Endocranial shape changes during growth in chimpanzees and humans: A morphometric analysis of unique and shared aspects

Journal of Human Evolution 59 (2010) 555e566

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Endocranial shape changes during growth in chimpanzees and humans: A morphometric analysis of unique and shared aspects Simon Neubauer*, Philipp Gunz, Jean-Jacques Hublin Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, D-04103 Leipzig, Germany

a r t i c l e i n f o

a b s t r a c t

Article history: Received 26 June 2009 Accepted 27 June 2010

Compared to our closest living and extinct relatives, humans have a large, specialized, and complex brain embedded in a uniquely shaped braincase. Here, we quantitatively compare endocranial shape changes during ontogeny in humans and chimpanzees. Identifying shared and unique aspects in developmental patterns of these two species can help us to understand brain evolution in the hominin lineage. Using CT scans of 58 humans and 60 chimpanzees varying in age from birth to adulthood, we generated virtual endocasts to measure and analyze 29 three-dimensional endocranial landmarks and several hundred semilandmarks on curves and the endocranial surface; these data were then analyzed using geometric morphometric methods. The ontogenetic shape trajectories are nonlinear for both species, which indicates several developmental phases. Endocranial shape is already distinct at birth and there is no overlap between the two species throughout ontogeny. While some aspects of the pattern of endocranial shape change are shared between humans and chimpanzees, the shape trajectories differ substantially directly after birth until the eruption of the deciduous dentition: in humans but not in chimpanzees, the parietal and cerebellar regions expand relatively (contributing to neurocranial globularity) and the cranial base flexes within the first postnatal year when brain growth rates are high. We show that the shape changes associated with this early “globularization phase” are unique to humans and do not occur in chimpanzees before or after birth. Ó 2010 Elsevier Ltd. All rights reserved.

Keywords: Virtual endocasts Brain Geometric morphometrics Semilandmarks Ontogeny Hominin evolution

Introduction Compared to our closest living and extinct relatives, humans have a large, specialized, and complex brain, which is embedded in a uniquely shaped braincase. The size and shape differences between adults of different hominin1 species are the product of different ontogenetic patterns, as the tempo and mode of brain growth during individual development affect size as well as the overall shape of the brain. Of these two aspects of ontogenetic change, only size change has been studied so far, whereas most discussions of shape change have focused only on specific local aspects, such as the cranial base angle. Here, we quantify global endocranial shape and compare the ontogenetic patterns of endocranial shape change in humans and chimpanzees.

* Corresponding author. E-mail addresses: [email protected] (S. Neubauer), [email protected]. de (P. Gunz), [email protected] (J.-J. Hublin). 1 Throughout the text we use the term “hominin” to refer to humans and their extinct ancestors (tribe Hominini). 0047-2484/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jhevol.2010.06.011

Among primates, species differences in brain growth patterns are well documented (Leigh, 2004), but there exists no agreement about the absolute and relative amount of these differences and their relevance for cognitive abilities and life history. To compare postnatal patterns of brain growth in species with different body sizes and different adult brain sizes, most researchers rely on proportional brain size based on cross-sectional growth series. While some have argued that neonatal proportional brain sizes are similar in humans and chimpanzees, or that the differences are insignificant (Kennedy, 2005; Vinicius, 2005), most studies have found that humans achieve a smaller amount of adult brain size at birth than chimpanzees and all other non-human primates (Martin, 1983; Smith and Tompkins, 1995; Coqueugniot et al., 2004; Leigh, 2004; DeSilva and Lesnik, 2006; Hublin and Coqueugniot, 2006). Some of the disagreements stem from the considerable uncertainties that are unavoidable when one computes a single ratio such as average proportional adult brain size at birth from a crosssectional sample, as absolute brain sizes are highly variable within each age group (see Hublin and Coqueugniot, 2006; Leigh, 2006). Moreover, the use of brain weights or endocranial capacities adds another source of discrepancy between results obtained by various

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authors (Hublin and Coqueugniot, 2006). DeSilva and Lesnik (2006) used resampling statistics (i.e., related every neonate to every adult of the cross-sectional sample) to show that brain size at birth in humans is about 30  5% of adult brain size and brain size at birth in chimpanzees is about 40  6% of adult brain size, which confirms that there is a difference in proportional neonatal brain size. After birth, human brain growth proceeds at fetal growth rates for nearly a year, or even longer, with subsequent decelerated brain growth for a prolonged period; the period of high growth rate and the duration of overall brain growth are shorter in chimpanzees (Holt et al., 1975; Martin, 1983; Smith and Tompkins, 1995; Coqueugniot et al., 2004; Hublin and Coqueugniot, 2006). Jolicoeur et al. (1988) and Leigh (2004) also described high growth rates shortly after birth but argued that there is barely a difference in duration of subsequent slower brain growth between humans and chimpanzees. In both species, however, the cessation of brain growth is loosely correlated with the eruption of the first permanent molar. An important aspect of endocranial shape, the cranial base angle, has been widely discussed from an ontogenetic as well as an evolutionary perspective and has been related to brain size (Weidenreich, 1941; Biegert, 1963; Enlow, 1968; Gould, 1977; Dean, 1988; Ross and Ravosa, 1993; Ross and Henneberg, 1995; Spoor, 1997), facial dimensions and orientation (Dabelow, 1929, 1931; Weidenreich, 1941; Schultz, 1960), mode of locomotion (Dabelow, 1929, 1931; Weidenreich, 1941; Schultz, 1960), and dimensions of the vocal tract (Lieberman et al., 1972; Laitman and Crelin, 1976; Laitman and Heimbuch, 1982). Lieberman and McCarthy (1999) showed that the cranial base rapidly flexes postnatally in humans for about two years, whereas the cranial base in chimpanzees extends over a more prolonged period of skeletal growth. Geometric morphometric analyses have also shown that, in humans, the lateral aspects of basicranial morphology mature later than the midline aspects (Bastir and Rosas, 2006, 2009; Bastir et al., 2008). Several more recent studies highlight the complex interrelationships between brain size, facial size and orientation, and basicranial morphology (Enlow, 1990; Trenouth and Timms, 1999; Jeffery and Spoor, 2002; Jeffery, 2005; Bruner and Ripani, 2008; Hallgrimsson and Lieberman, 2008; Lieberman et al., 2008; Bruner et al., 2010; Bastir et al., 2010a). Therefore, ontogenetic shape changes of the braincase do not exclusively reflect brain volume increase as the cranial base acts as an interface between the brain and the face. As the face continues to grow after the cessation of brain growth, endocranial shape continues to change due to the integration between different parts of the skull. However, shape changes during early ontogeny e when the cranial bones are not fully ossified and the cranial sutures are still open e are largely driven by the rapidly growing brain, especially in the frontal and parietal areas (see Moss and Young, 1960). Aims of this study In this study, we compare the ontogenetic patterns of overall endocranial shape change between humans and chimpanzees. Rather than studying the brain directly, we use geometric morphometric methods (Bookstein, 1991; Slice, 2007) to study the shape changes of endocasts from birth to adulthood. This will make it possible in future studies to analyze fossil specimens using the same approach. Endocasts e imprints of the brain and the surrounding tissues into the internal table of cranial bones e can serve as proxies for brain morphology (see, for example, Holloway, 1978; Falk, 1980, 1986, 1987; Bruner, 2004; Holloway et al., 2004) because of the highly coordinated growth and development of the brain, the meninges, and the cranial bones (Moss and Young, 1960; Sperber, 1989; Enlow, 1990).

Evolutionary developmental studies are often set in a heterochronic framework to relate morphological differences between closely related species to differences in the rates and timing of morphogenesis (e.g., Gould, 1977; Godfrey and Sutherland, 1996; Vrba, 1998; Rice, 2001; Vinicius and Lahr, 2003; Vinicius, 2005). In this context, humans are commonly referred to as paedomorphic (juvenilized), and, sometimes more specifically, neotenic (i.e., juvenilized shape at the same adult size as a result of slower development and same duration of growth [Gould, 1977]). In the classic approaches to heterochrony, size, age, and shape are considered as single variables. Therefore, not all heterochronic terminology (Gould, 1977; Shea, 1989; Godfrey and Sutherland, 1996; Rice, 1997) easily translates to empirical multivariate morphometric studies that use many shape variables (for a review and discussion of geometric morphometrics and heterochrony, see Mitteroecker et al., 2005). When we define an ontogenetic shape trajectory as an ontogenetic sequence of specimens in shape space, we can apply heterochronic terminology (e.g., extension and truncation) to describe changes between two groups that have overlapping trajectories. Parallel trajectories imply that postnatal morphogenesis follows a common pattern across different species in which the speciesspecific differences that are already distinct at birth are maintained throughout ontogeny (i.e., two species do not have the same shape at any time during ontogeny but share the same pattern of shape change). Sometimes, such parallel trajectories are referred to as “generalized heterochrony” (e.g., Zollikofer and Ponce de León, 2004). When two trajectories are divergent, however, then postnatal morphogenesis contributes to the adult morphological differences between species and accentuates inter-specific differences that are already present at birth. When developmental trajectories in shape space are non-linear, this creates additional methodological challenges with regards to formal tests about common aspects of development, as this precludes simple statistical tests about parallel versus divergent trajectories (see discussion below). Our aim here is to establish whether or not aspects of endocranial developmental patterns are shared between chimpanzees and humans, and whether or not there are species-specific aspects. Both chimpanzees and modern humans have evolved considerably since the last common ancestor (most evident since the discovery of Ardipithecus; White et al., 2009), but those aspects that are shared between these two species are likely to represent conserved ancestral growth patterns. Craniofacial shape trajectories Recent morphometric comparisons of craniofacial development have shown that primates have, on a large scale, similar patterns of postnatal development with few alterations of the duration, amount, and sometimes the direction of shape change. Most morphological differences that separate adults of different groups are already established at the time of birth, and while postnatal developmental trajectories of several craniofacial regions are not parallel, they are very similar among closely related species. This has been shown among great apes (Bruner and Manzi, 2001; Ackermann and Krovitz, 2002; Mitteroecker et al., 2004b; Cobb and O’Higgins, 2007), between humans and great apes (Penin et al., 2002; Bastir and Rosas, 2004; Cobb and O’Higgins, 2004; Mitteroecker et al., 2004a,b; Viðarsdóttir and Cobb, 2004), between humans and Neanderthals (Ponce de León and Zollikofer, 2001; Zollikofer and Ponce de León, 2004), and among human populations (Viðarsdóttir et al., 2002). It can be shown that when several anatomical “modules” (i.e., the face and the neurocranium, or vault and cranial base) with different underlying linear developmental processes are analyzed together, the overall developmental trajectories of two groups diverge in shape space even when only one module develops differently (Mitteroecker

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et al., 2005). When shape trajectories comprise multiple linear developmental processes, they are non-linear in shape space (Mitteroecker and Huttegger, 2009). Unlike in traditional studies of body size or brain size versus age where non-linear growth trajectories indicate different growth rates and growth spurts (e.g., Humphrey, 1998; Leigh, 2004), non-linear developmental shape trajectories, such as those reported by Mitteroecker et al. (2004a,b, 2005), Bulygina et al. (2006), O’Higgins et al. (2006), Neubauer et al. (2009), and Bastir et al. (2010a), indicate multiple developmental phases, as the underlying geometry of the trajectory in shape space comprises several diverging partitions (cf. Mitteroecker and Huttegger, 2009, for a detailed discussion of the properties of morphospaces). Endocranial shape trajectories Against the multitude of facial developmental studies stands the dearth of studies documenting endocranial shape changes during development, as methods for analyzing the relatively featureless surface of endocasts have only recently been introduced (Gunz et al., 2005; Specht et al., 2007). In the first comprehensive study of endocranial form changes throughout human ontogeny, we have recently shown that this developmental trajectory is non-linear (Neubauer et al., 2009). Based on this result, we suggested that the non-linearity of the trajectory indicates multiple underlying developmental phases, which can be approximated by three linear parts: an early perinatal phase, a childhood phase, and an adolescent phase.

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absolute endocranial size, for which it is known that both the adult values and growth curves differ for humans and chimpanzees. Furthermore, dental eruption is correlated with important life history variables e the eruption of the permanent first molar is loosely correlated with attaining adult values of brain size, the eruption of the second molar is associated with the adolescent growth spurt, and the eruption of the third molar coincides with the completion of somatic growth and sexual maturity (Smith, 1989; Smith and Tompkins, 1995; Smith et al., 1995; Robson and Wood, 2008). A definition of the developmental age groups and sample distribution according to species and age groups is provided in Table 1. The cross-sectional nature of our sample imposes several constraints with regards to interpretation of the results (see, for example, Boas, 1892; Tanner, 1978). Ideally, longitudinal data are used to compute developmental trajectories, but such ontogenetic series comprising chimpanzees and humans from birth to adulthood are not available. We therefore use developmental simulations (cf. McNulty et al., 2006) to show that the average shape trajectories used here represent reasonable estimates for the individual trajectories (see below). Statements about the timing of ontogeny, however, necessarily remain tentative and will have to be confirmed when longitudinal data become available.

Virtual endocasts and landmark data A priori hypotheses We expect that endocasts of humans and chimpanzees are already distinct at the time of birth. We also expect that the two species share aspects of endocranial postnatal shape change: common patterns of development were previously found for different cranial regions, and morphogenesis is an integrated process to incorporate all the size and shape changes of the entire craniofacial complex. We hypothesize, however, that postnatal ontogeny contributes to species-specific morphology, either by extending or truncating shape change along trajectories in a common direction (same shape change but different amount) or via different shape changes for part of the postnatal period. The latter is possible because non-linear trajectories can describe the same shape changes in some segments but different shape changes in others. If aspects of shape change in the course of human morphogenesis are not found in chimpanzees, and these aspects contribute to uniquely human features, then we expect that they are informative for human brain evolution. Material and methods Sample Our cross-sectional samples comprise dried crania of 58 human (Homo sapiens) and 60 chimpanzee (Pan troglodytes) specimens of various ages (comprised of collections from the Medicine Faculty of Strasbourg, the University of Vienna, the University of Leipzig, the University of Freiburg, the Max Planck Institute for Evolutionary Anthropology, the Muséum National d’Histoire Naturelle Paris, and the Naturkundemuseum Berlin). All specimens were CT (computer tomography) scanned at facilities near their respective repositories (BIR ACTIS 225/300, Siemens Sensation 16, Siemens Plus 4 Volume Zoom) and CT images were reconstructed with a pixel size between 0.2 mm and 0.5 mm and a slice thickness between 0.2 mm and 1.0 mm. Dental age groups were used as surrogates for endocranial development instead of size. This facilitates the comparison of individuals at comparable ontogenetic stages irrespective of

We generated virtual endocasts for all specimens by a combination of two- and three-dimensional, semi-automated segmentation of the CT images following the protocol described in Neubauer et al. (2009). These virtual endocasts were used for the sliding procedure of surface semilandmarks. Furthermore, we acquired three-dimensional coordinates of 307 landmarks and semilandmarks on curves and surfaces (Fig. 1). We digitized 29 anatomical landmarks defined on endocranial bony structures like sutures, foramina, and points of maximum curvature (Table 2), as well as densely spaced points along bilateral and midsagittal endocranial curves. These curves (see Fig. 1) compartmentalize the endocranial cavity and are, in part, attachment sites for dural tensors, the falx cerebri, and the tentorium cerebelli. The curve on the sphenoid wing separates the anterior and the middle cranial fossa, the petrous curve delineates the middle from the posterior cranial fossa. The curve on the upper border of the transverse sinus forms the boundary between the posterior cranial fossa and the vault. Curves on the basioccipital clivus and the foramen magnum give additional information about the morphology of the posterior cranial fossa as well as basicranial angulation. The midsagittal profile curve from foramen caecum to opisthion approximates midsagittal vault form. To resample these curves to the same point count, we computed cubic splines through the densely spaced coordinates digitized along the curves and placed semilandmarks equidistantly along them. To place the surface semilandmarks, we measured a mesh of coordinates on the cerebral and cerebellar surfaces of one reference individual. This mesh was warped to

Table 1 Human and chimpanzee sample. Age group

Dentition

Humans

Chimpanzees

1 2 3 4 5 6

no teeth erupted incomplete deciduous dentition complete deciduous dentition M1 erupted M2 erupted M3 erupted

7 7 19 6 0 19 58

7 5 7 12 7 22 60

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Figure 1. Landmark set. Red spheres: anatomical landmarks; black spheres: semilandmarks on curves; blue small spheres: surface semilandmarks. (a) Landmarks and semilandmarks shown on the cranial base. Curves compartmentalize the endocranial cavity. (b) Landmarks and semilandmarks shown on the segmented virtual endocast. Surface semilandmarks capture the morphology between anatomical landmarks and curves. (c) Landmarks and semilandmarks are used to generate a triangulated surface of the endocast. Curve semilandmarks are connected along curves. (d) Triangulated surface of landmark set shown in relation to the bony brain capsule. This surface has landmarks and semilandmarks as vertices only (a down-sampled version of the segmented endocast), and is used to visualize shape change during ontogeny.

every specimen according to anatomical landmarks and curvesemilandmarks using the thin-plate spline algorithm. These warped points were then projected onto the surface of the virtual endocasts following Gunz et al. (2005, 2009a,b), Grine et al. (2010) and Neubauer et al. (2009). To remove the influence of the arbitrary spacing of the semilandmarks, they were allowed to slide along tangents to the curves and tangent planes to the surface so as to minimize the bending energy of the thin-plate spline interpolation function between each specimen and the Procrustes consensus configuration. This was done in an iterative process of sliding and projecting back onto the cubic splines of curves and the surface of virtual endocasts until convergence (Bookstein, 1997; Bookstein et al., 1999; Gunz et al., 2005). Detailed explanations of the measurement protocol and discussion about methodological details, advantages, limitations, and alternative approaches of sliding semilandmarks can be found elsewhere (Perez et al., 2006; Neubauer et al., 2009). All specimens were measured by one observer (SN). Intra-observer error, as assessed from analysis of repeated measurements, was small and did not affect specimen affinity (Neubauer et al., 2009). Landmarks and semilandmarks after sliding were superimposed using generalized least-squares Procrustes analysis (Gower, 1975; Rohlf and Slice, 1990). This removed information about location and orientation from the raw coordinates and scaled each specimen to unit centroid size. The resulting Procrustes shape variables were used in geometric morphometric analyses as outlined below.

Table 2 Used landmarks. M: midsagittal landmarks, B: bilateral landmarks (measured on the left and right side). Endocranial landmarks M M M M M M M M M B B B B B B B B B B

anterior sphenoid spine foramen caecum endobregma endolambda internal occipital protuberance opisthion basion endosphenobasion dorsum sellae anterior clinoid process optic canal superior orbital fissure foramen rotundum foramen ovale petrous apex internal accustic meatus maximum curvature point between transverse and petrous curve foramen jugulare hypoglossic canal

Analytical methods We performed a principal components analysis (PCA) of the Procrustes shape variables and visualized shape change along principal components (PCs). The convex hulls are based on dental age groups; the ontogenetic trajectories are shown by connecting group means of subsequent age groups. We also plot average shape trajectories obtained by resampling; we bootstrapped (with replacement) the mean within each age group and connected the bootstrapped means of subsequent age groups. This visualizes the uncertainty of the age group means that is due to the crosssectional nature of the sample. To avoid potential projection artifacts of PCA, we visualized the shape changes during ontogeny as the shape differences between age group means computed using all Procrustes coordinates (i.e., all dimensions of shape space) rather than visualizing only single PCs (Neubauer et al., 2009; for a detailed discussion of this issue see Mitteroecker and Gunz, 2009). Developmental simulations As discussed above, it is difficult to investigate similarities and differences between non-linear trajectories because a test cannot be based on the question of parallelism or divergence. Here, we assess the similarity of chimpanzee and human average shape trajectories using developmental simulations (cf. McNulty et al., 2006). McNulty et al. (2006) used developmental simulations to assess the phenetic affinities of the juvenile Australopithecus africanus cranium Taung, and simulated the developmental trajectories using linear regressions of facial shape variables on dental stages. To test the validity of their approach, they applied the same method to juvenile crania of extant humans, bonobos, common chimpanzees, and gorillas, and checked whether or not the simulated adults fell within the range of the true respective adults. Our simulations were computed in the same spirit, but rather than using regressions, we added the average shape trajectory (the vectors between the mean shapes of consecutive dental age groups) to subadult configurations to account for the non-linearity of the trajectories. If subadults of species A that develop along the shape trajectory of species B look like adults of species A, then ontogenetic trajectories are interchangeable. When trajectories, or at least parts thereof, are interchangeable, this indicates shared aspects of ontogenetic shape change between humans and chimpanzees. We also used developmental simulations to test whether or not the average developmental trajectories obtained from our crosssectional sample represent a reasonable estimate of individual developmental trajectories. We applied the mean shape trajectory

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(the series of vectors between consecutive age groups) to each neonate and compared the endocranial shape of these simulated adults to the actual adults of the sample. Results Endocranial shape variation The ontogenetic signal is clearly detectable along PCs 1e3 by visual inspection of the PC scores of consecutive age groups (see Fig. 2). These three components explain 76% of total sample variation. Higher PCs do not show a clear trend of PC scores from younger to older age groups and are not further described here. The chimpanzee as well as the human ontogenetic trajectories are both non-linear in their geometry. There is no overlap of humans and chimpanzees throughout ontogeny, i.e., they do not have the same endocranial shape at any time during development after birth. The bootstrapped age group means and the similarity of the resulting average trajectories demonstrate that the uncertainty stemming from the cross-sectional nature of the sample does not affect the interpretation of ontogenetic patterns. The first principal component describes shape variation from a globular endocast with a narrow cerebellar region, a flexed cranial base, and an anteriorly oriented foramen magnum to an

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anteroposteriorly elongated endocast with a wide cerebellar region, an extended cranial base, and a posteriorly oriented foramen magnum. This component describes overall differences between the two species, humans having negative PC scores and chimpanzees having positive PC scores. Principal component 2 summarizes shape variation from an endocast with an extended cranial base, a posteriorly oriented foramen magnum, a small cerebellar region, inferiorly oriented temporal poles, and an inferiorly oriented cribriform plate to an endocast with a flexed cranial base, an inferiorly oriented foramen magnum, a larger cerebellar region, anteroinferiorly oriented temporal poles, an anteroinferiorly oriented cribriform plate, and a higher cerebral region with expanded parietal areas. Principal component 3 contrasts narrow endocasts with a low cerebral region, a posteriorly oriented foramen magnum, and an anteroinferiorly oriented cribriform plate and wide endocasts with a high cerebral region, an inferiorly oriented foramen magnum, and an inferiorly oriented cribriform plate. Human age groups 1 and 2 do not overlap along PCs 2 and 3. The age difference between the oldest individual of age group 1 (nearly 4 months old) and the youngest individual of age group 2 (6 months old) is over 2 months. Therefore, we interpret the “discontinuity” between human age groups 1 and 2 as a sampling

Figure 2. Endocranial shape space. (a) PC 1 versus PC 2, (b) PC 1 versus PC 3. Humans are shown in blue and chimpanzees in green. Age groups are coded by numbers 1e6. Semitransparent convex hulls indicate the variation of age groups. Mean shapes of each age group are connected with a solid line to the subsequent age group. Thin lines are shown between bootstrapped age group means to demonstrate the low uncertainty of the mean trajectory caused by the cross-sectional samples. One fetal chimpanzee specimen (“f”) indicates that prenatal shape change in chimpanzees does not correspond to perinatal human shape change (from age group 1 to age group 2). Shape change along the PCs is visualized as mean shapes plus/minus 2 standard deviations (2 SDVs) from the sample mean.

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artifact, as a considerable amount of (size and) shape change occurs in 2 months during this perinatal period. We visualized ontogenetic shape change in Procrustes space along linear segments between age group means that approximate the complex geometry of the ontogenetic trajectories in the first three PCs (Fig. 3). We thereby include the ontogenetic shape variation of all dimensions of shape space rather than interpreting a single PC that on its own does not describe one ontogenetic signal. Chimpanzee early shape changes In chimpanzee early ontogeny (from age group 1 to age group 2; Fig. 3a), the posterior cranial fossa becomes relatively enlarged and projects backwards. The adjacent regions above the transverse sinus, including the occipital, parietal, and posterior temporal areas, follow this shape change. The sagittal and parasagittal frontal areas expand relatively. The rest of the parietal and frontal areas diminish relatively. The anterior cranial fossa becomes narrower and relatively reduced. Chimpanzee juvenile to late period shape changes Thereafter (from age group 2 to age group 6; Fig. 3b), the posterior cranial fossa expands and rotates in a posterior direction, which also leads to a reorientation of the foramen magnum. Lateral frontal, parietal, and occipital areas become relatively reduced. Sagittal and parasagittal frontal areas, as well as orbital areas, enlarge

relatively and the cribriform plate reorients. The middle cranial fossa expands relatively and the temporal poles rotate anterolaterally and superiorly. The cranial base extends as the posterior and anterior cranial fossae shift and rotate away from each other. Human early shape changes In human early ontogeny (from age group 1 to age group 2; Fig. 3c), the posterior cranial fossa becomes relatively enlarged including a rotation of the foramen magnum. Relative parietal expansion is accompanied by pronounced parietal bossing. The posterolateral temporal regions widen, and the prefrontal and orbital regions as well as the anterior temporal poles become relatively reduced. The cranial base flexes and the interpetrosal angle increases. Overall, the endocast becomes more globular. Human juvenile shape changes Thereafter (from age group 2 to age group 4; Fig. 3d), the posterior cranial fossa expands relatively, but in a more inferior direction without a change in foramen magnum orientation as compared to the previous shape change. The sagittal and parasagittal frontal areas enlarge relatively while the lateral frontal, parietal, and occipital areas get relatively reduced. The anterior cranial fossa diminishes relatively and rotates superiorly. The temporal poles rotate medially and the temporal lobes widen laterally.

Figure 3. Visualization of ontogenetic shape change. Endocasts shown are triangulated surfaces of the landmark set and do not contain any additional points. Curve semilandmarks are connected with lines. Left side: mean shapes of all age groups for chimpanzees and humans. Right side: Differences between age groups are visualized; the younger age group is shown in gray, the older age group is shown in transparent green and green outlines for chimpanzees, and transparent blue and blue outlines for humans. Thin-plate spline grids in the midsagittal plane are shown in lateral view. (a) Shape difference between chimpanzee age groups 1 and 2; (b) shape difference between chimpanzee age groups 2 and 6; (c) shape difference between human age groups 1 and 2; (d) shape difference between human age groups 2 and 4; (e) shape difference between human age groups 4 and 6.

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Human late period shape changes Finally, in late ontogeny (from age group 4 to age group 6; Fig. 4e), the relative height of the posterior cranial fossa is reduced and a relative posterior projection of the occipital area develops. The parietal and adjacent frontal areas become relatively reduced while the anterolateral frontal, prefrontal, and orbital areas expand relatively. The temporal poles rotate anterolaterally and superiorly and the posterior temporal areas rotate superolaterally.

Developmental simulations When the mean trajectories are applied to neonatal specimens (or the mean trajectory starting from age group 2 to specimens of age group 2), the simulated adults (Figs. 4 and 5: simulated human adults, H1, H2; simulated chimpanzee adults, C1, C2) are barely distinguishable from the measured adults (H, C). The mean estimated trajectory based on our cross-sectional sample is therefore a reasonable estimate of the “real” individual trajectories.

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Developmental simulations based on the other species’ trajectories demonstrate differences and similarities between the human and chimpanzee ontogenetic trajectories. When the human trajectory is applied to chimpanzee neonates (C4) and the chimpanzee trajectory is applied to human neonates (H4), the simulated adults exhibit endocranial shapes that seem to be a mixture of species-specific morphological features that are already established at birth and features that arise during the other species’ postnatal ontogeny (Figs. 4a and 5: C4 and H4). These simulated adults neither resemble humans nor chimpanzees at any stage of development. Therefore, ontogenetic trajectories of humans and chimpanzees differ and postnatal ontogeny contributes to speciesspecific morphology. Because endocranial shape seems to change differently in early ontogeny than in later ontogeny (see Figs. 2 and 3a,c), we repeated developmental simulations without considering shape change from age group 1 to age group 2. When mean trajectories starting with age group 2 of one species are applied to specimens of the same age group from the other species, simulated adults (Figs. 4b

Figure 4. Developmental simulations. (a) The ontogenetic trajectories (dashed lines, blue for the human trajectory and green for the chimpanzee trajectory) are applied to neonatal specimens. (b) Later ontogenetic trajectories (from age group 2 onwards) are applied to specimens of age group 2. Simulated adults based on the human trajectory are shown in blue, while simulated adults based on the chimpanzee trajectory are in green. H1: human adults simulated from human neonates along the human trajectory; H2: human adults simulated from human age group 2 along the later human trajectory; H3: human adults simulated from human age group 2 along the later chimpanzee trajectory; H4: human adults simulated from human neonates along the chimpanzee trajectory; C1: chimpanzee adults simulated from chimpanzee neonates along the chimpanzee trajectory; C2: chimpanzee adults simulated from chimpanzee age group 2 along the later chimpanzee trajectory; C3: chimpanzee adults simulated from chimpanzee age group 2 along the later human trajectory; C4: chimpanzee adults simulated from chimpanzee neonates along the human trajectory. The “f” represents the fetal chimpanzee as in Fig. 2.

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Figure 5. Visualization of actual and simulated adults. (a) human adults and (b) chimpanzee adults. Mean shapes of human (H) and chimpanzee (C) adults are shown in the middle, mean shapes of simulated adults according to the species’ own trajectory are shown to the left, and mean shapes of simulated adults according to the other species’ trajectory are shown to the right (blue wire frames indicate simulations based on the human trajectory, green wire frames indicate simulations based on the chimpanzee trajectory). H1eH4 and C1eC4 correspond to the simulations shown in Fig. 4. Note that H3 and C3 resemble H and C, respectively, but H4 and C4 do not, indicating that early ontogenetic shape change is different, but, thereafter, shape change is similar in humans and chimpanzees.

and 5: H3 and C3) resemble the actual adults. Therefore, humans and chimpanzees share some aspects of ontogenetic endocranial shape change for part of their postnatal ontogenies. Subtle differences between actual adults (Fig. 5: H and C) and simulated adults (Fig. 5: H3 and C3) are due to (1) the fact that the trajectories are similar but not identical, and (2) different amounts of shape change along the trajectories. Adults simulated according to the other species’ trajectory seem to be shifted along a shared trajectory: simulated humans (H3) are “over-grown” in relation to actual adults (H), and simulated chimpanzees (C3) did not yet achieve the endocranial shape of the measured chimpanzees (C, see Fig. 4b). Discussion Differences and similarities of species-specific shape trajectories We found non-linear ontogenetic trajectories for both species (Fig. 2). Such complex trajectories are in accordance with previous studies on the morphogenesis of endocranial morphology and parts thereof (Bastir and Rosas, 2009; Neubauer et al., 2009), and indicate multiple underlying linear phases of shape changes (Mitteroecker and Huttegger, 2009). Humans and chimpanzees are separated for the entire course of postnatal ontogeny and the geometries of their ontogenetic shape trajectories are different. Therefore, our results support the hypotheses that (1) endocranial shape is already distinct at birth, and (2) postnatal morphogenesis contributes to the adult differences between humans and chimpanzees. The ontogenetic patterns of shape change are markedly different in early ontogeny (between dental age groups 1 and 2), but are very similar from age group 2 onwards, implying shared aspects of ontogenetic shape changes for most of the postnatal period (Figs. 2 and 4). Shape differences that are already established at birth comprise different configurations of the cranial base and associated vault shape; in humans, the cranial base is flexed and the vault is already globular, and, in chimpanzees, the cranial base is extended and the vault anteroposteriorly elongated. Different perinatal shape change Our results show that humans have a perinatal phase of shape change before they enter a common ontogenetic pattern that is shared with chimpanzees. These early human shape changes do not exist in chimpanzees after birth and contribute to what Lieberman

et al. (2002) have termed “neurocranial globularization” by relative parietal expansion, relative expansion of the posterior cranial fossa, as well as basicranial flexion. Perinatal shape change in chimpanzees is similar to their entire postnatal ontogeny. The differences between early and subsequent shape changes in chimpanzees are the relative growth of cerebellar and posterior cerebral areas that only take place perinatally (compare shape change visualized in Fig. 3a,b). There are two alternative interpretations for the human perinatal shape changes that were not found in chimpanzees: either this phase does exist in chimpanzees, but it occurs prenatally, or this phase is unique to humans. Humans achieve a smaller percentage of adult brain size at birth than chimpanzees (Holt et al., 1975; Martin, 1983; Smith and Tompkins, 1995; Coqueugniot et al., 2004; Leigh, 2004; DeSilva and Lesnik, 2006; Hublin and Coqueugniot, 2006). If chimpanzees had an analogous “globularization phase” before birth, this would align with the idea of developmental retardation in humans, as humans are delayed in achieving proportional brain size, and delayed in shape changes that we found directly after birth in humans but not in chimpanzees. The following lines of evidence, however, suggest that chimpanzees do not have a ”globularization phase” before birth. Around birth, humans also have a relatively anteroposteriorly elongated endocast. It is not until the perinatal phase of shape change that humans achieve the amount of globular shape that is so typical for modern humans. Chimpanzee neonates have an even more pronounced anteroposteriorly elongated endocast than human neonates (comparing chimpanzee and human neonates in Fig. 3 and their position along PC 1, which contrasts globular versus elongated endocasts). Therefore, it is unlikely that they underwent shape changes contributing to globularity before birth. Comparative data of prenatal shape changes in primates are very rare; we measured one fetal chimpanzee specimen and included it in our analysis (“f” in Fig. 2, unknown gestational age, cranial capacity is about one-third of a chimpanzee neonate). As only a single fetal specimen was available, we do not consider this a formal test of our hypothesis, but the shape change from this fetus to the chimpanzee neonates is an indication that chimpanzees do not have a “globularization phase” before birth. Aspects of prenatal endocranial shape change studied previously included the cranial base angle. Jeffery (Jeffery and Spoor, 2002; Jeffery, 2003, 2005) has shown that the midline cranial base extends (retroflexes), the petrous bones orient coronally, the

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supratentorial volume enlarges, and the anterior cranial base grows faster than the posterior cranial base prenatally in humans as well as in non-hominoid primate species (macaques and howler monkeys). The rate of change is often different but the direction of change is shared among macaques, howler monkeys, and humans (Jeffery, 2003). This prenatal extension of the cranial base is shared among all studied non-human primates, and is the exact opposite of the human perinatal shape changes during the “globularization phase” in which the cranial base flexes. Based on the shape of chimpanzee endocasts at the time of birth, the endocranial shape of a chimpanzee fetus, and the well documented prenatal shape changes of the cranial base, we therefore consider it highly unlikely that chimpanzees have a prenatal “globularization phase” comparable to what we find in humans after birth. We suggest that the perinatal pattern of endocranial shape change associated with the “globularization phase” is uniquely human, and does not exist in chimpanzees (and presumably other non-human primates) before or after birth. To formally test this issue, future studies should incorporate prenatal, three-dimensional shape data of chimpanzees, humans, and other species. It is worth noting that the differences between the shape trajectories of humans and chimpanzees occur in early ontogeny when brain growth rates are high and cranial bones are not fully ossified. Therefore, it can be assumed that it is the rapidly growing brain that drives endocranial shape change and that the differences found between humans and chimpanzees relate to differences in brain development. Shared postnatal shape change After distinct species-specific perinatal development, shared aspects of ontogenetic shape change include a relative expansion of the posterior cranial fossae, the sagittal and parasagittal frontal areas, and the orbital areas, the anterolateral and superior rotation of the temporal poles, and a relative reduction of lateral frontal, parietal, and occipital areas. Previous studies (Richtsmeier and Lele, 1993; Richtsmeier and Walker, 1993; Bruner and Manzi, 2001; Ponce de León and Zollikofer, 2001; Ackermann and Krovitz, 2002; Penin et al., 2002; Zollikofer and Ponce de León, 2004) have suggested similar (i.e., parallel) postnatal ontogenetic trajectories among extant and extinct hominoids for different craniofacial regions, implying a common developmental pattern after birth. Because ontogenetic trajectories in our study are interchangeable when one does not consider perinatal shape change, we propose that the trajectories for the endocranium are very similar only after deciduous teeth start to erupt. However, the amount of shape change and its duration during this period is different. Therefore, shape differences achieved along a shared trajectory could be partly underlain by heterochronic processes. When we interchange the average ontogenetic trajectories of chimpanzees and humans after the eruption of the deciduous dentition, we find that human adults have more “juvenile” shapes along a shared trajectory than chimpanzees (see extended and truncated shape trajectories in Fig. 4b). Furthermore, chimpanzees reach adulthood (i.e., erupt their M3s) earlier than humans (Smith et al., 1994), implying a shorter duration for a larger amount of shape change. However, humans and chimpanzees do not have the same endocranial shape at any point in postnatal development (their ontogenetic trajectories do not overlap), but “only” share the pattern of shape change along which humans undergo less change than chimpanzees. Furthermore, we analyzed a cross-sectional sample with dentally aged specimens here, lacking a continuous age variable that is very important in determining neoteny as previously discussed by Shea (1989), Godfrey and Sutherland (1996), and Rice (1997). Therefore, it is

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difficult to use terms like “paedomorphy,” and, even more so, “neoteny,” in our approach. Analyses of longitudinal data are required to investigate timing differences in more detail. In chimpanzees, the relative reduction of calvarial parts is associated with the rotation of the anterior and posterior cranial fossae away from each other. It has been described earlier that the midline cranial base in chimpanzees extends continuously during postnatal ontogeny (Lieberman and McCarthy, 1999). Most versions of the traditional cranial base angles are still significantly different between age groups 5 and 6 in chimpanzees (Lieberman and McCarthy, 1999). Our data show that not only the midline, but also the entire cranial floor extends and confirms that the cranial base continues to extend even in the latest ontogenetic stage prior to adulthood. In humans, on the other hand, posterior projection of the occipital area, relative expansion of prefrontal and orbital areas, and modifications of the middle cranial fossa e including the forward projection of the temporal poles, along with the modifications in the anterior cranial fossa and widening of the temporal areas e accompany flattening of the upper neurocranium. While the midline cranial base angle in humans is relatively stable after 2 years of age (Lieberman and McCarthy, 1999), these lateral shape changes, resembling shape changes in chimpanzees, still occur during adolescence (see also Bastir and Rosas, 2005, 2009). As mentioned in the introduction, facial growth, as well as increase in brain volume, influence endocranial shape change. In late ontogeny, cranial bones are sturdier and the brain grows at lower growth rates and finally stops increasing in size, but the lateral cranial base and the face continue to grow and mature later than the midline base and the cessation of brain growth (Buschang et al., 1983; Bastir et al., 2006). This leads to increased morphological co-variation and mutual influences between the endocranial base and the face. Therefore, late endocranial shape changes when adult brain size has already been attained may be more linked to facial growth than to brain growth. The influences between face and endocranium probably increase, and the influences between brain and endocranium probably decrease with increasing age and decreasing brain growth rates. The amount of endocranial shape change in later ontogeny is larger in chimpanzees than in humans, probably because chimpanzees grow a larger, more prognathic face that also influences the shape of the cranial base. Support for the morphological interactions between facial and basicranial growth is provided from analysis of prenatal human ontogeny (Jeffery and Spoor, 2002, 2004; Jeffery, 2005), analysis of postnatal human ontogeny (Bastir et al., 2004; Bastir and Rosas, 2005, 2006), analysis of the craniofacial morphology of different mouse strains as model organisms (Hallgrimsson and Lieberman, 2008; Lieberman et al., 2008), and analysis of fossil hominins in a comparative framework (Rosas et al., 2006; Bastir et al., 2008, 2010b). Evolutionary implications We interpret those aspects of endocranial ontogenetic shape changes that are shared between humans and chimpanzees as conserved; they were probably already established in the last common ancestor. Furthermore, we can speculate that similar differences found in the ontogenetic patterns here account for differences between humans and our fossil relatives. It is especially intriguing that neurocranial globularity and flexed cranial bases emerging in early human, but not chimpanzee, ontogeny are traits typical for anatomically modern Homo sapiens as compared to archaic Homo (Lieberman et al., 2002). A globular braincase is related to modifications of the parietal, frontal, and temporal areas and flattening of the occipital area (Lieberman et al., 2002; Bruner et al., 2003; Bruner, 2004; Bastir et al., 2008). Bastir et al. (2010a) suggested that the influence of facial size in

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addition to the influence of brain size could explain how Neanderthals and some other Pleistocene Homo specimens have less flexed cranial bases than modern humans, although their brain sizes are within the same range. In studying endocasts of adult specimens, relative parietal expansion contributing to neurocranial globularity was found to be unique in modern humans as compared to Neanderthals and other archaic Pleistocene Homo specimens (Bruner et al., 2003; Bruner, 2004). Our own species could have changed the pattern of early endocranial shape change to achieve a large brain in adulthood, while other large-brained Pleistocene Homo achieved similar adult brain sizes via an archaic shape change pattern. This hypothesis was put forward by Bruner et al. (2003) to explain the shape differences between adult modern and archaic humans and is further supported by our results. These authors not only found that modern humans are distinct from archaic humans (including Neanderthals) in their endocranial shape, but also that Neanderthals are different from other archaic (i.e., early to middle Pleistocene) Homo specimens along a presumably allometric trajectory. This finding is consistent with the idea that the large Neanderthal brains were developed by retaining an ancestral developmental pattern of brain growth, from which the modern human developmental trajectory departs. The comparison between humans and our closest living relatives helped to identify a period of ontogeny that seems to be relevant for the evolution of our uniquely complex brain and differences compared to the brains of archaic humans. It seems that not only prenatal but also early postnatal periods are relevant. Several juvenile Neanderthal specimens are preserved that could be included in analyses. Therefore, the hypothesis that Neanderthals had no “globularization phase” but achieved brain sizes comparable to anatomically modern humans via an archaic developmental pattern can be tested within this framework. Endocranial shape and cognitive abilities It is tempting to speculate about brain function and cognitive abilities and the underlying morphological changes of the brain during ontogeny and ultimately during evolution. Cognitive and behavioral abilities may be linked less to brain or endocranial size and endocranial shape, but more to the internal organization of the brain (i.e., cell proliferation, synaptogenesis, wiring, myelination; Sowell et al., 2003, 2004; Olesen et al., 2003; Gogtay et al., 2004; Giedd, 2004; Nagy et al., 2004; Casey et al., 2005). However, in the absence of fossilized brains, endocasts are the only evidence we have of the brain anatomy of fossil hominins. We want to emphasize that the “globularization phase” that distinguishes humans from chimpanzees occurs in early ontogeny, an essential period for maturational processes of internal brain organization (Herschkowitz, 2000; Gale et al., 2004). These different endocranial shape changes at least partly reflect developmental differences in the brain. We suggest that these differences could potentially be related to profound structural changes in the internal organization of the brain and thus to behavioral and cognitive development. Clinical studies of brain development suggest a link between the tempo and mode of brain growth, internal brain organization, and behavior and cognition. For example, in autistic children, deficits in higher-order social, emotional, and communication functions have been linked to fast brain growth rates in the first years of life (Courchesne et al., 2003). Courchesne and colleagues (Courchesne and Pierce, 2005; Courchesne et al., 2007) have suggested that autism is characterized by over development of local brain connectivity but underdevelopment of the connectivity between brain regions that are far apart. If it holds true that the “globularization phase” is unique to modern humans and therefore not present (or much shorter) in archaic humans, then analyses of

endocranial ontogenetic patterns will become pivotal for understanding hominin brain evolution. Conclusions We used CT data to generate virtual endocasts, landmarks, and sliding semilandmarks in a geometric morphometric analysis to quantify endocranial shape, and described and compared the ontogenetic patterns of endocranial morphology in humans and chimpanzees. We found non-linear, complex trajectories for both species, showing that humans and chimpanzees differ in the pattern of perinatal ontogenetic shape change but share aspects of endocranial morphogenesis thereafter for most of their postnatal ontogeny. The difference in the geometry of the trajectories contributes to the adult morphological differences between the two species and accentuates differences that are already present at birth. Similar shape changes could be “conserved” among hominins but the amount of shape change and timing issues contribute to differences between species. The perinatal “globularization phase” in humans does not exist in chimpanzees, and probably not even prenatally, and contributes to adult human features that are not only unique as compared to chimpanzees but also as compared to other large-brained Pleistocene Homo species. To substantiate the developmental evolutionary hypotheses presented in this paper, further analyses of more species, prenatal data, and fossil specimens are required. This approach yields new insights into endocranial morphogenesis and thereby opens up new possibilities for investigating hominin brain evolution. Acknowledgements We thank the following people for access to specimens and acquisition of CT data: C. Boesch, H. Coqueugniot, C. Feja, M. von Harling, B. Herzig, J.L. Kahn, F. Mayer, F. Renoult, U. Schwarz, K. Spanel-Borowski, H. Temming, F. Veillon, G.W. Weber, A. Winter, and A. Winzer. Thanks to C. Rowney who proofread our English and to K. Britton, F. Spoor, and A. Sylvester for discussion. The comments by S. Leigh, as well as the associate editor and two anonymous reviewers helped to substantially improve the manuscript. This work was supported by EU FP6 Marie Curie Actions grant MRTNCT-2005-019564 “EVAN” and by the Max Planck Society. References Ackermann, R.R., Krovitz, G.E., 2002. Common patterns of facial ontogeny in the hominid lineage. Anat. Rec. 269, 142e147. Bastir, M., Rosas, A., 2004. Comparative ontogeny in humans and chimpanzees: similarities, differences and paradoxes in postnatal growth and development of the skull. Ann. Anat. 186, 503e509. Bastir, M., Rosas, A., 2005. Hierarchical nature of morphological integration and modularity in the human posterior face. Am. J. Phys. Anthropol. 128, 26e34. Bastir, M., Rosas, A., 2006. Correlated variation between the lateral basicranium and the face: a geometric morphometric study in different human groups. Arch. Oral Biol. 51, 814e824. Bastir, M., Rosas, A., 2009. Mosaic evolution of the basicranium in Homo and its relation to modular development. Evol. Biol. 36, 57e70. Bastir, M., Rosas, A., Kuroe, K., 2004. Petrosal orientation and mandibular ramus breadth: evidence for an integrated petroso-mandibular developmental unit. Am. J. Phys. Anthropol. 123, 340e350. Bastir, M., Rosas, A., Lieberman, D.E., O’Higgins, P., 2008. Middle cranial fossa anatomy and the origin of modern humans. Anat. Rec. 291, 130e140. Bastir, M., Rosas, A., O’Higgins, P., 2006. Craniofacial levels and the morphological maturation of the human skull. J. Anat. 209, 637e654. Bastir, M., Rosas, A., Stringer, C., Manuel Cuétara, J., Kruszynski, R., Weber, G.W., Ross, C.F., Ravosa, M.J., 2010a. Effects of brain and facial size on basicranial form in human and primate evolution. J. Hum. Evol. 58, 424e431. Bastir, M., Rosas, A., Tabernero, A.G., Peña-Melián, A., Estalrrich, A., de la Rasilla, M., Fortea, J., 2010b. Comparative morphology and morphometric assessment of the Neandertal occipital remains from the El Sidrón site (Asturias, Spain: years 2000e2008). J. Hum. Evol. 58, 68e78.

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