The governing processes that shaped the hominoid cranial base: A morphometric study with special reference to the internal basicranium

Transcription

1 Tel-Aviv University Sackler Faculty of Medicine The Dr. Miriam and Sheldon G. Adelson Graduate School of Medicine The Department of Anatomy & Anthropology The governing processes that shaped the hominoid cranial base: A morphometric study with special reference to the internal basicranium THESIS SUBMITTED FOR THE DEGREE DOCTOR OF PHILOSOPHY BY Alon Barash SUBMITTED TO THE SENATE OF TEL AVIV UNIVERSITY May 2014

2 This work was supervised by Prof. Yoel Rak

3 I. Abstract 1. Introduction I Development & Anatomy The phylogeny of the primate cranial base 1.3 The australopithecines 1.4 Previous studies on early hominids cranial base 1.5 Methods by which the cranial base is studied Aims of study Material & Methods Data source & collection 3.2 Methods 3.3 fossil material Results The hominid cranial base in the midsagittal plane Introduction Materials &Methods Results Discussion Appendix (I-II) The cranial base with reference to its internal aspect in the horizontal plane Introduction Materials &Methods Results Discussion Appendix D Geometric morphometric analysis of the endocranium and internal cranial base

4 4.3.1 Introduction Materials &Methods Results Discussion Appendix (I-II) Conclusions Cited literature תקציר בעברית II.

5 I. Abstract The hominid cranial base is the treasure trove of the skull and as such, it has been studied extensively over the past 150 years. While its complex topography is well noted, as is the major differences between humans and great apes, very few studies focus on comparative morphology of early hominids. These hominids hold data to the true nature of the basicranium morphocline, and thus must be included in any evolutionary study relevant to this area. The aim of this study is to try to decipher which of several possible processes shaped the human and hominid cranial base. In the first part, we turned our attention to the midsagittal plane. Many papers contrast ape morphology with human morphology and conclude that the massive brain expansion, characterizing modern human evolution, is the main mechanism that shaped the unique basicranial morphology of Homo sapiens. However, relatively few papers did a comprehensive comparative study of the cranial base that included early hominids. Thus, three main groups were studied: humans, chimpanzees, and early hominids. We also included juvenile chimpanzees and humans. We followed the contour of the midsagittal basicranium, starting from the posterior aspect of the occipital bone, through the foramen magnum, clivus and the sphenoidal plane in the anterior cranial base. Angular measurements were first taken in relation to the Frankfurt horizontal plane. These include the nuchal plane, foramen magnum, clival line and planum sphenoideum. The second measurements, which did not require a reference plane, were angles that are formed between two adjacent segments of the cranial base: nuchal plane-foramen magnum; foramen magnum-clivus; clivus-sphenoid plane. I

6 Our results indicate that early hominids achieve human-like appearance very early in the fossil record. Almost all australopithecines measurements lie closer to humans than chimpanzees. Furthermore, it appears that the entire section of inion-opisthion-basionclivus behaves as one morphological unit by shifting to a more inferior-anterior position, and thus creating the steeper clival angle which is apparent in hominids. When taking into consideration the small brain volume of australopithecines, our results substantiate the important role that erect posture had on shaping early hominid cranial base. Juvenile Chimpanzees in many measurements tend to follow the human-hominids morphology. This might support the neonaty hypothesis postulated by Bolk in the early 20 th century. In the second part we studied the horizontal plane of the cranial base. Early hominids basicranium may represent either the changing morphology along the ape-human morphocline, or exhibit in part autapomorphic feature unique to them. We measured the angle of the superior petrosal sinus to the midsagittal line, the position of the foramen magnum to the bi-poria line and three foramina within the basicranium. This was done on gorillas, chimpanzees, australopithecines and humans. Our results indicate that while in humans and australopithecines the carotid canal has migrated to a more lateral position, the internal acoustic meatus and foramen ovale remained around the same position as in the primitive ape state. However, the orientation of the superior part of the petrous is about the same in apes and humans at around 50, while in early hominids the petrous is orientated more sagittaly at around 40 degrees. This is coupled with the known (though forgotten) fact that the foramen magnum orientation to the bi-poria line in early hominids is actually more anterior projecting than in humans.. While early hominids display mosaic morphology, they do tend to lie closer to the human state. However, these results II

7 indicate a distinct basicranial morphology of australopithecines that sets them apart from both modern humans and apes The cause for this morphology is unclear and could be due to the biomechanical constrains in early hominids. Finally, we studied the 3D morphometric shape of the basicranium. In most cases, observation of endocranial shape and size changes tend to focus on cortical expansion in humans, in a method that perhaps overshadows other evolutionary processes that happened in the lower endocranium. In order to asses changes within the lower endocranium, we used 3D geometric morphometric techniques to capture the shape of the whole endocranium in humans and chimpanzees. 229 landmarks and semilandmarks were acquired for the whole endocranium, out of which 122 landmarks and semilandmarks were acquired for the lower endocranium. After Procrustes superimposition, a principal component analysis was taken. Observing the complete endocranium we note that from chimpanzees to humans the upper calvaria donates to the major changes observed in the lower endocranium. Nonetheless, observing just the inferior part we note other morphological changes associated mostly with the posterior cranial fossa. Next, a color-coded vector map was produced and overlaid onto an average endocranium of the different species, in order to visualize shape differences between groups. Data was analyzed in three parts: we compared the whole endocranium without omitting size; the same was done while omitting size, thus observing just shape. Finally, we compared the shape of the lower part of the endocranium. We found that while including size, the upper part of the endocranium, explains entirely the observed shape changes. Omitting size brings out major changes in the frontal and parietal area, while III

8 some changes within the cranial base, such as anterior movement of the foramen magnum. Looking just at the lower endocranium, the major evolutionary changes become clear: anterior movement and angular changes of the posterior cranial fossa; expansion of the temporal lobes; and expansion of the cerebellar areas. Adding australopithecines into the analysis emphasizes the fact that major morphological changes took place long before brain expansion. Looking at the changes observed from australopithecines to humans, we see an uplift of the central cranial base. Thus we can note two distinct processes: the first, an early change to the cranial base, especially its posterior aspect, and a second later one in which the sella turcica area shifted upward. We postulate that the first change is due to bipedal locomotion or erect posture while the second change is due to brain expansion. Summing all parts of the study reveals an interesting and complex picture: early on human evolution australopithecines had acquired a basicranium similar to the human form. We note another drastic shape change coupled with the expansion of the brain in a later process. Although australopithecines do not seem to be part of our own lineage, they must represent a sister group, very similar to some unknown hominid, that set the path to the modern human appearance. IV

9 a c 1. Introduction b The cranial base is the treasure trove of the skull. Its concealed location at the inferior end of the cranium, encapsulated by numerous muscles, vessels and nerves, masks vast possibilities for physicians, anatomists, taxonomists and anthropologists. For physicians & anatomists it is a congregation of many anatomical structures - arteries that travel into the endocranium, Figure 1. The cranial base of Pan troglodytes. a- inferior view; b- superior view; c- midsagittal view veins that come out, nerve fibers that enter or exit the brain, origin and insertion of muscles and ligaments, and the link of the vertebral column and mandible to the skull. For taxonomists and anthropologists, its complex topography, abundant with foramina occupying different positions and orientations, holds a wealth of information that can be described, ascribed, evaluated and compared within species or between species. We can speculate, based on our understanding and knowledge of the anatomy and taxonomy, about its structural, functional and biomechanical significance. Although many papers have been published on this fascinating region, there are still many questions regarding the growth, formation, morphology, as well as the influence of the different components of the cranial base on other elements of the skull, their functional importance and its evolutionary significance. 1.1 Development & Anatomy The cranial base is an anatomical unit that is comprised of several bones. It is the most primitive part of the skull (de Beer, 1937), and it is the architectural base for the brain Page1

10 and face. The formation of the cranial base begins in the second month of embryonic life Nasal capsule Presphenoid cartlage Orbitosphenoid cartilage Postsphenoid cartilage Alisphenoid cartilage Parachondral cartilage Otic capsule Intermembranous ossification Endochondral oossification Occipital sclerotomes Figure 2. Adult cranial base indicating sites of primordial cartilages of chondrocranium (Black) and extent of endochondral & intermembranous ossification (After Sperber, 1989) as an irregular set of cartilaginous platforms named the chondrocranium. It is made of two types of cells: a condensation of neural crest cells and paraxial mesoderm located in the ectomeninx (Sperber, 1989; Figure 2). This bilayer origin is extremely important to the growth and formation of the skull base, as it may manifest in several pathological conditions of the developing cranium. By the seventh week in utero, the ectomeninx will grow around the base of the brain, and will differentiate into nine groups of paired cartilaginous precursors (Kjaer, 1990). The chondrocranial precursors anterior to the notochord are derived solely from the neural crest, while the posterior ones are derived from the mesoderm (Couly et al., 1993). Thus, the middle of the developing sphenoid body marks the division between pre- and post-chondral portions of the cranial base that are embryologically distinct. At least 41 ossification centers, that appear about 8 weeks in utero, are responsible for the transformation of the chondrocranium into basicranium (Kjaer, 1990). In general, ossification starts with the mesodermally derived cartilages toward the caudal end of the chondrocranium and proceeds rostrally and laterally, forming the four major bones that comprise the skull base: the ethmoid, most of the sphenoid, parts of the temporal and the occipital bones. The ethmoid forms the center of the anterior cranial fossa, and part of the nasal cavity from three ossification centers (Hoyte, 1991). The sphenoid body is formed by fusion of the pre-sphenoid and basi- Page2

11 sphenoid around the pituitary gland and from the sella turcica. The greater and lesser wings of the sphenoid develop from the fusion of the ali-sphenoid and orbito-sphenoid cartilages to the body (Sasaki & Kodoma, 1976). Later, the lateral and medial plates, as well as portions of the greater wings ossify inter-membraneously. The temporals, which form much of the lateral aspect of the cranial base, ossify from several ossification centers, some of which are inter-membraneous, including the squamous, tympanic and zygomatic regions (Sperber, 1989). The petrous and mastoid parts of the inner ear form the otic capsule (Hoyte, 1991). The occipital comprises four bones surrounding the foramen magnum. The squamous portion Figure 3. Cartilages of the fetal chondrocranium. The vomer & maxilla are of intermembranous origin (After Sperber, 1989) is primarily the intra-membranous bone of the cranial vault, except for the nuchal region, which ossifies endochondrally from two separate centers (Srivastava, 1992) and fuses with the lateral exoccipitals on either side of the foramen magnum that fuse with the basioccipital. Three important principles steer the growth of the basicranium (Figure 3). First, the center (the oval-shaped region around the sphenoid) is formed much faster than its surroundings. This is presumably because almost all vital cranial nerves and major blood vessels perforate the cranial base around this region (Sperber, 1989). Second, the pre- and post-chondral parts grow independently, reflecting their distinct embryonic origins. Third, most of the growth in the three cranial fossae occurs independently. The anterior cranial fossa is bounded inferiorly by the lesser wing of the sphenoid and the ethmoid in the middle. Anteriorly and laterally, it is surrounded by the frontal bone. The Page3

12 butterfly shaped middle cranial fossa is enclosed anteriorly by the lesser wing and the anterior part of the greater wing of the sphenoid, and laterally and inferiorly by the greater wing of the sphenoid as well as parts of the temporal bone (the squama and the part anterior to the petrous part). It is medially bordered by the sella turcica and the body of the sphenoid bone. Its posterior rim is made mainly by the petrous part of the temporal bone. The posterior cranial fossa is bounded anteriorly by the dorsum sella, anteriorly and laterally by the posterior margins of petrous part of the temporal bone, and posteriorly and inferiorly by the occipital bone. The three cranial fossae grow in Figure 4. Superior view of human cranial base. Distribution of resorptive growth fields (-) and depository growth fields (+) (After Enlow, 1990) (Figure 4). complex series of events mainly through driftmovement of osseous parts away from another region through bone deposition on one surface and resorption on its opposing surface, and displacement-movement of osseous parts towards another region through direct bone deposition or deposition in an adjoining bone Four main types of growth processes occur within the cranial fossae. Anterior-posterior growth is formed mainly through displacement and drift; medio-lateral growth through displacement and drift; supero-inferior growth through drift; and angulation by flexion-extension (Lieberman et al, 2000a). Several differences exist in the growth and development of the basiocranium between human and non-human apes. Noticeably, in the anterior-posterior plane, the nuchal plane rotates downwards to become more horizontal in humans while it moves in the reverse way in non-human primates to become more vertical. The foramen magnum in non-human primates drifts Page4

13 posteriorly through resorption at its posterior end and deposition at its anterior end (Giles et. al. 1981). In humans, in contrast, it remains centered (Lugoba & Wood, 1990). Lateral growth occurs mainly through drift (Sperber, 1989). Superior-inferior growth is an important process as the brain grows mostly superiorly, anteriorly and laterally (de Beer, 1937). The middle cranial fossa drifts inferiorly and anteriorly to accommodate the growing temporal lobes in humans. Angulation is another important growth process. The flexion and extension of the cranial base affects the relative positions of the three cranial fossae as well as the face, brain and the pharynx. There have been numerous attempts to quantify pre- and post-chordal angulation, starting with Huxley (1867). While the postchordal line is easily defined and measured as the clivus, the pre-chordal can be obtained by several methods, consequently yielding different results (Lieberman & McCarthy, 1999). It is important to bear in mind that while the human cranial base flexes postnatally, the nonhuman primate cranial base extends postnatally, possibly through different locations and mechanisms (Liberman & McCarthy, 1999). This might indicate that the cranial base is an important phylogenetic marker that has changed throughout hominid evolution. 1.2 The phylogeny of the primate cranial base Many of the processes and factors that govern and control the shape, size and relations within the cranial base as well as its cranial surroundings have been studied extensively. Of interest to this study are those that integrate the evolutionary reasons for these changes. In most quadrupeds the skull base is almost straight and oriented throughout its length in an almost horizontal manner, ending in a posteriorly projecting foramen Page5

14 magnum (Enlow & McNamara, 1973). This was also noted by DuBrul & Laskin (1961) who stated that The basic plan of the mammalian skull is laid out along quite simple lines. The cranial base, as a forward extension of the vertebral axis, seems to govern its gross form. In many studies, brain size has been nominated as one of the main reasons for the prominent change that took place in hominoid evolution. As the size of the brain grew throughout primate evolution, especially with regards to the cerebrum and cerebellum, several interconnected processes took place. Aside from the obvious and direct growth of the upper calvaria, the facial area also exhibits marked changes (Enlow & McNamara, 1973): first, the eyes become more medially oriented (for more than one reason) causing a decreased interorbital gap. This reduces the size of the bones that construct a protruding nasal apparatus. Secondly, as the olfactory bulbs reduce in size due to a decreased sense of smell, a smaller snout is required. Thirdly, as the snout reduces in size, the naso-maxillry, and the dental complex with it, can further reduce in size. An important conclusion made by Enlow & McNamara (1973) is that A flattened, vertically disposed, orthognathic facial profile is the summated, composite result in man. The eyes are directed horizontally while the spinal cord is aligned vertically, a combination set up by the cranial base flexure caused by differential brain expansion. The facial composite is placed within the recess or pocket formed by this flexure. This assumption is also supported by indirect observations that the rate and timing of growth in the anterior cranial base appear to track those of the masticatory system (Ashton, 1957; Enlow, 1975). Ross & Ravosa (1993), however, did not find supportive evidence for this hypothesis. Page6

15 Indeed, one of the most prominent morphocline in hominoid evolution seems to be a growing flexion of the cranial base, with its distinct manifestation in Homo sapiens in which, while viewing from the mid-sagittal plane, the cranial base is broken around the sella turcica into two discrete parts: an anterior, horizontal part and a posterior, almost vertical part (Libereman et al, 2000a). As a result, the foramen magnum in humans points inferiorly Figure 5: A midsagittal view illustrating the supposed relations between basicranial flexion, brain size, and inclination of the foramen magnum. a: Tupaia; b: Pan; c: Australopithecus; d: Homo (After Aiello and Dean, 1990) and even slightly anteriorly, while in apes it projects posteriorly and inferiorly (Bigert, 1963) (Figure 5). It is important to remember, however, that the embryologic origin of this condition might actually be misleading. Some studies on the growing cranial base claimed that it is humans that retain the primitive state of the position of the FM, while apes are those that undergo rapid and extensive modification to re-orient it to a more posterior position (Lugoba & Wood, 1990). The notion that humans retain primitive features in their cranial anatomy, collectively known as neoteny or pedomorphism, is based on the early works of Louis Bolk. The prominent Dutch anatomist stated in 1910 that during the postfoetal development of the [primate] skull the foramen magnum is shifted occipitally. I had not expected this result. (pp. 373). The idea was further developed by S.J. Gould in his 1977 book Phylogeny and Ontogeny. Even so, these ideas are not widely accepted nowadays, and were refuted in many studies (Penin et al, 2002; Ackermann, 2002; Mitteroecker et al, 2004; but see Somel et al, 2009 for a different approach). Still, the marked changes between human and non-human primates Page7

16 cranial bases calls for an evolutionary explanation. Two main reasons are quoted as the reasons for the flexion of the cranial base: brain size and bipedal locomotion (Enlow et al., 1971;; Ross & Ravosa, 1993;; Ross & Henneberg, 1995). The spatial packing hypothesis suggests that as the brain increased in size during hominoid evolution, the cerebrum developed around a much milder changing diencephalon & brain stem, which caused it to flex onto its base (Enlow, 1968). Alternatively, the spherical enlargement of the cerebrum is due to optimization of the length that the white axonal fibers have to travel to the different parts of the telencephalon and diencephalon (Ross & Henneberg, 1995). Some authors claim that the large cerebellum of primates prevents a posterior growth of the brain, leading to a spherical cortex (Dean, 1988). Be the reason as it may, all these lead to a flexion of the brain that in turn influences the growth process of the cranial base, and causes it to flex to anterior-horizontal and posterior-vertical parts, thus causing the movement of the foramen magnum to a more inferior and anterior position (Bigert, 1963). The problem arising from this hypothesis is that some hominid fossils such as the Australopithecines exhibit an inferiorly oriented foramen magnum, without any apparent increase in brain size, compared to other closely related primates (See Kimbel et al., 2004). Because of this, other authors claim that the flexion of the cranial base is mainly due to the bipedal locomotion adapted by hominids (Dart, 1925; Moore et al., 1973; Demes, 1985). The hominids erect posture calls for a move of the vertebral column to a more vertical orientation, which is achieved easily by moving the foramen magnum to a more inferior position, as can be seen in most extinct hominids (Tobias, 1967). It is also easier biomechanically to balance an erect head by moving the foramen magnum to a more antero-inferior position (Shultz, 1942). The problem with this Page8

17 assumption is that many animals that maintain their vertebral column in a vertical orientation, like camels, giraffes, birds etc. have no difficulty achieving a perpendicular vertebral column and hold their heads with a posterior foramen magnum, prognathic skull and no cranial base flexion (Shultz, 1942). There is still a question waiting for an answer: Why did early hominids, as well as humans, re-orient their foramen magnum and flex their cranial bases? 1.3 The australopithecines The australopithecines are one of the best known and most studied groups in human evolution. They are considered by many to represent a group of hominids that are a close representative of the early stem that branched from an early chimpanzee-like common hominoid ancestor towards the human form, and as such they offer a unique opportunity to capture the early stages of the hominid cranial base changes. Although it has been almost 90 years since the first discovery of Australopithecus africanus - the Taung child in the exact taxonomic relationships within that group, as well as its relationships to other taxonomic groups, has been a matter of great debate. It is not the intention of this section to fully review the taxonomic status of australopithecines, but merely to point out some issues relevant to my study concerning this group. Among paleoanthropologists there is a debate as to the number of australopithecine species and their nomenclature (See Wood & Richmond, 2000 for summary), but here I shall discuss just the four major species that are the most complete, well defined taxonomically, and were available for my study: A. afarensis, A. africanus, A. robustus (sometimes referred to as Paranthropus robustus), and A. bosiei (sometimes referred to Page9

18 as Paranthropus boisei). While A. afarensis and A. bosiei are found solely in East Africa, A. africanus and A. robustus are known only South Africa. Many studies suggests that A. afarensis, a name first given by Johanson et al. (1978), is the most primitive and generalized form of this genus (White et al, 1981; Kimbel et al, 1984; Kimbel et al, 2004). The oldest representatives probably appeared around million years ago (mya), Figure 6: The skull of A. afarensis, A.L (Courtesy of Yoel Rak) spreading over a geographic range from northern Ethiopia to northern Tanzania. Although there are many sites associated with A. afarensis remains, the two main localities, which yielded the most numerous and important finds, are the Laetoli site in the Serengeti plains of northern Tanzania, and the Hadar site in the Afar Basin of Ethiopia. The Laetoli site is quite scarce in fossils, about 28 pieces, mostly teeth or maxilla and mandible fragments. It does, however, hold one of the most interesting and significant finds in human evolution: a trail set of two hominid footprints dated to 3.6 mya (Leakey & Hay, 1979), which in many aspects exhibits similar morphology to that of humans (Raichlen et al, 2010). The Hadar site was first surveyed in the late 1960s early 1970s by Maurice Taieb, who was later joined by Donald Johanson, Yves Coppens and Jon Kalb, forming the International Afar Research Expedition (IARE) in The first fossil of A. afarensis, a knee joint, was found by Johanson on October 30, For the next four years, the Afar locality around the Kada-Hadar River was dug extensively yielding several hundred fossils of hominids and other mammals. Due to political unrest, excavations ceased in 1977 and were only resumed in 1990 by the Hadar Research Project team. In 1992 the first virtually complete Page10

19 A. afarensis skull was discovered by Yoel Rak, probably belonging to a large male (Kimbel et al, 1994; Figure 6) followed by the discovery of a female skull in 2000 (Kimbel & Rak, 2010). The major cranial features that distinguish A. afarensis from the great apes and other early hominids are the inferior projecting foramen magnum, a more vertically orientated face with a protruding lower snout, and a laterally thickened and coronally aligned supraorbital region. The postcranium of A. afarensis is known from now two essentially complete skeletons: A.L (Johanson et al, 1978), known as Lucy, and a newly discovered partial male skeleton from Woranso-Mille in the western part of the central Afar depression (Haile-Selassie et al, 2010). These skeletons indicate that A. afarensis was fully biped, but with limb proportions intermediate between apes and humans. With the discovery of older taxons from Africa, mainly Sahelanthropus tchadensis (Brunet et al, 2002), Ardipithecus ramidus (White el al, 1994; White et al, 2009), and Australopithecus anamensis (Leaky et al, 1995; White et al, 2006), A. afarensis is not considered the most primitive or basal hominid, but it is by far the most studied one due to the large number of fossil remains. As Kimbel sums up in his 2009 paper (pp.39), while A. afarensis remains neither the oldest nor most apelike hominin species, it continues to be a principal record of transformation of major structuralfunctional system in hominin evolution A. africanus, as noted above, was the first African hominid to be discovered. This first fossil was a source of great debate partially because it is the skull of a young individual, estimated to be 3 years old (Lacruz et al, 2005), and partially because of common beliefs at the time about the antiquity and origin of mankind (Washburn, 1973). Over the years, A. africanus has been discovered in other cave sites, all in South Africa, all intermixed Page11

20 with animal bones, mostly within hard breccias. Beginning in the late 1930s, the Sterkfontein site started yielding numerous fossils of A. africanus (Figure 7), mostly from the member 4 strata. From the first discoveries in Sterkfontein - the TM 1511 skull, it was clear that these fossils taxonomy resembled the Taung skull. Nevertheless, Broom (1936) stated it advisable to place the new form in a distinct species, and named it Australopithecus transvaalensis, only to transfer it to another, new genus Plesianthropus transvaalensis, some 2 years later (Broom, 1938). To date, more than 600 A. africanus remains are known from Sterkfontein, and although some scholars consider all material coming for member 4 strata to belong to A. africanus, there is a debate about the taxonomic affinity of some other fossils like STS 19 (Kimbel & Rak, 1993; Ahern, 1998). Makapansgat is another cave site in South Africa, which had started as limestone quarry in , and has yielded many fossils, all associated with A. africanus. The Figure 7: Robert Broom chiseling out the skull of STS 5, A. africanus. first find in 1947, MLD 1 was initially thought by Dart (1948) to be responsible for the animal bone accumulation within the cave, thus naming it Australopithecus prometheus, after the Greek mythological Titan, the champion of humankind, who stole fire from Zeus and gave it to humans. A. africanus is considered a highly variable species (Wood, 1992). There are, however, some characters that define it (White el al, 1981; Johanson, 1985; Lockwood & Tobias, 1999; Wood & Richmond, 2000). The face is broader and less prognathic than that of A. anafernsis; a thickened lateral margin of the nasal aperture, known as anterior pillars, is clearly visible; a steeply rising inferior border of the zygomatic process; a Page12

21 reduction of the anterior teeth coupled with enlargement of the posterior teeth, compared to A. anafernsis. Lockwood & Tobias (1999) sum up: [A. africanus] may most clearly be diagnosed as a combination of usually plesiomorphic traits shared with A. afarensis and usually derived traits shared with one or all of A. robustus, A. boisei and early Homo (pp 680). The first A. robustus discovery was by a schoolboy, Gert Terblanche, in The fossil, a maxillary fragment with a first molar, was bought indirectly through a third person by Robert Broom, who later tracked down the boy, found his school, and gave a lecture about the cave sites of the area in return for a tour of the site where Gert found the fossil. The site, named Kromdraai, is a twin brecciated cavity-filled cave located about 2km north-east of Sterkfontein. Starting with this one piece, Broom dug out many other fragments belonging to the same skull, naming it TM To date (Schwartz & Tattersall, 2005) about 29 fragments were found, representing probably 9 individuals (Thackeray et al, 2001). The best known site to preserve A. robustus remains is Swartkrans cave (Figure 8). The site is located just over 1km west of Sterkfontein and was initially dug by Robert Figure 8: SK 48, a typical specimen of A. robustus. Notice the anterior pillars and zygomatic- maxilary fossa (Courtesy of Yoel Rak) Broom in November 1948 with the private funding of Wendel Phillips. Immediately after the beginning of excavation they found the right half of a juvenile mandible, SK 6 that Broom assigned at first to a new species- Paranthropus crassidens or solid tooth, due to the massive jaw holding gigantic, thick enamel teeth. The excavations were continued Page13

22 until Broom s death in 1951, and were followed by Robinson until the late 1950s. In 1996 excavation was resumed by C.K. Bob Brain, and continued until the end of the 1980s. To date, over 300 fossils have been recovered from Swartkrans. A. robustus is the slender representative of the robust australopithecines. As such, it shares some synapomorphies with A. bosiei. Some of the main morphological characteristics of A. robustus include (from Rak, 1983; Suwa, 1997; Keyser, 2000): a sagittal crest; a strong postorbital constriction; zygomatico-maxillary fossa; anterior pillars; low position of the infaorbital foramen; extensive squamo-parietal overlap; temporomandibular joint that is lateral to the cranial vault; smaller anterior teeth than in A. africanus or A. afarensis coupled with large posterior teeth;; molarization of premolar teeth;; thick enamel;; and flat molar wear. Rak (1983) notes that A. robustus in South Africa, should probably be considered a relic that continued to exist in the south and that represents the prototype from which A. boisei evolved (pp. 121). A. boisei represents the peak of the robust morphocline. The first discovery of this massive grinding-machine hominid was in July 1959 by Mary Leaky, at Olduvai Gorge, Tanzania (Figure 9). In his field notebooks, Louis Leaky first named the creature Titanohomo mirabilis, or miraculous giant man (Johanson, 1996). Although Leaky noticed the similarities the specimen had to South African fossils, such as sagittal crest, reduction in anterior teeth size - both Paranthropus traits, coupled with high cranial vault, smaller M 3 than M 2 (a trait also seen in other Australopithecines), he ultimately placed it in its own genus Zinjanthropus, and named the species bosiei, after Charles Boise who financed Leakey s expeditions (Leaky, 1959). One of the main features of the Olduvai Gorge site is that at least three different hominid species occupied the site, Page14

23 probably simultaneously: A. boisei (OH 5), H. habilis (OH 62) and H. erectus (OH 9). Of about 65 specimens that were dug, only a few are of A. boisei, but to date OH 5 skull is one of the best preserved early hominid remains. Lake Turkana, formally known as Lake Rudolf in northern Kenya, holds a record for more than 4 million years of hominid occupation. On the east side of the lake, Koobi Fora represents a formation Figure 9: OH 5, the type specimen of A. bosiei. Notice the flat, massive face with a fitted, reconstructed mandible (Courtesy of Yoel Rak) dating from mya. The site was known to be rich in vertebrate fossils from the Neogene since the early 20 th century, but its importance to human evolution was recognized by Richard Leaky beginning in a 1967 survey (Leaky et al, 1970). Among the hundreds of fossil hominids found are the famous Homo ergaster KNM-ER 3738 and KNM-ER 3883, Homo rudolfensis KNM-ER 1470 and Homo habilis KNM-ER Koobi Fora is also rich in A. boisei remains: KNM-ER 406, one of the most complete A. boisei skulls; KNM-ER 407, complete calvaria including the skull base; KNM-ER 732, face with most elements of the calvaria, probably that of a young female; KNM-ER 23000, calvaria missing the face and the basi-occipital. Work is still ongoing today by the Koobi Fora Research Project ( with many fossils still found each season. On the west side of Lake Turkana there are a series of other sites: Lomekwi, Lokalalei and Nachukui. These relatively new sites were discovered by a team led by Richard Leaky and Alan Walker in 1985 and are dated between mya. The most important discovery so far is an almost complete skeleton of a juvenile Homo erectus (referred to by some as H. ergaster) KNM-WT 15000, discovered by Kamoya Kimeu in 1984 (Walker & Leakey, 1993). A Page15

24 year after the discovery of the Turkana boy, an almost complete cranium of A. boisei (referred to by many as A. aethiopicus after Arambourg & Coppens, 1968 'Paraustralopithecus aethiopicus' mandible; see Walker et al, 1986) was found. It is currently dated to about 2.5 mya, making it one of the oldest remains of A. bosiei. Another important site that holds A. boisei remains is in the Shungura Formation in the Omo Valley. The lower Omo River basin located in southern Ethiopia, emptying into the northern part of Lake Turkana, has been studied extensively since the 1960s (Arambourg et al, 1967). Over 220 fossils have been recovered, mostly fragments, mostly dated between 2-3 mya. As noted above, A. boisei manifests the peak of the robust morphocline. It thus represents the following features (Wood & Richmond, 2000; Wood, 1991; Rak, 1983): a massive, flat face (sometimes the nasal area is actually sunk into the face) combined with a small neurocranium; high developed sagittal crest; complex, overlapping parietotemporal suture, noticed even in juvenile specimens (Rak & Howell, 1978); a relatively deep, laterally-extensive mandibular fossa for the condyle of the mandible; the mandible itself is the largest and most robust of any known hominin species; the dentition combines very large and crowded, thick enameled molars as well as premolars; the anterior teeth are extremely small. 1.4 Previous studies on early hominids cranial base The cranial base of early hominids has caught the attention of early researchers, starting with the discovery of the Taung Child in In this section I will review only papers that deal primarily and directly with the hominid cranial base. Many papers about basicranium of individual fossils have been published. These include the important early Page16

25 works on the South African material by Dart (1925) describing the Taung child and the 1948 papers on the Makapansgat skulls, as well as Broom, Robinson & Schepers works (1946; 1950) about the fossils from the Sterkfontein cave, and Tobias (1967) in his comprehensive monograph about the OH 5 skull. These important monographs tend to lack quantitative comparative data, mainly due to the scarcity of other fossil material (although collections of ape and human materials were available at the time, but were not used). More recently, Kimbel et al (1984), in the first extensive review on the composite reconstruction of the skull of A. afarensis, include an analysis of the skull base with some quantitative data comparing it to other known fossils of the time. In their review, they include data on the orientation and position of the occipital squama and the foramen magnum. Their results established the primitive and pleisomorphic nature of A. afarensis, compared to other, robust Australopithecines. Brown et al (1993) describe KNM-ER and compare it to other A. boisei in order to determine its taxonomic affinity, but use very little comparative data about the cranial base. The same descriptive analysis is made for the Drimolen skull, A. robustus from South Africa (Keyser, 2000); Omo 323, A. boisei from Ethiopia (Alemseged et al, 2002); and SKW 18, A. robustus from Swartkrans (de Ruiter et al, 2006). Surprisingly, to this day, very few papers actually deal with measuring australopithecines cranial base features in order to identify the evolutionary, morphological and biomechanical relation between them and other extant and extinct groups. This is despite the fact that at least from the mid 1980s onward, quite a large sample had been accumulated for study. An example of this is an article by Ross & Ravosa (1993) who state that We suggest that the high degree of basicranial flexion in humans can be explained as an extreme instance of a general rule that large brains Page17

26 relative to BL [Basicranial length] tend to be associated with increased basicranial flexion, without measuring any fossil hominid. Dart, in his milestone paper describing the first Australopithecus africanus, notes that head balancing index i.e. the position of the foramen magnum, is more similar to that found in men that in apes. He argues that the poise of the skull upon the vertebral column, points to the assumption by this fossil group of an attitude appreciably more erect than that of modern anthropoids (Dart, 1925;; pp 197). Keith in his book New Discoveries Relating to the Antiquity of Man, rejected Dart s view and pointed out that based on the Taung skull, there was no reason for believing, on the evidence supplied by the skull, that the posture of Australopithecus differed from that of the young chimpanzee or gorilla (Keith, 1931; pp 113). But with the discovery of more mature skulls in South Africa, especially with the work of Broom (1938) and Broom & Robinson (1952), it became evident that these creatures manifested features in their cranial bases that were unique to the hominid clade. More studies about the cranial base were published along the years, and these can be divided into two types: those dealing with the midsagittal view and those dealing with the norma basilaris view. The studies dealing with the midsagittal line concentrate on the position and orientation of the foramen magnum (Ashton & Zuckerman, 1951; Luboga & Wood, 1990); basicranial flexion (Ross & Henneberg, 1995) or both (Tobias, 1967; Kimbel et al, 1984; Lieberman et al, 2000; Kimbel et al, 2004; Kimbel & Rak, 2010). These studies tend to emphasize the intermediate state of the hominids cranial base (this is especially true for the early studies) or the synapomorphic state of the australopithecines cranial base, shared with humans. Very few papers venture out of the midsagittal line and use bilateral structures Page18

27 for study. These include Dean & Wood (1981; 1982), who performed a landmark-based metrical analysis of the basilar part of the skull base and showed a difference between robust and gracile australopithecines and early Homo. Spoor (1997) did a CT based analysis of STS 5 and other early hominids, using the internal aspect of the cranial base. He has shown that, generally, the basicranial shape is correlated with brain size. Ahern (2005) studied the position of the anterior border of the foramen magnum (i.e. Basion) in relation to the bicartoid and biporion chords, and found that basion to bicarotid distance is a good indicator for taxonomically identifying Plio-Pleistocene samples as members of the hominid clade. 1.5 Methods by which the cranial base is studied The methods by which the cranial base has been studied are as numerous as the studies themselves. The early founding fathers of physical anthropology like Virchow (1857) and Broca (1871) noticed l angle sphénoidal, and Topinard (1891) in his La transformation du crâne animal en crâne humain stirred one of the earliest discussions about the role of the cranial base in anthropoid evolution. Cameron (1927) wrote about the the main angle of cranial flexion, while Weidenreich in his papers of 1943, 1945 and 1947 addresses the role of the brain in the shaping of the cranial base, although he initially thought that bipedal posture and locomotion were the causes of the cranial base shape (Weidenreich, 1924). Most of these early studies, as well as many current studies, were performed using the mid-sagittal plane and the Frankfurt horizontal plane as the registration line to measure angles or distances. Many authors in the s addressed the issue of cranial deformations and their manifestation in the cranial base (Moss, 1955, Page19

28 1958; Young, 1959; McNeill & Newton, 1965). Some of these studies were done by observing deformed human skulls either artificially or as a result of pathogenic processes (such as micro- or macro-cephalic individuals, hydrocephaly, etc.). More recent studies have tried to gain better knowledge of the embryological growth process of the skull base (see the thorough review by Lieberman et al, 2000). Several methods have been revised to register the flexion between the anterior and posterior sella. Among these we can find the nasion-sella-basion of Björk (1955); Landzert s sphenoidal angle defined by the angle formed by clival plane to the ethmoidal plane of Landzert (1866) also used by Ross & Ravosa (1993); basion-sella foramen cecum by Cousin et al, (1981), Spoor (1997) and Figure 10: Common cranial base angles. CBA1 is the angle between the basion-sella (Ba-Sl) line and the sella-foramen caecum (Sl-FC) line. CBA4 is the angle between the midline of the postclival plane, and the midline of the planum sphenoideum (After Lieberman et al, 2000) Lieberman & McCarthy (1999); orbital angle by Anton (1989) using the basion-sella and the plane of the superior orbital roof. One of the main drawbacks of these methods is the fact that the measured points themselves are subject to considerable variability due to individual size, growth rate, age, species-specific anatomy, etc. It is also important to bear in mind that all these studies take the Frankfurt horizontal plane as the reference plane usually through lateral radiograph. Any use of ordinary lateral radiograph is bound to hold some degree of inherent imprecision, because of the inaccuracy of creating a lateral radiograph while the skull is exactly orientated to the FHP (Pancherz & Gökbuget, 1996). This has probably led to great variety in the results obtained by some studies. For example, the association Page20

29 between brain size and cranial base angulation depends on the method used: If one measures the basion-sella-foramen cecum to brain volume as Spoor (1997) did, then humans have the predicted flexion as expected by the regression line predicted through other Haplorines. If, on the other hand, we use Ross & Henneberg s (1995) method, the basion-clivial point-sphenoidale-planum, humans actually have less than the predicted flexion. Thus, cranial base angle and its relation to the orientation of the foramen magnum and bipedal walking is another layout that has turned out to be difficult to prove. Strait & Ross (1999) captured the head-neck angle in living primates through videotaping primates with their habitual head posture. Their conclusion was that cranial base and foramen magnum orientation had little to do with bipedal walking. The same conclusion was reached by Lieberman (2000) through the study of the orientation of the foramen magnum in relevance to clivus and orbital axis. With the introduction of new technologies such as spiral CT, MRI and 3D data acquisition, it is easy to gain data sets in elaborate ways in order to shed new light on these problems. The use of advanced statistical methods such as multivariate analysis might bring an improved understanding to relationships of the different structures of the cranial base and their anatomical significance. It is also essential not to forget the classical methods. The use of caliper and regular ruler may prove highly vital, if one uses the right dataset and analysis. The practical approach in this study will be made through use of both techniques. The most important key issue to bear in mind, regardless of measuring methods, is that one must quantify the right set of measurements on the right set of data in order to obtain meaningful results. Page21

30 2. Aims of study The morphological, taxonomic and anatomical importance of the cranial base has long been determined. Despite the numerous works done on this fascinating area, it is still unclear what are the main driving forces that shaped the cranial base, and their chronological order. Was it just endocranial shape and volume, or does erect posture and bipedal locomotion also play an important role? Incorporating early hominids into the study might reveal some answers to these questions. We thus divided our study into three parts: 1) What is the nature of the cranial base in the midsagittal view? More specifically does including early hominids into the study changes the results obtained in previous studies? 2) What is the nature of the cranial base in the horizontal view? How does this relate to the sagittal view, and what can we learn from the similarities or differences between the two aspects? 3) What is the nature of the relationship between the whole endocranium vs. its lower part? Can one influence the other, and can we break down the endocranium into distinct evolutionary part? The "results" part in this work is subdivided into individual manuscripts, as these parts are on different stages of publication. The last chapter summarizes all previous chapters and discusses the entire body of work in order to understand the morphocline of the evolution of the cranial base P age 22

31 3. Material & Methods 3.1 Data source and collection The material used in this work was comprised from four sources: living humans, dry skulls of apes, fossilized hominids and high quality casts of hominids. Data were obtained through CT scans of the four groups. The human sample was acquired through routine medical CT scans performed on patients in a hospital in Israel for diagnostic purposes, mostly head-related. The scanning machine was a Phillips Brilliance 64, set with the standard settings of 120kV, 30mA and 1.5mm slice thickness. For this study, and according to the Helsinki agreement, the output DICOM files were anonymized except for age and sex data. About 200 scans were obtained, including males, females and children. Scans that seemed to manifest head trauma involving cranial deformation or those exhibiting congenital deformations or malformations were excluded from the study. The current Israeli population, as exhibited in the scans, is characterized by a mixture of nationalities from different origins and thus represents a wide variability of morphology due to both shape and size. The ape skulls came from two main sources: about 20 of the chimpanzees (Pan troglodytes) are from the Harvard University Zoological Collections, obtained in the 1920s-30s from Central Africa. Very little is known about the origin, locality, age and other individual data of the specimens. Most individuals seem to be wild shot as is evident from the bullet holes or machete cut marks on the crania. They were scanned by J.J. Hublin (personal communication) with a medical CT with the same settings as for living humans. Sex and approximate age were determined by me. Few other chimps and gorillas came from the Digital Morphology Museum, KUPRI, at Page23

32 Kyoto Japan ( This collection is well document as specimens arrived from known location around Japan. Other apes, including two gorillas (Gorilla gorilla), three chimpanzees and one orangutan (Pongo pygmaeus), came from the osteological collection of Yoel Rak, obtained over the years from local zoos in Israel, and for which age and sex is either known or easily identified. The original fossil hominids included two specimens: STS 5 from Sterkfontein, South Africa and MLD 37/8 from Makapansgat, South Africa. Both specimens were scanned by the Anthropology Department at the University of Vienna and virtually reconstructed by Simon Neubauer as part of his Master s degree under Gerhard W. Weber (personal communication). The fossil casts are made either of high quality plastic resin or dental quality plaster, and represent an accurate copy of the original specimen. I scanned the following casts: A.L , A.L. 882, A.L from the Afar locality in Ethiopia; KNM-ER 23000, KNM-ER 407, KNM-ER 406 from east Turkana Lake locality in Kenya; OH 5 from the Olduvai Gorge in Tanzania; Omo from the Shungura Formation in Ethiopia; KNM-BC 1, known as the Chemeron temporal, from Baringo Basin, Kenya. I scanned all the casts at the Sheba Medical Center (Tel-Hashomer) using standard CT settings. The taxonomic affinity, morphology and methods of reconstruction will be discussed separately in the methods section. It is worth to note that since I analyze large anatomical structures, the use plastic or plaster casts should not influence the results. All casts were created from the original fossils, and by skilled personal. 3.2 Methods Some of the methods employed in this study were used for specific-type analysis and are discussed in their appropriate sections. In this section I will discuss a Page24

33 number of methodological issues in greater detail than in specific chapters, because the results chapters were written in manuscript form, which necessitates a limited discussion of methodological issues. The methods discussed below include 1) scanning, importing and aligning each specimen, 2) linear and geometric morphometrics data, and 3) the fossil australopithecines taxonomic affinity, geological setting and virtual reconstruction. Creating, importing and aligning each specimen The main rationale of using data from CT scans stems from the three facts: 1) It is the most accurate and easy way to measure data simultaneously from both outside Figure 10: Soft tissue identification from a CT scan: 3 landmarks of the insertion of the two medial rectus muscles, and the origin of the left medial rectus muscle (from OSIRIX software) and inside the specimen. Using radiographs can achieve the same goal, but it is far less accurate, as identifying landmarks might prove difficult, depending on the quality of the radiograph and the abilities and knowledge of the researcher. One can also easily obtain soft tissue landmarks. 2) 3D data is extremely easy to obtain and landmark locations are very easy to validate by visually viewing & rotating the specimens in 3D space. Specimens can also be cut on any plane for a better inner view. 3) Landmarks are easily repeatable and in case of mistake, or if there is a necessity to add landmarks, there is no need to repeat all of dataset alignment and landmark acquisition, as would be the case if an X-ray or a Microscribe device were used (Figure 10). Acquiring landmarks from digital data is a fairly easy process. We can extract 3D landmarks of type I, II and III from the surface mesh created. Landmarks are Page25

34 defined by Bookstein (1991) as either Type I, which are anatomical structures that can be identified easily in each specimen such as foramina, meeting of sutures, etc; Type II, which are points of maximum or minimum height such as the tip of the mastoid process, opisthocranion, etc; and Type III, which are landmarks over curvature sometimes equally spaced, and sometimes in the form of semi-landmarks, a method used here, and summarized in Gunz et al, 2009; Zelditch et al, 2004; Bookstein, 1997). All scanned material whether living, dry skull, fossil or plastic cast, were imported into Amira software ( This platform is the most commonly used data visualization and manipulation software in many paleoanthropological studies today (Nishimura et al, 2007; Gunz & Harvati, 2007; Spoor et al, 2008; Neubauer et al, 2009; Bastir & Rosas, 2009; Jeffery & Cox, 2010; Benazzi & Senck, 2011). The data were converted from the original sequential DICOM files into surface mesh models and saved as either Amira mesh surface (*.surf) or other commonly used mesh types such as AutoCAD DXF, stereolithoraphy STL, or Stanford PLY. Each skull was then reconstructed using Amira, Rapidform ( and 3D max ( The process and technique used for each case is discussed in conjunction to the relative specimen, as not all methods were used in each reconstruction. After the reconstruction process, all specimens were aligned to the Frankfurt Horizontal plane in the same 3D axis system. Using 3D max software, I have created a plate and a one beam running across the plate to represent the midsagittal line, and three beams that transverse the midsagittal beam to aid in placing the skulls within the plate. The plate was imported it into Amira. All specimens were aligned in such a way that each Page26

35 skull was immersed in the middle of the plate with the middle beam transecting the midsagittal line of the skull and the posterior beam transecting the skull through the two external acoustic meatus, running exactly through the porion. The skulls were then rotated so that the left orbitale was touching the plate (Figure 11). Figure 11: STS 5 aligned to the Frankfurt horizontal plane using a plate as reference plane Linear and geometric morphometrics data Collecting data is the most important part of any scientific research. If one aims to study and distinguish closely related species, or to follow the evolutionary morphocline of hominids, then counting the number of fingers or teeth, for example, is useless and will produce erroneous results. If one measures the length of the humerus, a clear distinction will be found between most if not all of the African great apes. It is thus extremely important to measure meaningful data, regardless of the measuring technique. Two types of data collecting exist: qualitative and quantitative. The first step in any taxonomic, morphological or biomechanical work - paleontological or modern - is the qualitative assessment of the similarities and differences between the studied species. Many characteristics can only be addressed qualitatively, as they are too small, possess complex topography or are difficult to Page27

36 capture quantitavely. However, the use of distinct qualitative anatomical traits to distinguish between two closely related taxons may be problematic, as finding a unique, autapomorphic feature that separates the species becomes a difficult task. Some of the traits, like keels, torui and protuberances, may be debatable as these may not appear the same to all eyes. Two main types of data were used in this study: linear or angular measurements and landmark-based analysis. Linear measurements are the most common method of data collection in most morphological studies. As noted above, it is sometimes enough to compare the length of a humerus in order to taxonomically separate chimpanzees and humans. Linear measurements can be taken directly from a specimen using devices such as a caliper or goniometer, or from a photo or x-ray. It can also be taken using indirect methods such as acquiring two 3D landmarks and calculating the distance between them using the equation: d ( x z. The same is true for angular measurements x1 ) ( y2 y1) ( z2 1) using three 3D landmarks: a b c arccos where a, b and c can be calculated 2ab according to a distance equation. Another measurement method is through vector analysis, and since vector analysis plays an important role throughout this work, it is worthy of some detailed explanation. Since the dot product of two vectors (representing two lines) is a b a b cos, it is easy to extract the angle θ by cos a b ( ). We can also find the angle of a line to a plane, for example, the angle a b between opisthion-basion and the Frankfurt Horizontal Plane (FHP). This would actually be the most mathematically accurate way to measure the inclination of the Page28

37 foramen magnum to the FHP. The equation of plane τ is Ax+By+Cz+d=0, while vector n has a,b,c components. The angle between plane τ and vector n is ω, is given by the equation: sinω A 2 B Aa Bb Cc 2 C 2 a 2 b 2 c 2. We can also calculate the angle between two intersecting planes, using the normal vector of each plane: cos ^ 1 ^ 2 a 2 1 a a 1 b b b c c c a b 2 2 c 2 2. This equation will be widely used in the first section of the analysis. Lastly, we can also fix problems of skull asymmetry using the same basic techniques. Most animals possess a bilateral symmetry, meaning that the midsagittal plane bisects the head into two identical, mirrored parts (of course, as with any biological organism, the two parts are never exactly the same, but for our purposes, we assume it to be). This means that we can correct the asymmetry by projecting landmarks from the normal side onto the other distorted or missing aide, in order to obtain the averaged mirrored image, and thus correct the deformation. When we define a plane (in our case the midsagittal), any normal vector crossing that plane will have two equivalent points along both sides of the axis of the vector. We define the original point P 1 and the mirror point P m, then p m p 1 2* distance* nˆ, and the distance is ( p 1 p) nˆ then p m p1 2* n*( p1 n) 2* n*( p n). Since p nˆ 1 is constant, then k p nˆ p * n p * n p * n and p m p * nˆ *( p nˆ) 2* nˆ * k. We x x y y z z can now split the equation into x, y, and z components: p p p mx my mz p 1x p p 1y 1z 2 * n 2 * n 2 * n x y z * ( p * ( p *( p 1x 1x 1x * n * n * n x x x p p p 1y 1y 1y * n * n * n y y y p p p 1z 1z 1z * n ) 2 * n z * n ) 2 * n * n ) 2 * n z z x z y * k * k * k Page29

38 All of these equations were imported into Microsoft Excel software, and the measurement processes were automated in order to minimize any potential for errors such as copying and pasting. Geometric morphometric (GM) techniques are widely used, and are becoming very popular. The purpose of GM is to quantitatively research the shape changes of a series of objects. It is very important to note that linear measurements do not quantify the shape of an object but only its attributes. The first attempts to use GM took place as early as the late 19 th century (see Bookstein, 1998 for complete historical background) with the work of Galton, who introduced the correlation coefficient and applied it to a variety of morphological measurements on humans. In 1907 he invented a method to quantify facial shape that was later named two-point shape coordinates. An important step was made with the work of d'arcy Thompson in the beginning of the 20 th century, in which he constructed deformation grids illustrating how a part of one organism may be described as a distortion of the same part in another individual. Thompson s approaches are visually appealing, but the drawings were made by hand without any reference to a formal mathematical algorithm. It was only towards the end of the 1980s, with the growing power of computers that the full potential of GM came to light. The main advantage and power of the current ability of GM is its capability to visually explore statistical shape changes. The landmarks themselves do not have statistical value before we can separate the shape from other factors such as size, orientation in space and position, which are usually not relevant to the analysis. The first step after acquiring a set of homologous landmarks is to superimpose all specimens onto each other in order to minimize those effects. This is Procrustes superimposition and is performed in three steps: 1) Moving the sets of landmarks so that all specimens share the same centroid; 2) Scaling the landmarks so Page30

39 they all have the same centroid size by the square root of the summed squared deviations of the landmarks from their centroid; and 3) Rotating all shapes until the sum of the squared Euclidian distances between homologous landmarks is minimal. In traditional multivariate statistical analysis, tests are applied to a set of measurements that usually do not share common units or comparable ranges. Thus, traditional statistical analysis is usually based on correlation matrices and comprises the full range of multivariate techniques and statistical tests. In GM, on the other hand, since all variables possess the same units, the analysis is based on a covariance matrix. The results of these multivariate analyses, such as principal component analysis, can be visualized as actual shapes or shape deformations in the geometry of the original specimens. The original shape landmarks can be superimposed and deform the target shape to visually and statistically follow shape changes. The fossil material In this section I shall describe the fossils that were used in this study. The history and taxonomy of each fossil will be discussed. As most of the fossils are not complete or suffer from deformations, I will also discuss the specific procedure of each reconstruction. A.L This specimen (Figure 12) represents the first complete skull of A. afarensis to be found. It was found on 26 February 1992 by Yoel Rak (Kimbel et al, 1994). It came from beneath the BKT-2 tephra which dates to mya and above the Kada Hadar tuff which dates to 3.18 mya (Walter, 1994). The skull was recovered in about 50 fragments which were joined to form 8 major parts. After reconstruction, the skull still suffered from deformations and breakage. These were corrected on the plastic cast, as described in Kimbel et al (1994, pp17-20). Even after this the skull still holds Page31

40 some asymmetries: it has a marked right bow, when viewed from an inferior view. Also, the facial area holds some deformities. In my reconstruction, the bowing of the skull was virtually corrected using the method described in the geometric morphometric section of the methods. Figure 12: Basal view of A.L Left, the original reconstructed skull scan with obvious right bow; right, symmetrized reconstruction. Notice that some asymmetries still exist, especially in the temporal fossa region. A.L A.L (Figure 13) represents the first complete skull of a female A. Afarensis. It was found in 2000 by the late Dato Adan, an Afar member of the Hadar Research Project (Kimbel & Rak, 2010). It was discovered on the surface of the KH-1 submember which is dated to around 3.1 mya (Kimbel & Delezne, 2009). The specimen was found about 3 km east of the site where A.L originated and about 8km east of the A.L locality. The skull was found in more than 200 Page32

41 fragments, and was cleaned and reconstructed to an almost complete state, although it still suffers from taphonomic distortion: it is unsymmetrical with a left bow, when observed from an inferior view. To correct this asymmetry we used the same method that was used for A.L , as described in the geometric morphometric section of the methods. As a result the skull is almost symmetrical, although it still possesses some asymmetries in the dental arcade malar and zygomatic arch areas. Figure 13: Basal view of A.L Left, the original reconstructed skull scan with obvious left bow; right, fixed reconstruction. Notice that some asymmetries still exist, most noticeably in the zygomatic arch. A.L The Afar Locality 333 was discovered by Michael Bush, a graduate student of Donanld Johanson, in 1975 (Johanson, 1976). The site, comprising of adjoining hillsides and drainage gullies below them, were filled with hominin fossils. Major excavations at the site took place between 1975 and 1977, and yielded more than 200 Page33

42 fossils, most of them surface finds estimated to represent at least 13 individuals. The most famous is A.L , an almost complete though taphonomically deformed skull of a young A. afarensis. As almost all fossils were found on or near the surface, it is assumed that they died at the same time, possibly due to some local event such as flood (Johanson, 1980). Because of this, the site has been known as the "first family", and indeed most research has pointed out that all specimens are representative of A. afarensis (Johanson et al, 1982; Gordon et al, 2008). A.L (Figure 14) consists of two calvaria parts that were used in conjunction with the A.L facial fossil in the original composite reconstruction of A. afarensis (Kimbel et al., 1984a; Kimbel and White, 1988), preceding the discovery of the complete skull of A.L The right fragment consists of the temporal bone, including the petrous, glenoid fossa, almost complete mastoid process, but missing most of the squama and zygomatic process. It also holds parts of the basioccipital including the digastric fossa and occipital condyle. The more complete left side includes an almost complete temporal bone, with a deformed petrous bone and a missing zygomatic process, most of the parietal bone exceeding the midline and parts of the occipital bone including the nuchal lines, small portions of the margin of the foramen magnum, but missing the occipital condyle. When aligning the two parts it appears that there is a taphonomic deformation: the right side projects much more inferiorly than the left side. This is particularly evident when examining the skull from an anterior view. Thus, in order to utilize this specimen, two procedures have been taken: first, to restore those parts that are missing from one side to the other and second, to realign the calvaria. Since the left side is more complete, I duplicated that part. Using rapidform, I cut out the deformed right petrous and copied the left, complete part onto it. The same was done for the occipital condyle and foramen magnum. Because the two parts now overlap in Page34

43 their superior (parietal) area as well as in the lower occipital area, aligning the two halves was an easy task. In order to make sure that this reconstruction is correct, measurements from the original A. afarensis reconstruction including occipital condyle breadth, bicarotid breadth, and maximum skull breadth, were taken and compared. The skull is still missing the anterior part of the cranial base such as basion, clivus and the entire sphenoid bone, although the posterior margins of foramen ovale are visible within the temporal bone as is the case in some early hominids (Tobias, 1967). With the current reconstruction, although not perfect, we can safely measure many of the cranial base features of this specimen. Figure 14: A.L a- basal view of original fossil; b- anterior view of original fossil; c- inferior view of reconstructed fossil; d- anterior view of reconstructed fossil. Notice the marked asymmetry of the petrous in the original compared to the reconstructed model and the foramen magnum area in the original compared to the reconstructed model. Page35

44 STS 5 This complete skull (Figure 15) was acquired by one of the most original methods applied in prehistory studies: dynamite blast (Potze & Thackeray, 2010). In 1947 using the help of limestone miners, Robert Broom, assisted by John Robinson, blew up parts of Sterkfontein Member 4 cave site area, (known as the Sterkfontein Type Site, hence STS). After a few explosions, they discovered two parts of a complete skull in the hard breccia. The parts were taken back to the Transvaal Museum in Pretoria, where they were mechanically prepared using a hammer and chisel (Broom, 1947). Aside from the obvious breakage line, visible mainly on the left side, the skull is complete aside from the teeth that apparently were lost postmortem. Some delicate parts, like the orbits were not freed of the breccia. These parts were virtually cleaned by Simon Neubauer, then at the Department of Anthropology, University of Vienna, and made available to this study (personal communication). To this day, STS 5 is considered one of the best representatives of A. africanus. Figure 15: STS 5 matrix free virtual model. Left, superior view with skullcap removed; Right, inferior view. Page36

45 STS 19 STS 19 (Figure 16) is another skull that came from Member 4 in Sterkfontein cave. It has an almost complete cranial base on the left side, while the right side is missing elements from the temporal bone like the glenoid fossa and the occipital bone. On the left side, the zygomatic arch is complete connecting anteriorly into a remnant of the zygomatic bone. The posterior part of the maxilla is also visible on the left side still holding the M 3 tooth. All foramina on the skull base as well as the occipital condyle, clivus, sphenoidal sinus, parts of the pterygoid plates, and the posterior nasal opening are visible. The reconstruction of this skull was done by duplicating the left side and then aligning and superimposing it on the right side. Since a substantial part of the right side is also complete, this process was fairly easy. The taxonomic affinity of STS 19 is a source of great debate. When Broom & Robinson first described it in 1950, they noticed the human proportions of the posterior cranial fossa. Schepers (1950) in the same volume claimed that "The manner in which the cerebellum has come to be shifted forward and below the cerebral occiput is most striking. The general arrangement is that found for the human brain, especially Homo sapiens". (pp 102). In spite of these insights, they classified the skull with the rest of the Member 4 material as Plesianthropus transvaalensis, later to be renamed A. africanus. Clarke (1977) in his PhD thesis also noticed the Homo-like morphology of STS 19, especially in the sphenoid and temporal bones, but he also considered the possibility that A. africanus, with STS 19 included simply displayed a wide range of variability. Kimbel & Rak (1993) defined 12 features that in STS 19 resemble those of Homo- such as the inclination of the tympanic plate, the size of the postglenoid process, the existence of vaginal process, the shape of the lateral Page37

46 pterygoid plate, and others. Ahern (1998), based on the same traits, has shown the contrary. Figure 16: STS 19. Left, superior view of original specimen; Right, reconstructed model. MLD 37/8 MLD 37/8 (Figure 17) is the most complete specimen recovered from Makapansgat. It was found in 1958 by James W. Kitching (Dart, 1958; 1962) in a limestone quarry. The skull was found in two separate blocks of breccia. The first, left side was found on site, while the second, right side was found a year later while going over the 60 tons of pink breccia that the first half came from. The two halves were cleaned and combined. The skull is missing its anterior portion but almost all of the neurocranium is present. According to Dart (1959a), the anterior aspect was weathered or eroded away. Dart (1962) also speculated that some of the anterior damage to the skull was pre-mortem and is probably due to predatory activity. The inner matrix of the skull was never cleaned, probably due to technical difficulties at Page38

47 the time. The endocranium was restored virtually by Simon Neubauer (Neubauer et al, 2004) and was made available to this study by Gerhard Weber of the University of Vienna and Simon Neubauer, currently at the Max-Planck Institute in Leipzig. Figure 17: MLD 37/38. Left, superior cut view of the matrix filled endocranial cavity; Right, matrix-free model. KNM-ER 407 This fossil (Figure 18) came from the lower unit in Ileret (area 10) locality, dated to around 1.85 mya (Feibel et al, 1989). It was found in several fragments in 1969 by Mwongela Muoka (Isaac et al, 1971). Although the fossil suffered some preand post- fossilization damage, it was carefully reconstructed by Ron Clarke (Day et al, 1976). The cranium is almost complete, lacking only the face. Due to its small size and gracile form, it is presumed to be that of a female A. Boisei. After restoration, the skull consists of three parts: two forming the cranial base with attached portions of occipital, temporal, parietal and sphenoid, and one part of the calotte consisting mainly of the parietals. The skull exhibits taphonomic deformation and post-mortem breakage: on the left side, the area above the external auditory meatus is fragmented Page39

48 as is the mastoid area. The petrous seems to be in the correct orientation, but has shifted upward. The parietal bone is partially deformed and is less oblique than in its original anatomical state. The occipital condyle is also deformed, with a sagittal bend. The right side of the calvaria is smaller than the left, lacking part of the mandibular fossa. The petrous is misaligned, and projects superiorly; it has departed from the occipital bone. In order to reconstruct the cranial base, I used the right side, and added part of a mirrored left side in order to complete the occipital area all the way to the midline. I also reoriented the petrous bone to a more inferior position (although this does not affect the petrous sagittal orientation). I then duplicated and mirrored this part to complete the skull. Measurements were taken from the original and the cast to ensure that the reconstruction was feasible. Figure 18: KNM-ER 407. Left, two main fragments of the unreconstructed specimen. Right, reconstructed model. Notice the symmetry in the foramen magnum region and the absence of the projecting part of the mandibular fossa in the reconstructed model. KNM-ER This specimen (Figure 19), which consists of much of the calvaria, was found in 1990 by Bwana Kyongo in area 104 in Koobi Fora, Kenya (Brown et al, 1993). It was excavated in 1990 by Meave & Richard Leakey, Carol Ward, and Alan Walker, Page40

49 and the following year by Barbara Brown & Alan Walker. The geological age is slightly less than 1.9 mya, as it comes from the KBS Tuff level (Feibel et al, 1989). It was found in green lacustrine cement-like sands, suggesting that it was deposited on a shore or in a near-shore environment. The fossil contains the frontal, both parietal, both temporal with a small portion of the sphenoid, and most of the occipital, lacking the foramen magnum area (although opisthion is present). The bones were found separated from each other by a short distance, and they were probably detached prefossilization. The frontal bone shows a slight taphonomic deformity and is not completely aligned with the rest of the calvaria. From the shape of the supraorbital ridge, the developed sagittal crest, the protruding mandibular fossa, and a flaring zygomatic arch, it is considered to be that of a young male A. boisei. In my analysis, since the foramen magnum and its surroundings are not present in KNM-ER 23000, I imposed a scaled and landmark-fitted model of OH 5 onto it, as these two fossils are very similar in shape, size and age (Brown et al, 1993). Figure 19: KNM-ER Left, original scanned model; Right, OH 5 imposed on KNM-ER Notice the overall similarity in shape and size between the two fossils. Page41

50 OH 5 The skull of Zinjanthropus boisei (Figure 20) was discovered by Mary Leakey on July 17, 1959 (Leakey, 1959). It was found near the surface, as it began to erode from the slopes surrounding it. Despite the fact that the skull was completely broken, almost all the cranium was present, suggesting that all breakage was due to taphonomic activity of the clay that the skull rested in. The skull, with its hundreds of fragments was carefully reconstructed to 6 major parts. It is important to note that the posterior parts including the occipital, temporal, parietal and sphenoid do not connect directly to the anterior maxillary and frontal parts. The skull was reconstructed twice: first by the Leakeys and then, with slight adjustments, by Ron Clarke under the supervision of Philip Tobias. This reconstruction was later published in Tobias monograph on the skull in Tobias was also the one to sink the Zinjanthropus, together with Paranthropus into one genus - Australopithecus (Tobias, 1967, pp 232). In my study, no virtual reconstruction was necessary, aside from aligning the four neurocranial parts. Figure 20: OH 5. Left, inferior view; Right, superior view with the parietal bones cut. Page42

51 4.1 The hominid cranial base in the midsagittal view Introduction Figure 1. Midsagittal view of the cranium of Homo sapiens The hominid cranial base drew the attention of anthropologists from the onset of research in the field. In particular, the suggested part that the basicranium plays in erect posture and brain and facial development has been the subject of numerous studies since the beginning of modern research in physical anthropology. The midsagittal plane (Figure 1), transecting the skull through the occipital, parietal, sphenoid, ethmoid, frontal, and the sutures between the palatine and maxillary bones, holds important morphologic data. The importance of structures along this plane was noted long ago, beginning possibly with the work of the famous French naturalist Louis-Jean-Marie Daubenton (1764) titled Memoire sur les differences de la situation du grand trou occipital dans l'homme et dans les animaux, in which he noted the marked differences between the inclination of the foramen magnum (FM) in different animals including apes and humans. Bolk, in a 1910 paper, used a mediagram, a midsagittal craniograph tool, to calculate his index basalis for the position of the FM in primates, ranging between fetuses and adults. He notes that during the post foetal development of the skull [of apes] the foramen magnum is shifted occipitally. I had not expected this result. (Bolk 1910a, pp. 373). In a second paper appearing in the same volume, he studied the orientation of the FM (Bolk, 1910b) and noted the same primate morphology, which he contrasted by the fact that in humans, P age 43

52 the foramen magnum seems to retain its primitive, fetal position. Keith (1910) describes a new craniometer he designed specifically to record external and internal midsagittal measurements of the skull. Cameron (1927) in his article about the Pituitary-Nasion- Basion angle speculates that A vast evolutionary gap exists between the anthropoids and man, with regard to the size of this angle. This is logically the space where the various 'missing links' would have to fit in. With the discoveries of early hominids in South Africa in the s, the monographs describing these fossils paid much attention to the midsagittal plane and especially to the position and orientation of the FM. Examples of this can be found in the material from Sterkfontein and Swartkrans (Broom & Schepers, 1946; Broom, Robinson & Schepers, 1950; Broom, & Robinson, 1952). Franz Weidenreich in his review of the Asian and African hominids (1947) claims that the more central localization of the occipital foramen in relation to the total basal length of the skull, are the effect of one and the same transformative process, the final cause of which is the adjustment of the skull to the acquisition of erect posture. (pp. 407). More recently, some studies have focused on the clinical significance of the special human basicranial shape and its bearing on laryngeal size and position, and its relation to speech and respiration (Laitman et al, 1979; Davidson, 2003; Jeffery, 2005; Lieberman, 2007; Lieberman et al, 2008;) and dental-related problems (Andersen & Popovich, 1983; Kerr & Adams, 1988; Dibbets, 1996; Klocke et al, 2002; Polat & Kaya, 2007). Evolutionary oriented studies have focused on contrasting the human and the primate cranial base, mainly through FM morphology and the cranial base flexion or angle (CBA; Figure 2). Luboga & Wood (1990) studied the location and orientation of the FM in humans and the two Pan species. Their results indicate that there is an allometric effect P age 44

53 on the FM position in relation to cranial size, but not to the inclination of the FM. They have also tried to assess the role of FM to early hominids taxonomic affinity, and relate it to the differences found between australopithecines and the Figure 2: Some methods used to measure the cranial base angle (After Lieberman, 2000) suggested early homo skull of KNM- ER 1813, concluding that the latter is probably not part of early hominids hypodigm. In 1993, Ross & Ravosa conducted a comparative study on the link between CBA, facial kyphosis and brain size. Reviewing 68 species of apes, they found that in haplorhines, the cranial base angle decreases as the brain volume increases relative to basicranial length. CBA was also found to be correlative to the orientation of the face and the axis of the orbits. They concluded that these results corroborate Gould s idea from 1977 on the connection between a flexed basicranium, large brain and short cranial base. Two years later, Ross & Henneberg (1995) found that relative to their brain size, humans have less CBA than expected, in comparison to other primates. They also extended Ross & Ravosa s (1993) study, to include fossil material - STS 5, MLD 37/38, OH 9, and Kabwe. They found that hominids tend to have a more flexed basicranium than any other primate relative to their brain size, and that they appear to resemble Homo sapiens. They state that if basicranial flexion is a mechanism for accommodating an expanding brain among non-hominid primates, other mechanisms must be at work among hominids. Strait (1999) studied the P age 45

54 connection between the different brain parts to CBA and basicranial length. He found that the basicranial length scales with a very strong negative allometry relative to body mass, due to the fact that non-cortical parts of the brain also scale negatively with body mass. A short cranial base coupled with non-cortical brain components is thus also related to body mass. Ross et al. (2004) tested different modes for modeling of the CBA. Since some studies, as noted above, have suggested that humans actually have a less flexed cranial base relative to brain size than predicted from other primates, a question has risen as to the possible mechanisms constraining the CBA. In their view, basicranial flexion can still be explained as a mechanical consequence of brain enlargement relative to basicranial length. One of the most recent studies to date by Lieberman et al (2008), tested the degree of influence that the face and brain size have on CBA. This was done using several mouse mutant lines. In their opinion, the cranial base represents the sum of interactions between the brain, face and components within the cranial base itself. Unfortunately, very few papers deal with comparative morphology of extinct and extant hominids cranial base. Recently, Kimbel & Rak (2010) conducted a morphological study based mainly on A.L , a female Australopithecus afarensis. Their study compared several features of her midsagittal cranial base such as nuchal area height relative to the FHP, location and orientation of the FM, basi-oociptal length, and CBA. In most indexes, australopithecines either resemble modern humans or have markedly different values than those of apes. Since early hominids brain volume is about the same as most of the African great apes, they concluded that posture and locomotion are the most feasible reasons for early hominids cranial base shape. P age 46

55 However, almost all previous works viewed the cranial base as a set of separate, distinct features, such as nuchal plane, FM, Clival plane, etc., and although the basicranium develops from two distinct embryonic origins (Nie, 2005), we postulate that it might actually act as one cohort structure. To further substantiate this analysis, I will also include juvenile chimpanzees and humans in the study. Although these are not valid taxonomic groups, they might help us to understand the nature of the change that the cranial base went trough. As noted by Bolk (1909; 1910), Mitteröcker et al, (2004) Berge, (1998) juvenile form of taxonomically close species tend to be more similar than their adult form. Thus, the object of this research is to assess the entire midsagittal shape of the basicranium from its posterior parts through the middle and to the anterior cranial fossa in apes, humans, and early hominids, in order to decipher which of two distinct processes initiated the morphocline to modern humans cranial base morphology: erect posture (possibly coupled with bipedal locomotion) or brain size Materials & methods The sample comprised of 30 skulls of recent Homo sapiens from Israel that included an equal number of males and females, 12 skulls of juvenile Homo sapiens, aged from newborns to 24 months, 30 skulls of Pan troglodytes from the Harvard zoological collection, 6 skulls of juvenile Pan troglodytes and 7 skulls of Gorilla gorilla from the Japanese Digital Morphology Museum, KUPRI ( All skulls were scanned in a medical CT and converted into surface mesh in Amira software ( for reconstruction, landmark data acquisition, and linear measurements. Mathematical and P age 47

56 statistical procedures were performed in Microsoft Excel and SPSS. The fossil material came from a variety of sources, and naturally not all specimens could be used for all measurements. Two skulls, MLD 37/38 (Dart, 1959; appendix I, figure 1a) and STS 5 (Broom, 1947; appendix I figure 1b) were scanned and cleaned (virtually) by Simon Neubauer (Neubauer, 2004, & pers. comm.). These skulls did not require any further reconstruction, as they are almost complete, aside from the face of MLD 37/38, which is missing. Two skulls were found by the Hadar Research Project team in Ethiopia. A.L (appendix I, figure 2a), a large male A. afarensis was reconstructed and published by Kimbel et al, 2004, as was A.L (appendix I, figure 2b), a female A. afarensis (Kimbel & Rak, 2010). Both skulls were scanned from casts made by Yoel Rak. After the original reconstruction, the skulls still suffered from lateral asymmetry due to taphonomic distortion, which was corrected using the methods described by Mitteroecker & Gunz (2009), mainly through mirroring one side onto the other. OH 5, the famous A. boisei (Leakey, 1959; appendix I, figure 3a) was scanned from the three-parts cast made by the Wenner-Gren Foundation and realigned in virtual space. KNM-ER (Brown et al, 1993; figure 3b), a male A. boisei lacking the face and parts of the cranial base, was scanned from a cast, and did not receive any virtual treatment, although it does suffer from minor taphonomic distortions, especially to the frontal bone. STS 19 (Broom et al, 1950; appendix I, figure 4a) is regarded by some as A. africanus (Ahern, 1998) or an early Homo by others (Kimbel & Rak, 1993). The skull, in which most of the calvaria, facial area and parts of the right basicranium are missing, was reconstructed by duplicating the complete left side, mirroring, aligning and superimposing it onto the right side. A.L , representing A. afarensis from the P age 48

57 famous first family site (Kimbel et al, 1982; appendix I, figure 4b), consists of two calvaria parts that were used initially with the A.L face in the original reconstruction of A. afarensis (Kimbel et al., 1984; Kimbel & White, 1988). This specimen suffers from taphonomic deformation: the inner right side projects inferiorly compared to the left side, and some basicranial elements are missing from one or the other side. Virtual reconstruction was performed on the skull: I restored the missing parts from one side to the other - the occipital condyle, the foramen magnum margins, the mastoid process, and the parietal bone. Since the left side is more complete, I duplicated that part. Using rapidform I cut out the deformed right petrous and copied the left side onto it. The same was done for the occipital condyle and foramen magnum. Because the two parts now overlap in their top (parietal) area as well as in the lower occipital area, aligning the two halves was an easy task. In order to make sure that this reconstruction was correct, measurements from the original A. afarensis reconstruction including occipital condyle breadth, bi-carotid breadth, and maximum skull breadth, were taken and compared. The same techniques were used for KNM-ER 407 (Day et al, 1976; appendix I, figure 5) calvaria. I used the right side, and added part of a mirrored left side in order to complete the occipital area all the way to the midline. I also reoriented the petrous bone to a more inferior position (although this did not affect the petrous sagittal orientation). I then duplicated and mirrored this part to complete the skull. Measurements were taken from the original and the cast to ensure that the reconstruction was feasible. Data from two specimens, KNM-ER 406 and KNM-WT 17000, were taken from previous work of Kimbel et al (2004). In order to compare angles between specimens and species, a reference plane is required. The most commonly used is the Frankfurt Horizontal plane P age 49

58 (FH). All specimens were aligned to the FH by creating a virtual plate and sinking each skull in the plate so that the three points defining the FH were exactly on the plane of the plate. The problem with some specimens is that the three points defining the plane do not necessarily exist on fragmentary fossils. While many studies approximate the orientation of these specimens to the FH (Tobias, 1967; Kimbel et al, 1984; Luboga & Wood, 1990), it is problematic. Thus, correct alignment of the incomplete specimens is a task in itself. In the process used here, I first acquired equivalent landmarks from an incomplete fragment and a complete, taxonomically close, specimen. Then, I superimposed the fragmented specimen onto the complete one, thus enabling us to approximate its orientation. Although the constellation of the three landmarks defining the FHP might be variable, it does not seem to be the case in living humans and apes (Barash, in preparation). This was done on the following specimens: A.L was warped onto A.L ; MLD 37/38 and STS 19 were warped onto STS 5; OH 5, KNM-ER and KNM-ER 407 were warped onto KNM-ER 406. Endocranial volumes were calculated for all specimens by creating a 3D model of each specimen s endocranium and applying the SurfaceArea module in Amira. All specimens were aligned to the FHP by creating a horizontal plate and sinking each specimen in such a way that the three points defining the FH (when available) were in line Figure 3: STS 5 aligned to the FHP with the plate (Figure 3). The specimens were then cut virtually through the midsagittal plane, and viewed P age 50

59 laterally, from the left side. The specimen was oriented so that the FHP runs exactly across the screen in the lateral view. Angles were acquired directly in Amira using the angle measurement tool. The first set of data obtained was of angles formed by the inclination of segments comprising the cranial base to the FH, as was previously done in many studies. For the second part, I measured angles formed by two adjoining parts in the cranial base. This was done in order to eliminate the need for an external reference plane and to evaluate the nature of relations between the segments that form the sagittal cranial base. In the third part, I assessed the former two data sets to brain volume in each group. For the first dataset (Figure 4), I measured the following segments. 1) The inclination of the inion-opithsion (planum nuchale, PN). It is important to note that I did not measure inion itself, but an inner part, midway between inion and endo-inion, within the diploë of the skull. This landmark will be referred to as inion*. It was done in order to eliminate the marked differences in inion size shape and position that can be seen within species, between males and females, and juvenile and adult specimens. 2) Opisthionbasion, or the inclination of the FM, one of the most common measurements in cranial base studies. A negative sign indicates that the FM is facing Figure 4: Measured landmarks and lines. The horizontal line represents the FHP. Note inion*, and the clival & sphenoidal lines. forward. 3) Medullary Clival line. For this measurement I did not use specific landmarks like the basion-sella (Spoor, P age 51

60 1997) or the basion-clivus points (Ross & Henneberg, 1995), but rather the overall inclination of the clivus as seen from the midsagittal view. This was done because the area of the pituitary gland, including sella trucica, dorsum sella, and tuberculum sella varies considerably (Venierat os et al, 2005; Bergland et al, 1968), affecting the inclination of the clivus if one tries to measure its angle to the FHP by placing two points on the inferior and superior ends. 4) The anterior part of the basicranium. I used the planum sphenoideum (PS), the area that extends from the most posterior point of the anterior cranial fossa (as part of the body lying between the greater wing of the sphenoid) to the PS point, the most anterior point on the surface of the midline anterior cranial base, just posterior to the cribriform plate. This area is clearly seen in a lateral view of the midsagittal plane. I did not include the area of the cribriform plate, or the foramen cecum, as it is highly influenced by the size of the olfactory blubs as an outcome of the sense of smell (McCarthy, 2001). A positive number indicates that the PS is facing anteriorly, while a negative number indicates that the PS is facing posteriorly. For the second dataset (Figure 4) the following angles were measured: 1) Inion*-opisthion-basion. 2) opisthion-basion-clival line 3) clival lineplanum sphenoideum. In addition to these measurements I also calculated endocranial volume for each specimen (Figure 5). The volumes were size scaled by two methods. Figure 5: Para-sagittal cut through Pan paniscus skull exhibiting the endocranial surface The first was the square root of endocranial volume divided by biorbital length as was P age 52

61 used by Kimbel et al (2004). Since many of the fossils lack their faces, I also calculated the square root of endocranial volume divided by biporion length. The two methods yielded similar ratio to the other angular measurements, suggesting that biporion works well as a scaling factor. For each measurement, student t-test was applied for statistical significance. P age 53

62 Results Angles relative to the FHP. One important factor to remember is that the FHP represents the most widely used and well known reference plane. We must however remember that like all biological measurements, the landmarks making this plane are also subject to their own inherent variation (as noted by Weidenreich, 1943; see plate 87), both between and within species and as such, close measurements must be evaluated with caution. In the first segment, the PN angle to the FH was measured (figure 6). Gorillas averaged at 75.3 (SD=5.19; range ); adult Figure 6: Boxplot graph of the angle formed by the planum nuchale and the FHP. Note the position of Juvenile chimps and Australopithecines. chimpanzees (SD=8.87; range ); Juvenile Chimpanzees 45.3 (SD=8.47; range ); australopithecines (SD=3.6; range ); adult humans (SD=8.6; range ); and juvenile humans 39.4 (SD=9.4; range ). Interestingly, the juvenile chimpanzees measured angles are much lower than their adults average, putting them very close to australopithecines and humans. The two adult ape species differ significantly from the juvenile chimps, australopithecines and humans. Humans are significantly different from australopithecines and juvenile chimps, but at a much lower degree of confidence. There is no significant difference between the juvenile and adult human form. There is a tendency among extinct hominids to exhibit a more horizontal PN from A. afarensis to A. africanus to A. boisei. This was speculated by P age 54

63 Robinson (1958), but probably due to a small sample size he did not investigate this morphology further. STS 19, a taxonomically debated specimen (Ahern, 1998; Kimbel & Rak 1993), falls very close to the human average (Figure 7) The second segment measured is the inclination of the foramen magnum (Figure 8). Gorillas FM projects backwards with an average of (SD=4.29; range ); chimpanzees (SD=7.05; range 9.9- Figure 7: Planum Nuchale inclination to FH in different fossils and extant species. Note the location of juvenile chimps, STS 19 and the more horizontal configuration in robust compared to gracile australopithecines. 40.5), juvenile chimpanzees 8.61 (SD=3.58; range 5-15); australopithecines, displaying a wide range of FM inclinations with an average angle of 6.72 (SD=9.88; range ); adult humans FM projects inferiorly and slightly anteriorly with an average of (SD=4.21; range (+)7.4); and Figure 8: Boxplot of the inclination of Foramen magnum to FHP juvenile humans which display the is the most anteriorly projecting FM: (SD=6.3; range (+)4.4). All groups differ significantly from each other, except juvenile chimpanzees and australopithecines. P age 55

64 The clival plane (Figure 9) is most horizontal in gorillas with an average of (SD=6.3; range ); chimpanzees average with (SD=5.26; range ); juvenile chimpanzees (SD=3.81; range ); australopithecines (SD=8.53; range ); adult humans display the steepest angle of (SD=4.27; range ), while juvenile humans have an average angle of (SD=7.79; range ). The two adult apes do not differ from Figure 9: Boxplot of clival plane to the FHP. Note the position of juvenile chimps with the other apes. each other, as do australopithecines and juvenile humans, while the other groups display a significantly different, though small, average. The PS (Figure 10) in gorillas tilted upward, forming an angle of (SD=5.93; range ); adult chimpanzees (SD=5.21; range ); juvenile chimpanzees (SD=5.21; range ); australopithecines display the most intermediate position of PS: 3.05 (SD=7.84; range ); adult Figure 10: Boxplot of the Sphenoid plane to the FHP. Note the position of juvenile chimps and australopithecines. humans PS are tilted downward P age 56

65 with an angle of 6.13 (SD=5.5; range ); and juvenile humans display a very similar morphology to the adult form: 6.74 (SD=5.47; range ) When contrasting these angles to the scaled brain volume defined as brain volume/biporion length (Figure 11), a well known pattern (Kimbel et al, 2004, Kimbel & Rak, 2010) emerges: australopithecines and humans exhibit very similar basicranial morphology. Interestingly, to a large extant this morphology is also shared by juvenile chimpanzees. Brain Volume Biporion Brain Volume Biporion Gorilla gorilla Pan (Adult) Pan (Juvenile) Australopithecines Adult Homo Juvenile Homo a 0.10 b Inion*-Opisthion FHP Opisthion-Basion FHP Brain Volume Biporion Brain Volume Biporion c 0.10 d Clivus FHP Sphenoid FHP Figure 11: Scatter plot of relative brain size (y-axis) to the angles related to the FHP. a) Planum nuchale; b) Foramen magnum; c) Clival plane; d) sphenoid plane. Note the position of juvenile chimps and australopithecines. P age 57

66 Angles formed by two adjoining segments. The first segment is the angle that is formed by Inion*-opisthion-basion (Figure 12). In Gorillas the angle is (SD=6.92; range ); in adult chimpanzees it is (SD=6.4; range ); juvenile 160 Planum nuchale Foramen magnum cohort chimpanzees have an angle of (SD=3.52; range ); in Inion*-Opisthion_Basion australopithecines it is (SD=9.62; range ); in adult humans it is (SD=6.96; range ); and in juvenile humans it is Figure 12: Boxplot of the PN-FM cohort. Note the location of the juvenile chimps. (SD=7.24; range ). There is a significant difference between gorillas and chimpanzees and the three other groups: juvenile chimpanzees, australopithecines and adult humans, but no difference within juvenile chimpanzees, humans and australopithecines. Juvenile humans seem to 150 Foramen magnum clival plane cohort resemble the adult ape group more than any other group. Opisthion-Basion-Clivus The second segment is the opisthion-basion-clival line (Figure 13). Gorillas display an angle of (SD=8.08; range ); adult chimpanzees display Figure 13: Boxplot of the FM-Clival plane cohort. Note the location of the juvenile chimps & juvenile humans. an angle of (SD=7.62; range ); juvenile P age 58

67 chimpanzees display an angle of (SD=7.31; range ); australopithecines have an angle of (SD=6.72; range ); adult humans have an angle of (SD=6.83; range ); and juvenile humans have an angle of (SD=6.65; range ). Surprisingly only the two juvenile groups are significantly different from the adult groups. The CBA, as defined here by clival plane-planum sphenoideum (Figure 14), measures 160 Clival plane Sphenoid plane (SD=7.9; range ) in gorillas; in adult Clivus-Sphenoid plane chimpanzees it is (SD=8.65; range ); juvenile chimpanzees display an angle of 147 (SD=4.67; range ); in australopithecines it Figure 14: Boxplot of the CBA. Note the location of the juvenile chimps with the other apes. is (SD=9.89; range ); in humans it is (SD=5.8; range ); and in juvenile humans it is (SD=11.46; range ). Interestingly, the CBA actually separates between apes and humans, in both adult and juvenile groups, while placing australopithecines within the human group. P age 59

68 Discussion FH relative angles. The inclination of the PN is considered to be a manifestation of erect posture by some researchers (Robinson, 1958; Tobias, 1967; Olson, 1981, Dean & Wood, 1984). As the FM migrated inferiorly and anteriorly, as part of erect posture adaptation, the nuchal muscles drifted downward to support the head (Schultz, 1955; Dean, 1985). However, several other authors (White et al, 1981; Kimbel et al, 1984; Kimbel & Delezene, 2009; Kimbel & Rak, 2010) doubt the role of the PN in erect posture or bipedal locomotion, at least in A. afarensis, in which one of the proposed plesiomorphic characters is the steepest nuchal plane among unequivocal hominids (Kimbel et al, 1984, pp. 374). In my results, A. afarensis does exhibit the steepest PN among hominids (49, n=3), but in fact, it is about 20 gentler than chimpanzees, and only about 5 different to all other hominids, and approximately 10 to humans. It is apparent that hominids display a close resemblance to the human form, suggesting in my view that erect posture is one of the main mechanisms, if not the only one, that shaped this segment. The inclination and position of the FM in extant hominidae is a widely discussed topic in the literature (Bolk, 1910b; Le Gros Clark, 1955; Tobias, 1967; Adams & Moore, 1975; Luboga & Wood, 1990; Kimbel et al, 2004; Kimbel & Rak, 2010). Our analysis on the inclination of the FM differs only slightly from the results obtained by others (Lugoba & Wood, 1990; Kimbel et al, 2004). Hominids display a wide range of FM inclination from 18.7 in STS 5 to -8.3 in the reconstructed cranial base of KNM-ER 407. Most early hominids display a posterior projecting FM, although it is more horizontal, averaging at 6.7 compared to 22 of chimpanzees. The fact that there is no correlation between FM P age 60

69 inclination and geological age, species taxonomy, gender or robusticity, suggests that other factors aside from erect posture or bipedal locomotion have been shaping the human FM. Among these factors, the growing human brain, especially the cerebellum that occupies the posterior cranial fossa, might actually drive the FM to move forward, while anteriorly, it might be constrained by our low positioned larynx (Laitman et al, 1979; Davidson, 2003). This might also explain the more anteriorly inclined FM of juvenile humans: -10 compared to -4 in adults: as the viscerocranium grows rapidly in the early years of life, less "room" is available for the laryngeal complex, thus it descends downwards, and the FM moves backwards. The inclination of the clival line greatly differs between apes and humans. It is much steeper in humans than in gorillas and chimps, while australopithecines exhibit an intermediate morphology, closer to the human shape. As noted above, this change has been long noticed by many scholars, and was given several explanations. Interestingly and importantly, the clivus separates between all apes, including juvenile chimpanzees on one side and all humans and hominids on the other. Thus, clival inclination coupled with endocranial volume, especially with regards to juvenile chimps, emphasizes that it is not brain volume that influenced the shape of the cranial base. The same correlation is found in PS: all apes form one group, while australopithecines and all humans form the other. In my view, the fact that early hominids display a more vertical clival plane than apes, coupled with differences in the orientation of the PS, is another manifestation of the evolutionary change that took place in the cranial base due to erect posture or bipedal locomotion. It seems that as the clivus became more erect, probably as an outcome of the downward migration of the PN-FM complex, it created a more acute angle with the PS. P age 61

70 This might happen because the anterior end of the PS is anatomically and developmentally connected to the visual and olfactory apparatuses, making its location and orientation constrained geometrically, thus preserving its spatial position. The tendency of the PN, FM, and clival plane to move together suggests a pleiotropic connection between these structures, throughout the midsagittal plane of the cranial base: the PN shifted from about 70 in apes to about 40 in humans; in turn, the FM shifted from about 25 in apes to -5 in humans, and the clival plane shifted from about 30 in apes to about 55 in humans. The peculiar and unique morphology of juvenile great apes was observed, as noted above, by Bolk as far back as Since humans and juvenile apes retain the same primitive morphology, he suggested a "foetalisation" (or retardation, in later papers) phenomenon, in which through inhibitory influence of the endocrine system, humans retain their infantile appearance (Bolk, 1922). This view met with much criticism (see Shea, 1989), stating mainly that the ontogeny of human evolution is a complicated series of events that cannot be explained by a simple neoteny process. However, Bolk s views are still debated today, and although the complexity and nature of human evolution is indeed a complex of non- and inter- related events, at least some processes can be explained by the foetalisation processes (see Leiberman et al, 2007, for example). Other mechanisms that possibly involved are fetal development and obstetrics constraints that might influence the rate, shape and size of development of apes and humans. Unfortunately, very little data exists on these subjects in the literature. To name one exception, Drews et al (2011) performed an ultrasound study of fetal development in Pan paniscus, claiming that in the first 6 months of development, humans, chimps and P age 62

71 bonobos are very similar in development, and that humans differ from that pattern in later stages of pregnancy. Another important aspect arising from this analysis is the fact that chimpanzees manifest a higher degree of difference to humans and australopithecines than gorillas do. This tendency is not confined to the cranial base: Rak et al (2007) showed a similar tendency in some aspects of the mandible. It is an interesting pattern that will require further study, with larger groups, to ensure that it is not a false outcome of a small sample. Angles formed by two adjoining segments. The results of this part are generally similar to the FH results, thus implying that comparing the species based on a problematical reference plane is indeed valid. The first segment inion*-opisthion-basion, represents the inclination of the PN, coupled with the FM. In my results, chimpanzees and gorillas differ from humans, and to a lesser extent from australopithecines, but the two hominid groups pose a similar morphology. Juvenile chimps posses a similar morphology to australopithecines and humans. Oddly, juvenile humans seems more similar to adult great apes than to juvenile chimpanzees or even adult humans. this might be an outcome of a small sample size (12), but it might also be explained, by the fact that the occipital region is the first part to emerge out of the birth canal (Rosenberg & Trevathan, 2002). Tobias (1967, pp 43) briefly notes that the the planum nuchale of the occipital squama is tilted at only a slight angle to the plane of the foramen magnum which, in turn, is tilted upwards at an angle of 7 to the F.H. Unfortunately, he does not supply further data to compare it with other apes or humans. Since the PN has become more horizontal (to the FHP) by 30, a similar change in the relation between the PN and the FM would be expected. Indeed, the FM has also changed its inclination by about 26 corroborating P age 63

72 Tobias's observation. The fact the australopithecines exhibits a similar morphology to humans is manifested by the same pattern: as the PN rotated about 22, the FM has changed about 17. The next segment is opisthion-basion-clivus. This segment is also discussed by Tobias (1967, pp 47) On the one hand, the the hominid tendency to change the plane of the foramen magnum will tend open out the OBP angle. On the other hand, the hominid tendency towards inbending of the basicranial axis It might be expected then that little change would come about this in this angle. Because of this Tobias argues that we find that gorilla have a very similar angle to that of OH 5 and STS 5. In my results, there is very little difference between apes, australopithecines and humans. However, this segment displays a very interesting morphology: juvenile chimps and humans display a blunt angle compared to all others. This might be an indication of an early, developmental or neurological constraint that implies to both species. The Clival plane-sphenoid plane has been studied substantially, through different methods and defining landmarks, as the cranial base angle. In my results there is a difference between apes and humans & australopithecines, but similar to the clival plane angle to the FH, juvenile chimps display a similar morphology to the other apes. Our findings strongly suggest that the basic configuration of the cranial base is similiar in apes, early hominids and humans. The posterior cranial fossa has shifted as one cohort structure, downward and forward around the sella turcica. The fact that australopithecines display morphology similar to that of humans, coupled with their small endocranial volume, implies that erect posture and bipedal locomotion are the main factors that shaped the early stages of the cranial base. The special morphology of juvenile P age 64

73 chimpanzees, in many cases contrasting to the adult form, hints at complicated obstetrics constraints that will require further study. P age 65

74 Appendix I: Midsagittal sections of fossil hominids used in this study a b Figure 1: a) Midsagittal view of MLD 37/38; b) Midsagittal view STS 5. Reconstructed from original. Courtesy of Gerhard Weber & Simon Neubaur; University of Vienna & Max Planck Institute, Leipzig. a b Figure 2: a) Midsagittal view of A.L ; b) Midsagittal view of A.L Reconstructions made form casts, courtesy of Yoel Rak., Tel Aviv university. a b Figure3: a) Midsagittal view of OH-5; b) Midsagittal view of KNM-ER Reconstructions made form casts, courtesy of Yoel Rak. Page 66

75 a b Figure 4: a) Midsagittal view of A.L333-45; b) Midsagittal view STS 19. Reconstructions made form casts, courtesy of Yoel Rak. Figure 5: Midsagittal view of KNM-ER 407. Reconstruction made form casts, courtesy of Yoel Rak. Page 67

76 Appendix II: Adjoining segments angles Inion-opisthion-Basion opisthoin basion-sella clivius-sella-cecum Endocranial volume Biorbital Biporion Brnvol/bior Brnvol/bipor PriCT 24 ggm PriCT 23 ggm Gorilla goriila Gorilla gorilla Gorilla gorilla coll Gorilla gorilla coll Gorilla juv Gorilla Average Stdev Max Min HvdC Juvenile pan PriCT troglodytes PriCT PriCT PriCT HvdC Average Stdev Max Min PriCT TUA Adult TUA pan troglodytes TUA TUA HvdC HvdC HvdC HvdC HvdC HvdC HvdC Page 68

77 HvdC HvdC Adult HvdC pan troglodytes HvdC HvdC HvdC HvdC HvdC HvdC PriCT HvdC HvdC HvdC HvdC HvdC HvdC HvdC PriCT Average Stdev Max Min MLD 37/ A.L Australopithecines A.L A.L KNM-ER OH STS STS KNM-ER KNM-ER KNM-ER Average Stdev Max Min Page 69

78 7228m m m f m f f f f f f f f f m m Adult 3895f Homo sapiens 3902f m m m m f f f f m f f m Average Stdev Max Min Page 70

79 7891f1m m24m m11m m7m m16m f0m Juvenile 3898f24m Homo sapiens 3897m24m m10m m0m m8m f4m Average Stdev Max Min Inion-opisthion-Basion opisthoin basion-sella clivius-sella-cecum Gorilla/ juv chimp Gorilla/ chimp Gorilla/ Aus gorilla/ human E-08 Gorilla/ juv human E-05 Chimp/ juv chimp Chimp/ Aus Chimp/ human E E-15 Chimp/ juv human E E-10 Juv/ Aus Juv/ human E-08 Juv/ Juve human Aus/ human Aus/ Juv human E Human/ Juv human E Page 71

80 4.2 The cranial base with reference to its internal aspect in the horizontal plane Introduction The scientific view that morphology implies hierarchical order and relations between organisms was established long ago. Even the notion of evolving species dates long before Charles Darwin and his predecessors, like Jean-Baptiste Lamarck, suggested it. Edward Tyson states in his 1699 book "Orang-Outang, sive Homo Sylvestris: or, the Anatomy of a Pygmie" that "Now notwithstanding our Pygmie does so much resemble a man in many of its parts, more than any of the ape-kind, or any other Figure 1: Homo Sylvestris (From Tyson, 1699) animal in the world that I know of" (Tyson, 1699; pp 2). In the publication of On The Origin of Species", Darwin only briefly mentions, toward the end of the book, that "Light would be thrown on the origin of man and his history" (Darwin, 1859; pp 488). Twelve years later, Darwin begins his "Descent of Man" in somewhat apologetic words: "During many years I collected notes on the origin or descent of man, without any intention of publishing on the subject, but rather with the determination not to publish, as I thought that I should thus only add to the prejudices against my views" (Darwin, 1871; pp 1). Nevertheless, the book did suggest Africa as the cradle of human evolution, based on morphological similarity between apes and humans: "In each great region of the world the living mammals are closely related to the evolved species of the same region. It is, therefore, probable that Africa was formerly inhabited by extinct apes closely allied to the gorilla and chimpanzee; and, so these two species are now man s nearest allies, it is somewhat more probable that our early progenitors lived on the African continent than elsewhere " (Darwin, 1871; pp 199). However, Darwin s (and Huxley's) conclusion was in minority. The main P age 72

81 anthropologists of the time stated that man (or at least Caucasian man) originated from Asia. One of the leading voices of that concept was Ernst Haeckel who wrote that "For many and weighty reasons we hold the monophyletic hypothesis to be the more correct, and we therefore assume a single primæval home for mankind, where he developed out of a long since extinct anthropoid species of ape... Most circumstances indicate southern Asia as the locality in question." (Haeckel, 1887; pp ).Two important discoveries made at the end of the 19 th century and the beginning of the 20 th century corroborated Haeckel's suggestion. In 1891, Eugène Dubois, a Dutch doctor and paleontologist, discovered in Java, Indonesia, the skeletal remains of an unknown hominid, which he named Pithecanthropus erectus (Dubois, 1894), following Haeckel's proposal. Several years later, in England, Charles Dawson presented the Piltdown skull (Dawson & Woodward, 1913). Although it is known today as a forgery, in the first half of the 20 th century, the Piltdown man was almost unanimously incorporated into the human lineage. It was into this background that the first australopithecine was discovered, and brought to the scientific community. In 1922, Raymond Dart took a position as Head of Anatomy in the new medical school at the University of Witwatersrand in South Africa (Dart, 1959b). As part of the anatomy lab, Dart wished to established a museum with a comparative skeletal collection, including primates. He therefore staged a competition between his students, in which the winner would be the one who would bring the most interesting and unusual bones. The prize was five pounds (Trinkaus & Shipman, 1993, pp 229). One of Dart's students and lab instructor, Josephine Salmons, brought a fossilized skull of a baboon, from a limestone quarry in Taungs. Since, at that time, Anthropoid skulls were not known in South Africa, Dart asked for more fossils to be delivered to him. Toward the end of 1924, two crates containing more fossils were brought to Dart. In one of the crates he discovered a natural endocast, the face and partial P age 73

82 mandible (Figure 2). After meticulously removing the matrix, Dart realized the importance of his discovery. On February 7, 1925 Dart published in Nature : "Australopithecus africanus: The man-ape of South Africa" in which he states: Apart from this evidential completeness, the specimen is of importance because it exhibits an extinct race of apes intermediate between living anthropoids and man (Dart, 1925; pp 195). However, Dart's observation was widely dismissed. In the following issue of Nature, the next week, the leading anthropologists in England - Arthur Keith, Grafton Elliot Smith, Arthur Smith Woodward and W. L. H. Duckworth, unanimously and ferociously attacked Dart. Woodward ends his remarks on the find with a personal note Figure 2: Raymond Dart, with the Taungs child and the Nature paper "Palaeontologists will await with interest Prof. Dart's detailed account of the new anthropoid, but cannot fail to regret that he has chosen for it so barbarous (Latin-Greek) a name as Australopithecus" (Woodward, 1925; pp 236). It was only with the discovery of the first adult skull of Australopithecus that Dart's views and discoveries began to be accepted. In the 1930s Robert Broom, an early supporter of Dart's ideas, began looking for more australopithecine skulls. Broom, in his sixties, a former medical doctor & a paleontologist working on mammal-like-reptiles, was fascinated by the possibility of hominid evolution in South Africa. Broom worked in limestone caves, blasting with dynamite and going through the rubble, looking for fossils. Twelve years after the discovery of Taungs, in the caves of Sterkfontein, Broom discovered a partial natural endocast articulated to a fragmentary skull (Broom, 1936). As more fossils were uncovered, more paleoanthropologists accepted the African continent as the cradle for human evolution, and the australopithecines as the transitional form between apes and humans. In 1947, Keith wrote in Nature, "I am now P age 74

83 convinced, on the evidence submitted by Dr. Robert Broom, that Prof. Dart was right and that I was wrong; the Australopithecinae are in or near the line which culminated in the human form" (Keith, 1947; pp 377). The large quantities of fossils originating from South African sites, especially Sterkfontein, Swartkrans, Kromdraai & Makapansgat, led to the formation of several species: Australopithecus africanus, Plesianthropus transvaalensis, Australopithecus prometheus, Paranthropus robustus, Paranthropus crassidens and more. In 1954, John Robinson lumped them into two Genera: Australopithecus, containing one species, A. africanus and Paranthropus containing two species, P. Robustus & P. paleojaveanicus (now considered Meganthropus or Homo erectus). Ever since the 1970s, fossil australopithecines are being discovered in east Africa, mainly in the rift valley areas of Tanzania, Kenya and Ethiopia. The discovery of the most gracile and apparent primitive from, A. afarensis, in the Hadar formation of Ethiopia, has led prominent paleoanthropologists to place it as a representative morph for the major early changes that the human morphocline went through. Kimbel summarizes in 2009 (pp.39), while A. afarensis remains neither the oldest nor most apelike hominin species, it continues to be a principal record of transformation of major structuralfunctional system in hominin evolution. Although there is still Figure 3: Australopithecus afarensis, A.L , from the Hadar formation of Ethiopia taxonomic debate about the origins and affinities of the australopithecine group (see Wood & Richmond, 2000), most paleoanthropologists recognize four distinct species that are well represented in the fossil record: A. afarensis, A. africanus, A. robustus (sometimes referred to as Paranthropus robustus), and A. Bosiei (sometimes referred to as Paranthropus boisei). While A. afarensis and A. bosiei are P age 75

84 found solely in East Africa, A. africanus and A. robustus are known only in South Africa. Thus, over the course of time, beginning perhaps with Tyson, the hierarchical paradigm has brought australopithecines (most of the time A. afarensis, and to a lesser extent A. africanus) to be the ancestor or a very close form to later homo lineage. Examples of this can be found in many articles, as well as most textbooks today (Johanson & Edey, 1981, pp 284; Larsen, 2008, pp 293; Boyd & Silk, 2009, pp 271). However, over the years, there have been some voices that challenged the ancestral position of australopithecines in general and A. afarensis in particular. Olson (1981) studied the exteriorposterior basi-cranium including the shape of the supramastoid crest, mastoid process, the digastric muscle origin and the inferior nuchal lines. His main focus was on the (then) newly discovered Afar material, especially A.L and A.L He concludes "In addition, the analysis of the Hadar remains indicates that the A.L cranium possesses a series of unique characteristics that identify it as a member of the Paranthropus clade" (Olson, 1981, pp 122). In his view, the Taungs child is the only fossil that is a direct ancestor of the human lineage, calling it "Homo africanus". Olson extended this view in 1984 at a symposium held in New York marking the opening of "Ancestors: Four million years of humanity" exhibition. He also compares A.L to the Taungs specimen (Olson, 1985), and concludes that the former is a derived specimen of the Paranthropus clade, while the later is part of the human lineage, as inferred from its nasal morphology. In his views, A. afarensis is a derived taxon, with affinity to other robust australopithecines. Olson s ideas were not accepted, because many other studies indicated a different picture, as can be read in the same volume by authors like Kimbel et al (1985), Rak (1985) and others. An interesting and more influential work was done by Falk & Conroy (1983). They studied early hominids endocranial structure, and noticed that all P age 76

85 australopithecines, excluding A. africanus 1, display an apomorphic specialization in their venous drainage pattern. In humans, great apes and most extinct Homo species, blood is drained from the brain through the transverse sinus continuing the sigmoid sinus and out of the endocranium through the internal jugular vein. In australopithecines, there is a different drainage system through an occipito-marginal sinus, running inferiorly from the confluence of sinuses to the occipital sinus and marginal sinus, emptying into the jugular foramen (Figure 4). According to Figure 4: The alternative drainage system of Australopithecines, as seen in the occipital bone. a- Homo sapiens; b- Australopithecus afarensis (After Falk & Conroy, 1983) Falk & Conroy (1983), this unusual drainage system is an alternative method that developed in order to provide a solution for circulatory demands associated with erect posture. Some works tried to refute this observation, claiming that the variation within the human lineage is too large to apply any taxonomic or functional significance to this trait. Kimbel notes, "Available evidence of venous sinus pattern distribution among Plio- Pleistocene Hominidae provides little or no rationale for revising the phylogenetic scheme of Johanson and White (1979) nor the functional adaptive interpretation elaborated by White et al. (1981)" (Kimbel, 1984b, pp 261). Two years later, Falk (1986) returns to the subject, stating that many discrepancies exists between her own observation and interpretation and the ones found by Kimbel (1984). However she uses a larger sample size and various species, concluding that robust australopithecines are descended from A. afarensis and not from A. africanus. In another work, Rak (1991) studied the pelvic shape of A. afarensis (A.L ), noticing its wide inlet. According to his study the purpose of this unique 1 Since the publication of Falk & Conroy (1983) some A. africanus fossils were found that manifest occipitomarginal sinus- see Tobias & Falk, 1988 P age 77

86 morphology is an adaptation to bipedal walking, mainly by minimizing the vertical displacement of the center of mass. In humans, on the contrary, the elongation of the legs is used to answer the same biomechanical problem. Rak notes that "Lucy s pelvis does not represent simply an intermediate stage between a chimpanzee-like hominoid and Homo sapiens, nor is it essentially a modern human pelvis. Although clearly bipedal and highly terrestrial, Lucy evidently achieved this mode of locomotion through a solution all her own" (Rak, 1991, pp 289). The most significant research, challenging the paradigm of the ancestral role of australopithecines in human evolution was published by Rak et al. (2007). In the paper, the authors studied the mandibular ramal morphology of the genus. It seems that all australopithecines possess similar morphology, in which the coronoid process is higher than the condylar process; the base of the coronoid constitutes much of the ramal width, thus making the mandibular notch closer to the condylar process. Importantly, this morphology is common to gorillas but it is not represented in chimpanzees, orangutans and humans. Since all australopithecines display this derived morphology they conclude that "Au. afarensis is simply too derived to occupy a position as a common ancestor of both the Homo and robust australopith clades" (Rak et al, 2007; pp 6571). Previous studies on the cranial base The importance of the morphology of the cranial base to the study of human evolution was noted long ago. Dart, in his first article about the Taungs baby, writes about the "head balancing index", an index of relation between basion-prosthion and basion-inion: "It is significant that this index, which indicates in a measure the poise of the skull upon the vertebral column, points to the assumption by this fossil group of an attitude appreciably more erect than that of modern anthropoids" (Dart, 1925, pp 197). The discovery and the description of the South African P age 78

87 material by Broom, Robinson & Schepers led to a series of books and papers, which deal in part with the shape of the basicranium. Over the years, the cranial base received much attention in the description of new fossils, but these usually lacked wide range of comparative data and were confined to fossils, humans or apes, but usually not the three groups together. An example of this can been found in Tobias (1967) on the skull of OH 5; Brown et al (1993) on KNM-ER 23000; and Alemseged et al (2002) on Omo 323. Furthermore, most comparative studies only used the midsagittal plane, considering mainly the orientation and location of the foramen magnum and the basicranial flexion: Ashton & Zuckerman (1951); Luboga & Wood (1990); Ross & Henneberg (1995); Kimbel et al (1984); Lieberman et al (2000b); Kimbel et al (2004); and Kimbel & Rak (2010). To this date, only few papers venture outside the midsagittal plane: Dean & Wood (1981, 1982) did a landmark based metrical analysis of the basilar part of the skull base, and showed a difference between robust and gracile australopithecines and early Homo. Spoor (1997) preformed one of the earliest uses of CT technology for studying hominid fossils, by observing the internal structure of STS 5 and other early hominids. He has shown that, generally, basicranial shape is correlated with brain size. Ahern (2005) has studied the position of the anterior border of the foramen magnum (i.e. basion) in relation to the bicartoid and biporion chords, and has found that basion to bicarotid distance is a good indicator for taxonomically identifying Plio-Pleistocene samples as members of the hominid clade. Importantly, aside from Spoor (1997), virtually no taxonomic study has been done on the internal structure of the cranial base. Thus, in this work, I will bring further evidence, from the internal and external morphology of the cranial base that all australopithecines belong to one clade, and that they probably did not take any part in forming the human lineage. In order to achieve this, I will not only use apes, humans and australopithecines but also juvenile chimpanzees and humans. Observing the shape P age 79

88 of juveniles might helps to better understand the nature of change that the cranial base went through, even though these are not valid taxonomic entities. This is because young forms of taxonomically close species tend to be similar compared to their adult form Material & Methods The sample for this study included 30 skulls of modern humans, consisting of an equal number of males and females and 12 skulls of juvenile humans aged from newborns to 24 months from Israel; 30 skulls of adult Pan troglodytes and 6 skulls of juveniles from the Harvard Zoological Collection and the Japanese Digital Morphology Museum, KUPRI (Available freely through and 7 skulls of Gorilla gorilla also from KUPRI & Israel. All specimens were scanned using medical CT. The fossil material came from a variety of sources: some were scanned from the original specimens, while others were scanned from high quality casts. Some fossils were complete enough to use as is, while others required virtual reconstruction (Figure 5). Two skulls, MLD 37/38 (Dart, 1959; appendix I, figure 1a) and STS 5 (Broom, 1947; appendix I, figure 1b) were scanned and cleaned (virtually) by Simon Neubauer (Neubauer, 2004, & pers. comm.).these skulls did not require any further reconstruction, as they are almost complete, aside from the face of MLD 37/38, which is missing. The Hadar Research Project team in Ethiopia found two skulls. A.L (appendix I, figure 2a), a large male A. afarensis, was reconstructed and published by Kimbel et al, 2004, as was A.L (appendix I, figure 2b), a female A. afarensis (Kimbel & Rak, 2010). Both skulls were scanned from casts, molded by Yoel Rak. After the original reconstruction, the skulls still suffered from lateral asymmetry due to taphonomic distortion. This was corrected using the methods described by Mitteroecker & Gunz (2009), mainly through mirroring one side P age 80

89 onto the other. OH 5, the famous A. boisei (Leakey, 1959; appendix I, figure 3a) was scanned from the three-parts cast made by the Wenner-Gren Foundation and realigned in virtual space. KNM-ER (Brown et al, 1993; figure 3b), a male A. boisei lacking the face and parts of the cranial base, was scanned from a cast, and did not receive any virtual treatment, although it does suffer from minor taphonomic distortions, especially to the frontal bone. STS 19, from Sterkfontein, (Broom et al, 1950; appendix I, figure 4a) is regarded by some as A. africanus (Ahern, 1998) or early Homo by others (Kimbel & Rak, 1993). The skull, in which most of the calvaria, facial area and parts of the right basicranium are missing, was reconstructed by duplicating the complete left side, mirroring, aligning and superimposing it onto the right side. A.L , representing A. afarensis from the famous first family site (Kimbel et al, 1982; appendix I, figure 4b), consists of two calvaria parts that were used initially with the A.L face in the original reconstruction of A. afarensis (Kimbel et al., 1984; Kimbel and White, 1988). This specimen suffers from taphonomic deformation: the inner right side projects inferiorly compared to the left side, and some basicranial elements are missing from one or another side. Virtual reconstruction was done on the skull: I restored those parts that are missing from one side to the other - the occipital condyle, the lateral margins of the foramen magnum, the mastoid process and the parietal bone. Since the left side is more complete, I duplicated that part. Using rapidform I have cut out the deformed right petrous and copied the left side onto it. The same was done for the occipital condyle and foramen magnum. Because the two parts now overlap in their top (parietal) area as well as in the lower occipital area, aligning the two halves was an easy task. In order to make sure that this reconstruction was correct, measurements from the original A. afarensis reconstruction, including occipital condyle breadth, bicarotid breadth, and maximum skull breadth, were taken and compared. The same techniques were used for KNM-ER 407 (Day P age 81

90 et al, 1976; appendix I, figure 5) calvaria. I used the right side, added part of a mirrored left side in order to complete the occipital area all the way to the midline, and I also reoriented the petrous bone to a more inferior position (although this not affect the petrous sagittal orientation). I then duplicated and mirrored this part to complete the skull. Measurements were taken from the original and the cast to ensure that the reconstruction was feasible. KNM-ER 406, a robust A. bosei, was scanned with a surface scanner, thus only the external part was available for study. Data from two specimens SKW 18 and KNM-WT were taken from previous work of Kimbel et al (2004). In order to compare angles between specimens and species, a reference plane is required. The most commonly used is the Frankfurt Horizontal plane (FH). All specimens were aligned to the FH by creating a virtual plate and sinking each skull in the plate so that the three points defining the FH were exactly in the plane of the plate. The problem with some specimens is that the three points defining the plane do not necessarily exist on fragmentary fossils. While many studies approximate the orientation of these specimens to the FH (Tobias, 1967; Kimbel et al, 1984; Luboga & Wood, 1990), it is problematic. Indeed, aligning incomplete specimens is a task in itself, in which the virtual working space is also useful. I have superimposed the fragmented specimen onto a complete and taxonomically close fossil that enables us to approximate its original orientation. Thus, using Amira software and the SurfaceLandmarkWarp module, this procedure was performed on the following specimens: A.L was warped onto A.L ; MLD 37/38 and STS 19 were warped onto STS 5; OH 5, KNM-ER and KNM-ER 407 were warped onto KNM-ER 406. The skullcap was cut in order to reveal the internal structure of the endocranium. The first measure was the angle formed by the petrous of the temporal bone and the midsagittal line. A line was drawn following the superior petrosal sinus, to the midline of the skull, and the angle P age 82

91 was measured. The second measurement was the location of the basion compared to the biporia line. This was done by two methods: first, by placing a biporia line, and then measuring the length between the midpoint of that line and basion. The basion-biporia length was then divided by the total length of the foramen magnum (basion-opisthion), in order to minimize size effect. In the second method, I used landmarks to mathematically calculate the same distances. Using Amira, landmarks were placed on the left and right porion, basion and opisthion. By applying a simple Euclidian distance formula: d = (x 2 x 1 ) 2 + (y 2 y 1 ) 2 + (z 2 z 1 ) 2, each distance was measured in order to validate the results. A positive value indicates that the basion is posterior to the biporia line, while a negative value indicates that the basion is more anterior to the biporia. I also acquired 10 landmarks within the cranial base: porion ( 2), basion, opisthion, internal acoustic meatus ( 2), inferior opening of the carotid canal ( 2) and foramen ovale ( 2). These landmarks were used to visually assess the spatial configuration and orientation of the foramen magnum & petrous bone Results Petrous bone orientation: In the first part, the orientation of the petrous bone to the midsagittal plane was calculated (Figure 6). When possible, both the right and left petrous bones were measured and averaged. In all apes and humans the petrous is more coronally oriented than in australopithecines. In adult chimpanzees it forms an angle of (range ; P age 83 Figure 5: Boxplot view of petrous bone orientation in all groups. Note the location of the Australopithecines, and STS 19.

92 sd=2.47 ); in gorillas the angle is (range ; sd=2.08 ) and in juvenile chimpanzees it is more horizontal, (range ; sd=3 ). In humans the angle is (range ; sd=2.8 ) while in juvenile humans it is (range ; sd=2.09 ). In australopithecines the angle is more sagittal averaging (range ; sd=3.43 ). When removing STS 19, in which the angle is 48.35, from the australopithecines average, the average is (sd=1.8 ). The removal of STS 19 from the australopithecines cohort was considered before, and is still debated in current literature. Statistically, australopithecines differ from both apes (p<0.0002) and humans (p< ), while apes and humans are similar. The two juvenile groups are similar to each other (p=0.57), while they differ from their adult form: p<0.01 for the chimpanzees and p< for humans. There is no correlation between taxonomic affinity or robusticity and any of the above angles: A.L , A. afarensis displays the most horizontal petrous (35.4 ) right before KNM ER 407, an A. boisei. In the same manner A.L a robust A. afarensis, has almost the same petrous orientation as STS 5, a gracile, probably female, A. africanus. The overall distribution of all australopithecines is quite small ranging from 35.4 to when omitting STS 19. Basion biporia relation: In the second, part the distance between basion and the midpoint of the biporia line was measured. This distance was divided by the total length of the foramen magnum, in order to minimize the size effect (Figure 7). In all apes the total length of the foramen magnum, including basion is behind the biporia line. Relative to the total length of the FM, in chimpanzee s P age 84 Figure 6: Boxplot view of the location of basion to biporia. Star indicates an extremely posterior FM of a large gorilla male.

93 basion is 33.89% (range ; sd=11.6) behind biporia; in gorillas it is 39.96% (range ; sd=14.73) behind biporia; and in juvenile chimpanzees it is 17.68% (range ; sd=9.34) behind biporia. In humans, basion is also behind the biporia line, averaging as the total length of the FM at 6.64% (range ; sd=9.27) of the total length of the foramen magnum. In juvenile humans, basion occupies a more posterior position of 13.96% (range ; sd=7.96). In australopithecines to the contrary, basion is anterior to the biporia line, as the average position is % (range ; sd=13.29). This number is even higher if we omit STS 19 (as was done in the petrous bone orientation), which displays the most posterior projecting basion (14.74), from the calculations: % (range (- 2.11); sd=9.75). Statistically, all adult groups differ from each other but australopithecines tend to resemble humans: apes to humans: p< ; apes to australopithecines: p< ; humans to australopithecines: p< As with the petrous bone orientation, there is no correlation between the position of basion and the specimen taxonomic affinity. A. afarensis ranges between % for A.L and % for A.L There is also no connection between robusticity and position of basion: KNM-ER 406 displays one of the most modest anterior placements of basion, only -2.11% while KNM ER is evaluated to be % anterior to the biporia line. Spatial configuration: In this part, I first superimposed specimen specific configuration onto to biporia, both in location and length, in all species groups. Each group average was then superimposed onto the other groups (Figure 8a). This view summarizes what was Figure 7: Superimposition of the average of the three adult groups. Blue: apes; orange: humans; green: australopithecines. a- groups aligned to biporia; b- groups aligned to average of landmarks excluding porion. P age 85

94 seen in the previous parts: australopithecines display more sagittaly-oriented petrous bones, and this seems to be coupled with an anterior position of basion, although there is no direct speciesspecific correlation between the two measurements. For the second part, I superimposed the different configurations according to the average of other landmarks but porion (Figure 8b). This was done in order to test whether the basion moved forward or rather the poria moved backward. As seen in the superimposition figure, basion is still the most anterior point in australopithecines, compared to other species Discussion Petrous bone orientation: The orientation of the petrous axis was measured externally by Dean & Wood (1981; 1982) as the angle between the carotid canal and the anterior tip of the petrous bone. In their results, great apes and humans are markedly different: about 70 vs. 45 respectively. Generally, gracile australopithecines resemble apes, while robust australopithecines resemble modern humans. However, direct measurement of the internal orientation of the petrous bone was only done in one research, prior to the current one. Spoor (1997) studied, among other angles, the orientation of the posterior petrosal surface to the sagittal plane. His results differ from the ones obtained in my study: humans exhibit an average of 55 (compared to 49.3 in my study). Two australopithecines measured by Spoor were also included in the present study. STS 5 has an angle of 44 in Spoor s study, compared with 40 in my analysis. OH 5 has an angle of 47, compared with in my analysis. WT17000, which I did not have access to, displays an angle of 45. Apes in Spoor s analysis display a more sagittal angle than humans, and fossil australopithecines are more similar to apes than humans: chimpanzees have an angle of 48 (similar to my results), while gorillas display an angle of the 42 (compared to 48.5 in my results). In my results, humans and apes possess a very similar angle of around 50 compared to P age 86

95 39 in australopithecines. According to Spoor's interpretation, fossil hominids display an intermediate form between humans and apes. The same view is held by du Brul (1977), claiming that as the brain grew in size, the petrous bone became more coronally oriented. Since australopithecines had a brain volume similar to that of chimpanzees, this assumption must be dismissed. The adult form of both chimps and humans are different than the juvenile form: in both juvenile species, the petrous is oriented more coronally at about 54, while the adults pose an angle of 49. It is interesting to note this observation, as it might indicate a parallel ontogenetic pattern, common to both species. Basion - biporia distance: The fact that australopithecine s basion is more anteriorly displaced than any of the other great apes has been previously documented. Dean &Wood (1981; 1982) noted the same phenomenon, but they attribute it to the shortening of the cranial base, especially in robust australopithecines and possibly parallel evolution between different hominid species. In Dean & Wood (1981, 1982) gorillas possess a posteriorly located basion, while humans are intermediate to australopithecines. In my results, gorillas, chimpanzees and humans are similar to each other in that they possess a basion that is posterior to the biporia line. This is characteristic also to the juvenile forms. The average location of the basion in the juvenile form of both species is about 15% behind biporia. In adult humans basion shifts forward to about 6%, while in adult apes it shifts backward to about 36%. As with other cranial base characters, the juvenile forms of both species display an intermediate form, closer to one another than to their own taxonomic affinity, suggesting a similar developmental process. In australopithecines, to the contrary, the basion is anterior to the biporia line. It is important to keep in mind that complete skulls of A. afarensis were only discovered in the 1990s, and therefore Dean & Wood only had a small sample of gracile australopithecine, mainly A. africanus, including the problematic STS 19 P age 87

96 specimen (See Kimbel & Rak, 1993; Ahern, 1998). From the 11 fossil australopithecines measured in this study, including both robust and gracile forms, a different picture arises: within australopithecines, the location of the basion is not correlated to specific taxonomic affinity. A.L , a male A. afarensis, manifests the most anterior projecting basion, while KNM-ER 406, one of the most robust A. bosiei that has a modest anterior projecting basion, falls next to MLD 37/8, a gracile A. africanus. Therefore Dean & Wood's (1981, 1982) interpretation seems inadequate, as all australopithecines as a group are significantly different from apes and humans. The similarity between apes and humans and the fact the australopithecines poses different morphology reinforce the taxonomic connection between the two recent groups, and the basic common structures that form their cranial base. With australopithecines, several possible scenarios might explain their special morphology, and a possible connection between the two observations. One possibility is that the sagittal orientation of the petrous bone or the anterior displacement of the basion might be connected to a specific genotype common to all australopithecines, without having any functional significance in itself. Another possibility is that in order to balance the head on the occipital condyles, the foramen magnum shifted forward and the two petrous bones reoriented to a more sagittal position, thus allowing this forward migration. The head-balancing hypothesis was suggested before (Schultz, 1942; 1955), but was largely dismissed, as many other animals do not balance their heads, but relies on other mechanisms, such as strong posterior neck musculature (Ross & Ravosa, 1993).With the data presented here, we might have to rethink Schultz's suggestion. Be that as it may, most importantly, australopithecines form an out-group to all other species, both in the location of basion and in the orientation of the petrous bones. This is not expected from a group that is supposed to occupy part of the space as one of the earliest ancestral genus or species between P age 88

97 humans and chimpanzees. Indeed, as a group, australopithecines may very well be close to the split between apes and humans, but over the years we are slowly accumulating a growing body of evidence to strengthen the notion that the derived morphology of australopithecines on the one hand, and the shared morphology between humans and apes on the other, suggests that none of the currently known australopithecines can be considered ancestral to later homo lineage. We should thus search yet again for other candidates to fill the gap in these early stages of human evolution. One possible such candidate might be Ardipithecus ramidus (Gen Suwa et al., 2009) in which according to the published data (see figure 3a; page 68e3), basion is exactly in line with biporia. The similar morphology displayed by the juvenile form of both chimpanzees and humans might suggest that Louis Bolk's ideas about the unique postnatal growth of the human child should be reconsidered. P age 89

98 Appendix I r.petr l.petr avrg %fm-bipor t-test Petrous Basion Adult Pan troglodytes Chimps - gorilla hvdc Chimps - juv. chimps hvdc Chimps - aus E E-11 hvdc Chimps - humans E-14 hvdc Chimps - juv humans E E-07 hvdc hvdc Gorilla - juv chimps hvdc Gorilla - aus E E-06 hvdc Gorilla - humans hvdc Gorilla - juv humans hvdc hvdc Juv chimps - aus E E-05 hvdc Juv chimps - Humans hvdc Juv chimps - juv humans hvdc hvdc Aus -humans E E-06 hvdc Aus - juv humans E E-07 hvdc hvdc hvdc Humans - Juv humans E hvdc hvdc hvdc hvdc hvdc Pan Pan.tau Pan.Tau Pan.tau PriCT 278 ptm PriCT 12 ptf Juvenile Pan troglodytes PriCT 14 juv PriCT 10 juv Prict 6 juv PriCT juv HvdC HvdC page 90

99 Appendix I r.petr l.petr avrg %fm-bipor Gorilla gorilla Gorilla prict Gorilla coll Gorilla coll PriCT 23 ggm PriCT 24 ggm Gorilla juv Gorila adult Australopithecines AL AL STS OH KNM KNM MLD 37/ SKW KNM STS page 91

100 Appendix I r.petr l.petr avrg %fm-bipor r.petr l.petr avrg %fm-bipor Adult Homo sapiens Juvenile Homo sapiens 72588m f1m m m24m f m11m m m7m f m16m f f0m f f24m f f24m f m10m m m0m f m8m f f4m f f m f f f m m m m f f f f m f m f page 92

101 4.3 3D morphometric analysis of the cranial base Introduction The hominoid basicranium manifests a complex topography, which is influenced by several underlying processes. The unique anthropoid basicranial morphology, along with the taxonomic and functional implications, did not escape the eyes of early anthropologists like Virchow (1857) and Broca (1871) who noticed l angle sphénoidal. Topinard (1891) in his paper La transformation du crâne animal en crane humain stirred one of the earliest discussions about the role of the cranial base in anthropoid evolution. Cameron (1927) wrote about the The main angle of cranial flexion, noting that a vast evolutionary gap exists between the anthropoids and man, with regard to the size of this angle. This is logically the space where the various 'missing links' would have to fit in. Indeed, the growing flexion of the midsagittal plane of the cranial base is one of the most prominent features throughout human evolution, and as such it has been studied extensively (Laitman et al, 1979; Luboga & Wood, 1990; Ross & Ravosa, 1993; Ross & Henneberg, 1995; Jeffery, 2005; Lieberman et al., 2008;, Kimbel & Rak, 2010). While most writers correlate cranial base flexion to the hominid encephalization process (Strait, 1999; Ross et al., 2004), others claim that bipedal or erect posture is the basic driving mechanism underlying these changes. Another set of studies focused on the changing hominid endocranial morphology, size and shape, but usually observed the entire endocranium, and not the skull base area in particular (Holloway, 1968; Falk, 1983; Schoenemann, 2006; Bruner & Holloway, 2010), thus placing much attention on the growing calvaria and cerebrum and its neurological or cognitive significance. Be that as it may, very few basicranial studies venture outside the midsagittal realm, and even fewer studies incorporate fossil hominids with extant species. One such outstanding study is the work of Dean & Wood Page 93

102 (1981) and Dean & Wood (1982). In these papers, linear and angular measurements of the cranial base in norma basilaris were taken and compared between extant hominoids and several australopithecines specimens. They note several morphological changes between apes and humans, and several hominid features that exist in both humans and australopithecines. These include an anterior displacement of the foramen magnum; shortening of the cranial base, and lateral displacement of the vascular openings. They also note differences between gracile and robust australopithecines, and suggest parallel evolution between the robust clade and Homo sapiens. It is important to remember that at the time these articles were published little was known about the skull of A. afarensis (the complete skull that was unearthed in the 1990s) and its taxonomic affinity. In spite of the importance of these papers, and the fact that they have been cited well over 60 times, only a handful of studies continued the examination of the shape of the Figure 1. a parasagittal cut of the skull, with the endocranium protruding. cranial base outside the mid-sagittal plane (Spoor, 1997; Ahern, 2005). More recently, several articles were published dealing with the overall 3D morphology of the endocranium (Figure 1), with reference to the cranial base. A series of papers (Neubauer & Hublin, 2012; Neubauer et al., 2010; Neubauer et al., 2009; Gunz et al., 2010) studied the developmental morphology and ontogeny of the cranial base in apes, humans and Pleistocene homo, using geometric morphometric techniques. The main conclusion of these studies is that chimps and humans have a different rate of endocranial development: while both species posses a non-linear growth rate, the cranial base flexes and the parietal and cerebellar regions expand faster in humans, contributing to the globular shape of the adult human brain. Interestingly, they (Gunz et al., 2012) found that Neanderthals appear to Page 94

103 follow chimpanzees rather than humans growth pattern. This means that for some evolutionary reason, humans developed a unique endocranial growth pattern, by which, in the first 3 years of life, the brain grows not in a linear manner but in a logarithmic one. Other recent studies include those of Bastir and colleagues (Bastir et al. 2011; Bastir et al., 2010; Bastir & Rosas, 2009), who worked on the cranial base of humans, apes and other early Homo species, to conclude that it is Homo sapiens that is highly specialized and uniquely different, compared to other hominids. In his view, this is the result of the human brain s reorganization not only through size, but also through specific shape changes in the temporal lobes and orbito-frontal cortex. Thus, these changes may contribute to human behavioral, social and cognitive abilities. He also concludes that the posterior aspect of the cranial base seems to be unrelated to its anterior parts and the face. To date, very little work has been done on the internal aspect of the basicranium, especially incorporating early hominids. Thus, the aim of this research will be a 3D morphological study of the entire endocranium, particularly the internal aspect of the cranial base, in three groups: Chimpanzees, Humans and Australopithecines. In order to capture the complex topography, I used landmark-based geometric morphometric techniques, and compared size and shape changes of the whole endocranium and shape changes of the internal basicranium between the groups Materials & methods The sample comprised 30 skulls of recent adult Homo sapiens from Israel (15 males, 15 females), 30 skulls of adult Pan troglodytes retrieved from the EVAN network, and 4 skulls of early hominids: A.L a large male A. afarensis from the Hadar site, reconstructed and published by Kimbel et al (2004); A.L a female from the Hadar site reconstructed and published by Kimbel & Rak (2011); STS-5 from Sterkfontein, one of the most complete A. Page 95

104 africanus ever found, published by Broom (1947); and MLD 37/8, an almost complete neurocranium published by Dart (1959). The former two skulls are relatively complete, and were virtually cleaned by Simon Neubauer (2004 & personal communication). All skulls were scanned in a medical CT machine under bone setting modality, with slice thickness of about 0.5mm. Each skull was then converted into a surface mesh in Amira software ( and saved in Wave Object (*.obj) format. Skulls were imported into EVAN Toolbox ( for landmark acquisition and data analysis. The principles and techniques used in this research, are summarized in Figure 2. 3D model of human endocranium. Blue point represent type I & II landmarks; Yellow point semi-landmarks Gunz et al (2009); Mitteroecker & Gunz (2009); and Zelditch et al (2004). The landmarks in my analysis consisted of two types: 31 type I or II and 198 semi-landmarks engulfing the whole endocranium, and 26 type I or II landmarks and 96 semi-landmarks for the basicranium (See Table 1, page 106) for summary of landmarks data). For each group, a template specimen was used, onto which all the other specimens landmarks & semi-landmarks were projected. Analysis was broken down into two parts. In the first analysis, species were superimposed using a generalized least-squares method, followed by principal component analysis. The shape-space was studied for the first two PC with ± 2 SD, in order to evaluate the main themes of shape variation. PC analysis for the entire endocranium and for just the basicranium was done on all groups, between chimps and humans; chimps and australopithecines; and australopithecines and humans. In the second analysis, I superimposed the specimens twice: once leaving size, and once omitting size. This was done in order to evaluate the relations between size and shape, and their Page 96

105 contribution to the observed morphological variation. A color coded vector map was created in order to highlight those regions that manifest the greatest morphological change. Colors ranged from blue to red, with red manifesting the greatest morphological change. Again, this was performed separately for the whole neurocranium and the basicranium. It is important to note that the reason for making two separate analyses one for the whole endocranium and one for the lower basicranium - was to evaluate whether the top part of the endocranium, due to the enormous cerebral expansion in humans, might overshadow other important morphological changes that occurred in the lower part of the internal cranial base. I postulated that major adaptive changes had taken place long before any major changes in the cerebrum size and shape, due to bipedal locomotion or erect posture Results Principal component analysis: It is important to realize that we are observing the extreme shape variation of the principal components, not necessarily the real group average form. These morphs help us to better understand the nature of the differences between the groups, and the underlining processes. We first look at chimpanzees and humans. Contrasting these two groups brings out the major evolutionary shape variation between the species. It is mportant to note that if we try to compare the endocranial shape without omitting size, we see a collapse in all PCs except the first one, as it contributes 100% of the observed variation. This is due to the immense cerebral outgrowth in humans. Therefore, it is important to observe shape only, while omitting size. In the first shape analysis (Figure 3, page 107) we study the complete endocranium. The first PC eigenvalue separates chimps from humans, and contributes and explains 56.8% of the total variance, while the second PC is much less significant, contributing only 11.1%. All other PCs do not seem to have any biological importance, contributing less than 5% each. Extreme Page 97

106 differences are observed in the shape of the upper calvaria: elongated in chimps vs. round, globular in humans. The shape of the frontal lobes is also remarkably different: in humans this area has expanded laterally, bringing out the familiar, rectangular endocranial human shape as seen from a superior or inferior view. From the inferior aspect, the folding of the cranial base around the inferior aspect of the pituitary fossa is apparent. This folding seems to originate in the frontal lobes, brainstem and inferior temporal area. The olfactory fossa is smaller in humans, becoming almost completely engulfed by the growing frontal lobes. All together, two main processes are apparent: first, the extreme outgrowth of the cerebral area; second, the folding of the inferior endocranium, both by the forward movement of the posterior cranial fossa and the downward movement of the frontal area. This analysis sums up the prevailing knowledge of the main processes that the hominid endocranium underwent throughout evolution, and is well documented in the literature (see Lieberman et al., 2000 for a detailed review). Examining just the inferior part of the endocranium (Figure 4, page 107) reveals a similar picture. We note major changes to the inferior frontal area, and a re-orientation of the foramen magnum and posterior cranial fossa. It is mportant to note that again, the first PC explains 49.70% of the variation of the sample, while the second explains only 9.07%. This is explained apparently by the observation that major morphological reorganization occurred in the lower part of the endocranium, and not just in the superior part. In the second analysis, I compared chimps to australopithecines. Interestingly, observing the complete endocranium (Figure 5, page 108) reveals that the first and second PCs are very similar in their eigenvalues, each contributing about 20% to the overall distribution of the sample. This is explained by the overall morphological similarity between these two groups. Yet observing the entire endocranium does bring forth some important differences. A prominent globular change in the upper endocranium is apparent, giving Page 98

107 australopithecines rounder upper calvaria. This is opposed to the elongated, flattened cerebral area of chimpanzees. Although endocranial volume in these two species is similar, this might indicate an early evolutionary reorganization of the brain. The three cranial fossae are better defined in australopithecines, an outcome of the overall globular shape of their calvaria and deepening of the temporal lobe and cerebellum. Observing the inferior aspect of the whole endocranium, we note transformation of other areas. The olfactory fossa is smaller in australopithecines. The inferior temporal lobes have grown laterally together with the diencephalon and brainstem area, giving a wider, more open middle cranial fossa. The foramen magnum has migrated anteriorly, and this is coupled with a horizontally placed petrous in chimps vs. a vertical one in australopithecines. Looking just at the inferior part (Figure 6, page 108), we note that the first PC eigenvalue now separates the two groups contributing to 23.48% of the variation, while the second PC eigenvalue only adds 12.31% to the sample variation. This probably means that the changes in the inferior endocranium are prominent, and might actually be overshadowed when observing the entire endocranium. The major differences observed in the inferior aspect are enlargement of the temporal lobes, as they grew inferiorly and laterally. The olfactory fossa did not reduce in size, but has shifted inferiorly, as part of a reorientation of the frontal lobe area. The petrous has dramatically changed from an almost horizontal orientation to a vertical one in australopithecines. The foramen magnum has shifted inferiorly in australopithecines, and is now pointing downward instead of backward in chimps. All together, from the inferior view, we note a change from a teardrop shape to a more rectangular shape in australopithecines. Finally, we follow the changes between australopithecines and humans. In the complete endocranium (Figure 7, page 109), the first PC eigenvalue contributes 32.5% to the overall variation, while the second PC eigenvalue adds 17.7%. Observing the complete Page 99

108 endocranium, we note that, surprisingly, many morphological changes that appear between australopithecines and humans are quite similar, and in some aspects, seem to follow the overall shape changes that were observed between chimps and australopithecines. The entire sagittal and coronal circumference of the endocranium is much rounder in humans, giving it a sphere-like appearance. It is also apparent that the entire posterior aspect of the brain has grown inferiorly and laterally, thus reorienting the foramen magnum to a more inferior and anterior position. Owing to the enlargement of the cerebral areas, the central diencephalic and its surroundings seem smaller and narrower than the equivalent area in australopithecines. Looking just at the inferior part (Figure 8, page 109), we see that the first PC eigenvalue accounts for 21.4% of the variation and the second PC eigenvalue for 18.52%. These are somewhat lower percentages compared to the complete endocranium, suggesting that differences in the lower endocranium are more subtle. Some of the more noted changes are lateral or coronal growth, coupled with shortening in the sagittal plane. There is also apparent increase in the overall shape of the posterior cranial fossa, as it migrates anteriorly and laterally. Vector map analysis: In this analysis, we first observed the complete endocranium twice: first after superimposing and retaining the size of the average form, and second, omitting the size thus only examining shape differences. We then proceeded to study just the inferior endocranium. Comparing chimps to humans including size (Figure 9, page 110), the overall globular enlargement of the cerebrum is very prominent. The frontal, parietal and parts of the occipital lobes grew out averaging about 2.5cm and the temporal lobes grew about 2cm. The brainstem and diencephalic areas grew about 1cm, and there is no apparent change in the olfactory area. The outer growth is uniform in its directions, explaining the familiar globular human cerebral shape. This growth around the diencephalic area might seem to be erroneous, or an artifact of the Page 100

109 superimposition process, but the even placement of the 229 landmarks around the endocranium lowers the probability of such a problem. Omitting size and observing only shape changes (Figure 10, page 110), the picture is a bit different. The most prominent transformed areas are the frontal areas, including the olfactory fossa. This entire area has shifted mostly anteriorly and inferiorly toward the diencephalon. The parietal area has grown mostly superiorly contributing to a more round cerebral shape. We also note the change in the position of the foramen magnum, as it shifted inferiorly and anteriorly. This analysis emphasizes the importance of observing shape and not size when looking for morphological changes between forms. Observing the inferior endocranium (Figure 11, page 110) brings out the major differences in location and orientation of the foramen magnum and the diencephalic area. Most noticeably, the foramen magnum and posterior part of the cerebellar area has shifted anteriorly and inferiorly. The brainstem has moved superiorly and anteriorly, while the diencephalic area has moved superiorly and posteriorly. The whole central part of the cranial base seems to have obtruded toward the cerebral peduncle and midbrain area, thus contributing to the globular shape of the human endocranium. The next analysis is the differences between chimpanzees and australopithecines. The obvious resemblance between these two groups is their endocranial volume, which is very similar, around 400cc. Thus, this analysis gives us good opportunity to compare size-shape vs. shape only. Indeed the differences between the two complete endocranial analyses are small (Figures 12 & 13, page 111). When observing the complete endocranium without omitting size, the major areas exhibiting differences are at best about 0.5cm apart. In both cases we note a change in the frontal area as it grew anteriorly, laterally and inferiorly. The posterior part of the petrous area has shifted posteriorly, while the anterior has shifted slightly laterally. This movement contributes to the more sagittally oriented petrous in australopithecines. Interesting to Page 101

110 note, in both analyses the inferior frontal gyrus (Broca s area or Brodmann s 44-45) became more pronounced in australopithecines on the left side. The enlargement of Broca s area in great apes has been noted before (Cantalupo & Hopkins, 2001) although its functional significance is not well understood. There are many articles addressing the origin and development of brain laterality (Holloway & De La Coste-Lareymondie, 1982; Falk, 1987; Balzeau et al., 2012), although very few articles provide direct data derived from observing early hominids. In the case of the differences between chimpanzees and australopithecines, observing just the basicranium (Figure 14, page 111) reveals a similar pattern to that of the whole endocranium. Again, this is an important observation, namely that once the upper, over-sized calvaria does not influence our analysis, other morphological changes become apparent. We thus observe the main processes that shaped the basicranium: the anterior-inferior movement of the forman magnum; medial movement of the posterior petrous coupled with lateral movement of the anterior part; and enlargement of the left inferior frontal gyrus, compared to the right side. Finally, we look at the differences between australopithecines and humans. While retaining size, the picture (Figure 15, page 112), not surprisingly, is very similar to what was observed between chimpanzees and humans. The upper cerebrum has shifted outward homogenously about 2.5cm, with much less movement in the central inferior area. Again, this is due to the massive cerebrum enlargement, overshadowing other morphological changes. Turning to shape differences only (figure 16, page 112), we see that the morphological changes of the upper endocranium are somewhat different from those observed in chimps to humans: the frontal and parietal lobes have grown outward, but to a lesser extent. There is an overall medial movement of the temporal lobes. This is not because these areas became smaller, but it marks a more pronounced lateral fissure, probably due to sizerelated enlargement of the frontal and temporal lobes. The cerebellum has shifted, possessing a Page 102

111 more anterior and medial location, reaching its familiar position completely under the occipital lobes. This movement is not symmetrical: the left lobe is more globular than the right one. Looking only at the basicranium (figure 17, page 112), we note that the foramen magnum has shifted mostly anteriorly, but also that the sella turcica seems to have elevated, causing its surroundings, namely the clivus, the temporopolar area (Brodmann 38) and the anterior end of the petrous, to shift upward and towards the hypophyseal fossa. The olfactory fossa becomes smaller as it moved upward into the frontal lobe Discussion Studying the 3d morphological changes of the endocranium and cranial base requires special attention. This is because, as in all biological processes, many different underlying and interweaving causes may play a part in the shape and outcome of the final morph. Thus, looking just at two ends of the process, chimps and humans, might be misleading when trying to decipher the true hominid morphocline. It is therefore imperative to remember that we do not possess the complete fossil record for this specific human evolutionary anatomy. Many of today s researchers tend to imply that it is recent human immense brain volume that is responsible for the shape of the endocranium and cranial base. In our analysis, when observing the differences between chimps and humans, we see a pattern that seems to corroborate the above studies: the cerebrum, having grown more-or-less homogeneously outwards, now engulfs the entire sub cortical areas, and the cerebellum has pushed the brainstem forward. This growth is so immense, that it contributes to 100% of the variation in differences between chimps and human. Compared to the changes in the upper endocranium, the lower part seems to have modified less extensively. However, when observing just the basicranium, the shape changes between the two species stand out. This phenomenon is very important to note: since the growth of the cerebrum is so massive, Page 103

112 it overshadows other processes within the endocranium. If we omit size altogether from this analysis, this observation sticks out, and we note that while the frontal and parietal areas have been modified dramatically, the same has happened to the foramen magnum, as it rotated inferiorly and anteriorly. If no other analysis had been conducted, our conclusion would have been that brain volume has contributed almost solely to the shape of at least the internal aspect of the basicranium. However, the incorporation of fossil hominids changes this picture. The case of the morphological changes between chimps and australopithecines highlights several important aspects of the nature of the evolutionary morphocline that early hominids went through. This analysis is especially important since australopithecines have endocranial volume similar to that of chimps - 487cc (compared to 378cc in chimps), thus allowing us to assess the nature of true shape vs. size changes. Indeed, comparing the two complete endocranium analyses reveals a similar picture: the anterior frontal lobes have grown anteriorly and inferiorly, about 5mm (compared to about 25mm in humans). The left side of the inferior frontal gyrus has grown more than the right side. These two features suggest that a cognitive change that already began in primates took a leap forward in early in hominids, as the entire frontal lobe and particularly the inferior frontal gyrus are closely related with higher brain functions and abilities (Schoenemann, 2006; Holloway, 1996). The posterior petrous area has shifted medial-posteriorly, while the anterior part has moved lateral-anteriorly. This is due to the fact that the petrous in australopithecines are more sagittal in their orientation, compared to a coronal placement in both humans and African great apes, as is discussed in other chapter in this thesis. We also note a change in the foramen magnum, as it moved to a more inferior and anterior location. This change in more pronounced when viewing just the inferior cranial base, as we noted that the area behind the foramen magnum has moved as well. Studying the changes between these two groups Page 104

113 enables us to realize that early in human evolution, major morphological changes occurred in the internal aspect of the cranial base. As most of the cerebrum maintained its basic shape and size, we observe the rearrangement of the posterior cranial fossa, in particular the foramen magnum area. This conclusion supports the hypothesis that it is bipedal walking or erect posture that contributed to the early shaping of the cranial base. The changes between australopithecines and humans superficially seem to resemble the changes between chimps and humans. When observing the complete endocranium without omitting size, we do get a very similar picture to that of chimps: the upper calvaria have homogenously grown outward, aside for the temporal lobes, adding about 2.5cm in each direction. Importantly, when size is discarded, we see a different pattern from the one observed in chimps and humans. We see that the frontal lobe has shifted backward, while the parietal lobe shifted upward. This shape change gives the human endocranium its overall globular appearance. The cerebelar area has also shifted medialy and laterarly, perhaps indicating a reorganitazion of the cerebellum as it grew in size and shape. Most notably, we observe the uplifting of the sella turcica area, pulling its surroundings towards it. In particular, we observe a more vertical clival area, coupled with a more horizontal plenum sphenoidum. The middle cranial fossa, especially its inferior-medial parts, also exhibits the same general rearrangement. While the reason for this morphological change is not completely clear, I postulate, as was suggested by others (Ross & Henneberg, 1995), that as the cerebrum grew, the diencephalon and the thalamus moved to a more central position in order to minimize the average distance between different brain parts. This later chronologic change contributed greatly to the familiar human endocranial appearance, which is well noted in the interal cranial base. We thus observe a mosaic of evolutionary change, spanning time and changing between species. It seems that the first early phase, observed between chimps and australopithecines, influenced Page 105

114 mostly the frontal lobe area and more importantly to this study, the posterior aspect of the cranial base, reorienting the foramen magnum and its surroundings. The most feasible explanation is that erect posture or bipedal locomotion caused this change. As with many other osteological elements, upright posture was the first component in skeletal modification on the path towards modern human appearance. The later phase, the expansion of the cerebrum, further contributed to the globular endocranial form. The underlining mechanism behind this later phase is completely different, and may be attributed to a process of centralization of the diencephalon. Although in this work I have focused on the cranial base, it did not escape my attention that other important processes appeared in the endocranial shape change. As an example, the differences between the left and right inferior frontal gyrus may indicate better motor and linguistic capabilities. This does not mean, of course, that australopithecines spoke. As we know from primate studies (Rizzolatti & Arbib, 1998; Hopkins & Leavens, 1998) this specific area is closely related to facial expression and hand gestures, which are also forms of complex communication. The inferior aspect of the cranial base also deserves a new look, using the above techniques, as it may hold other important anatomical and morphological clues to the evolutionary path of the human species.. Page 106

115 Table I: Landmark definition Landmark definition 1 Anterior clinoid process left Most posterior point on the anterior clinoid process 2 Anterior clinoid process right 3 Anterior temporal left Most anterior point on the temporal lobe within the 4 Anterior temporal right middle cranial fossa 5 Basion Anterior end of foramen magnum 6 Clivus (inferior) Three point along the clival line between basion and 7 Clivus (medium) dorsum sella 8 Clivus (superior) 9 Confluence of sinus Point were transverse, superior sagittal & occipital sinuses meet 10 Foramen cecum Foramen anterior to crista galli 11 Foramen ovale left Most anterior point on the rim of the foramen ovale 12 Foramen ovale right 13 Hypoglossal canal left Most anterior point on the inner aspect of the 14 Hypoglossal canal right hypoglossal canal 15 Internal acoustic meatus left Most anterior point on the inner aspect of the internal 16 Internal acoustic meatus right acoustic meatus 17 Opercular gyrus left Most inferior point on the bulge made by the opercular 18 Opercular gyrus right part of the inferior temporal gyrus 19 Opisthion Posterior end of the foramen magnum 20 Posterior cranial fossa left Most posterior point within the inferior cranial fossa 21 Posterior cranial fossa right 22 Planum sphenoidale Most posterior point on posterior-medial border of the lesser wing of the sphenoid. bone 23 Anterior petrous left Most anterior point on the temporal petrous 24 Anterior petrous right 25 Posterior petrous left Most posterior point on the temporal petrous 26 Posterior petrous right 27 Anterior falx Most anterior-inferior point of the frontal crest 28 Sylvian point left Point of division between the branches of the lateral 29 Sylvian point left fissure 30 Occipital crest Most inferior point on the occipital crest, just before the bifurcation of occipital sinus into 31 Anterior cranial fossa 19 semi-landmarks defining the surface of the anterior cranial fossa 32 Curves 20 semi-landmarks defining the borders between the anterior, middle and posterior cranial fossa 33 Middle cranial fossa 20 semi-landmarks defining the middle cranial fossa 34 Posterior cranial fossa 37 semi-landmarks defining the posterior cranial fossa 35 Calvaria 100 semi-landmarks defining the superior calvaria Total 229 landmarks & Semi-landmarks P age 107

116 Shape differences between chimpanzees and humans. Figure 3: Complete endocranium shape differences. Note the high eigenvalue of the first PC and the major change in the shape of the cerebrum. Figure 4: Inferior part of the endocranium shape differences. Note the basicranial flexion between the anterior and posterior cranial fossae. Page 108

117 Shape differences between chimpanzees and australopithecines Figure 5: Complete endocranium shape differences. Note the globular endocranial shape of australopithecines. Figure 6: Inferior part of the endocranium shape differences. Note the orientation of the foramen magnum and the petrous. Page 109

118 Shape differences between australopithecines and humans Figure 7: Complete endocranium shape differences. Note the globular shape of human endocranium and the location and shape of the foramen magnum and its surroundings. Figure 8: Inferior part of the endocranium shape differences. Note the lateral expansion of the human cranial base and the petrous orientation Page 110

119 Vector map analysis of shape differences between chimpanzees and humans Figure 9. Complete endocranium, size retained. Note 000 the homogenous outgrowth. Left: inferior view; Right: lateral view. Figure 10. Complete endocranium, size omitted. Note the growth in the frontal, parietal and foramen magnum areas. Left: inferior view; Right: lateral view. Figure 11. Inferior endocranium size omitted. Note the major change around the medial part of the middle cranial fossa. Left: inferior view; Right: lateral view. Page 111

120 Vector map analysis of shape differences between chimpanzees and australopithecines Figure 12. Complete endocranium, size retained. Note the same basic shape with changes to the frontal, inferior temporal and foramen magnum areas. Left: inferior view; Right: lateral view. Figure 13. Complete endocranium, size omitted. Note the changes in the frontal area, left inferior frontal area, posterior temporal area & foramen magnum area. Left: inferior view; Right: lateral view. Figure 14. Inferior endocranium, size omitted. Note the inferior temporal area, and the area posterior to the foramen magnum. Left: inferior view; middle: lateral view; right internal view. Page 112

121 Vector map analysis of shape differences between australopithecines and humans Figure 15. Complete endocranium, size retained. Note the the homogeneous outgrowth, similar to chimp and human shape change. Left: inferior view; Right: lateral view. Figure 16. Complete endocranium, size omitted. Note the change in the frontal and parietal areas, and the upward shift in the area around the sella turcica. Left: inferior view; Right: lateral view. Figure 17. Inferior endocranium, size omitted. Note the upward shift in the area around the sella turcica. Left: inferior view; Middle: lateral view; Right: internal view Page 113