 1972, and references therein). However, it has become clear that the primate brain exhibits a substantial amount of intraspecific variability in sulcal anatomy and cytoarchitectural boundaries (Geyer et al., 2001; Rademacher et al., 2001). In some cases, the relationship between sulcal landmarks and functional areas is maintained within a species (Holloway et al., 2003), but in others it varies within species (Sherwood et al., 2003). It might not be possible to make detailed interpretations of brain function from endocasts alone. Information about fossil hominin brain evolution is not limited to the hard-tissue fossil record. Natural endocasts are a form of trace fossil that record, often in unusual detail, the endocranial morphology of an individual. Archeologists also claim that artifacts reveal information about the evolution of the hominin CNS. Tools, art, and other artifacts found in association with hominin remains provide direct evidence of the capacity of a species for specific behaviors, something that fossils cannot reveal. The combination of paleontological and archeological evidence provides more insight into the brain function of fossil hominins than either of these two lines of evidence could generate on their own.
294 The Hominin Fossil Record and the Emergence of the Modern Human CNS 4.18.2.2 Data Interpretation
In a specimen of an extant taxon, the size and shape of the brain can be estimated from either the brain itself or, indirectly, from cranial measurements. In a fossil specimen, measurements are taken from either an endocast (natural or synthetic) or from a fossil neurocranium. In general, the same measurement methods are used for endocasts and whole brains, and similar methods are applied to extant and fossil neurocrania. However, there are several reasons why data taken from contemporary taxa and data taken from fossil specimens might not be comparable and suggestions have been made to correct for the discrepancies. First, it is important to appreciate that the volume of an endocast is the volume of the neurocranial cavity (i.e., endocranial capacity or endocranial volume). Endocranial volume includes not only the volume of the brain, but also the space occupied by meninges, extracerebral cerebrospinal fluid (CSF), and cranial nerves. Second, all fossils, including endocasts and cranial fossils, are imperfect representations of the hard tissues they represent. Problems include incompleteness and plastic deformation. Incomplete fossils require that assumptions are made about the size and shape of the missing parts, and deformation may be difficult to detect when the form of the undeformed brain is unknown. Matrix can fill and widen cracks, expanding the size of the fossil beyond the size of the original bone. Virtual methods have recently been developed to correct for such deformation. Third, even well-preserved fossils present sampling problems that affect interspecific comparisons. For example, we do not know the chronological age of individual fossils, yet if the individual is immature it may be necessary to estimate the size of the equivalent adult. However, ontogenetic age is difficult to estimate even in extant animals, let alone in a fossil species for which we will never have a satisfactory reference sample. In addition, sexual dimorphism may introduce substantial variation in brain volume within a species. In hominin species with a sparse fossil record, overrepresentation of a particular sex might give an inaccurate impression of the species true mean and range of brain size.
4.18.2.3 Brain Size Measures and Estimates
cited in the literature and found that for this relatively complete Paranthropus boisei fossil cranium 15 different endocranial volume estimates are given ranging from 500 to 750 cm3. Holloway (1983b) has devised a useful system for indicating the reliability of endocranial volume measurements which uses a letter code for the method used and a number code for the reliability of the measurement. 4.18.2.3.1 Measurements of the volume of a brain or of a solid endocast by water displacement The preferred way to determine the volume of a brain or an endocast, natural or artificial, is by water displacement according to Archimedes principle. For extant species this is done using postmortem brains, but how well does this method measure brain size? For postmortem samples, one or more of the following confounding factors needs to be taken into account: time from death to measurement, time from death to fixation, fixation method and preparation prior to measurement, whether the leptomeninges and CSF are included, adequacy of dissection, and shrinkage. For example, what Stephan and others (Stephan et al., 1970, 1988; Stephan, 1981) call brain weight includes meninges, hypophysis, and any nerves still attached to the brain (Heiko Frahm, personal communication). Similarly, the largest brain mass data sets for modern humans (Dekaban and Sadowsky, 1978) and chimpanzees (Herndon et al., 1999) include leptomeninges and CSF in the brain mass estimates. Jerison (1973) estimates that the effect of including or excluding variables such as these can cause measurements to differ by as much as 20%. Holloway et al. (2004a, 2004b) found that weighing the water displaced by an endocast was a more consistent method than measuring its volume. Volumes measured using artificial endocasts might be underestimates of the true volume because endocasts are likely to have undergone shrinkage (Gingerich and Martin, 1981; Broadfield et al., 2001). 4.18.2.3.2 Measurements of the volume of the endocranial cavity 4.18.2.3.2.(i) Packing methods Packing methods involve filling the cranial cavity with small particles such as mustard seed, sintered glass beads, or shotgun pellets, and then determining the volume of the packing material. Different types of fillers can produce slightly different endocranial volume estimates (Miller, 1991). For fossil crania, packing methods are sometimes preferred over water displacement of a latex endocast because the problem of endocast shrinkage is avoided. However, because of
The brain sizes of fossils can be obtained from a variety of methods that vary in their accuracy and precision. For example, de Miguel and Henneberg (2001) reviewed the brain size estimates for OH 5
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variation in techniques for settling the packing material, these methods almost certainly underestimate the true endocranial volume (Gould, 1978, 1996). 4.18.2.3.2.(ii) Filling methods Filling methods are like packing methods, but involve a fluid rather than a solid. Uspenskii (1954) describes a method in which a rubber balloon is put into the cranial cavity and then filled with water. Similar values (mean difference 1.67 cm3) were obtained with this method and with water displacement, but packing with millet seed resulted in smaller (mean difference 65.4 cm3) values than those obtained using the balloon method (Uspenskii, 1954). 4.18.2.3.3 Estimating volumes from slices 4.18.2.3.3.(i) Cavalieris principle Using Cavalieris principle, it is possible to produce an unbiased estimate of total brain volume from measurements of the cross-sectional area of a sample of brain sections (Stephan, 1981, p. 3; Gundersen and Jensen, 1987). Cavalieris principle can be used to determine brain volume from actual and virtual brains. Serial sections of brains mounted onto slides undergo shrinkage as a result of fixation and embedding, so volume measurements determined from slidemounted sections need to be corrected accordingly. In early papers, the effect of shrinkage was overlooked. Stephan (1981) advised researchers to generate an individual conversion factor (Cind) for a brain with known mass and known volume: Cind Volume of fresh brain : Serial section volume
are enough to yield reliable estimates of mean brain volume, with a coefficient of error (CE) of approximately 5% (Mayhew and Olsen, 1991). The CE decreases as the number of slices increases (e.g., for 28 slices, CE < 1%). There are several advantages to using in vivo MRI volumes over autopsy brain volumes. In vivo MRI brain volumes avoid biases inherent to using autopsy brains; for example, autopsy brain samples overrepresent aged individuals. In vivo MRI volumes are not affected by changes in brain volume due to the elapsed time between death and measurement or fixation. Peters et al. (1998) compared the results of cross-sectional studies in which human brain volumes were obtained either in vivo by MRI (or nuclear magnetic resonance, NMR) or from autopsy brains. They found large discrepancies between the means of the different samples (even in cases in which the same method was used), but they did not identify the way in which the autopsy and MRI volumes differed. 4.18.2.3.3.(iii) Postmortem MRI Peters et al. (2000) compared estimates of brain volume obtained from MRI and from water displacement in autopsy specimens. They found that provided thin MRI slices (11.25 mm) were used, MRI volumes did not differ significantly from water displacement volumes. However, MRI volumes were found to be overestimates when thicker slices (5 mm) were used. 4.18.2.3.3.(iv) CT slices and virtual endocasts A widely applicable and noninvasive way in which to accurately estimate fossil endocranial volumes is by using two-dimensional (2-D) computed tomography (CT) slices. It is possible to use these slices to obtain an endocranial volume in two ways which yield similar results: (1) either directly using Cavalieris principle, or (2) through the construction of virtual endocasts (e.g., Conroy et al., 1998). Increasingly popular, a 3-D virtual endocast is a 3-D model of the fossil constructed from the 2-D CT slices (Zollikofer et al., 1998; Tobias, 2001; Zollikofer, 2002). For matrix-filled skulls, thresholding to distinguish between local object densities is the method used to separate the walls of the fossil neurocranium from the matrix at their interface (Conroy and Vannier, 1985; Conroy et al., 1990; Zollikofer et al., 1998). Fragmentary specimens are completed using mirror-imaged parts from the opposite side (e.g., Conroy et al., 2000a), or scaled parts 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
Stephan (1981, p. 4) list conversion factors for specific types of fixation, ranging from 1.54 to 2.4. Aside from mismeasurement due to shrinkage, the only disadvantage with using sections as opposed to water displacement is that the former estimates volume, rather than measuring it. However, what the estimate loses in precision it may gain in accuracy, since imaging makes it possible to be sure that only brain tissue is included. 4.18.2.3.3.(ii) In vivo MRI Magnetic resonance imaging (MRI) has recently begun to be applied to comparative samples of living hominoid species in order to obtain volumes of both entire brains and particular brain regions (e.g., Rilling and Insel, 1999; Semendeferi and Damasio, 2000; Sherwood et al., 2004). Comparison of MRI volumes with volumes obtained by water displacement have established that as few as 56 MRI slices per brain
296 The Hominin Fossil Record and the Emergence of the Modern Human CNS
virtual endocast. If there is uncertainty about the dimensions, several potential endocrania are created to establish a range of endocranial volumes, from which a most likely endocranial volume can be determined (Conroy et al., 2000b). The virtual endocast technique was tested on 10 Homo sapiens crania whose endocranial volumes were measured using a mustard seed filler; it was found that the difference between the measured and virtual endocast volumes was around 2% (Conroy et al., 1998). 4.18.2.3.4 Measuring incomplete endocasts 4.18.2.3.4.(i) Partial endocast method Tobias (1964, 1971, p. 64) introduced a method for estimating endocranial volume. The method, which has become known as the partial endocast method, involves taking a complete endocast with known endocranial volume, reducing it to the anatomy preserved in the fossil of interest, and then determining what proportion of the complete endocast is represented by the reduced endocast. This provides a conversion factor to estimate complete endocranial volume for the specimen for which there is only a partial endocast. This method was originally used to determine the volume of OH 7, the type specimen of H. habilis, and its large endocranial capacity (estimated by the partial endocast method to be 675 680 cm3; Tobias, 1964), was one of the reasons given for including the new taxon in the genus Homo (Leakey et al., 1964). This spawned a debate revolving around the reliability and taxonomic implications of the original estimate, in which alternative methods to determine endocranial volumes from partial endocasts were suggested (Pilbeam, 1969; Wolpoff, 1969, 1981; Holloway, 1983d; Vaisnys et al., 1984). 4.18.2.3.4.(ii) Reconstructed endocast method Synthetic and natural endocasts are typically reconstructed using plasticene to fill in missing areas. If only small parts of bilateral structures are missing on one side the necessary reconstruction does not require much guesswork. Holloway (1973, 1975) distinguishes between minimal plasticene reconstruction (method A) and extensive plasticene reconstruction involving close to half the total endocast (method B). Endocast reconstruction should be re-evaluated as additional fossils are discovered, and new, improved, methods should be applied to existing endocasts, not just to newly discovered evidence. Holloways method involves making one endocast reconstruction based on comparisons with specimens belonging to the same hypodigm, or to members of different fossil hominin hypodigms (e.g., P. robustus and P. boisei) with brains that
are similar in size and shape. Reconstructions made independently by different researchers provide a test of reliability. For example, the differences between the endocranial volumes of Holloways (914 cm3) and Broadfields (921 cm3) reconstructions of the Sambungmacan 3 calvaria are minimal (Broadfield et al., 2001).
4.18.2.3.5 Extrapolations from ecto- and endocranial linear metrics Several formulas have been suggested to estimate brain volume from linear dimensions of the endocranial cavity of crania, or endocasts. MacKinnon et al. (1956) compared linear measurements of the cranial cavity taken from radiographic images to mustard seed endocranial capacities for 52 modern human crania. They devised the following formula, which predicts endocranial volume with an error of 0.62% (0.87 cc in a 1400 cc cranium): V 0:511=2LHW LBW ; where L is endocast length from frontal pole to occipital pole, W is maximum width (usually taken at the level of the superior aspect of the temporal), B is the distance from bregma to basion, and H is the distance from vertex to the deepest portion of the cerebellar lobes. Holloway (1973, p. 450) applied this formula to endocasts, but he replaced the value of 0.51 with f, a variable determined for each taxon: V f 1=2LHW LBW : It is not advisable to calculate endocranial volume from external head or cranial measurements. Simmons (1942) found that crania with similar external perimeter measurements had different internal capacities, and Wickett et al. (1994) found that head perimeter measurements were not significantly correlated with total brain size. Bookstein et al. (1999) found that some of the factors responsible for the differences between the external and the internal cranial form were independent, so the inability of external head dimensions to accurately predict endocranial volume is not surprising. Further, there are particular problems with applying formulas designed for modern humans on fossil hominins. Formulas that have been developed to estimate modern human endocranial volume, such as those of Welcker (1885), Pearson (1926), and Manouvrier (1898), do not provide accurate estimations of the cranial capacity of fossils (Olivier and Tissier, 1975). Olivier and Tissier (1975) developed formulas specifically designed for archanthropians and paleoanthropians, but the fact that members of the taxon H. heidelbergensis fall into both
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categories suggests that the reliability of this approach is dependent on having a satisfactory taxonomy.
4.18.2.4 Comparing Different Types of Measurements and Estimates
Brain size can be measured as a volume or as a weight (or mass). European authors tend to use weight whereas American authors tend use mass, but in most cases these terms are used interchangeably. For consistency we will refer to masses in grams (g) and volumes in cubic centimeters (cm3). 4.18.2.4.1 Brain tissue mass from brain mass Measurements reported as brain mass from autopsy brains typically include the leptomeninges (i.e., the arachnoid and pia mater) as well as whatever CSF remains in the ventricles (Peters et al., 1998). Volumes taken from MRI or stained sections measure brain tissue volume from which the volume of the meninges and the CSF are excluded (Peters et al., 1998). This is comparable to the net brain volume calculated by adding up brain volumes for various brain components (e.g., Stephan, 1981). In modern humans, the meninges and CSF are estimated to contribute an additional 183 g for males and 132 g for females (Peters et al., 1998). Thus, for male modern humans: Brain tissue mass g Brain mass g 183; and for female modern humans: Brain tissue mass g Brain mass g 132: 4.18.2.4.2 Brain mass from brain volume For a sample of 78 adult human brains, the brain tissue was found to have an average specific mass of 1.032 g cm3 (Zilles, 1972). Thus, Brain mass g Brain volume cm3 1:032: The specific mass of the brain has also been determined by comparing rodent brain weights with volumes to give an average specific mass of 1.036 g cm3 (Stephan, 1960). Thus, Brain mass g Brain volume cm3 1:036: This suggests that brain mass is c. 3% larger than brain volume (but see Jerisons argument below). 4.18.2.4.3 Brain volume from endocranial volume Brain volume and endocranial volume ( cranial capacity) are not identical. Endocranial volume is larger as it also includes meninges, CSF,
and cranial nerves. Few data are available for actual brain volume and endocranial volume from the same specimen because it is difficult to remove the brain from the brain case without causing damage to either. Novel imaging techniques could improve our understanding of this relationship, although in practice different techniques are used to visualize soft (MRI) and hard (CT) tissues. Pickering (1930) found a correlation between nonfixed brain volume as determined by water displacement and endocranial volume measured with mustard seed in a sample of 29 modern humans, using the following conversion formula (r2 0.805): Brain volume Endocranial volume 0:8598: In other words, approximately 14% of the endocranial volume does not represent brain volume. 4.18.2.4.4 Brain mass from endocranial volume Count (1947) suggested a value of 0.876 g cm3 for brain mass/endocranial volume, so that: Endocranial volume cm3 Brain mass g 1:14; Brain mass g Endocranial volume cm3 1:14: Ruff et al. (1997) used an equation that acknowledged the allometric nature of the relationship between endocranial volume and brain mass (see Martin, 1990). Ruff et al. derived brain mass from endocranial volume using a regression based on brain masses from Stephan et al. (1970) and cranial capacities from Martin (1990) for 27 primate species (r2 0.995): Brain mass g 1:476 Endocranial volume cm3 0:976 : Jerison (1973, p. 30) does not recommend converting endocranial volumes into brain volumes or brain masses. Apparently, the specific gravity of the mammalian brain ranges from 0.9 to 1.1; for example, brain mass (in g) is approximately 5% larger than endocranial volume in insectivores (Bauchot and Stephan, 1967), whereas brain mass (in g) is approximately 3% smaller than endocranial volume in a cat (Jerison, 1973).
4.18.2.5 Indices for Estimating and Comparing the Relative Sizes of Brains
The relationship of brain size to body size, analyzed by Snell (1891), was the basis of Dubois index of
cephalization (Dubois, 1897), which related brain size to (1) body size and somatic functions, and (2) the encephalization of psychic functions. Jerison and Martin have further investigated the relationship between brain size and body size, and have made contributions to the most widely used measure of relative brain size, the encephalization quotient. 4.18.2.5.1 Encephalization quotient Some researchers (e.g., Jerison, 1973; Martin, 1990) do not consider absolute brain size to be an appropriate way to compare the mental capacities of different species. Nor is it useful to compare the brain/body ratio, because this ratio decreases with increasing body size. The solution has been to plot log brain mass on log body mass, from which is derived the allometric formula: E kPb ; where E is brain size, P is body size, k is the allometric coefficient, and is the allometric exponent. It has been suggested that different taxonomic groups tend to have a similar value for (reflecting a consistent functional relationship), but different values for k (reflecting different grades; Martin, 1981). This is usually expressed as the log-transformed linear equation: logE logk blogP: The key variable is typically referred to as the scaling coefficient. For all mammals, Jerison (1961, 1973) observed that the relationship between brain size and body size was described by the equation Brain mass 0:12 Body mass2=3 : Jerison developed Dubois proposal for an equation to quantify encephalization (Dubois, 1897), and derived what he referred to as the encephalization quotient (EQ): EQ Brain mass=0:12 Body mass2=3 : Encephalization occurs when there is a departure from the general relationship between brain size and body size. Encephalization occurs in mammals and birds, but is rare in other vertebrates. Encephalization is explained by Jerisons (1973) additive theory of brain size: E Ev Ec, where E is brain size, Ev is brain size determined by body size, and Ec is associated with improved adaptive capabilities. According to his theory, if Ec 0, then the brain is of a size sufficient for somatic maintenance. If one assumes there is a relationship between brain size and neuron number, and if Ec > 1, then the brain has extra neurons designated to deal with
extracorporeal pressures. The presence of extra neurons is referred to as encephalization. A scaling coefficient value of 2/3 (or 0.66) was suggested for several sets of mammals (Snell, 1891; Jerison, 1955, 1961, 1973; Gould, 1975), but a later study suggested that a scaling coefficient of 3/4 (or 0.75) is more appropriate (Martin, 1981). Based on this, Ruff et al. (1997) used the following equation to generate EQ in hominins: EQ Brain mass=11:22 Body mass3=4 : A scaling coefficient of approximately 3/4 (i.e., 0.78) was also described for a comprehensive sample of primates (Bauchot and Stephan, 1969), although subsets of primates have a wider range of values. The scaling coefficient of nonhuman hominoids (i.e., the apes) is much lower (e.g., EQ 0.58; Bauchot and Stephan, 1969). 4.18.2.5.2 Other standards for brain size comparison Although brain size is most often considered in relation to body mass, other standards for comparing brain size have been used. Some authors suggest that the scaling relationship between brain mass and body mass is a surrogate measure for some underlying variable (e.g., Harvey and Krebs, 1990). CNS or CNS-related standards of comparison are sometimes preferred because they vary less intraspecifically, and measure brain versus nervous system information flow. All standards have advantages and disadvantages. Krompecher and Lipak (1966) were the first to suggest scaling brain size against the mass of another CNS structure (the spinal cord); subsequently, Passingham (1975) scaled brain mass to a CNS-related structure (the foramen magnum). The latter method has the advantage that it uses a hardtissue structure that is occasionally preserved in the hominin fossil record. The absolute size of the spinal cord gives an indication of total neuronal input and output to the brain. In fact, an index of brain size to nonbrain CNS size provides a direct measure of Jerisons extra neurons. On the other hand, it has been suggested that body mass is better for use in scaling relationships precisely because, unlike the CNS or CNS-related structures, it is independent of brain mass (Stephan et al., 1988). Radinsky (1967) suggested that foramen magnum area was a good estimate of body size, although it is less variable within a species than is body mass. However, others have suggested that foramen magnum area is linked more closely with brain size than with overall body size (Jerison, 1973; Gould, 1975; Martin, 1981). In fact, the relationship of the size of a
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given CNS or CNS-related structure to body mass is variable. For example, the relationship between body size and foramen magnum/medulla size may be strongly influenced by specializations such as adaptation to water (Stephan and Dieterlen, 1982; Stephan and Kuhn, 1982). Finally, it has been suggested that CNS structures make better standards because they vary less within a species than body mass does (Radinsky, 1967). One reason why body mass varies so much is that it comprises several components, including muscle mass and adipose tissue, which are themselves variable (Pitts and Bullard, 1968). Muscle tissue, which is well innervated, and other components of fat-free mass scale more closely to CNS mass than does the mass of the less well-innervated adipose tissue (Schoenemann, 2004). This finding has implications for certain questions about the scaling of brain size to body size. For example, the difference between male and female brain mass might be partially explained by the fact that male body mass contains proportionally more muscle (Manouvrier, 1903; Ankney, 1992; Gould, 1996). Along these lines, when scaled to fat-free mass, it has been suggested that the very muscular Neanderthals would have much smaller relative brain size than would modern humans (Schoenemann, 2004). 4.18.2.5.3 Measure of brain organization: A/S ratio Scaling brain size to other appropriate parts of the CNS gives a direct indication of the size of the brain in relation to the amount of input and output. Hebb (1949) advocated replacing brain/body size comparisons with an A/S (association cortex/primary sensory cortex) ratio, since the primary sensory areas are related to input from an animals surroundings, whereas association areas are involved in higher-level cognitive processing. This procedure is also advocated by Holloway, who discussed in detail the problems associated with basing intelligence on brain/body size relationships (Holloway, 1968, 1979; Holloway and Post, 1982).
4.18.2.6 Major Lines of Fossil Evidence for CNS Evolution, Plus Other Endocranial Morphology
contexts are data from extant primates from the endocranium and brain, and from the vertebral column and spinal cord. There is a dearth of data about the CNS of extant hominoids, so most inferences should be treated as preliminary. The extant hominoid data tend to be based on very small samples (e.g., one or two individuals per species, and often the same individuals are used in several studies), and, with respect to the cerebral cortex, rely on gross morphological landmarks as proxies for functional regions (see The Development and Evolutionary Expansion of the Cerebral Cortex in Primates). 4.18.2.6.1.(i) Absolute and relative brain size Sample mean EQs are calculated using the formula of Ruff et al. (1997), which is based on Martin (1981), and using the calculation for estimating brain mass from endocranial volume of Ruff et al. (1997), based on Martin (1990). A list of endocranial volumes used here is available from the authors upon request; mean body mass estimates are from Skinner and Wood (in press). For more information, see Section 4.18.2.5.1. 4.18.2.6.1.(ii) Left occipital right frontal (LORF) petalia This asymmetrical pattern, with a wider and more posteriorly protruding left occipital pole, and a wider right frontal lobe, is typical of modern humans, and is statistically significantly related to right-handedness; that is, left-handed and ambidextrous people are more likely to be symmetrical or have the opposite pattern (Le May, 1976). Although petalias are also common in great apes (Le May, 1976; Le May et al., 1982), they are less frequent than in humans and rarely involve both the frontal and the occipital lobes (Holloway and de LacosteLareymondie, 1982). 4.18.2.6.1.(iii) Orbital surface of frontal lobe The orbital surface of the frontal lobe is blunt and expanded in modern humans. In contrast, it is beaked and pointed in African apes. This region corresponds to cytoarchitectural area 10, which is involved in planning future actions, abstract thinking, and undertaking initiatives (Semendeferi et al., 2001). A regression of nonhuman primate area-10 volumes against brain volumes shows that humans have a larger than expected area-10 volume, but the residual (6%) is less striking than for other regions (Holloway, 2002). 4.18.2.6.1.(iv) Fronto-orbital sulcus The frontoorbital (or orbitofrontal) sulcus typically incises the orbitolateral border of the frontal lobe of African apes, but is rarely present on modern human brains (Falk, 1980b). Due to the opercular
Particular attention is paid to fossil anatomy that can be used to make inferences about the functional anatomy of the CNS. In addition, non-CNS related aspects of endocranial morphology are included. 4.18.2.6.1 CNS-related fossil evidence The categories described below are the major lines of evidence that can be used to infer CNS evolution from the hominin fossil record. Their comparative
expansion of the frontal lobe in humans, this sulcus has probably been shifted so far posteriorly that it now comprises the anterior limiting sulcus of the insula, giving modern human brains a distinctly shaped lateral edge of the frontal lobe (Connolly, 1950, p. 330). The human frontal lobe (Semendeferi et al., 1997; Semendeferi and Damasio, 2000) and its cortex (Semendeferi et al., 2002) have volumes expected for an ape of similar brain size. It has been suggested that the human prefrontal cortex is larger than expected for a primate with a similar sized brain (Deacon, 1997), and that it has a higher than expected white/gray matter ratio (Schoenemann et al., 2005), but these inferences are not reliable (Semendeferi et al., 2002; Sherwood et al., 2005). Note, however, that even if the frontal lobe did not become relatively larger, it is still possible for the prefrontal cortex to become relatively larger within it. 4.18.2.6.1.(v) Brocas cap region Brocas cap as seen on endocasts represents portions of Brodmann areas 47 and 45 (Broadfield et al., 2001). Brocas cap overlaps with (but does not exactly correspond to) Brocas language area. Brocas area corresponds to the Brodmann cytoarchitectural areas 45 and 44 (respectively, pars triangularis and pars opercularis of the inferior frontal gyrus) (Aboitiz and Garcia, 1997). In the majority of modern humans, the left hemisphere is dominant for language (see The Evolution of Language Systems in the Human Brain), and Brocas region on the left hemisphere is asymmetrically enlarged in comparison to the contralateral areas 45 and 44 (Amunts et al., 1999). Although an enlarged Brocas cap is a characteristic of modern humans, it does occur, albeit more rarely, in apes (Holloway, 1996). Questions persist about whether the African ape Brocas area homologue exhibits modern humanlike asymmetry (Holloway, 1996; Cantalupo and Hopkins, 2001; Sherwood et al., 2003). Investigators have drawn attention to modern humanlike Brocas cap asymmetry in fossil hominin endocasts, in particular to those specimens in which the left side is larger than its homologue on the right. They also describe overall size and convolutional detail, particularly in fossils where only one hemisphere is present. Because an asymmetry in which the left Brocas area is larger than the right (L > R) is related to right-handedness is a characteristic of most modern humans, attention is drawn to cases in which Brocas area L > R asymmetries are found along with LORF L > R asymmetries. 4.18.2.6.1.(vi) Temporal poles Modern human endocasts have anteriorly expanded, laterally
pointed temporal poles (Falk et al., 2005), in contrast to African apes, which have rounded temporal poles. In modern humans, the anterior lateral temporal pole, particularly in the left hemisphere, is involved in human face recognition and naming (Damasio et al., 1996; Grabowski et al., 2001). The corresponding monkey area, TG, also functions in visual learning and recognition (Horel et al., 1984; Nakamura and Kubota, 1995). 4.18.2.6.1.(vii) Lunate sulcus 4.18.2.6.1.(vii).(a) Primary visual cortex reduction The lunate sulcus (LS) is within the secondary visual area, close to the anterior border of the primary visual cortex. Modern humans have a more posteriorly located primary visual cortex than do the great apes. Most modern human brains lack an LS, but when present it is situated more posteriorly than it is in the great apes. A regression of occipital lobe volumes against mean brain volumes from small samples of diverse primate species suggests that modern humans have substantially less (121%) primary visual cortex than expected for a nonhuman primate of similar brain size (Holloway, 1992). Although chimpanzees typically have a relatively larger primary visual cortex than do modern humans, a minority of chimpanzees show repositioning of the LS to a more modern humanlike posterior position (Holloway et al., 2003). Holloway et al. (2003) used this point to argue that the hypothetical paninhominin common ancestor must also have had within its population individuals with reduced primary visual cortices, so you would expect this condition in early hominins such as Australopithecus afarensis. The LS may be unique among the cortical sulci visible on endocasts in that it might provide information about the proportion of cortex allocated to distinct functional categories, and provides an estimate of the aforementioned ratio of association to sensory cortex (Holloway, 1966, 1968). 4.18.2.6.1.(vii).(b) Parietal expansion The posterior location of the LS indicates relative reduction of the primary visual cortex and relative expansion of the posterior parietal association cortex. The posterior parietal lobe is concerned with several aspects of sensory processing and sensorimotor integration (Lynch, 1980; Hyvarinen, 1981). The superior parietal lobule subcomponent is involved in visuomotor tasks, including finger movements (Shibata and Ioannides, 2001). The inferior parietal lobule subcomponent is involved in language and calculation abilities, and it is greatly expanded in humans compared to monkeys (Simon et al., 2002). Derived modern human behaviors involving the posterior
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parietal lobe include enhanced social behavior, including communication, tool-making, and tool use (Holloway et al., 2004a). Bruner et al. (2003) suggested that the unique globular shape of the neurocranium of H. sapiens is related to an additional expansion of the parietal lobe in modern humans. Bruner (2004) associated the manufacture of more sophisticated tools and refined language ability with this difference. 4.18.2.6.1.(viii) Posterior cranial fossa A cerebellar quotient (CQ actual/predicted value) was obtained when recent modern human cerebellar volume (determined from posterior cranial fossa volume) was regressed against brain volume (determined from endocranial capacity) minus cerebellar volume (Weaver, 2001, 2005). Extant hominoid brain data suggest that the modern human cerebellum is smaller than would be expected for an ape of similar brain size (Rilling and Insel, 1998; Semendeferi and Damasio, 2000). The difference between modern human and great ape relative cerebellar volumes is statistically significant, although less dramatic when considered along with the range of inferred relative cerebellar volumes found within the hominin fossil record (Weaver, 2005). The cerebellum of modern humans is relatively larger than that of some earlier hominins, perhaps because its size is linked to the complexity of cognitive functions (Weaver, 2005). 4.18.2.6.1.(ix) Thoracic vertebral canal Differences in thoracic vertebral canal size between humans and nonhuman primates have been related to unique aspects of breathing in human speech (MacLarnon, 1993). The thoracic part of the vertebral canal and the spinal cord segments which it encases (in modern humans, T2S2) are enlarged in modern humans compared with nonhuman primates. It is inferred that this difference is due to an increase in the size of the anterior horns of the spinal cord and of nerves stemming from the segments which innervate the mid or lower trunk region. Some of these nerves innervate intercostal muscles and a set of abdominal muscles that are responsible for the fine control of breathing in modern human speech (Campbell, 1968, 1974; Gould and Okamura, 1974). Modern human speech involves long, punctuated, and modulated utterances (Draper et al., 1959; Campbell, 1968; Hixon and Weismer, 1995), which require respiratory control mechanisms far beyond those necessary for nonhuman primate vocalizations. For example, it appears that in modern human speech the exhalatory portion of 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). MacLarnon and Hewitt (1999) explored several alternate hypotheses for increased thoracic vertebral canal size in humans, including postural control for bipedalism, endurance running, and parturition, but found that none were congruent with the fossil and neurological evidence. 4.18.2.6.2 Other endocranial morphology Endocasts preserve information about cranial venous sinuses and meningeal arteries. These may have taxonomic significance, although there is no evidence that their morphology is related to brain function (Holloway et al., 2004a). 4.18.2.6.2.(i) Cranial venous sinuses Modern humans, apes and most hominins have a dominant transverse-sigmoid cranial venous sinus system. In contrast, a subgroup of hominin taxa have a dominant occipital/marginal (O/M) sinus system; that is, the occipital and marginal sinus complex is enlarged, and the transverse and sigmoid sinus complex is reduced (Falk and Conroy, 1983). The functional relevance of variations in the cranial venous sinus system is not clear. The radiator hypothesis (see Constraints on Brain Size: The Radiator Hypothesis) interprets the cranial blood drainage specializations of hominin taxa as an epigenetic adaptation to bipedalism (Falk, 1986, 1990). These specializations include an enlarged O/M sinus system, multiple hypoglossal canals, and augmented emissary vein foramina. African apes have none of these anatomical features, except multiple hypoglossal canals. Within the hominin clade, different combinations of these traits occur. Both Au. afarensis and Paranthropus (P. boisei and P. robustus) have high frequencies of an enlarged O/M sinus system, and the latter has high frequencies of posterior condyloid foramina and multiple hypoglossal canals, but low frequencies of mastoid and parietal foramina. There is a trend in the hominin clade toward the modern human condition (e.g., an increase in the number of mastoid and parietal foramina in H. erectus and later Homo), and a decrease in the frequencies of an O/M venous sinus system (in Au. africanus and Homo). Multiple hypoglossal canals are found in Pan and generally within the hominin clade. Braga and Boesch (1997a) investigated the incidence of these venous channels in African apes and hominins. They did not find statistically significant differences between Paranthropus and African apes with respect to the frequency of condylar canals, nor did they find statistically significant differences between
Paranthropus, Australopithecus, and African apes with respect to the frequency of divided hypoglossal canals, mastoid canals, and parietal and occipital foramina. Further, they suggest that, if differences did exist, these would probably be due to differences in brain size between African apes and hominins. The statistical arguments are set out in subsequent papers (Braga and Boesch, 1997b; Falk and Gage, 1997). 4.18.2.6.2.(ii) Meningeal arteries Descriptions of meningeal vessels are confused by the fact that several descriptive systems have been used to categorize the patterns of these vessels, and homologies between the vascular systems of different species are uncertain (see Falk, 1993; Grimaud-Herve, 1997; Holloway et al., 2004a). Meningeal vessels are meningeal arteries and veins that supply blood to the neurocranium and also to the dura mater (Holloway et al., 2004a). Of the three components of the meningeal arterial system (anterior, middle, and cerebellar), the middle has undergone the greatest change in hominin evolution (Falk, 1993; Grimaud-Herve, 1994; Holloway et al., 2004a). In modern humans, the middle meningeal artery is divided into an anterior (bregmatic) branch which primarily supplies the frontal region, and a posterior (lambdatic) branch which primarily supplies the parietal region (Netter, 1997). In addition, there is an obelic (middle) branch, which varies in its relationship to the other two branches, and which serves as the basis for Adachis (1928) simplistic classification of human meningeal artery configurations. This system has influenced paleoanthropologists, but it is not applicable to nonhuman taxa because it assumes that meningeal arteries enter the middle cranial fossa through its floor, which is the case for nearly all modern humans. In the great apes some or all of the meningeal arteries may enter through the back of the orbit (Falk, 1993).
the DNA is compared, but at a relatively crude level. In DNA sequencing, the base sequences of comparable sections of DNA are determined and then compared. The results of hybridization (e.g., Caccone and Powell, 1989) and sequencing studies of both nuclear and mtDNA (e.g., Bailey et al., 1992; Horai et al., 1992; Gagneux and Varki, 2001; Wildman et al., 2002, 2003) are virtually unanimous in suggesting that modern humans and the African apes are more closely related to each other than any of them is to the orangutan. They also suggest that modern humans and modern chimpanzees, i.e., commom chimpanzees and bonobos, both (belonging to the genus Pan) are more closely related 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 analysis of genome-wide gene expression profiles of the anterior cingulate cortex (ACC) also supports these relationships (Uddin et al., 2004). Thus, if we accept that the hominin twig of the Tree of Life may extend back in time to c. 8 Mya, and that the earliest unambiguous hominin is probably Au. anamensis (see below), then between 8 and 4 Mya we would expect to find primitive hominin and primitive panin taxa, and close to 8 Mya we should expect to see evidence of the common ancestor of panins and hominins. Not all of these primitive taxa, be they hominins, panins, or members of another clade, are direct ancestors of modern humans and chimpanzees. Some will belong to extinct panin and hominin subclades and it is also possible there were major clades for which we have no living representative.
4.18.3.2 Terminology
4.18.3 The Hominin Fossil Record

4.18.3.1 Defining Hominins
Molecular biology has revolutionized our knowledge of the relationships within the great ape clade of the Tree of Life. Relationships between organisms can now be pursued at the level of the genome instead of having to rely on morphology (traditional hard- and/or soft-tissue anatomy, or the morphology of proteins) for information about relatedness. Comparisons of the DNA of organisms have been made using two methods. In DNA hybridization, all
Paleoanthropologists have differed, and still do differ, in the way they classify the higher primates. We have tried to avoid using technical terms, but some are necessary in order to understand the implications of the different classifications. Linnean taxonomic categories immediately above the level of the genus (i.e., the family, the subfamily, and the tribe) have vernacular equivalents that end in id, ine, and in, respectively. In the past, H. sapiens has been considered to be distinct enough to be placed in its own family, the Hominidae, with the other great apes grouped together in a separate family, the Pongidae. Thus, modern humans and their close fossil relatives were referred to as
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hominids, and the other great apes and their close fossil relatives were referred to as pongids (Table 1). However, this scheme is inconsistent with the overwhelming evidence that modern humans and chimpanzees are more closely related to each other than either is to the gorilla or to the orangutan. Some researchers advocate combining modern humans and chimps in the same genus (e.g., Wildman et al., 2003), which, according to the rules of zoological nomenclature, must be Homo. We adopt a less radical solution. The taxonomy we prefer lumps all the great apes including humans into a single family, the Hominidae (Table 1), and recognizes three subfamilies within the Hominidae:
Ponginae for the orangutans, Gorillinae for the gorillas, and Homininae for modern humans and chimpanzees. The latter subfamily is broken down into two tribes: Panini (or panins) for chimpanzees, and Hominini (or hominins) for modern humans. The latter is further broken down into two subtribes: one, Australopithecina, which includes only extinct hominin genera; and the other, Hominina, for the genus Homo, which includes the only living hominin taxon, H. sapiens. Thus, modern humans are hominids (family), hominines (subfamily), and then hominins (tribe). Modern humans and all the fossil taxa judged to be more closely related to modern humans than to chimpanzees are called hominins; the chimpanzee equivalent is panin. We use australopith when we refer to taxa belonging to the subtribe Australopithecina.
4.18.3.3 Organizing the Hominin Fossil Record
Table 1 A traditional taxonomy and a modern taxonomy that take account of the molecular and genetic evidence that chimpanzees 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
The classification of the hominin fossil evidence is a controversial topic. Some researchers favor recognizing relatively few taxa, whereas others think that more species and genera are needed to accommodate the observed morphological diversity. We use a relatively speciose (or splitting) taxonomy, but we also provide an example of a less-speciose (or lumping) taxonomy so that readers can appreciate how the evidence for human evolution would look if interpreted in a different way. The taxa included in the two taxonomies are listed in Table 2. Some of the taxon names are used in different senses in the speciose and less-speciose taxonomies. When we refer in the text to the hypodigm (the fossil evidence referred to that taxon) of one of these taxa in the speciose taxonomy we generally use the less-inclusive interpretation of the taxon, sensu stricto (s.s.). To save space we omit the sensu stricto if we are not making a particular distinction between members of the taxon sensu lato and members of the taxon sensu stricto (e.g., Au. afarensis means Au. afarensis, s.s.). When we refer to the same taxon in the more inclusive taxonomy (i.e., the hypodigm is larger), the Linnean binomial is followed by sensu lato (e.g., Au. afarensis sensu lato or Au. afarensis s.l.). This indicates that we are using the taxon name in a looser sense. Table 2 demonstrates how the less-speciose taxonomy maps onto the morespeciose one. The temporal spans of the taxa in the speciose taxonomy are illustrated in Figure 1. The age of the first and last appearances of any taxon in the fossil record (called the first-appearance datum, or FAD, and last-appearance datum or LAD) almost certainly 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 S. tchadensis O. tugenensis Ar. kadabba Ar. ramidus s.s. Au. anamensis Au. afarensis s.s. K. platyops Au. bahrelghazali Au. africanus Au. garhi P. aethiopicus P. boisei s.s. P. robustus H. habilis s.s. H. rudolfensis H. ergaster H. erectus s.s. H. antecessor H. heidelbergensis H. neanderthalensis H. sapiens s.s. H. floresiensis Less-speciose taxonomy Ar. ramidus s.l. Au. afarensis s.l. Au. africanus P. boisei s.l. P. robustus H. habilis s.l. H. erectus s.l. H. sapiens s.l. H. floresiensis Age (Mya) 7.06.0 6.0 5.85.2 4.54.4 4.23.9 3.93.0 3.53.3 3.53.0 3.02.4 2.5 2.52.3 2.31.3 2.01.5 2.41.6 1.81.6 1.91.5 1.80.2 0.70.5 0.60.1 0.20.03 0.19present 0.0900.012 Age (Mya) 7.04.4 4.53.0 3.02.4 2.51.3 2.01.5 2.41.6 1.90.2 0.7present 0.0900.012 Type specimen TM 266-01-060-1 BAR 100000 ALA-VP-2/10 ARA-VP-6/1 KNM-KP 29281 LH 4 KNM-WT 40000 KT 12/H1 Taung 1 BOU-VP-12/130 Omo 18.18 OH 5 TM 1517 OH 7 KNM-ER 1470 KNM-ER 992 Trinil 2 ATD6-5 Mauer 1 Neanderthal 1 None designated Liang Bua 1 Crania X X X ff X X X X X X X X X X X X X X X X Dentition X X X X X X X X X X X X X X X X X X X X X X Axial Upper limb Lower limb
X X X X X
X X ff X X
X ? ? X X X ?
X ? ? X X ? X X X X X X
X X ?
X X X
X X X
Taxa included from long taxonomy Ar. ramidus s.s., Ar. kadabba, S. tchadensis, O. tugenensis Au. afarensis s.s., Au. anamensis, Au. bahrelghazali, K. platyops Au. africanus P. boisei s.s., P. aethiopicus, Au. garhi P. robustus H. habilis s.s., H. rudolfensis H. erectus s.s., H. ergaster H. sapiens s.s., H. antecessor, H. heidelbergensis, H. neanderthalensis H. floresiensis
Skeletal representation key: X, present; ff, fragmentary specimens; ?, taxonomic affiliation of fossil specimen(s) uncertain.
taxa. Nonetheless, FADs and LADs provide an approximate temporal sequence for the hominin taxa. The heights of the columns of those taxa with good, well-dated, fossil records (e.g., Au. afarensis and P. boisei) are a reasonable estimate of the temporal range of those taxa, but the heights of other columns marked with an asterisk (e.g., S. tchadensis and Au. bahrelghazali) reflect uncertainties about the age of the taxon because either the sample size is too small, or because the estimates of temporal range are not reliable. For various reasons it is very unlikely that we have a complete record of hominin taxonomic diversity, particularly in the pre-4-Mya phase of hominin evolution. This is because intensive explorations of sediments of this age have been conducted for less than a decade, and because these investigations have been restricted in their geographical scope. Thus, the fossil 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 bear this in mind when formulating and testing hypotheses about any aspect of hominin evolution, especially the evolution of bipedalism. We have not used lines to connect the taxa because the constraints of existing knowledge suggest that there are only two relatively well-supported subclades within the hominin clade, one for Paranthropus taxa, and the other for postH. ergaster taxa belonging to the Homo clade. Without more well-supported subclades it is probably unwise to try to identify specific taxa as ancestors or descendants of other taxa.
4.18.3.4 Review of Individual Hominin Fossil Taxa
Each hominin taxon is placed in one of six informal grades (Huxley, 1958) based on a combination of brain and postcanine tooth size and on inferred
H. sapiens H. neanderthalensis
305
H. heidelbergensis *
H. floresiensis * H. erectus
H. antecessor * H. rudolfensis P. robustus
P. boisei
H. ergaster H. habilis
Au. garhi * Au. bahrelghazali * P. aethiopicus * Au. africanus * Au. afarensis Au. anamensis *
3
Anatomically modern Homo
K. platyops *
4
Premodern Homo
Ar. ramidus Ar. kadabba *
Transitional hominins Megadont archaic hominins

O. tugenensis *
Archaic hominins
7
Possible and probable early hominins
S. tchadensis *
Mya
Figure 1 Speciose hominin taxonomy.
locomotor mode. The six grades are: possible and probable primitive hominins (PH); archaic hominins (AH); megadont archaic hominins (MAH); transitional hominins (TH); premodern Homo (PMH); and anatomically modern Homo (AMH) (Figure 1). Several taxon samples are too small to do other than make an informed guess about the grade of the taxon. Within each grouping, the taxa are listed in order of their first appearance in the fossil record. Unless homoplasy (shared morphology not derived from the most recent common ancestor) is more common than we anticipate, there is little doubt that recent hominin taxa (i.e., post-H. ergaster taxa in group PMH) are more closely related to modern humans than to chimpanzees. These taxa all have absolutely and relatively large brains, they were obligate bipeds, and they have small canines, slender jaws, and small chewing teeth. However, the closer we get to the split between hominins and panins the more difficult it is to find features we can be sure fossil hominins possessed and fossil panins, or taxa in any other closely related clade, did not. In the early stages of hominin evolution it may be either the lack of panin features or relatively subtle differences in the size and shape of the canines, or in the detailed morphology of the limbs, that mark out hominins. We are conscious that many readers might be unfamiliar with the details of the hominin fossil
record, so we provide basic information about the morphology of each taxon. The formal way to cite a taxon name is to give the Linnean binomial, followed by the name(s) of the authors and the date of the paper that introduced the taxon. Conventionally, this citation is not placed in parentheses. However, when a taxon has been moved from its initial genus, the original reference is placed within parentheses followed by the revising reference: for example, Homo erectus (Dubois, 1892) Weidenreich, 1940. Further details about most of the taxa and a more extensive bibliography can be found in Wood and Richmond (2000). Recent relevant reviews of most of these taxa can be found in Hartwig (2002) and Wood and Constantino (2004).
4.18.4 Review of Hominin Taxa

4.18.4.1 Possible and Probable Primitive Hominins
This category includes one species, Ardipithecus ramidus, which is almost certainly a member of the hominin clade, one species, Sahelanthropus tchadensis, which is a possible hominin, and two species, Ardipithecus kadabba and Orrorin tugenensis, which may be hominins. Taxon name. Sahelanthropus tchadensis Brunet et al., 2002.
Temporal range. c. 76 Mya. Initial discovery. TM 266-01-060-1 an adult cranium; Toros-Menalla, Chad, 2001 (Brunet et 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 has been made in a virtual reconstruction (Zollikofer et al., 2005), plus several mandibles and some teeth. Characteristics and inferred behavior. Cranial: A chimp-sized animal displaying a novel combination of primitive and derived features. Much about the base and vault of the cranium is chimp-like, but the relatively anterior placement of the foramen magnum, the presence of a supraorbital torus, the lack of a muzzle, the small, apically worn canines, the low, rounded molar cusps, the relatively thick tooth enamel, and the relatively thick mandibular corpus (Brunet et al., 2002) suggest that S. tchadensis does not belong in the Pan clade. Postcranial: No evidence. Conclusion: It is either a primitive hominin, the common ancestor of hominins and panins, or it belongs to a separate clade of hominin-like apes. CNS-related fossil evidence. The endocranial volume is estimated to be between 350 and 370 cm3, the smallest of any adult hominin, and within 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 100000 fragmentary mandible; Tugen Hills, Baringo, Kenya, 2000 (Senut et al., 2001). Source(s) of the evidence. The relevant remains come from four localities in the Lukeino Formation, Tugen Hills, Kenya. Nature of the evidence. The 13 specimens include three femoral fragments. Characteristics and inferred behavior. Cranial: The discoverers admit that much of the critical dental morphology is ape-like (Senut et al., 2001, p. 6). Postcranial: The femoral morphology has been interpreted (Pickford et al., 2002; Galik et al., 2004) as suggesting that O. tugenensis is an obligate biped, but some researchers interpret the radiographs and CT scans of the femoral neck as indicating a mix of bipedal and nonbipedal locomotion. Conclusion: O. tugenensis could prove to be a
hominin, but it is more likely that it belongs to another part of the adaptive radiation that included the common ancestor of panins and hominins. CNS-related fossil evidence. None. Taxon name. Ardipithecus kadabba HaileSelassie et al., 2004. Temporal range. 5.85.2 Mya. Initial discovery. ALA-VP-2/10 partial mandible; 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 morphology is less ape-like than that of O. tugenensis, but more ape-like than that of Ar. ramidus. The researchers who found it suggest that it closely approaches the extant and fossil ape condition (Haile-Selassie et al., 2004, p. 1505); they also suggest that the morphology of the caninepremolar complex of S. tchadensis, O. tugenensis, and Ar. kadabba is so similar that they may belong to one genus, or even one species (Haile-Selassie et al., 2004). Postcranial: Ar. kadabba has been suggested to be a biped on the basis that the shape of the proximal articular surface of the fourth proximal phalanx of the foot resembles that of Au. afarensis, but similar morphology may also be found in the quadrupedal African apes. Conclusion: Ar. kadabba is probably a member of an extinct clade closely related to hominins and panins. CNS-related fossil evidence. None. Taxon name. Ardipithecus ramidus (White et al., 1994) White et al., 1995. Temporal range. c. 4.54.4 Mya. Initial discovery. ARA-VP-1/1 right M3; Aramis, Middle Awash, Ethiopia, 1993 (White et al., 1994). (NB: if a mandible, KNM-LT 329, from Lothagam, Kenya, proves to belong to the hypodigm, then this would be the initial discovery.) Type specimen. ARA-VP-6/1 associated upper and lower dentition; Aramis, Middle Awash, Ethiopia, 1993 (White et al., 1994). Source(s) of the evidence. A site called Aramis in the Middle Awash region of Ethiopia. A second suite of fossils, including a mandible, teeth, and postcranial bones, recovered in 1997 from five localities in the Middle Awash, that range in age from >5.7 to 5.2 Mya were initially allocated to this taxon (Haile-Selassie, 2001), but they were
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subsequently transferred to Ar. kadabba (see above). Nature of the evidence. The published evidence consists of isolated teeth, a piece of the base of the cranium, and fragments of mandibles and long bones. A fragmented associated skeleton has been found and is being prepared and reconstructed. Characteristics and inferred behavior. Cranial: The remains attributed to Ar. ramidus share some features in common with living species of Pan, others that are shared with the African apes in general, and, crucially, several dental and cranial features are shared only with later hominins such as Au. afarensis. Its chewing teeth are relatively small, and the thin enamel covering on the teeth suggests that the diet of Ar. ramidus may have been closer to that of the chimpanzee than to that of modern humans. Postcranial: Judging from the size of the shoulder joint, Ar. ramidus weighed about 40 kg. The position of the foramen magnum suggests that the posture and gait of Ar. ramidus was respectively more upright and bipedal than is the case in the living apes. Conclusions: The discoverers initially allocated the new species to Australopithecus (White et al., 1994), but they subsequently assigned it to a new genus, Ardipithecus (White et al., 1995). Of the hominin taxa in this category, Ar. ramidus, is the most likely to be an early hominin. CNS-related fossil evidence. A crushed cranium has been reported, but no details have been published.
Source(s) of the evidence. Allia Bay and Kanapoi, Kenya. Nature of the evidence. The evidence consists of jaws, teeth, and postcranial elements from the upper and lower limbs. Characteristics and inferred behavior. Cranial: The main differences between Au. anamensis and Au. afarensis relate to details of the dentition. In some respects the teeth of Au. anamensis are more primitive than those of Au. afarensis (e.g., the asymmetry of the premolar crowns, and the relatively simple crowns of the deciduous first mandibular molars), but in others (e.g., the low cross-sectional profiles, and bulging sides of the molar crowns) they show similarities to Paranthropus (see below). Postcranial: The upper limb remains are australopith-like, but a tibia attributed to Au. anamensis has features associated with obligate bipedality. CNS-related fossil evidence. None. Taxon name. Australopithecus afarensis Johanson et al., 1978. Approximate time range. c. 43 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 earliest hominin to have a comprehensive fossil record including a well-preserved skull, several crania, many lower jaws, and sufficient limb bones to be able to estimate stature and body mass. The collection includes a specimen, AL-288, that preserves just less than half of the skeleton of an adult female. Characteristics and inferred behavior. Cranial: It has incisors that are much smaller than those of extant chimpanzees, but the premolars and molars of Au. afarensis are relatively larger than those of the chimpanzee. Postcranial: The hind limbs of AL288 are substantially shorter than those of a modern human of similar stature. The range of body mass estimates is from 25 to >50 kg. The upper limb, especially the hand, retains morphology that most likely reflects a significant element of arboreal locomotion. The size of the footprints, the length of the stride, and stature estimates based on the length of the limb bones suggest that the standing height of adult individuals in this early hominin species was between 1.0 and 1.5 m. Direct evidence of the
4.18.4.2 Archaic Hominins
This group, which includes all the remaining hominin taxa not conventionally included in Homo and Paranthropus, subsumes two genera, Australopithecus and Kenyanthropus. As it is used in this and many other taxonomies, Australopithecus is almost certainly not a single clade, but until researchers can generate a reliable phylogeny there is little point in revising its generic terminology. Taxon name. Australopithecus anamensis Leakey et al., 1995. Approximate time range. c. 4.23.9 Mya. Initial discovery. KNM-KP 271 left distal humerus; Kanapoi, Kenya, 1965 (Patterson and Howells, 1967). Type specimen. KNM-KP 29281 an adult mandible with complete dentition and a temporal fragment that probably belongs to the same individual; Kanapoi, Kenya, 1994.
locomotion of either Au. afarensis or another synchronic hominin comes from the 3.6 Mya hominin footprint trails at Site G in the Laetolil Formation, at Laetoli, Tanzania. If we assume that the skeletal evidence from Hadar and the trace fossil evidence from Laetoli represents one taxon, and if we weigh the primitive and derived characteristics observed in the Hadar pedal remains and in the Laetoli footprints, the form and function of the Au. afarensis locomotor system was not modern humanlike. CNS-related fossil evidence. Endocranial: Au. afarensis is represented by at least 15 specimens that preserve endocranial anatomy and some for which endocranial volume can be estimated. The estimated mean adult endocranial volume is 446 cm3 (n 5; range 387550). The range is interpreted as reflecting a substantial degree of sexual dimorphism. The average of the two largest crania (probable males) is 125 cm3 greater than that for the three smallest crania (probable females). These values are larger than the average endocranial volume of a chimpanzee, and if the estimates of the body size of Au. afarensis are approximately correct then relative to estimated body mass the brain of Au. afarensis is substantially larger than that of Pan. The sample mean EQ for Au. afarensis is 2.5. Holloway has long argued that the primary visual cortex is relatively reduced in size in Au. afarensis, as is apparent in two specimens, AL 162-28 (Holloway, 1983a; Holloway and Kimbel, 1986) and AL 288-1 (Holloway et al., 2004a). However, he allows that another specimen (AL 333-45) may have a proportionately larger, more ape-like, primary visual cortex. Other evidence presented by Holloway et al. for brain organization in Au. afarensis is ambiguous. There may be evidence of a slight left occipital petalia in one specimen (AL 333-45), but a juvenile specimen (AL 333-105) retains the ape pattern of an inferior frontal orbital sulcus (Holloway et al., 2004a). On the other hand, Falk (1985b) argues that Au. afarensis (particularly AL 162-28) has an entirely ape-like sulcal pattern with no evidence of a relatively reduced primary visual cortex, and with an ape-like condition of a cerebellum projecting posteriorly beyond the occipital lobe, a suggestion Holloway and Kimbel (1986) and Holloway et al. (2004a) dismiss as a misinterpretation due to the way the fossil was oriented. Vertebral canal: This species is represented by four sets of vertebras. The most complete set of vertebras includes 15 vertebral elements belonging to AL 288-1, of which the thoracic vertebras have been used 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 by inference a lack of fine control of breathing for speech, and thus the lack of a complex vocal language ability (MacLarnon and Hewitt, 1999). Behavioral interpretations: Both Holloway and Falk recognize that the brain of Au. afarensis shows some degree of reorganization toward the modern human condition. However, a point of contention between these authors has been the relative location of the LS, and the coincident reduction of the primary visual cortex and expansion of the parietal association cortex cortex. Some Au. afarensis brains have a posteriorly placed LS, but some chimpanzee brains also have a posteriorly placed LS (Figure 2b) (Holloway et al., 2003). Holloway et al. (2003) argue that the hypothetical paninhominin common ancestor must also have had within its population individuals with reduced primary visual cortices, so you would expect this condition in early hominins such as Au. afarensis. Other endocranial morphology. Cranial venous sinuses: Eight Au. afarensis from Hadar (AL 33345, Al 333-105, AL 333-114, AL 333-116, AL 16228, AL 444-2, AL 288-1, and AL 439-1) have an enlarged, and thus presumably dominant, occipital marginal sinus system (Kimbel et al., 2004; Falk et al., 1995). However, LH 21, and probably AL 224-9 and AL 427-1b, lack an enlarged occipital marginal sinus system. Meningeal vessels: Present, but not diagnostic.
Taxon name. Kenyanthropus platyops Leakey et al., 2001. Approximate time range. c. 3.53.3 Mya. Initial discovery. KNM-WT 38350 left maxilla fragment; Lomekwi, West Turkana, Kenya, 1998 (Leakey et al., 2001). Type specimen. KNM-WT 40000 a relatively complete cranium but it is criss-crossed by matrixfilled cracks; Lomekwi, West Turkana, Kenya, 1999 (Leakey et al., 2001). Source(s) of the evidence. West Turkana, and perhaps Allia Bay, Kenya. Nature of the evidence. The initial report lists the type cranium and the paratype maxilla plus 34 specimens including three mandible fragments, a maxilla fragment, and isolated teeth some of which may also belong to the hypodigm, but at this stage the researchers are reserving their judgment about the taxonomy of many of these remains (Leakey et al., 2001). Some of them have only recently been referred to Au. afarensis (Brown et al., 2001).
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Lunate sulcus
Occipital pole (OP)
(a)
Parallel sulcus
(b)
Lunate sulcus
(c)
Lunate sulcus
Midsugittal plane (Approx.)
pf lb
L
Reconstruction (Plasticene) Temporal lobe Cerebellum
oci si Snd
(d)
(e)
mmv
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, 287293, 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 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 manape of South Africa. Nature 115, 195199, 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, 242245. Copyright 2005 AAAS.
Characteristics and inferred behavior. Cranial: The main reasons why Leakey et al. (2001) did not assign this material to Au. afarensis are its reduced subnasal prognathism, anteriorly situated zygomatic root, flat and vertically orientated malar region, relatively small but thick-enameled molars, and the unusually small M1 compared to the size of the P4 and M3. Some of the morphology of the new genus, including the shape of the face, is Paranthropus-like, yet it lacks the postcanine megadontia that characterizes Paranthropus. Postcranial: No evidence. Conclusion: The authors note that the face of the new material resembles that of H. rudolfensis (see below), but they rightly
point out that the postcanine teeth of the latter are substantially larger than those of KNM-WT 40000. K. platyops apparently displays a hitherto unique combination of facial and dental morphology. Some researchers contend that KNM-WT 40000 is an Au. afarensis cranium that is distorted by the matrix-filled cracks. CNS-related fossil evidence. No estimate of endocranial volume is given, although it is apparently australopith-like in size. Taxon name. Australopithecus bahrelghazali Brunet et al., 1996. Approximate time range. c. 3.53.0 Mya.
Initial discovery. KT 12/H1 anterior portion of an adult mandible; Koro Toro, Chad, 1995 (Brunet et 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 an isolated tooth. Characteristics and inferred behavior. Cranial: Its discoverers claim that its thicker enamel distinguishes the Chad remains from Ar. ramidus, and that its smaller mandibular symphysis and more complex mandibular premolar roots distinguish it from Au. afarensis. Otherwise, there is too little evidence to infer any behavior. Postcranial: No evidence. Conclusion: This taxon may be a regional variant of Au. afarensis. CNS-related fossil evidence. None. Taxon name. Australopithecus africanus (Dart, 1925). Approximate time range. c. 3.0 2.4 Mya. NB: it remains to be seen whether the associated skeleton Stw 573 from Member 2 (Clarke and Tobias, 1995; Clarke, 1998, 1999, 2002) and the 12 hominin fossils recovered from the Jacovec Cavern since 1995 (Partridge et al., 2003) belong to the Au. africanus hypodigm. Samples of quartz grains from Member 2 and the Jacovec Cavern have recently been dated to c. 4.24.0 Mya using ratios of the 26Al and 10Be radionuclides (Partridge et al., 2003). Initial discovery. Taung 1 a juvenile skull with partial endocast; Taung (formerly Taungs), now in South Africa, 1924. Type specimen. As above. Source(s) of the evidence. Most of the evidence comes from two caves, Sterkfontein and Makapansgat, with other evidence coming from caves at Taung and Gladysvale. Nature of the evidence. This is one of the best, if not the best, fossil record of an early hominin taxon. The cranium, mandible, and dentition are well sampled. The postcranium and particularly the axial skeleton is less well represented in the sample, but there is at least one specimen of each of the long bones. However, many of the fossils have been crushed and deformed by rocks falling onto the bones before they were fully fossilized. Characteristics and inferred behavior. Cranial: Au. africanus had relatively large chewing teeth and apart from the reduced canines the skull is relatively ape-like. Postcranial: Overall, the postcranial remains of Au. africanus suggest that this hominin could engage in both arboreal and bipedal locomotion. The Sterkfontein evidence
suggests that males and females of Au. africanus differed substantially in body size, but probably not to the degree they did in Au. afarensis (see above). Conclusion: This is a hominin with a mixed locomotor mode, part climbing and part bipedal walking. CNS-related fossil evidence. Endocranial: Au. africanus is represented by at least 15 specimens representing the neurocranium, many of which are natural endocasts. Au. africanus endocasts are unique among hominin endocasts in that they preserve a great deal of convolutional detail (Falk, 1987). This species has the most studied (and debated) endocast morphology of any fossil hominin species. The estimated mean adult endocranial volume for Au. africanus is 460 (n 9; range 428 515). The sample mean EQ for Au. africanus is 2.8. An early claim for reorganization of the cerebral cortex, in the form of a relatively reduced primary visual cortex and relatively expanded parietaloccipital association areas, was made by Dart (1925) on the basis of a humanlike posteriorly located LS on the Taung child endocast (Figure 2c). This observation is the focus of a long-standing debate over the identification and location of the LS, including support for Darts view (Holloway, 1975), one author arguing 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 impossible to know the position with certainty (Le Gros Clark, 1947; Holloway, 1985; Tobias, 1991). The debate over the location of the Taung LS developed into a larger debate between Falk and Holloway about whether brain reorganization preceded brain size increase. On the one hand, Holloway (Holloway, 1975, 1983a, 1984, 1985, 1988b) and Holloway et al. (2004a, 2004b) maintain that Taung and other Au. africanus specimens demonstrate aspects of humanlike brain organization. Holloway does not maintain that a particular line clearly represents the LS, but states that for Taung there is no good evidence for a LS in a typical anterior pongid position (Holloway et al., 2004a, p. 97). In addition, Holloway et al. claim that two other specimens (Stw 505 and Sterfontein Type 3) also show a relative reduction in primary visual cortex size, based on the position of the LS (see Figure 2d) (Holloway et al., 2004a, p. 97). In addition, they find evidence of a humanlike brain morphology associated with right-handedness. Two specimens (Sts 5 and Sterfontein type 2) have Brocas cap regions which demonstrate a trend toward a modern humanlike pattern, and one of these (Sts 5) displays a slight LORF petalia (Holloway et al., 2004a). On the
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other hand, Falk (1980b, 1983b, 1985a) maintains and defends her interpretation of a more anterior, ape-like, position for the LS in Taung and other Au. africanus individuals. In addition, Falk points to other ape-like features of Au. africanus endocasts, most significantly the fronto-orbital sulcus. Falk (1980b) claims that Taung is ape-like in the position and size of the fronto-orbital sulcus at the lateral edge of frontal lobe (but see Holloway, 1981b). Five other Au. africanus endocasts (Sts 60, Type 2, Type 3, Sts 58, Sts 1017) are considered to have similar ape-like sulcal patterns, although based on much less evidence (Falk, 1980b). However, Falk et al. (2000) have pointed to derived, modern humanlike aspects of Au. africanus brain morphology that differentiate this species from Paranthropus. The orbital surface of the frontal lobe is blunt and expanded in Au. africanus (Sts 5, Stw 505, and see also the more fragmentary Type 2 and Sts 60) just as in H. sapiens (Falk et al., 2000). Anteriorly expanded, laterally pointed temporal poles also characterize Au. africanus and H. sapiens to the exclusion of Paranthropus (Falk et al., 2000). Vertebral canal: One set of 15 vertebras (Sts 14) and two individual vertebras (Sts 65, Sts 73) have been referred to this species. Au. africanus thoracic vertebral canals have a small cross-sectional area relative to those of modern humans. Behavioral interpretations: In the original description of the type specimen, Dart argued that Au. africanus demonstrates humanlike brain reorganization on the basis of the position of the LS. Although Falk does not concede the position of the LS, Falk et al. (2000) do agree that in other respects the Au. africanus brain has been reorganized relative to African ape brains. There are several examples showing an early start to a trend toward modern humanlike cortical reorganization (Falk et al., 2000). The enlarged orbital surfaces of the frontal lobes in Au. africanus are thought to indicate an expansion of area 10 prior to brain size increase. The anterior lateral regions of the temporal poles, which show a modern humanlike expansion in Au. africanus, are involved in visual learning and recognition. In addition, Au. africanus (Sts 5) is more modern humanlike than ape-like in the size and shape of its olfactory bulbs (Falk et al., 2000). In modern humans, olfactory bulbs are less than half the size of those of the apes. Furthermore, the fraction of functioning olfactory receptor genes is reduced in modern humans relative to apes (Gilad et al., 2003a), a finding that corroborates behavioral data that suggest modern humans do not rely on their sense of smell as much as apes do. Reduction of olfactory bulb size, and corresponding changes in
the dependence on smell (Gilad et al., 2003b), may have arisen early in hominin evolution. Falk et al. (2000) point to shared morphology in Au. africanus and H. sapiens to the exclusion of Paranthropus as evidence of an Au. africanusHomo lineage, but this is a highly contested proposal (e.g., Johanson and White, 1979). In spite of evidence for brain reorganization, there is no very strong evidence for brain morphology that can be related to language capacity. Moreover, the small vertebral canals in the thoracic region suggest a lack of fine breathing control, and thus the lack of complex vocal language ability. This conclusion is similar to that for Au. afarensis. Other endocranial morphology. Cranial venous sinuses: Most researchers who have studied the cranial venous sinuses of Au. africanus suggest that it retains a symplesiomorphic dominant transverse sigmoid sinus and lacks an enlarged O/M sinus (e.g., Sts 5, Sts 19, Sts 26, MLD 1 and MLD 37/38) (Tobias and Falk, 1988; Conroy et al., 1990; Falk et al., 1995). Two exceptions are Taung and Stw 187a, which have evidence for a dominant O/M sinus system (Tobias and Falk, 1988; Kimbel et al., 2004). Falk et al. (1995) argue that this unusual feature contributes to the uncertainty of Taungs taxonomic affinity. Holloway et al. (2004a) suggest that MLD 1 has an O/M sinus drainage system. Meningeal vessels: Saban (1983) drew distinctions between Australopithecus (i.e., Au. africanus) and Paranthropus (P. boisei and P. robustus) with respect 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 vessels that bifurcate into simple anterior and posterior branches, with no middle branch, in contrast to Paranthropus in which a middle branch is present.
4.18.4.3 Megadont Archaic Hominins
This group includes hominin taxa included in the genus Paranthropus and one other taxon, Au. garhi. The genus Paranthropus was reintroduced when cladistic analyses suggested that three of the four species in this grade formed a clade. Two genera, Zinjanthropus and Paraustralopithecus, are subsumed within the genus Paranthropus. Taxon name. Paranthropus aethiopicus (Arambourg and Coppens, 1968) Chamberlain and Wood, 1985. Approximate time range. c. 2.52.3 Mya.
Initial discovery. Omo 18.18 (or 18.1967.18) an edentulous 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 (KNMWT 17000), several mandibles (e.g., KNM-WT 16005), and isolated teeth from the Shungura Formation. No postcranial fossils have been assigned to this taxon. Characteristics and inferred behavior. Cranial: Similar to P. boisei (see below) except that the face is more prognathic, the cranial base is less flexed, the incisors are larger, and the postcanine teeth are not so large or morphologically specialized. When this taxon was introduced in 1968 it was the only megadont hominin in this time range. With the discovery of Au. garhi (see below) it is apparent that robust mandibles with similar length premolar and molar tooth rows are being associated with what are claimed to be two distinct forms of cranial morphology. CNS-related fossil evidence. Endocranial: One almost complete cranium is the only source of information about the CNS of P. aethiopicus. The estimated endocranial volume is 410 cm3 (Walker et al., 1986). Holloway et al. (2004a) describe a slight LORF petalial pattern, but no claims of humanlike brain organization have been made. Falk et al. (2000) suggest that this specimen retains aspects of ape-like brain morphology not found in Au. africanus. The olfactory bulb of P. aethiopicus is ape-like in size and shape, in contrast to Au. africanus (Falk et al., 2000). P. aethiopicus has an ape-like beak-shaped orbital surface of the frontal lobe, in contrast to Au. africanus and Homo. The P. aethiopicus temporal lobe is ape-like in both size and shape and contrasts with the morphology seen in Au. africanus and Homo, but it shares this trait with other Paranthropus taxa (Falk et al., 2000). Holloway (1988a) suggests that the cerebellum of this specimen is chimpanzee-like in that it is posteriorly protruding and laterally flaring, in contrast to the more modern humanlike tuckedunder cerebellum of P. robustus (SK 1585) and P. boisei (OH 5). The ape-like morphology and small brain size are consistent with the conclusion that this species was more ape-like than humanlike in terms of its cognition. Other endocranial morphology. Cranial venous sinuses: The lack of transverse sigmoid sinus grooves in KNM-WT 17000 is taken (by default) as evidence for an enlarged O/M sinus system in P. aethiopicus (Brown et al., 1993).
Taxon name. Paranthropus boisei (Leakey, 1959) Robinson, 1960. Approximate time range. c. 2.31.3 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 West Turkana, Kenya; Melema, Malawi. Nature of the evidence. P. boisei has a comprehensive craniodental fossil record. There are several skulls (the one from Konso being remarkably complete and well preserved), several well-preserved crania, and many mandibles and isolated teeth. There is evidence of both large and small-bodied individuals, and the range of the size difference suggests a substantial degree of sexual dimorphism. There are no postcranial remains that can, with certainty, 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 is larger and wider than that of P. robustus, yet their brain volumes are similar. The mandible of P. boisei has a larger and wider body or corpus than any other hominin (see P. aethiopicus above). The tooth crowns apparently grow at a faster rate than has been recorded for any other early hominin. The fossil record of P. boisei extends across about 1 My, during which there is little evidence of any substantial change in the size or shape of the components of the cranium, mandible, and dentition (Wood et al., 1994). Postcranial: There is, unfortunately, no postcranial evidence that can with certainty be attributed to P. boisei. CNS-related fossil evidence. Endocranial: The P. boisei neurocranium is represented by 11 specimens: OH 5 (Olduvai Gorge); Omo L-338Y-6 and Omo-323-1976-896 (Omo Shungura Formation); KGA-10-525 (Konso); KNM-ER 23000, KNM-ER 406, KNM-ER 407, and KNM-ER 732 (Koobi Fora); KNM-CH 304 (Chesowanja); and KNMWT 13750 and KNM-WT 17400 (West Turkana). The mean adult endocranial volume for P. boisei is 488 cm3 (n 10; range 400545 cm3). The sample mean 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 have slight LORF petalial patterns (Holloway et al., 2004a). For all other P. boisei endocasts, either it is not possible to determine whether a petalia exists,
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or this information has not been reported. For one specimen (KNM-WT 17400) the Brocas cap region is larger on the left side than on the right side, but it is not clear whether or not this is due to distortion (Holloway et al., 2004a). Three P. boisei have convolutional details in the occipital region, suggesting a reduction in the relative size of the primary visual cortex size (KGA-10-525, KNM-ER 23000, Omo L338Y-6). For all other P. boisei, it is either not possible to determine the key occipital landmarks, or this information has not been reported. The temporal lobe of KNM-WT 17400 is ape-like in its size and shape. This contrasts with morphology seen in Au. africanus and H. sapiens, but it shares this morphology with other Paranthropus taxa (Falk et al., 2000). Three P. boisei endocasts (KNM-ER 2300, KNM-WT 17400, and OH 5) have a pointed rostral frontal lobe. They share this morphology with P. aethiopicus and the great apes, and it contrasts with the condition in Au. africanus and modern humans (Falk et al., 2000). Vertebral canal: No evidence. Behavioral interpretations: There is more and better evidence for a more modern humanlike pattern of brain organization in P. boisei than in Au. afarensis. This may indicate that not only did Paranthropus brain size expand over time (Elton et al., 2001), but some brain reorganization may have occurred in this lineage. Certainly, the impact of brain size on brain morphology (e.g., Jerison, 1975) could be a contributing factor to this trend. Other endocranial morphology. Cranial venous sinuses: The cranial venous sinus system of P. boisei has been given much attention. Tobias (1967) first noted that OH 5 had an enlarged occipital marginal sinus system, a trait it shares with most other scorable P. boisei specimens: that is, KNM-CH 304 (Gowlett et 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 this is Omo L-338Y-6, because several authors (Rak and Howell, 1978; Holloway, 1981a; Kimbel, 1984; Holloway et al., 2002) have failed to confirm the presence of an enlarged O/M sinus system in this specimen (cf. Falk et al., 1995). The fossil KGA-10525 lacks an O/M sinus system (Suwa et al., 1997; Holloway et al., 2004a), although it has been suggested 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), like P. robustus, has three major branches of the middle meningeal vessels: anterior, middle, and posterior. However, Saban found only simple anterior and posterior branches for Omo 338y-6, now considered to
belong to P. boisei, but originally thought to be an non-megadont australopith (Walker and Leakey, 1988; White and Falk, 1999). Taxon name. Paranthropus robustus Broom, 1938. Approximate time range. c. 2.01.5 Mya. Initial discovery. TM 1517 an adult, presumably male, cranium and associated skeleton; Phase II Breccia, now Member 3, Kromdraai B, South Africa, 1938. Type specimen. As above. Source(s) of the evidence. Kromdraai, Swartkrans, Gondolin, Drimolen, and Coopers caves, all situated in, or near to, the Blauuwbank Valley, near Johannesburg, South Africa. Nature of the evidence. The fossil record is similar to but less numerous than that of Au. africanus. The dentition is well represented, some of the cranial remains are well preserved, but many of the mandibles are crushed and/or distorted. The postcranial skeleton is not well represented. Research at Drimolen was only initiated in 1992, yet already more than 80 hominin specimens have been recovered and it promises to be a rich source of evidence about P. robustus. Characteristics and inferred behavior. Cranial: The brain, face, and chewing teeth of P. robustus are larger than those of Au. africanus, yet the incisor teeth are smaller. Postcranial: It has been suggested that the thumb of P. robustus would have been capable of the type of grip necessary for stone tool manufacture, but this claim is not accepted by all researchers. The foot retains some arboreal capability, and the pelvic morphology suggests a relatively inefficient system for mass transfer, but the finger curvature is reduced, and it has more modern humanlike limb proportions and foot morphology, evidence that P. robustus was a more committed biped than, say, Au. afarensis, or H. habilis (see below). CNS-related fossil evidence. Endocranial: The P. robustus neurocranium is represented by at least six specimens: four from Swartkrans (SK 1585, SK 46, SK 54, and SK 859), one from Kromdraai (TM 1517), and one from Drimolen (DNH 7). The mean adult endocranial volume is 533 (n 4; range 450650). The sample mean EQ for P. robustus is 3.1. The evidence for modern humanlike aspects of brain morphology is much weaker than for P. boisei, in spite of the larger brain size of P. robustus. Two or three specimens (SK 1585, SK 859, and possibly SK 54) have slight left occipital petalias, but there is no indication of whether they also have right frontal petalias (Holloway et al., 2004a). It is not possible to tell whether the primary visual cortex is reduced in
SK 1585, SK 54, and SK 859, since for each of these endocasts the location of the LS and the interparietal sulcus cannot be determined with certainty (Holloway, 1975; Holloway et al., 2004a). One P. robustus individual (SK 1585) has a beak-shaped frontal lobe and a rounded temporal lobe ape-like traits shared with other Paranthropus, in contrast to the morphology of Au. africanus and Homo (Falk et al., 2000). Vertebral canal: There are a handful of vertebras associated with this species, none of which are thoracic vertebras, although there is one nearcomplete axis (SK 854). Other endocranial morphology. Cranial venous sinuses: All three P. robustus specimens with the relevant anatomy preserved demonstrate an enlarged O/M sinus system. These are SK 1585, SK 46, and SK 859 (Tobias, 1967; Holloway, 1972; Kimbel, 1984). Meningeal vessels: Saban (1983) found that one P. robustus endocast (SK 1585) had three major branches of the middle meningeal vessels: 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 mandibular corpus; Gamedah, Middle Awash, Ethiopia, 1990. Type specimen. BOU -VP-12/130 a cranium; Bouri, Middle Awash, Ethiopia, 1997 ( the prefix ARA was erroneously used in the text of Asfaw et al., 1999). Source(s) of the evidence. Bouri, Middle Awash, Ethiopia. Nature of the evidence. A cranium and two partial mandibles. Characteristics and inferred behavior. Cranial: Au. garhi combines a primitive cranium with largecrowned postcanine teeth. However, unlike Paranthropus (see above), the incisors and canines are large and the enamel lacks the extreme thickness seen in the latter taxon. Postcranial: A partial skeleton combining a long femur with a relatively long forearm was found nearby, but is not associated with the type cranium of Au. garhi (Asfaw et al., 1999); these fossils have not been formally assigned to Au. garhi. CNS-related fossil evidence. The single cranial specimen has an endocranial volume of 450 cm3, based on water displacement of a plaster model of the reconstructed endocast (reliability A1A2). Holloway et al. (2004a) described the endocast morphology, but there was no evidence of a modern humanlike brain reorganization. Other endocranial morphology. Meningeal vessels are present, but are not diagnostic.
4.18.4.4 Transitional Homo
This group contains two hominin taxa (H. habilis s.s. and H. rudolfensis) that are conventionally included within Homo, but which some researchers (e.g., Wood and Collard, 1999) have suggested might not belong in the Homo clade. Until we have the means to generate sound phylogenetic hypotheses about these and other early hominin taxa, it is not clear what their alternative generic attribution should be. Thus, for the purposes of this review, these two taxa are retained within Homo, but are referred to as transitional hominins. Taxon name. Homo habilis Leakey et al., 1964. Approximate time range. c. 2.41.6 Mya. Initial discovery. OH 4 fragmented mandible; Olduvai Gorge, Tanzania, 1959. Type specimen. OH 7 partial skull cap and hand bones; 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, Coopers and Drimolen, South Africa. Nature of the evidence. Mostly cranial and dental evidence with only a few postcranial bones that can be confidently assigned to H. habilis. Characteristics and inferred behavior. Cranial: All the crania are wider at the base than across the vault, but the face is broadest in its upper part. The jaws and teeth are absolutely small, but when related to estimated body mass they are larger than in other later premodern Homo taxa. Postcranial: The curved proximal phalanges and well-developed muscle markings on the phalanges of OH 7 also indicate the hand was used for more powerful grasping (such as would be needed for arboreal activities) than is the case in any other species of Homo. Conclusion: The jaws and teeth of H. habilis are absolutely small, but they are relatively large. Also, postcranial evidence suggests that H. habilis was capable of traveling arboreally and bipedally. CNS-related fossil evidence. Endocranial: The CNS-related fossil evidence for H. habilis comprises six crania, two from Koobi Fora (KNM-ER 1813 and KNM-ER 1805), and four from Olduvai Gorge (OH 7, OH 13, OH 16, and OH 24). Brains are larger in H. habilis than in Australopithecus and Paranthropus, with a mean adult endocranial volume of 609 cm3 (n 6; range 509687 cm3). The sample average EQ for H. habilis is 3.7. Most of the inferences about derived modern humanlike morphology in this species are controversial, mainly due to poor preservation of the
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relevant structures. Falk (1983a) has cast doubt on the allocation of KNM-ER 1805 to H. habilis on the grounds that it displays ape-like frontal orbital sulci at the lateral borders of the frontal lobes. The evidence for the petalial pattern in H. habilis is weak. Holloway et al. (2004a) claim that a single specimen, KNM-ER 1805, has a slight LORF petalial pattern, but the observation of frontal petalia is not reliable because of postmortem deformation (Begun and Walker, 1993; Holloway et al., 2004a). Tobias (1987) makes a case for language ability in H. habilis, but this is controversial as much of the derived anatomy he describes for H. habilis is not confirmed by other authors, who claim the fossils are too fragmented and distorted to justify these interpretations (Begun and Walker, 1993; Holloway et al., 2004a). Tobias (1987) suggests that OH 24, and probably OH 16 (but there is bone missing), have right frontal petalias. According to Tobias, the morphology of the fragmented of the frontal regions of the OH 7 and OH 16 endocasts is suggestive of a modern humanlike Brocas area, but Holloway et al. (2004a) see too few convolutional details to confirm this. The supramarginal angular gyri of the inferior parietal region corresponding to Brodmann areas 40 and 39, respectively are well developed in all four Olduvai H. habilis specimens (i.e, OH 7, 16, 13, and 24) (Tobias, 1987). Tobias states that these gyri are included in Wernickes area (although he allows that the areas definition is controversial). In fact, the inferior parietal lobule is probably not part of Wernickes language comprehension area, which is restricted to the left superior temporal cortex posterior to the primary auditory cortex (i.e., posterior part of Brodmann area 22) (Wise et al., 2001). However, as previously mentioned, the inferior parietal lobule is greatly expanded in humans compared to monkeys, a difference that has been correlated with the development of language and calculation abilities (Simon et al., 2002). Tobias (1987) mentions that in three H. habilis specimens (OH 24, OH 13, and OH 7) the superior parietal lobule is well developed, a characteristic also of Au. africanus (Dart, 1925; Schepers, 1946). Because the development is greater on the left size, he calls the asymmetry parietopetalia, but note that none of these specimens has the typical modern humanlike LORF petalial pattern. Holloway et al. (2004a) do not confirm these asymmetries, and instead they note that OH 7 and OH 24 are distorted and that this makes the identification of parietal petalias questionable, and that in OH 13 inferences about a parietal petalia depend on the way the specimen
is orientated. Holloway et al. (2004a) do not refer to the placement of the LS or to the size of the occipital lobe in H. habilis. However, Begun and Walker (1993) suggest that the occipital lobe in two H. habilis specimens (KNM-ER 1813 and KNM-ER 1805) is smaller and less projecting than in KNM-ER 1470, a cranium referred to H. rudolfensis. Vertebral canal: Unfortunately, no H. habilis thoracic vertebras are available to investigate potentially language-related aspects of spinal cord anatomy in this taxon. Behavioral interpretations: There is no evidence of modern humanlike Brocas cap morphology in H. habilis, nor is there any evidence for any reduction in the size of the primary visual cortex. In summary, the original suggestion that H. habilis is the earliest hominin with the cognitive capacity for language is no longer supported. Other endocranial morphology. Cranial venous sinuses: Three specimens (KNM-ER 1813, KNMER 1805, and OH 16) demonstrate the usual modern humanlike dominant transverse-sigmoid sinus system. Meningeal vessels: H. habilis endocasts for which the morphology is available (KNM-ER 1805, KNM-ER 1813, OH 7) have evidence of three major branches of the middle meningeal artery (Tobias, 1991; Holloway et al., 2004a). Taxon name. Homo rudolfensis (Alexeev, 1986) sensu Wood, 1992. Approximate time range. c. 1.81.6 Mya. Initial discovery. KNM-ER 819 mandible fragment; Koobi Fora, Kenya, 1971. Type specimen. Lectotype: KNM-ER 1470 cranium; Koobi Fora, Kenya, 1972 (Leakey, 1973). Source(s) of the evidence. Koobi Fora, and perhaps Chemeron, Kenya; Uraha, Malawi. Nature of the evidence. Several incomplete crania, two relatively well-preserved mandibles, and several isolated teeth. Characteristics and inferred behavior. Cranial: H. rudolfensis and H. habilis show different mixtures of primitive and derived, or specialized, cranial features. For example, although the absolute size of the brain case is greater in H. rudolfensis, its face is widest in its mid-part, whereas the face of H. habilis is widest superiorly. The more primitive face of H. rudolfensis is combined with a robust mandible and mandibular postcanine teeth with larger, broader crowns and more complex premolar root systems than those of H. habilis. The mandible and postcanine teeth of H. rudolfensis are larger than one would predict for a generalized hominoid of the same estimated body mass, suggesting that its dietary niche made mechanical demands comparable to those of the archaic
hominins. Postcranial: No postcranial remains can yet be reliably linked with H. rudolfensis. CNS-related fossil evidence. Endocranial CNSrelated data are preserved in three cranial specimens (KNM-ER 1470, KNM-ER 1590, and KNM-ER 3732). H. rudolfensis mean adult endocranial volume is 776 (n 3; range 750825), although when it is related to admittedly crude estimates of body mass (EQ 3.2) the brain of H. rudolfensis is not substantially larger than that of Paranthropus, and is smaller than that of H. habilis. KNM-ER 1470 has a modern humanlike Brocas region which is expanded on the left side (Tobias, 1975; Falk, 1983a; Begun and Walker, 1993; Holloway et al., 2004a), a feature that KNM-ER 3732 probably shares, although distortion obscures the interpretation of the morphology of this region. The clearly delimited, modern humanlike Brocas cap is taken by Holloway (1983c) to be suggestive of both language capacity and right-handedness, although he cautions that chimpanzees may also have well-developed Brocas caps. KNM-ER 1470 has a clear, modern humanlike LORF petalial pattern. Unlike H. habilis (KNM-ER 1805), KNM-ER 1470 lacks an ape-like fronto-orbital sulcus on the surface of the frontal lobe (Falk, 1983a). Holloway et al. (2004a) found no evidence of an LS or occipital lobe reduction in H. rudolfensis. However, Begun and Walker (1993) mention that the occipital lobe in the H. rudolfensis specimen KNM-ER 1470 is larger and more projecting than in two H. habilis specimens (KNM-ER 1813 and KNM-ER 1805). Vertebral canal: No vertebras are known for this taxon. Behavioral interpretations: H. rudolfensis (in particular, KNM-ER 1470) represents the oldest undisputed evidence of modern humanlike brain anatomy and it possesses features suggestive of language ability and right-handedness (Falk, 1983a; Holloway et al., 2004a). In support of these interpretations, Toth (1985) has inferred that contemporaneous stone tools were produced by predominately right-handed hominins. Interestingly, there is much more evidence of modern humanlike CNS-related anatomy in H. rudolfensis than in H. habilis. Also noteworthy, the debate over particular convolutional details lessens with the appearance of Homo. This is in part due to the fact that the endocranial convolutions of Homo are less obvious than those of archaic hominins. Falk (1980a, 1980b) notes that frontal convolutions should be the focus of endocast studies as these are more visible. This visibility contrasts with the relatively poor preservation of the LS in premodern Homo (Falk, 1991).
Other endocranial morphology. Cranial venous sinuses: H. rudolfensis does not show any evidence of an enlarged O/M sinus system. Meningeal vessels: One specimen (KNM-ER 1470) has separate anterior, middle, and posterior branches of its middle meningeal artery (Holloway et al., 2004a).
4.18.4.5 Premodern Homo
The species in this category are all usually assigned to the Homo clade. However, at least one species, H. ergaster, has a brain size that overlaps with that of archaic and transitional hominins. Taxon name. Homo ergaster Groves and Ma zak, 1975. Approximate time range. c. 1.91.5 Mya. Initial discovery. KNM-ER 730 corpus of an adult mandible with worn teeth; Koobi Fora, Kenya, 1970. Type specimen. KNM-ER 992 well-preserved adult mandible; Koobi Fora, Kenya, 1971. Source(s) of the evidence. Koobi Fora, West Turkana, Kenya; Dmanisi, Republic of Georgia. Nature of the evidence. Cranial, mandibular, and dental evidence, including a remarkably complete associated skeleton of a juvenile male individual from Nariokotome, West Turkana. Characteristics and inferred behavior. Cranial: Two sets of features are claimed to distinguish H. ergaster from H. erectus. The first comprises features for which H. ergaster is more primitive than H. erectus, with the most compelling evidence coming from details of the mandibular premolars. The second set comprises features of the vault and base of the cranium for which H. ergaster is less specialized, or derived, than H. erectus. The small chewing teeth of H. ergaster imply that it was either eating different food than the australopiths, or that it was preparing the same food extraorally. This could have involved the use of stone tools, or cooking, or a combination of the two. Postcranial: Postcranial similarities to modern humans suggest these hominins were habitual bipeds. Conclusion: Overall, H. ergaster is the first hominin to combine modern human-sized chewing teeth with a postcranial skeleton (e.g., long legs, large femoral head, etc.) apparently committed to long-range bipedalism, and to lack morphological features associated with locomotor and postural behaviors related to arboreality. CNS-related fossil evidence. Endocranial: Relevant fossil evidence for H. ergaster comprises three well-preserved crania from Africa (Koobi Fora, and West Turkana), and four crania from
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Dmanisi in the Republic of Georgia. The adult mean endocranial volume of the six H. ergaster specimens is 762 cm3, with an average of 851 cm3 for the three African specimens, and a much lower average of 675 cm3 for the three Dmanisi specimens with published endocranial volume estimates. The sample average EQ for H. ergaster is 2.8. When the Dmanisi specimens (for which no body mass has been estimated) are excluded, the EQ for the three African specimens of H. ergaster is 3.1. Convolutional details are known only for the three African specimens. Two specimens have modern humanlike LORF petalial patterns (KNM-WT 15000, KNM-ER 3883), whereas the third specimen (KNM-ER 3733) has a less pronounced asymmetry (Begun and Walker, 1993; Holloway et al., 2004a). All three specimens seem to have a modern humanlike asymmetry of the Brocas cap region, with the evidence for this pattern being clearest in KNM-ER 15000, whereas in the other two East African specimens the morphology in that area is uncertain (Begun and Walker, 1993; Holloway et al., 2004a). Occipital convolutional details are not preserved in any H. ergaster cranial specimen. Vertebral canal: The juvenile West Turkana (KNM-WT 15000) skeleton also includes a vertebral column. H. ergaster resembles earlier hominins and nonhuman primates in having relatively smaller thoracic vertebral canals than recent humans, suggesting that this hominin did not yet show the expanded canal that has been associated with more precise control of the muscles associated with speech (see entry for H. neanderthalensis for a discussion). Behavioral interpretations: Holloway et al. (2004a) interpret the cranial findings as clear evidence of right-handedness and language ability. In contrast, evidence from the vertebral canal suggests humanlike increased control of breathing; thus, speech most likely did not yet exist in these hominins. Great apes (Patterson, 1978; Gardner et al., 1989; Shapiro and Galdikas, 1999) and human infants (Bonvillian et al., 1983, 1997; Bonvillian and Patterson, 1999) lack the capacity for vocal language production, but they are able to communicate with hand signals. A study of a deaf sign-language user found that Brocas region maintains its function in nonvocal language (Corina et al., 1999; Corina and McBurney, 2001). Language-related cerebral anatomy might have existed as part of a complex of preadaptations to language, along with a series of cranial modifications seen in H. ergaster and H. erectus (MacLarnon and Hewitt, 2004). These data suggest that increased nonvocal language ability preceded vocal language.
Other endocranial morphology. Cranial venous sinuses: There is no indication of enlarged O/M sinus system for this taxon. Meningeal vessels: The anterior branch of the middle meningeal artery is especially well developed in H. ergaster crania such as KNM-WT 15000 (Begun and Walker, 1993), and KNM-ER 3883 (Holloway et al., 2004a). Anterior branches are characteristically more developed on endocasts of later African fossil Homo, including modern humans (Grimaud-Herve , 1994; Holloway et al., 2004a). Taxon name. Homo floresiensis Brown et al., 2004. Approximate time range. c. <9012 kya. Initial fossil discovery. LB1 partial adult skeleton; Liang Bua, Flores Indonesia, 2003 (Brown et 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 at least 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 endocranial volume. Postcranial: Femur and pelvic morphologies show affinities to H. habilis and Au. afarensis. Possibly associated with oldowan-like stone artifacts. Charred bones hint at control of fire. CNS-related fossil evidence. Endocranium: The endocranial volume estimate of LB 1 is 417 cm3. The H. floresiensis EQ, assuming a body mass of 26 kg, is 3.1; this is within the Australopithecus range. For comparison, if one assumes the low-end body mass estimate of 16 kg, the EQ is 4.5, and assuming the given the high-end body mass estimate of 36 kg, the EQ is a mere 2.4 the smallest of any fossil hominin. All inferences about H. floresiensis brain morphology were made by Falk et al. (2005), based on observations of both the LB1 fossil neurocranium and a virtual endocast. In endocranial shape, LB1 resembles classic Asian H. erectus. LB1 has a LORF petalial pattern. Details are not given, although the Brocas cap region is consistent with modern humanlike morphology (Falk et al., 2005). The endocast lacks ape-like fronto-orbital sulci; these are also absent in H. rudolfensis, but they are retained in other (smaller-brained) early hominins such as H. habilis and Au. africanus (Falk, 1980b, 1983a). The LS is posterior to the lambdoid suture, in a derived position which suggests relative reduction of the primary visual cortex at the expense of enlargement of posterior parietal association areas (Figure 2e). There are a few features in which the
H. floresiensis brain differs from the classic H. erectus brain. First, it is inferred that prefrontal cortex in the region of area 10 is expanded and much more convoluted than in H. erectus or Au. africanus (Falk et al., 2005). This aspect of H. floresiensis is significant because the prefrontal cortex is the region of the human brain that has most clearly increased in relative degree of gyrification (Zilles et al., 1988; Rilling and Insel, 1998). Second, LB1 has extremely wide temporal lobes. Interestingly, the temporal lobe is predicted to have undergone more change in the modern human lineage than has any other brain component (Semendeferi and Damasio, 2000), and it is larger in modern humans than predicted for a nonhuman primate of similar brain size (Rilling and Seligman, 2002). Third, the LB1 occipital lobe does not hang over the cerebellum. An occipital lobe that overhangs the cerebellum is a derived feature of H. erectus (Falk et al., 2005). Vertebral canal: No description available. Behavioral interpretations: H. floresiensis is a dwarfed hominin species in which the size reduction was more pronounced in the brain than the body. In spite of its small absolute and relative brain size, the H. floresiensis brain is at least as modern humanlike in its morphology as is the brain of H. erectus. Compared to classic H. erectus, H. floresiensis is more modern humanlike in having a well-developed temporal lobe and increased gyrification of the prefrontal region. Might the specialized brain morphology of H. floresiensis relate to the fact that this species has been associated with unusually sophisticated artifacts? At present, it is impossible to know. Many cognitive functions of the prefrontal and temporal regions (e.g., processing of auditory information, language production, higher-order processing of visual information, planning, and memory) are predicted to be emphasized in a species that is associated with stone tools. However, these areas are probably not the ones most involved in the act of stone toolmaking (see Stout et al., 2000). An alternative hypothesis is that in this species the temporal lobe and prefrontal cortex did not become relatively larger; rather, other structures (e.g., primary visual cortex) became relatively smaller more quickly. Domesticated mammals have relatively smaller brains and sensory structures than do their wild counterparts, with the size of the primary visual cortex and eyes being the most reduced a pattern that is also found in the fossil dwarfed bovid Myotragus (Ko hler and Moya ` -Sola ` , 2004). Other endocranial morphology. Cranial venous sinuses: Present, but not diagnostic. Meningeal
vessels: The configuration suggests that vessels that originate in the orbit contribute to the supply of the meninges overlying the temporal lobe; this feature is common 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 mandible fragment; 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., Olduvai Gorge, Melka Kunture), and possibly India (Hathnora). Nature of the evidence. Mainly cranial with some postcranial evidence, but little or no evidence of the hand or foot. Characteristics and inferred behavior. Cranial: The crania belonging to H. erectus have a low vault, a substantial, more-or-less continuous torus above the orbits, and the occipital region is sharply angulated. The inner and outer tables of the cranial vault are thickened. The body of the mandible is less robust than that of the australopiths and in this respect it resembles H. sapiens, except that the symphyseal region lacks the well-marked chin that is a feature of later Homo and modern humans. The tooth crowns are generally larger, and the premolar roots of many specimens are more complicated than those of modern humans. All the dental and cranial evidence points to a modern humanlike diet for H. erectus. Postcranial: The cortical bone of the postcranial skeleton is thicker than that in modern humans. The limb bones are modern humanlike in their proportions and have robust shafts, but the shafts of the long bones of the lower limb are flattened from front to back (femur) and from side to side (tibia) relative to those of modern humans. There is no fossil evidence relevant to assessing the dexterity of H. erectus, but if H. erectus manufactured Acheulean artifacts then dexterity would be implicit. The postcranial elements are consistent with a habitually upright posture and obligate, long-range bipedalism. CNS-related fossil evidence. Endocranial: At least 43 crania or cranial fragments preserve information about the CNS of H. erectus. The mean endocranial volume of H. erectus is 991 cm3 (n 36; range 7271260). The EQ for H. erectus is 3.9, and
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H.erectus shows aspects of modern humanlike brain organization similar to those described for H. ergaster. This taxon shows surprisingly little variability in endocast morphology. Holloway (1980), Broadfield et al. (2001), and Holloway et al. (2004a) drew attention to the very clear pattern of LORF petalial patterns and modern humanlike asymmetry of the Brocas cap region. There is some suggestion of a right-handers petalial configuration 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, and in many specimens the evidence exists for both the left 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 missing data or there is distortion in either the left occipital or right frontal regions (Ngandong 13; OH 9, 12; Sangiran 4, 10, 12; Zhoukoudian I L; Holloway et al., 2004a). However, Begun and Walker (1993) took a different position with respect to the existence of petalias in the Zhoukodian specimens that they examined. They state that no frontal petalias are evident for Zhoukoudian I L, II, III E, and III L, and no occipital petalias are evident for Zhoukoudian II and III E, although they do allow that occipital petalias are evident for Zhoukoudian I L and III L. Holloway et al. (2004a) do not describe the morphology of Zhoukoudian II. Most authors agree that the frontal lobe of H. erectus is derived toward the modern humanlike condition. Convolutional details of the frontal lobe are more modern humanlike than ape-like for Sangiran 2 (Ariens Kappers and Bouman, 1939; Weidenreich, 1943; Connolly, 1950). Brocas region is more modern humanlike in H. erectus than in earlier hominins. This was first mentioned by Dubois (1897), who noted that the type specimen (Trinil 2) had a fairly well-developed third (inferior) frontal convolution, the gyrus associated with Brocas area. In fact, the Brocas cap region is enlarged, and/or there is an asymmetry in which the left side is larger and better defined or protrudes more laterally in all scorable specimens (i.e., Ngandong 6 and 14, Sambungmacan 3, Sangiran 2, 3, 10 and 17, Trinil 2, and Zhoukoudian III E) (Holloway, 1980; GrimaudHerve , 1994; Holloway et al., 2004a). Holloway et al. (2004a) infer that H. erectus was capable of rudimentary language and was predominantly righthanded. In the occipital lobe, the LS has been identified in a few specimens (Sangiran 10, OH 12, Trinil 2) and in all it is in a posterior position. A possible exception is Sangiran 2 in which the identification of the LS is uncertain, and the sulcus referred to may
actually be a lateral calcarine sulcus in a position that would be unusual in modern humans. The two fossils from Olduvai (OH 9 and OH 12) resemble the Asian specimens in aspects of brain morphology. OH 9 has a strong left occipital petalia like other H. erectus and H. ergaster (due to missing data, whether or not there was a right frontal petalia cannot be determined). OH 12 has a posterior LS like other H. erectus (convolutional details in this region are not preserved in any H. ergaster specimen). However, whereas OH 9 is in the upper 50% of H. erectus endocranial volume, OH 12 has the smallest H. erectus endocranial volume and fits better with H. ergaster. The development of three cranial features (the tympanic plate, the bregmatic area of the cranial vault, and the subarcuate fossa) and a comparison of adult H. erectus endocranial volumes with that of the Mojokerto child, reveal an ape-like pattern of brain ontogeny for this specimen (Coqueugniot et al., 2004). Other endocranial morphology. Cranial venous sinuses: Three specimens (Zhoukoudian II, III E, and III L) have dominant transverse-sigmoid sinus systems, and one specimen (Trinil 2) has an O/M sinus system on the left and an enlarged transverse sinus on the right (Falk, 1986). Meningeal vessels: Weidenreich (1938) used a modern human-based system of classification in his description of the Zhoukoudian fossils which overlooked similarities between the H. erectus meningeal patterns and that of the apes; but he did note that H. erectus was primitive in having fewer ramifications than modern humans. In Falks re-evaluation of Weidenreichs description of the meningeal vessels (Falk, 1993), she concludes that they are ape-like to the extent that there is a high frequency of the meningeal arteries originating from the orbit rather than the floor. In comparison to modern humans, in Asian H. erectus specimens the obelic branch of the middle meningeal artery is more developed, and may have contributions from both the anterior and the posterior branches. Grimaud-Herve describes three regional patterns. First, it is common for the obelic branch to arise independently as a third major branch in Zhoukoudian endocasts (e.g., Zhoukoudian I L, III E). Second, the obelic branch bifurcates near the origin of middle branch in Trinil 2 and several Sangiran endocasts (e.g., Sangiran 17). Third, in most Ngandong endocasts, the obelic branch derives from the anterior branch but also has a contribution from the posterior branch; the anterior branch is often better developed than the posterior (e.g., Ngandong 3, 7). In the North African H. erectus Ternifine 4, a very ramified obelic branch stems from the anterior branch of the
middle meningeal artery (Saban, 1984; Holloway et al., 2004a). The developed anterior branch is said to be typical of African specimens of later taxa, but, as mentioned above, the developed obelic branch is also typical of H. erectus. The principal vessel of the anterior branch has posterior ramifications that run parallel to it in H. erectus, in contrast to their more oblique orientation in modern humans (Grimaud-Herve , 1994; see The Evolution of Parallel Visual Pathways in the Brains of Primates). Taxon name. Homo antecessor Bermu dez de Castro et al., 1997. Approximate time range. c. 700500 kya. Initial discovery. ATD6-1 left mandibular canine; Level 6, Gran Dolina, Spain, 1994. Type specimen. ATD6-5 mandible and associated teeth; Level 6, Gran Dolina, Spain, 1994. Source(s) of the evidence. Gran Dolina, Atapuerca, Spain. Nature of the evidence. The partial cranium of a juvenile, parts of mandibles and maxillae, and isolated teeth. Characteristics and inferred behavior. Cranial: Researchers who found the remains claim the combination of a modern humanlike facial morphology with large and relatively primitive tooth crowns and roots is not seen in H. heidelbergensis (see below). The Gran Dolina remains also show no sign of any derived H. neanderthalensis traits. Its discoverers suggest H. antecessor is the last common ancestor of Neanderthals and H. sapiens. CNS-related fossil evidence. The only H. antecessor cranium (ATD-15) has an estimated endocranial volume of 1000 cm3 (Bermudez de Castro et al., 1997). Taxon name. Homo heidelbergensis Schoetensack, 1908. Approximate time range. c. 600100 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 who see distinctions between the African and nonAfrican components of the hypodigm refer to the former as H. rhodesiensis. Nature of the evidence. Many crania but relatively little mandibular and postcranial evidence. Characteristics and inferred behavior. Cranial: What sets this material apart from H. sapiens and H. neanderthalensis (see below) is the morphology of the cranium and the robusticity of the postcranial
skeleton. Some brain cases are as large as those of modern humans, but they are always more robustly built with a thickened occipital region, an evenly projecting face with large separate ridges above the orbits, unlike the more continuous brow ridge of H. erectus. Compared with H. erectus (see above), the parietals are expanded, the occipital is more rounded and the frontal bone is broader. The crania of H. heidelbergensis lack the specialized features of H. neanderthalensis such as the anteriorly projecting midface and the distinctive swelling of the occipital region. H. heidelbergensis is the earliest hominin to have a brain as large as anatomically modern H. sapiens. Postcranial: the postcranial skeleton of H. heidelbergensis suggests that its robust long bones and large lower limb joints were well suited to long-distance bipedal walking. CNS-related fossil evidence. Endocranial: H. heidelbergensis is represented by at least 22 cranial fossils that preserve evidence of the CNS. The mean adult endocranial volume for H. heidelbergensis is 1242 cm3 (n 21; range 8801450 cm3). There is an increase in mean endocranial volume compared to H. erectus and H. ergaster. The EQ for H. heidelbergensis is 4.2. For all the specimens, the LS is in the modern humanlike posterior position, according to Holloway et al. (2004a). Broken Hill 1 was described by Smith (1928) to have an ape-like LS, but Holloway et al. (2004a) disagree with this interpretation. Holloway et al. (2004a) describe LORF petalial patterns in most specimens, and very pronounced asymmetrical Brocas regions in some specimens. This is most pronounced in Arago, which has very protruding Brocas caps on both sides. Unfortunately, several specimens are missing entire frontal lobes, and there is no specimen for which all the relevant language/handedness morphology is preserved. Other endocranial morphology. Cranial venous sinuses: Arago, Broken Hill, and Sale lack an O/M sinus system, although Guomde has an O/M sinus system (on both sides) and Swanscombe has an O/M sinus system on the right, not on the left (Falk, 1986). Meningeal vessels: The anterior branch of the middle meningeal artery is especially developed in African H. heidelbergensis. The anterior branch has a few anastomoses in Sale , and more numerous anastomoses in Broken Hill 1. In some European H. heidelbergensis (e.g., Swanscombe, Ehringsdorf 9), the anterior branch is more prominent and is the source of the obelic branch (Falk, 1986). In contrast, in one European H. heidelbergensis the posterior ramus is just as prominent as the anterior ramus (Falk, 1986). Taxon name. Homo neanderthalensis King, 1864.
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Approximate time range. c. >400 or 20030 kya. Initial discovery. Engis 1 a childs 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 for H. neanderthalensis has been found throughout Europe, with the exception of Scandinavia, as well as in the Near East, the Levant and Western Asia. Taxonomic note: The scope of the hypodigm of H. neanderthalensis depends on how inclusively the taxon is defined. For some researchers the taxon is restricted to fossils from Europe and the Near East that used to be referred to as classic Neanderthals. Others interpret the taxon more inclusively and include within the hypodigm fossil evidence that is generally earlier and less derived (e.g., Steinheim, Swanscombe and Atapuerca (Sima de los Huesos)). Nature of the evidence. Many specimens are burials and so all anatomical regions are represented in the fossil record. Characteristics and inferred behavior. Cranial: The distinctive features of the cranium of H. neanderthalensis include thick, double-arched brow ridges, a face that projects anteriorly in the midline, a large nose, laterally projecting and rounded parietal bones, and a rounded, posteriorly projecting occipital bone (i.e., an occipital bun). The size and wear on the incisors suggest that the Neanderthals regularly used their anterior teeth as tools, either for food preparation or to grip hide or similar material. Postcranial: Neanderthals were stout with a broad rib cage, a long clavicle, a wide pelvis, and limb bones that are generally robust with well-developed muscle insertions. The distal extremities tend to be short compared to most H. sapiens, but Neanderthals were evidently obligate bipeds. The generally well-marked muscle attachments and the relative thickness of long bone shafts point to a strenuous lifestyle. CNS-related fossil evidence. Endocranial: There are at least 27 neurocranial fossils preserving evidence of the H. neanderthalensis CNS. The mean adult endocranial volume for H. neanderthalensis is 1404 cm3 (n 27; range 11721740 cm3). The EQ for H. neanderthalensis is 4.7, smaller than that of H. sapiens. Neanderthals were often considered to have larger cranial capacities than H. sapiens, but this has recently been reconsidered in light of new estimates (Holloway et al., 2004a, pp. 301, 304305). Holloway et al. (2004a) suggest that Neanderthals have an overall modern humanlike brain shape, although there is occipital bunning in many specimens. Similarities with modern human brain shape
include broad, round, vertical prefrontal lobes, and wide, full parietal lobes. In contrast, Bruner et al. (2003) argue that brain shape in Neanderthals follows archaic (i.e., H. erectus and H. heidelbergensis) allometric trends for brain size expansion. In contrast, they suggest that modern humans show a different pattern of brain growth that emphasizes expansion of the parietal lobes. Distinct petalias are the norm for Neanderthals. Many have very strong petalias, although not all specimens display the LORF pattern. One of the crania with an atypical petalia (La Ferrassie 1) also has a larger Brocas area on the right than on the left, and in another (La Chapelleaux-Saints), a usual LORF petalial pattern is combined with a right dominant Brocas area. However, most have a modern humanlike pattern of Brocas area asymmetry. Holloway et al. (2004a) suggest that, in all the Neanderthals they looked at, the LS is posterior to the lambdoid suture, as it is in modern humans. They are most certain about the position of the LS in Monte Circeo I, where it is far posterior to the lambdoid suture. They are uncertain about the identification of, or make indirect inferences about, the location of the LS in Le Ferrassie 1, La Quina 5, Neanderthal, Spy I, and Spy II. In La Chapelle-aux-Saints, Boule and Anthony (1911) had originally suggested the LS was anterior to the lambdoid suture. This was disputed (Symington, 1916; Le Gros Clark et al., 1936), and Holloway et al. (2004a) point out that Boule and Anthony (1911) misidentified the LS, and that the real LS is posterior to the lambdoid suture. Holloway et al. did not look at the Krapina endocasts in detail, but they suggest that the Krapina specimens have more derived and modern features than Western European Neanderthals. Holloway et al. (2004a, p. 235) consider that, in terms of their CNS morphology, H. sapiens and H. neanderthalensis should only be separated at the subspecific level. Vertebral canal: At least four (Kebara, La Chapelle-aux-Saints, Shanidar 2, Shanidar 3) sets of Neanderthal fossil vertebras provide information about the size of the vertebral canal that transmits the spinal cord. Neanderthals resemble modern humans (and are different from all earlier hominins) in having enlarged thoracic vertebral canals relative to nonhuman primates. Increased muscular control associated with speech may explain the increase in spinal cord size in the Late Pleistocene hominins (MacLarnon and Hewitt, 1999, 2004). Behavioral interpretations. H. neanderthalensis is modern humanlike in terms of its endocranial volume, inferred spinal cord dimensions, and
3
3
log10 minimum thoracic canal CSA (mm2)
log10 minimum thoracic canal CSA (mm2)
R 2 = 0.8571
R 2 = 0.7646
2.5
2.5
Au. afarensis Au. africanus H. ergaster H. neanderthalensis H. sapiens
1.5 2.2
1.5 2.4 2.6 2.8 3 3.2 3.4 3.6 3.8 4 4.2 4.4 4.6 4.8 5 5.2 5.4
(a)
log10 endocranial volume (cm3)
(b)
log10 body mass (g)
Figure 3 Loglog 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 with anatomy consistent with spoken language, and archeological evidence of complex, possibly symbolic burial behavior, suggests that Neanderthals shared with their early modern human contemporaries many characteristics of modern human cognition. However, no Neanderthal remains are associated with artifacts that can unequivocally be interpreted as art, which would serve as undisputed evidence of symbolic behavior. In contrast, contemporaneous early modern humans are associated with art throughout Europe by the time of Neanderthals last appearance c. 28 kya, suggesting that these two hominin taxa differed in terms of culture and cognition (Klein, 1999). The increase in thoracic vertebral canal crosssectional area from early to late hominins might be explained by the corresponding increase in endocranial volume. The only Neanderthal for which both measures are available, La Chapelleaux-Saints, has the largest minimum thoracic vertebral cross-sectional area of any primate specimen listed (253 mm2 at T6) and a very large endocranial volume (1625 cm3) (MacLarnon and Hewitt, 1999, 2004, p. 188). MacLarnon and Hewitts conclusions are based on hominin values compared with a thoracic vertebral canal to body size scaling relationship for extant primates. But different taxa have different brain mass to body mass scaling relationships (Holloway and Post, 1982), and the relationship between brain size and spinal cord size is even more variable within large taxonomic groups (MacLarnon, 1995). A within-hominin spinal cord to brain size scaling relationship (or CNS scaling law) could account for the observed variation in spinal cord size (see Figure 3a). Further, the pivotal specimen for the argument of MacLarnon and Hewitt is a single
H. ergaster specimen a juvenile for which the growth trajectory is uncertain (see Coqueugniot et al., 2004, and references therein) and for which the small vertebral canal may be pathological (Ohman et al., 2002). This specimen sits on the regression line, and most hominin fossils plot above it (see MacLarnon and Hewitt, 1999; Figure 3b). A best-fit line for thoracic vertebral canal cross-sectional area against body mass for the fossil hominin specimens is much steeper than that for all primates (Figure 3b). Therefore, Neanderthals and modern humans have thoracic vertebral canal cross-sectional areas that fall within the range predicted for a hominin of similar brain size and body mass, although H. ergaster has a smaller thoracic vertebral canal cross-sectional area than expected for its body mass. Other endocranial morphology. Cranial venous sinuses: There is no evidence of an O/M sinus system in any Neanderthal specimen (Falk, 1986). Meningeal vessels: In some Neanderthal crania (Le Moustier, Neanderthal, La-Chapelle-aux-Saints), the posterior branch of the middle meningeal artery is as prominent as the anterior branch (Holloway et al., 2004a). In other Neanderthals (Gibraltar 1 and 2, Teshik Tash 1, Engis 2, La Ferrassie 1, La Quina H 5), the anterior branch is more prominent, and is the source of the obelic branch, as is common in modern humans. Both configurations found in Neanderthals were also found in European H. heidelbergensis (Holloway et al., 2004a).
4.18.4.6 Anatomically Modern Homo
This category includes all those specimens that lack the autapomorphies of premodern Homo taxa, or which cannot be distinguished from living H. sapiens.
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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 Lady of Paviland, found in Wales in 182223. Type specimen. Linnaeus did not designate a type specimen. Source(s) of the evidence. Fossil evidence of H. sapiens has been recovered from sites on all continents except the Antarctic. The earliest absolutely dated remains are from Omo Kibish (McDougall et al., 2005) and Herto (White et al., 2003) in Ethiopia. Taxonomic note: Researchers who wish to make a taxonomic distinction between fossils such as Florisbad, Omo 2, and Laetoli 18, and subrecent and living modern humans refer the African subset to H. (Africanthropus) helmei (Dreyer, 1935). Nature of the evidence. Many are burials so the fossil evidence is good, but in some regions of the world (e.g., West Africa) remains are few and far between. Characteristics and inferred behavior. Cranial: The earliest evidence of anatomically modern human cranial morphology in the fossil record comes from sites in Africa and the Near East. It is also in Africa that there is evidence for a likely morphological precursor of anatomically modern human morphology. This takes the form of crania that are generally more robust and archaic-looking than those of anatomically modern humans yet which are not archaic enough to justify their allocation to H. heidelbergensis or derived enough to be H. neanderthalensis (see above). Specimens in this category include Jebel Irhoud from North Africa, Omo 2 and Laetoli 18 from East Africa, and Florisbad and Cave of Hearths in southern Africa. There is undoubtedly a gradation in morphology that makes it difficult to set the boundary between anatomically modern humans and H. heidelbergensis, but unless at least one other taxon (e.g., H. neanderthalensis) is recognized the variation in the later Homo fossil record is too great to be accommodated in a single taxon. Postcranial: There are relatively few early H. sapiens postcranial fossils. CNS-related fossil evidence. Endocranial: Early modern H. sapiens have a mean endocranial volume of 1463 cm3 (n 79, range 10901880 cm3). The EQ for early H. sapiens is 5.3. The mean brain mass and EQ are within the range of recent modern human values. However, the extreme fossil endocranial volumes (when converted to brain masses, 11331799 g) fall outside of the range for a sample (n > 227) of recent modern humans aged 2030 years (12391526 g).
Fossil modern humans are essentially modern humanlike in shape and endocranial volume. The Jebel Irhoud crania (Jebel Irhoud 1 and 2) are also considered to be H. sapiens but are said to be Neanderthal-like in overall shape; for example, Jebel Irhoud 2 has some occipital bunning, and the Jebel Irhoud 1 cranium is low and broad. The two Jebel Irhoud endocrania show evidence of modern humanlike brain morphology, including a LORF petalial pattern, an asymmetrically enlarged left Brocas area, and a reduced primary visual cortex, plus taxonomic indicators not related to the CNS (mentioned below). As is the case of recent modern humans, the manifestation of the LORF petalia pattern is variable. Cro-Magnon III, Dolni Vestonice 3 and probably also Combe Capelle, and Brno 3 have typical LORF petalias. Predmosti 10 has one of the most extreme cases of the right-handers LORF petalial pattern, but there is no clear evidence of this pattern from the other specimens from the site (Predmosti 3, 4, and 9). Brno II has a reversed, lefthanders pattern of right-occipital and left-frontal petalias. Jebel Irhoud 1 and 2 provide the only evidence of asymmetrically enlarged left Brocas cap regions. The right side of Cro-Magnon III Brocas area is enlarged but the left is not preserved. Fossil and modern H. sapiens neurocrania are uniquely globular in shape (Lieberman et al., 2002), apparently having overcome constraints which cause H. neanderthalensis and archaic (i.e., H. erectus and H. heidelbergensis) neurocranial shape to plot along the same allometric trajectory (Bruner et al., 2003). Expanded temporal and possibly frontal lobes in modern humans possibly contribute to this morphological change (Lieberman et al., 2002). More recently, it has been suggested that volumetrically expanded parietal lobes have consequences for overall brain shape which contribute to the characteristic globularity of the human brain (Bruner et al., 2003). In comparison to the brains of earlier Homo, the modern human brain is shaped such that the anterior and posterior ends seem to approach each other from below. This is related to a decrease in relative endocranial length, a relative shortening of the frontal and occipital poles, and displacement of the cerebellum to a more inferior position (Bruner, 2004). Weaver (2005) suggests that relative cerebellum size differs between fossil modern humans and recent modern humans. The Early to Middle Pleistocene group (Au. africanus, P. boisei, H. habilis, H. rudolfensis, and H. erectus, H. heidelbergensis) does not differ significantly from recent modern humans or from the great apes with respect to CQ values (Weaver, 2005). However, the very low CQ values of the Late Pleistocene group (H. neanderthalensis and
H. sapiens) are significantly different from those of the Early to Middle Pleistocene group, the great apes, and from recent humans (Weaver, 2005). The shift toward larger CQ values in recent humans is said to be due to expansion of relative cerebellar size during a time of stasis in encephalization. Weaver suggests the cerebellum became expanded in recent humans to better manage the complex cognitive functions. However, this interpretation assumes that the Late Pleistocene group represents the condition directly ancestral to recent humans. The group with the lowest CQ values are Late Pleistocene hominins, which are all European, and the lowest value in the entire sample is from the Swanscombe specimen (CQ 0.60). The decrease to the CQ values characteristic of the European MiddleLate Pleistocene group may be due to shared ancestry or geographical convergence, and it may not necessarily indicate the condition which precedes that of recent humans. Other endocranial morphology. Cranial venous sinuses: Jebel Irhoud 1 and 2, Kanjera 1, and Predmost II and X have evident dominant transverse sinuses and no O/M system (Holloway et al., 2004a). Brno III has an enlarged O/M sinus on the right (its left side is strongly deformed), and Predmost IV has evidence of an O/M sinus system on the right but not on the left. Skhul I has an O/M system on both sides. Meningeal vessels: The number of ramifications and anastomoses is increased from the ape-like level seen in H. erectus (Weidenreich, 1943, p. 13) to the characteristic modern human condition (Saban, 1984; Grimaud-Herve , 1994). The principal vessel of the anterior ramus has posterior ramifications which run parallel to it in H. erectus, but which become more oblique inferoposteriorly relative to the more rounded occipital of recent humans (Grimaud-Herve , 1994). In modern humans, the anterior and obelic branches are more developed, and the posterior branch is less developed a pattern also seen in KNM-WT 15000. The anterior branch of the middle meningeal artery is well developed in fossil African H. sapiens, with numerous anastomoses in Jebel Irhoud (1 and 2) and Omo 2. In some fossil European H. sapiens, the obelic branch takes origin from both the anterior and posterior branches (Predmost 3, Predmost 4 left side, Dolni Vestonice 1, 2).
clade, it is necessary to consider the brain morphology of the most recent hypothetical common ancestor of modern humans and living chimpanzees. The principle of parsimony suggests the panin hominin ancestor possessed all shared derived features of extant humans and chimpanzees, but it would lack those features acquired solely along either the panin or the hominin lineages. It is difficult to reconstruct the paninhominin ancestor with certainty with respect to well-represented regions of the hard tissue fossil record, and it is particularly difficult to do so for CNS-related morphology for which the extant and fossil evidence is both sparser and more difficult to interpret. For simplicity, we will assume that the chimpanzee brain is equivalent morphologically to the primitive hominin brain. There is no significant evidence for derived chimpanzee brain morphology which is not also shared with modern humans, although chimpanzees are likely to have evolved CNS autoapomorphies related to species-specific behaviors, which may be brought to light by future hominoid comparative neuroanatomical studies.
4.18.5.2 Modern Human or Hominin Lineage
4.18.5 Trends in Hominin CNS Evolution

4.18.5.1 Primitive Brain Morphology
In order to determine whether a morphological feature is primitive or derived within the hominin
4.18.5.2.1 Earliest appearance of derived modern human morphology The data suggest that, whereas fully modern human brain morphology only occurs in recent humans, some aspects of modern human brain morphology are present in earlier forms (see Table 3). The aspect of modern human brain morphology that may have appeared earliest is the reduction of the primary visual cortex, as evidenced by the position of the LS. A posterior LS has been reported for some Au. afarensis specimens, but at the least this feature is variable within the taxon. Given the small sample it is difficult to tell whether the Au. afarensis brain really is derived in the direction of the modern human brain, or whether it expresses variability similar to that seen in chimpanzees. In contrast, there are several aspects of endocast anatomy derived in the direction of modern humanlike brain reorganization in Au. africanus, which has better evidence for a reduced primary visual cortex. In addition, Au. africanus shows evidence of: (1) a somewhat expanded, blunt orbitofrontal cortex, (2) anteriorly expanded, laterally pointed temporal poles, (3) an incipient LORF petalial pattern, and (4) a modern humanlike Brocas cap region. Although these features are not as pronounced as in modern humans, they can be interpreted as being derived in the direction of modern humans. The LORF petalial pattern and Brocas cap region
Table 3 Aspects of endocranial morphology and/or inferred CNS morphology Mean endocranial volume (cm3) Relative size of cerebellum (CQ)h
Taxon Pan troglodytes (M) Pan troglodytes (F) Recent H. sapiens (M) Recent H. sapiens (F) S. tchadensis O. tugenensis Ar. kadabba Ar. ramidus Au. anamensis Au. afarensis K. platyops Au. bahrelghazali Au. africanus Au. garhi P. aethiopicus P. boisei s.s. P. robustus H. habilis s.s. H. rudolfensis H. ergaster H. erectus s.s. H. antecessor H. heidelbergensis H. neanderthalensis H. sapiens s.s. H. floresiensis
a b
FAD (Mya)
EQ 1.6 1.9 5.1 5.4
LORF petalial patterna
Frontoorbital sulcusb
Orbital surface of the frontal lobec
Brocas cap regiond
Neurocranial globularitye
Temporal pole morphologyf
Lunate sulcus positiong
Thoracic vertebral canal i
P M I m m m I P M M M M M M M
P M P P M M
P M m P P P M
P M P m I M I M M M M I
P M P P P M
P M m P P P
P M P/M M M M M M M M M
1.2 1 0.8 1 1 0.9 0.9 0.9 0.8 0.7 0.7
P M P P P M M
7 6 5.8 4.5 4.2 3.9 3.5 3.5 3 2.5 2.5 2.3 2 2.4 1.8 1.9 1.8 0.7 0.6 0.2 0.19 0.090
365
446
2.5
460 450 410 488 533 609 776 763 991 1242 1404 1463 417
2.8
2.5 3.1 3.7 3.2 2.8 3.9 4.2 4.7 5.3 3.1
LORF (left occipital right frontal) petalial pattern (P) infrequent, rarely involves both frontal and occipital lobes; (M) usual. Fronto-orbital sulcus (P) present; (M) absent. c Orbitofrontal region (P) beak-shaped; (M) blunt and expanded. d Asymmetrical Brocas area (P) not asymmetrically enlarged; (M) L>R asymmetry. e Endocast shape (P) archaic; (M) globular, suggests expanded parietal. f Temporal pole morphology (P) rounded; (M) anteriorly expanded, laterally pointed. g Lunate sulcus position (P) anterior (some variability); (M) more posterior. h Taxon mean EQ (encephalization quotient) values, calculated from specimen CQ (cerebellar quotient) values (LSR-05 in Weaver, 2001). i Thoracic 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, Panlike 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, the earliest taxon for which there is evidence for humanlike brain organization (there are insufficient data for the other three aforementioned features until later Homo). In addition, H. rudolfensis is the earliest taxon not to have an orbitofrontal sulcus. Interestingly, there is no good evidence for a modern humanlike LORF petalial pattern and a Brocas cap region in H. habilis; indeed, there is evidence of an African ape-like orbitofrontral sulcus. Where data exist, H. erectus and H. ergaster endocasts tend to share the modern humanlike features that are found in H. rudolfensis. H. neanderthalensis is the earliest taxon known to have an expanded thoracic vertebral canal. A globular brain due to parietal lobe expansion has been proposed as an autoapomorphy of modern humans (Bruner et al., 2003). An increase in relative cerebellum size from fossil to recent anatomically modern humans might be a final refinement within this species. 4.18.5.2.2 Earliest appearance of increase in absolute and relative brain size Modern human mean brain mass for adults 2139 years old is 1450 g for males, and 1290 g for females (Figure 4, Table 4) (Dekaban and Sadowsky, 1978). The chimpanzee mean brain weight for adolescents and young adults (730 years) is 406 g for males and 368 g for females
(Herndon et al., 1999). In both species, average brain mass decreases in older individuals; for example, Dekaban and Sadowsky (1978) reported a 7.4% decrease (approximately 100 g) in modern human brain mass between 2030 years and 7080 years. In fact, the mean endocranial volumes from a more typical modern human autopsy data set (average age 65 years) are dramatically different (male 1308 g, female 1179 g) (Zilles, 1972). Sex is also an important consideration in brain size comparisons because male and female samples of hominoid taxa have significantly different brain sizes. It is not possible to know the sex of fossil specimens, and statistical methods of sexing are not possible for the small early hominin cranial samples. Therefore, fossil taxa are not assigned to sex, but are compared as whole taxon samples to samples of both sexes of extant taxa. Previously, absolute brain size has been used to determine a cerebral Rubicon criterion for inclusion in the genus Homo, variably set between 600 and 800 cm3 (Leakey et al., 1964). Currently, absolute brain size is thought to lack biological significance, since it does not give an indication of degree of encephalization, or the number of extra neurons (Jerison, 1973; Martin, 1990). However, aspects of brain morphology such as brain component volumes and degree of gyrification scale to absolute brain size (Zilles et al., 1988, 1989; Semendeferi and Damasio, 2000; Semendeferi et al.,
1750 1650 1550 1450 1350 1250
Chimpanzee mean (M) Chimpanzee mean (F) Modern human mean (M) Modern human mean (F) S. tchadensis Au. afarensis Au. africanus Au. garhi P. aethiopicus P. boisei P. robustus H. habilis H. rudolfensis H. ergaster H. erectus H. antecessor H. heidelbergensis H. neanderthalensis H. sapiens H. floresiensis 1.00 2.00 3.00 4.00 5.00 6.00 7.00
Brain mass (g)
1150 1050 950 850 750 650 550 450 350 250 0.00
FAD (Mya)
Figure 4 Chimpanzee and recent modern human male and female brain mass means are plotted, with y-axis bars and dashed lines showing ranges within two standard deviations. Fossil hominin brain mass individual specimen values are plotted with y-axis bars showing range within two standard deviations from the mean. FAD, first-appearance datum. For more information, see Table 4.
Table 4 Absolute and relative brain sizes for fossil and extant panin and hominin taxa Mean endocranial volume Minimun endocranial volume Maximum endocranial volume Mean brain massb 406 368 1450 1290 363 442 514 393 455 446 407 483 525 599 758 746 830 662 963 972 1200 1353 1408 414 Brain mass SD 39 37 20 30 69 40 7 33 Mean body mass 58 43 70 57 38 45 29 34
Taxona Pan troglodytes (M) Pan troglodytes (F) Recent H. sapiens (M) Recent H. sapiens (F) S. tchadensis Au. afarensis Au. afarensis (M?) Au. afarensis (F?) Au. africanus Au. garhi P. aethiopicus P. boisei P. robustus H. habilis H. rudolfensis H. ergaster H. ergaster (Africa) H. ergaster (Dmanisi) H. erectus H. antecessor H. heidelbergensis H. neanderthalensis H. sapiens H. floresiensis
a
FAD (Mya)
Number in sample 17 17 351 201 1 5 2 3 9 1 1 10 4 6 3 6 3 3 36 1 21 27 79 1
Minimum brain mass 347 308 1343 1239 385 486 385 424
Maximum brain mass 530 458 1526 1366 542 542 397 508
EQc 1.6 1.9 5.1 5.4 2.5 2.6 2.7 2.8
7 3.9
3 2.5 2.5 2.3 2 2.4 1.8 1.9
1.8 0.7 0.6 0.2 0.19 0.090
365 446 521 396 460 450 410 488 533 609 776 763 851 675 991 1000 1242 1404 1463 417
387 492 387 428
550 550 400 515
400 450 509 750 600 804 600 727 880 1172 1090
545 650 687 825 900 900 775 1260 1450 1740 1880
397 446 503 734 590 785 590 712 858 1135 1057
537 638 674 805 877 877 758 1218 1397 1669 1799
43 82 60 41 111 46 86 134 131 153 124
41 36 33 55 64 64 58 71 72 64 26
2.5 3.1 3.7 3.2 2.8 3.1 3.9 4.2 4.7 5.3 3.1
Sources: Chimpanzee brain and body mass data for individuals 730 years from Herndon et al. (1999). Recent modern human brain and body mass data for adults 2139 years (except minimum and maximum brain mass, which are for 2030 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. b Fossil endocranial volumes were converted into brain masses after Ruff et al. (1997). c EQ (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 taxons 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 consideration when investigating the evolution of the brain of modern humans. The smallest adult hominin brain belongs to the single cranial specimen of Sahelanthropus, the earliest possible hominin, and its endocranial volume falls slightly below the female chimpanzee mean. Single specimens of P. aethiopicus, Au. garhi, and H. floresiensis plot around the male chimpanzee mean. The Au. afarensis sample is not significantly different from the combined sex sample of chimpanzees (p 0.093), nor from the male chimpanzee sample (p 0.456), although it is significantly larger than the female chimpanzee sample (p 0.011) (all statistical comparisons are derived from a KruskalWallis test of significance). The Au. africanus sample is significantly different from the combined sex sample (p < 0.001), and the male (p 0.001) and female (p < 0.001) subsamples of chimpanzees. However, this does not suggest that the brain size of Au. africanus is significantly increased relative to chimpanzees and that of Au. afarensis is not; these two groups do not differ significantly from each other (p 0.385). Although the Au. africanus mean value (455 g) is only slightly larger than that for Au. afarensis (442 g), the range for Au. africanus is much smaller than that for the sexual dimorphic Au. afarensis (but see Reno et al., 2005 for an alternative interpretation that suggests only modest levels of sexual dimorphism in Au. afarensis). Au. afarensis attains higher individual brain mass estimates than Au. africanus. Early hominin fossil crania for which endocranial volume and body mass have been reliably estimated are extremely rare, making it impossible to do comparative statistical tests of EQs. However, given that early fossil hominins (e.g., Australopithecus and Paranthropus) have smaller estimated body masses than chimpanzees (mean body mass 58 kg for males, 43 kg for females; Herndon et al., 1999), any significant increase in relation to chimpanzee brain volume can be assumed to be an increase in both absolute and relative brain size (Table 4). Thus, the increase from the brain size of a chimpanzee-like hypothetical common ancestor to brains the size of those belonging to Au. afarensis and Au. africanus is evidence of an increase in relative brain size. This finding is further evidenced by the EQ values of Au. afarensis (2.5) and Au. africanus (2.8), which are well above those for chimpanzees (male EQ 1.7, female EQ 1.9), overlapping with those of Paranthropus (P. boisei EQ 2.5; P. robustus EQ 3.1), and approximating that of H. ergaster (2.8). By the appearance of H. rudolfensis and H. habilis, both absolute and relative brain size have clearly
departed from the Pan-like condition. H. habilis is the smallest-brained hominin for which all the specimen values fall outside of two standard deviations of the male chimpanzee mean. H. habilis and H. rudolfensis are significantly different in brain mass (p 0.02), and the entire range of H. rudolfensis values plot above the range of H. habilis values. However, when the brain mass data are seen in the light of body mass data, H. habilis (EQ 3.7) is more encephalized than H. rudolfensis (EQ 3.2). Relative brain mass in both H. habilis and H. rudolfensis is greater than that in Australopithecus and Paranthropus, and it approaches the values for H. erectus (EQ 3.9). In summary, although encephalization in the hominin lineage might have begun as early as Au. afarensis, it was evident in Au. africanus (in parallel to the encephalization of Paranthropus, see Section 4.18.5.3) and definitely by the time of the appearance of H. habilis and H. rudolfensis. 4.18.5.2.3 Appearance of derived modern human CNS morphology in relation to brain size Although there are hints of a trend toward a modern humanlike relative brain size and brain morphology in Au. afarensis, there is a lot of variability in the size and morphology of this taxon. Given small samples, one cannot be certain whether or not this variation is different from the variation seen in chimpanzees. Further, the functional and adaptive significance of these features in the early taxa is questionable. Modern humanlike endocranial anatomy in Au. afarensis might be a pre-adaptation which only acquires its modern functions in Au. africanus, H. rudolfensis, or in even later hominins. Most aspects of modern humanlike endocast morphology make an appearance in Au. africanus, but they do not yet show the fully modern form. The reason for their occurrence in this taxon is uncertain, but might be influenced by brain size increase, and it is quite possibly related to exceptional preservation of brain morphology in this taxon. The appearance of several aspects of modern brain morphology in Au. africanus complement the fact that this taxon is the first to have a brain size significantly different from chimpanzees. However, as a whole, the Au. africanus brain still differs considerably from the modern human brain, and any similarities are not considered sufficient to suggest a modern humanlike cognitive capacity or behavior for Au. africanus. This is in contrast to the more modern humanlike brain morphology of H. rudolfensis which is generally taken as evidence of more modern humanlike
329
cognitive capacities. Most notably, these features are suggestive of language ability and right-handedness, coincident with the first stone tools which apparently were made by right-handed hominins. This is associated with the earliest brain masses outside of what is expected for a chimpanzee, and an EQ higher than that of earlier taxa. However, H. habilis has a higher EQ than H. rudolfensis, and this later appearing hominin also has brain mass values outside of what is expected for a chimpanzee. It is not yet possible to tell whether the more modern humanlike brain morphology of H. rudolfensis, compared to H. habilis, is, or is not, size-related.
4.18.5.3 Brain Evolution in Other Lineages
The P. boisei mean value (483 g) for estimated brain mass is larger than the value for P. aethiopicus (407 g) and somewhat larger than the means for Au. africanus (455 g) and Au. afarensis (442 g). Further, the majority of the P. boisei specimens fall outside of two standard deviations of the male chimpanzee mean. Therefore, it is inferred that P. boisei has increased its absolute brain size relative to the primitive condition. The P. boisei sample mean is not significantly different (p 0.357) from that of the later occurring P. robustus sample, even though the 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 higher than those for male and female chimpanzees. However, the P. boisei EQ is smaller than that of Au. africanus and is similar to the Au. afarensis value. Given the lack of postcranial evidence, one cannot be certain that EQ has increased from P. aethiopicus to later Paranthropus taxa. These data are, however, consistent with the suggestion of a temporal trend for brain size increase within the Paranthropus lineage (Elton et al., 2001). There is little evidence to suggest modern humanlike reorganization of the Paranthropus brain. In particular, slight LORF petalial patterns are found in P. aethiopicus and P. boisei, and a posteriorly positioned LS has been identified in P. boisei. The evidence does not suggest that the Paranthropus brain becomes increasingly modern humanlike over time, as is the case for Homo. Further, Paranthropus retains ape-like beak-shaped orbital surface of frontal lobe and rounded temporal poles, differentiating it from Au. afarensis and H. sapiens. The modern humanlike endocranial features seen in Paranthropus most likely reflect a shared ancestry with the modern human lineage. Similarly, brain size increase in Paranthropus is
probably the continuation of a trend beginning in a common ancestor of Paranthropus and modern humans. There is presumed to be a decrease in absolute and relative brain size in H. floresiensis (Brown et al., 2004), but this trend might also apply to other fossil hominin taxa. H. floresiensis had a tiny brain (414 g), with an EQ (3.0) much lower than that of its presumed closest fossil relative, H. erectus. Interestingly, its EQ is higher than the one listed here for H. ergaster (2.8, includes Dmanisi) and only slightly lower than the EQ for African H. ergaster (3.1). Body mass estimates obtained from Dmanisi postcranial remains will refine the H. ergaster EQ. Given that H. ergaster is thought to have expanded outside of Africa, evidence from the relative brain size alone suggests that it, rather than H. erectus, may be the sister taxon of H. floresiensis. If so, this would indicate that EQ did not actually decrease in H. floresiensis, thereby solving one of the major puzzles of this taxon (Brown et al., 2004). It is noted that H. floresiensis possesses much morphology that is derived from the primitive ape-like condition. Several of these features are thought to be found in the most recent H. floresiensismodern human common ancestor (which may also be the most recent H. erectusmodern human common ancestor). Brain size increase and the appearance of some aspects of modern humanlike brain morphology occur in at least two hominin lineages. Both Paranthropus and Homo have absolutely and relatively larger brains than Australopithecus. However, only in Homo does brain size increase occur in parallel with the acquisition of modern humanlike brain morphology. Interestingly, H. floresiensis provides striking evidence that, even within Homo, estimated brain mass and inferred brain morphology can become disassociated.
Acknowledgments
We thank the Henry Luce Foundation, the GW Academic Excellence Initiative, the NSF IGERT Program, and NSF DIG No. 01-113 for support.
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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, 2956. Falk, D. 2004. Hominin brain evolution: New century, new directions. Coll. Antropol. 2, 5964. 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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4.

brain specific mass brain tissue volume

encephalization (syn. cephalization, ce phalisation)

encephalization quotient (EQ)

hominin (L. homin Man)

suture (L. sutura A Seam)

4.18.3 The Hominin Fossil Record

H. antecessor * H. rudolfensis P. robustus

Transitional hominins Megadont archaic hominins

Figure 1 Speciose hominin taxonomy.

4.18.4 Review of Hominin Taxa

4.18.4.2 Archaic Hominins

Occipital pole (OP)

4.18.4.4 Transitional Homo

log10 minimum thoracic canal CSA (mm2)

log10 minimum thoracic canal CSA (mm2)

Au. afarensis Au. africanus H. ergaster H. neanderthalensis H. sapiens

log10 endocranial volume (cm3)

log10 body mass (g)

4.18.5 Trends in Hominin CNS Evolution

EQ 1.6 1.9 5.1 5.4

LORF petalial patterna

Orbital surface of the frontal lobec

Brocas cap regiond

Temporal pole morphologyf

Lunate sulcus positiong

Thoracic vertebral canal i

1.2 1 0.8 1 1 0.9 0.9 0.9 0.8 0.7 0.7

1750 1650 1550 1450 1350 1250

Brain mass (g)

Number in sample 17 17 351 201 1 5 2 3 9 1 1 10 4 6 3 6 3 3 36 1 21 27 79 1

EQc 1.6 1.9 5.1 5.4 2.5 2.6 2.7 2.8

3 2.5 2.5 2.3 2 2.4 1.8 1.9

1.8 0.7 0.6 0.2 0.19 0.090

387 492 387 428

550 550 400 515

43 82 60 41 111 46 86 134 131 153 124

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