Bolks fetalization hypothesis its successors and critics

Forever young? Many contributions have emphasized the relevance of phylo-genetic conclusions from ontogenetic information (Minugh-Purvis and McNamara 2002). One of the most influential books on developmental change and (human) evolution is Stephen Jay Gould's Ontogeny and Phylogeny (1977). Tuttle's (1978 p 287) review of this book was not rhapsodic: "Perhaps the author attempted too much in this chubby volume [...] Time will tell whether it is in fact a hemicentennial classic as implied on the dust jacket.'' Well, in the meantime it has become probably one of the most frequently cited compendiums. Howell (2002 p xi) commented that "its effect was immediate, substantive and far-reaching.'' Looking briefly at the bibliographies of modern studies often gives the impression that the consideration of developmental change in human evolution began in 1977 (Coqueuniot et al. 2004). Here I focus partly on some of the "ancient'' morphological studies that negate "essentially neotenous'' ideas, to show how profound their explanatory power really is.

Why assume an impact on paleoanthropology? The ideas of Louis Bolk, a Dutch anatomist, have in fact had an enormous influence on scientists working in many different fields. The paleontologists Beurlen and Schindewolf (1936, 1950) supported a phenomenon called "proterogenesis" by pointing out that some evolutionary lineages that are present in successive strata may be interpreted as a process of maturing of former embryonic or postembryonic form levels. I mention these thoughts—although they do not deal with anthropological questions—because they show that Bolk's thoughts are part of a greater, speculative construct of evolutionary ideas. Portmann (1960) already assessed the situation by claiming that criticism of Bolk's considerations has to be criticism of the entire construct and argued that it is still in progress and may not be considered completed.

As Starck (1962) argued, Hilzheimer (1926, 1927) and others have pointed to morphological and physiological data to explain the principle of fetalization. Starck (1962) traced the hypothesis of neoteny back to Strickland and Melville (1848), but Bolk was the one who applied it to human evolution. A sequence of papers (the version of 1926 being the most frequently cited) takes us away to a non-Darwinian construct. So which are the essential elements?

Bolk (1926 p 5) split human characters into (1) primary and (2) consecutive features. Primary characters are those products of developmental factors that caused the origin of human morphology. Consecutive characters, on the other hand, are phenomena of bipedal adaptation. Hence, the primum mobile of human evolution is not bipedalism, the "secondary" characters of which strictly follow functional aspects. Bolk (1926) considered the primary human characters to be: (1) reduction of body hair, (2) form of the external ear, (3) the epicanthic eyefold (=Mongolian eyefold), (4) loss of pigmentation in skin, (5) orthognathy, (6) foramen magnum in a central position, (7) a long persistence of cranial sutures, (8) subcerebral position of orbits, (9) high relative brain weight, (10) position of the spinal column relative to the cranial cavity, (11) women's labia majora, (12) structure of hand and foot, (13) form of the pelvis, (14) women's sexual canal in a ventral position, (15) multipapillary kidneys, and (16) the branching pattern of the arch of the aorta [the last two characters are not mentioned by Gould (1977)]. What is the common denominator of these characters?

The characters listed by Bolk are phenomena which temporarily appear during primate ontogeny. Although Bolk (1926 p 44) differentiated the problem by separating (1) the relatives of Homo sapiens and (2) the development of human shape, as Slijper (1936 p 504) explained, he advocated the idea that our ancestor must have been an extant primate species. Characters of human fetaliza-tion consequently represent persisting ontogenetic primate characters. Human ontogeny therefore demonstrates conservative traits, while humans' primate ancestors showed "propulsive" (=advanced) characters. Bolk's (1926 p 26) bottom line is: H. sapiens represents a sexually mature primate fetus. However, how did he explain the inhibitive force that fixes man's physical appearance at a certain point in time?

"The obvious answer is: The slow progress of his life's course'' (Bolk 1926 p 470) and the fact that "human life progresses like a retarded film'' (Gould 1977 p 360). Bolk (1926 p 38) asserted that the development of dentition, consciousness, and the late closure of cranial sutures act as indicators of a dominant retardation phenomenon. The chain of causes starts with the modification of the endocrine gland function (for a modern hypothesis see Crockford 2002) by internal alteration, not by external factors of the environment (Bolk 1926 p 22).

Slijper (1936), another Dutch scientist, published an outstanding analysis that considered cetacean relationships, the fetalization hypothesis, and the clarification of fundamental terms. Ironically, Gould (1977 p 365) called Slijper's criticism "famous," which is quite euphemistic since even the German-speaking Starck (1962) complained about it as not being easy accessible and often ignored. One major problem of Bolk's idea is the subjective splitting of primary and consecutive features. Slijper (1936 p 509) recapitulated Bolk's scientific career and stated: "... we get the impression that Bolk did not present primary characters (mostly human) at first and discovered their fetal character afterwards, but rather observed a contrarian procedure: he discovered fetal characters and defined them subsequently as primary. This explains the remarkable correlation of primary features with fetal phenomena and diminishes its objective value.'' (My translation.) Slijper also denied any general neotenous influence on human ontogeny.

Two prominent morphologists concerned with primordial cranial studies were Benno Kummer and Dietrich Starck. In 1962, they published the first modern study on fetal Pan troglodytes (O Figure 3.2). Starck and Kummer followed Hofer (1958, 1960) in distinguishing basal and prebasal kyphoses. Gould (1977 p 378) excellently summarized their findings thus: (1) all fetal mammals have a prebasal kyphosis at the junction of the presphenoid and ethmoid bones (a bending with the concave side toward the body, as opposed to a lordosis), (2) this kyphosis decreases during ontogeny, the sphenoethmoidal angle opens out, and the face comes to lie in front of the cranium, (3) while the prebasal kyphosis develops within the basicranial axis during human ontogeny, a different kyphosis develops between the basisphenoid and presphenoid bones at the level of the dorsum sellae. This second kyphosis produces a secondary decrease in the sphenoethmoidal angle following the earlier increase conditioned by straightening of the prebasal kyphosis, (4) the "fetal'' value of the

O Figure 3.2

Dorsal aspect of a fetal cranial model of Pan troglodytes. Crown-rump length: 71 mm. Not to scale (modified from Starck and Kummer 1962)

O Figure 3.2

Dorsal aspect of a fetal cranial model of Pan troglodytes. Crown-rump length: 71 mm. Not to scale (modified from Starck and Kummer 1962)

Fetal Cranial Development

sphenoethmoidal angle in human adults does not reflect the retention of a fetal condition but arises from development of the new, sellar kyphosis. It is a new feature—not a paedomorphic retention.

Amazingly, Gould (1977 p 379) concluded: "These authors have used this single contention as the basis for a campaign against the hypothesis of fetalization ...'' A single contention? A campaign? To be blunt, Gould himself started a campaign. In relation to Bolk's explanation of skull development, Portmann (1960 p 586) already commented that "... skull development is a complex issue which makes Bolk's solution suspicious.'' (My translation.) Reflecting the development and evolution of the human chin, Vogel (1964) warned against too "localized'' a view and called for the consideration of the complexity and interaction of all developing skull components. Schwartz and Tattersall (2000) revisited the presence of a chin in hominins and examined the importance of developmental epiphenomena.

Furthermore, Gould (1977 p 379) claimed that the "... tradition of excellence in descriptive morphology is combined with a general avoidance of quantification, and this may have hindered a full assessment.'' He might have overlooked an essential part of Starck and Kummer's (1962 p 213) paper because "these findings can be characterized as quantitative...'': (1) different relative sizes of neurocranium and auditory capsule, (2) tegmen tympani, (3) frontal nasal region, (4) canaliculus chordae tympanic posterior, (5) commissura orbitonasa-lis, and others. Gould (1977 p 384), however, did not fall into the Bolkian trap of an all-or-nothing law. Instead, he argued that "most of the classic 'exceptions' to human paedomorphosis are really consequences of retarded development,'' which Gould described as being the central phenomenon of our heterochronic evolution. Yet his ideas represent an analytic continuation of the Bolkian hypothesis.

Starck and Kummer (1962) did not exclude retardation (as in the commis-sura orbitonasalis) as an important factor of human development, but they emphasized that accelerations (e.g., the earlier closing of the intermaxillary suture in Homo) as well as deviations (e.g., the basicranium), should influence specific developmental processes. Starck's (1962 p 23) summary revealed that the principles of human evolution cannot be understood through Bolk's hypothesis: Important structures of the skull, very often taken as a result of fetalization, are indeed progressive compared with the pongid skull. It is emphasized that the bending of skull base in man and apes is absolutely different, caused by different morphological structures. Identity of causal factors is not established, if we find external similarities, such as the same size of angles, of relative measurements or indices. This may happen by addition of completely different components.

This statement seems not to be a furor teutonicus but rather a well-balanced point of view. Hence, morphometrics might work, but the comparison of morphological details must occur in a correct manner. How do contemporary anthropologists interpret morphological changes of this important cranial region?

Developmental aspects concerning the evolution of the human cranial base The cranial base represents the oldest component of the vertebrate skull (De Beer 1985). Thus this ''conservative'' structure is profoundly important in reflecting man's phylogenetic history and comparing primates to reveal essential aspects of human evolution. The keystone of the primate skull is definitely the basicranium. Several regions, such as the upper airway, the brain, and other parts, impinge upon one another here and consequently interact during ontogeny (Moss et al. 1982; Dean and Wood 1984; Lieberman et al. 2000). Biomechanically, the cranial base supplies a platform on which the brain develops and around which the face grows. The cranial base also forms a bridge connecting the cranium with the rest of the corpus: providing conduits for all circulatory and vital neural connections, articulating with the mandible and the vertebral column, forming the roof of the nasopharynx, and connecting the sense organs in the skull. Lieberman et al. (2000

p 120) stated that ''the shape of the cranial base is therefore a multifactorial product of numerous phylogenetic, developmental, and functional interactions.''

Scientists are confronted with the problem of complicated circumstances in studying this truly important region. It is not only complexity that matters but also problematic ways of measuring. Furthermore, the fragmentary nature of fossil remains causes major difficulties. Novel analytical techniques, however, have helped to engross our thoughts over the past years. Different hypotheses exist that deal with ontogenetic spatial processes and their phylogenetic implications. I mainly follow Jeffery (2003) in reviewing some of the most popular versions. The general spatial-packing hypothesis states that the modern human basicranium is caused by a short cranial base and an enlarged brain. Ross and Ravosa (1993) and Ross and Henneberg (1995) revealed significant positive correlations between increases of relative brain size and cranial base flexion across adult primate taxa: correlation of increasing relative brain size with (1) a coronal reorientation of the petrous bones across extant primates (Spoor 1997), (2) a cranial base flexion using different measurements and landmarks (Spoor 1997; McCarthy 2001), and (3) a cranial base flexion after controlling for the influence of phylogenetic correlations (Lieberman et al. 2000). Enlow and colleagues (Enlow and Hunter 1968; Enlow 1976, 1990) also attempted to demonstrate a determination of cranial base flexion through increases in relative brain size during primate development. Jeffery and Spoor (2002) could not verify these authors' arguments. They analyzed specimens from 10 to 29 weeks of gestation and documented that petrous orientation remains independent of significant increases in relative brain size. Furthermore, a retroflexion of the midline cranial base with relative endocranial size increases has been suggested. This observation contradicts the predicted flexion pattern.

The infratentorial spatial-packing hypothesis has been revitalized by Dean (1988), who argued that having coronally oriented petrous bones and a highly flexed basicranium poses the spatial problem of fitting an enlarged cerebellum on a short posterior cranial base. Jeffery and Spoor (2002) showed that ontogenetic data, collected during the second and early third trimesters of human prenatal development, do not support Dean's (1988) claim. They indicate that the petrous orientation and cranial base angulation do not correlate with increases in infra-tentorial volume relative to posterior cranial base length.

The influence on skull form of patterns of brain growth is addressed by two interesting models. Hofer (1969) and Lieberman et al. (2000) favored the brain shape hypothesis, while Ross and Henneberg (1995), Chklovskii et al. (2002), and Sporns et al. (2002) supported a neural-wiring hypothesis. These ideas have in common a suggested necessary change in brain topography to maximize cognitive efficiency by reducing neural wiring lengths. The resulting spatial changes produce a petrous reorientation and cranial base flexion. Distinct volumetric scaling trajectories can be detected across adult extant primates for different regions of the brain (Stephan et al. 1981, 1984; Frahm et al. 1982, 1998; Baron et al. 1987, 1990). Dean and Wood (1984) and Strait (1999) further demonstrated an association of those trends with interspecific variations in basicranial angulation. Lieberman et al. (2000) also confirmed a significant correlation of cranial base flexion with increases of cerebral volume over brain-stem volume.

Moss et al. (1956) suggested that brain topography is shaped by differential encephalization patterns which lead to developmental changes in posterior cranial fossa morphology.

A few studies (Guihard-Costa and Larroche 1990, 1992; Jeffery 2002) on the human fetal brain showed greater increases in expansion of the supratentorial portion (containing the cerebrum) compared to the infratentorial portion (consisting of cerebellum and brainstem). However, the independence of human cranial base angulation and petrous orientation of changes from the volumetric proportions of the brain between the ages of 10 and 29 weeks gestation are corroborated by Jeffery and Spoor (2002).

Jeffery (2003) tested the key hypotheses by imaging fetal samples of Alouatta caraya and Macaca nemestrina using high-resolution MRI. He noted marked increases in brain size, especially "disproportionate increases in the size of the cerebrum'' (p 281), disproportionate growth of the anterior midline basicranium compared with the posterior midline basicranium, coronal reorientation of the petrous bones, and cranial base retroflexion. Contrary to the spatial-packing hypotheses, increase in relative brain size is not accompanied by flexion of the midline basicranium. Retroflexion is documented for the cranial base in both taxa. There is also little evidence supporting the spatial-packing hypothesis for the fetal period of the howler monkey and macaque due to significant and "seemingly" consistent associations with petrous orientation arise based on background covariations with somatic growth. Jeffery (2003) therefore suggested that laryngeal size might be the reason for basicranial retroflexion. He finally compared it to human fetuses and concluded that the establishment of notable interspecific differences in the basicranium occurs much earlier than in the phase he studied.

Craniofacial growth patterns have been studied by several scientists (Giles 1956; Shea 1983, 1985a, b; Jungers and Hartmann 1988; Ravosa 1991, 1992; Zumpano and Richtsmeier 2003; Cobb and O'Higgins 2004; Mitteroecker et al. 2004). Lieberman et al. (2000) provided a comprehensive review of primate cranial base studies. As Zumpano and Richtsmeier (2003) pointed out, many previous studies documented postnatal growth processes, usually beginning with growth during the juvenile period. The infant growth period has been incorporated by Ravosa (1992), Richtsmeier et al. (1993), or Shea (1983), while Zumpano and Sirianni (1994) compared fetal to postnatal craniofacial growth patterns. Collections of fetal primates very often do not contain representative specimens (Zumpano and Richtsmeier 2003 p 340). Yet it is desirable to attempt an integration of these stages since only a completely documented ontogeny delivers deeper insight to reveal whether heterochronic processes are responsible for the modifications that have occurred between human and nonhuman primates.

Zumpano and Richtsmeier (2003) investigated, for the first time, growth-related shape changes in the fetal craniofacial region of humans and pigtailed macaques (M. nemestrina), using three-dimensional comparative analysis via cross-sectional samples of CT image data. As they emphasized, a long tradition of studies concentrated on examining the sites of growth of the cranial base, the sites of cranial base flexure, and the determination of the cranial base angle (Bjork 1955; Ford 1956; Dubrul and Laskin 1961; Houpt 1970; Lavelle 1974; Bosma 1976; Lestrel and Moore 1978; Moore 1978; Sirianni and Van Ness 1978; Sirianni and Newell-Morris 1980; Ross and Ravosa 1993; Ross and Henneberg 1995; Zumpano and Richtsmeier 2003). Zumpano and Richtsmeier (2003) showed that decreases in human cranial base length are achieved through the differential growth of posterior and anterior elements. The length of the posterior cranial base decreases, while increases occur in the length of the anterior cranial base. They further argue that a cranial base angle decrease may lead to a total reduction in cranial base length in human fetuses. At a comparable stage, the fetal macaque cranial base does not show a corresponding reduction (increased basicranial flexion). The associated distinctiveness of the differences in midfacial growth and the progression of prenatal cranial base flexion are said to be a factor separating these two species. Zumpano and Richtsmeier (2003) also contradicted Bjork (1955) and Ford (1956) in noting a basicranial flexion—not a constant angle—during the fetal period. They further support Lestrel and Moore (1978), and Sirianni and Newell-Morris (1980) are also supported in assuming a constant macaque cranial base angle during fetal growth, although they report a lesser angle (153°). The human anterior cranial base undergoes more relative growth than the macaque anterior cranial base. For the posterior cranial base, no significant growth differences between these two species are observed. Zumpano and Richtsmeier (2003) speculated that the increases in relative length of the anterior cranial base in humans may reflect the faster rate of growth of the frontal lobes of the cerebral cortex in humans relative to macaques (Enlow and Hunter 1968; Moss and Salentijn 1969; Moss 1973; Sirianni and Newell-Morris 1980) and conclude, based on their own observations and the studies of Anemone and Watts

(1992) and Swindler (1985), that midface differences between humans and macaques reflect a delayed rate of maturation of the human deciduous dentition or an accelerated rate of development. In a tabula rasa manner, Zumpano and Richtsmeier (2003) supported earlier investigations in suggesting the occurrence of shape changes within the fetal craniofacial complex during the last trimester of fetal growth (Grausz 1991; Plavcan and German 1995) rather than assuming an isometric growth process that is, e.g., characterized by size increase without corresponding shape change (Mestre 1959; Houpt 1970; Kvinnsland 1971a, b; Lavelle 1974; Moore and Phillips 1980; Sirianni and Newell-Morris 1980; quoted from Zumpano and Richtsmeier 2003). Zumpano and Richtsmeier (2003 p 349) finally concluded that "fetal macaques and humans do not share a common pattern of relative growth of the craniofacial complex, both species undergo increases in mediolateral dimensions (widening) of the skull and increases in palatal and anterior cranial base length.''

One of the ultimate goals in paleoanthropology is to reveal the precise relationship of humans to the great apes, our closest living relatives. Morphological data favor the monophyly of the African great apes, while molecular biology unites humans and chimpanzees (Mann and Weiss 1996; Ruvolo 1997; Enard et al. 2002; Kaessmann and Paabo 2002). Wildman et al. (2003) even placed chimpanzees within Homo based on molecular data. Paabo (1999) emphasized the importance of investigating a few genes that are responsible for specific effects during ontogeny (or in adulthood) instead of concentrating on chromosomal rearrangements or the accumulation of point mutations. Hence, Mitteroecker et al. (2004 p 680) stated that "as it is difficult to study gene expression on a molecular level for the whole organism, we confine ourselves to the study of the morphological effects of gene expression during ontogeny.'' They therefore created a shape space where each specimen (that is, its landmark configuration) is represented by a single point. In this context, an ontogenetic trajectory corresponds to the ontogenetic sequence which belongs to one species within this space. As Klingenberg (1998) or O'Higgins (2000a, b) showed, geometric contrasts among ontogenetic shape trajectories distinguish the development of different species. Geometric morphometrics is a promising and complex method of collecting and interpreting data based on morphological patterns (Bookstein 1991; Marcus 1996; Dryden and Mardia 1998; Slice 2005).

Some hominid craniofacial growth studies, applying geometric morpho-metrics, found more or less parallel trajectories from dental stage I (which corresponds to the first permanent molar) to adulthood (Ponce de Leon and Zollikofer 2001; Penin et al. 2002). The development of hominid cranial morphology consequently diverges from that of the other apes in an early postnatal or prenatal stage. However, O'Higgins (2000a; O'Higgins et al. 2001) confirmed

Richtsmeier et al.'s (1993) assumption of related species subsequently diverging after a similar period of early development. In a comprehensive study, Mitteroecker et al. (2004) measured landmarks and semi-landmarks in relevant specimens following a few days after birth to reveal essential insights into hominid ontogeny. Several principal patterns can be deduced from the set of ontogenetic trajectories. The authors tested three specific hypotheses: (1) "pure heterochrony'' of human cranial growth relative to Pan is a valid interpretation if the ontogenetic trajectories are identical in shape space, (2) the divergence of human ontogeny corresponds to a similar developmental stage at which the great apes diverge among themselves, and (3) an early divergence of trajectories from common ontogeny could elucidate the considerable morphological differences between humans and great apes because early modifications in development explain drastic transformations of the adult form (Richardson 1999). Studying 206 adult and 62 subadult crania of Homo sapiens, Pan paniscus, P. troglodytes, Gorilla gorilla, and Pongo pygmaeus, Mitteroecker et al. (2004) collected three-dimensional coordinates of 41 homologous ectocranial anatomical landmarks on the face and cranial base. They demonstrated the expected pattern whereby the youngest specimens are much more similar than the adults (von Baer's omnipresent discovery). Already at birth, human craniofacial morphology differs markedly from apes (p 692) "in accord with previous studies based on more traditional methods'' (Starck and Kummer 1962; Dean and Wood 1984). The first hypothesis, in contrast, can be rejected because there is no sharing of a common ontogenetic trajectory. Penin et al. (2002) tried to revitalize the "neo-tenic theory'' sensu Gould (1977 p 365). They do not, however, support a "general, temporal retardation of development'' but rather stress that "all the bipedal traits studied, whether in the skull (basicranium) or postcranium (pelvis and femur, see above), do not result from neotenic processes but rather from structural traits'' (p 61).

Additionally, the second hypothesis is falsified, and the third hypothesis is supported, by an earlier divergence of the human growth trajectory from the common hominid allometry (Mitteroecker et al. 2004 p 692). The African apes also do not seem to be pure allometric variants of one single type. Mitteroecker et al. thus concluded (p 694) that "pure heterochrony does not sufficiently explain human craniofacial morphology nor the differences among the great apes.'' McBratney-Owen and Lieberman (2003) also provide insight into the postnatal ontogeny of facial position in H. sapiens and P. troglodytes by emphasizing that the ontogenetic integration of complex phenotypes, such as the face, occurs on multiple levels of development, and they further speculate about the effectiveness of ontogenetic analyses for testing hypotheses about natural selection.

Ackermann (2005) investigated similarities in cranial covariation patterns by obtaining measurements from 677 crania of adult and nonadult African apes and sub-Saharan humans to locate underlying developmental and functional causes for the patterning. Defining the points of divergence of the covariation patterns can offer insights into the action of selection on development. Ackermann's work shows that patterns of integration are similar (not identical) among adult African apes and sub-Saharan humans. Ontogeny documents a sharing of patterns, with each species showing contributions to total integration from the oral region as well as from the zygomatic and to a lesser extent the nasal regions. However, she documented important differences between apes and humans, stating: ''In particular, the lower overall integration within and lack of covariance structure similarity among adjacent ontogenetic stages in early human ontogeny differs from what we see in the other apes. It is not entirely clear why this might be so, although it indicates that selection was working in this lineage -either on humans or the apes - to distinguish them not only in morphology, but in variation patterning'' (p 195).

Quo vadis? Developmental aspects concerning the evolution of bipedalism I

have already mentioned Bolk's (1926 p 6) interesting ideas concerning human bipedalism "... since form became human the posture became upright'' (my translation). Summarizing his growth studies on primates, Schultz (1924 p 163) asserted that ''man in some respects is less specialized and has hence remained phylogenetically as well as ontogenetically more original and 'primitive' than various other primates.''

Structural and mechanical aspects of the locomotion of primates play a considerable role in many discussions of human evolution (Preuschoft 1971; Schaffler et al. 1985; Demes and Jungers 1993; Connour et al. 2000; Ruff 2002; see also Senut, Volume III). Schultz (1953) analyzed over 350 limb bone circumferences and related the results to locomotion. The evolution of bipedal walking has, naturally enough, inspired scientists to associate locomotor mode with the relative lengths of the forelimb and hindlimb bones (Schultz 1937; Napier and Napier 1967; Jungers 1982). Changes within the hominin lineage in the relative size of the upper and lower limb bones are indications of our transition to bipedality (McHenry 1978; Johanson et al. 1982; Wolpoff 1983; Hartwig-Scherer and Martin 1991; McHenry and Berger 1998; Asfaw et al. 1999; Richmond et al. 2002; Ward 2002).

A few French scientists (Berge 1998) have tried to integrate heterochronic processes into analyses of morphological changes during hominid evolution. These works have concentrated on such classic anthropological topics as the anatomy of the pelvis. Berge (1998 p 443) emphasized separating the debate on neoteny by negating the idea "that identical heterochronic processes occur in skulls and postcranial skeletons, although we know that the growth of cranial and long bones differs in time, rhythm and velocity.'' She studied the morphology of two adult pelves and a juvenile hip bone of australopiths, 60 juvenile and adult pelves of modern humans, and 150 juvenile and adult pelves of African apes. The results confirmed a marked difference of the pelvic growth pattern in African apes and humans as reflected in multivariate results, ontogenetic allometries, and growth curves. Two conclusions emerged: (1) a comparison of modern humans to juvenile and adult australopithecines reveals that a unique feature of Homo seems to be a prolonged growth in length of hindlimb and pelvis after sexual maturity, while pelvic growth of Australopithecus was probably closer to that of apes than to that of humans and that some pelvis traits of adult Australopithecus resemble those of neonate Homo. Furthermore, (2) at the time of human birth, the appearance of the acetabulo-cristal buttress and the cristal tubercle allows the addition of features, such as the attainment of a proportionally narrower pelvis, with more sagittally positioned iliac blades. In early childhood (as bipedalism is practiced), pelvic orientation and proportions change progressively, while other changes in proportions occur later with the adolescent growth spurt. Neonate Homo and adult Australopithecus show similar patterns concerning the position of the acetabulo-cristal buttress. This could suggest a later displacement during human evolution. Berge (1998) further documented a progressive displacement of the acetabulo-cristal buttress on the ilium occurring during human growth (from neonate to adult) and hominid evolution (from Australopithecus to H. sapiens). She finally suggested that evolution of pelvic morphology in hominids is based on a threefold process—predisplacement, acceleration, and time hypermorphosis— and rejected pure fetalization (p 457) by stating that "the present study demonstrates clearly that the concept of neoteny is irrelevant for the pelvis. The study rather implies an accelerated evolutionary process than a retarded one.''

Ruff (2003) examined the human development of femoral to humeral proportions using a longitudinal sample of 20 individuals measured radiograph-ically at semiannual or annual intervals from 6 months of age to late adolescence and also included anthropometric data such as body weights or muscle breadths. A series of limb bone length proportion studies included ontogenetic data (Lumer 1939; Schultz 1973; Jungers and Fleagle 1980; Buschang 1982a; Shea 1983; Jungers and Susman 1984). Ruff (2003) focused on other limb bone dimensions. He compared his results with a cross-sectional ontogenetic sample of 30 baboons. The results document that femoral/humeral length proportions, which are already close to those of adults, are present in human infants, while characteristically femoral/humeral diaphyseal strength proportions only develop after the adoption of bipedalism (at about 1 year of age). Between the age of one and three, a rapid increase in femoral/humeral strength occurs, and this is followed by a slow increase until mid-late adolescence (when adult proportions are reached). The femoral/humeral length ratio proportions slightly increases throughout growth. There is no apparent growth trajectory change at the initiation of walking and a small decline in late adolescence based on a later humeral growth in length. Also in early childhood, a sex difference in femoral/humeral strength proportions (but not length proportions) develops. Ruff (2003) therefore concluded that they must be largely independent of growth trajectories in strength and length proportions. Baboons (used as a baseline) show contrasting patterns of growth: much smaller age changes in proportions and particularly strength proportions. He therefore stated (p 342): ''Comparisons with an ontogenetic baboon sample highlight the specific nature of the human developmental pattern.''

Returning to Adolph H. Schultz, we have an excellent example of a convert. In his youth, Schultz was stimulated by the neoteny hypothesis (see earlier). Following several studies (1953, 1973) although, he rejected Bolk's idea and the theory of man's neoteny.

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