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Browridge structure and function in extant primates and Neanderthals.

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Browridge Structure and Function in Extant Primates
and Neanderthals
3Anthropological Research Laboratories and Department of Human Anatomy,
College of Medicine, Texas A&M University, College Station, Texas 77843
K E Y WORDS Primates
The structural characteristics of the supraorbital ridge in
three extent primate species and fossil Neanderthals are described in this
study. Surface morphology and patterns of trabecular organization as observed
in cross-sectional collections of Pupio, Mucucu and Pun are compared with similar traits encountered in the Pech de 1’Aze infant, Gibraltar child, and La
Quina 5, La Chapelle-aux-Saints, Broken Hill, Skhul V, Skhul IX, Tabun I and
Gibraltar adult Neanderthals. Periods of rapid appositional growth of the browridges by means of fine cancellous bone formation and its subsequent remodeling and consolidation are temporally correlated with dental development and
eruption sequences.
“Neanderthalman has been the object ofhypothesizing often going beyond what analysis of the materials
can justify. I wish to say here that we could benefit
from a quiet period of analysis.” W. W. Howells (‘74)
The purpose of this report is (1)t o identify
surface indicators of trabecular organization
and browridge formation in Neanderthals, (2)
to compare these data with similar information about macaques, chimpanzees, and olive
baboons, and (3) to demonstrate how these
comparisons can be used in addressing developmental, functional, and evolutionary
questions about browridge formation and craniofacial morphogenesis in primates.
Fossil hominid skulls considered are the
Pech de 1’Aze infant, the Gibraltar child, and
the La Quina 5, Broken Hill, Skhul V, Skhul
IX, Tabun I, Gibraltar and La Chapelle-auxSaints adults. Non-hominid specimens examined include skulls from 16 juvenile, adolescent, and adult rhesus macaque monkeys (M.
mulattul; and 20 chimpanzee (Pan) skulls
that ranged in age from infants t o adults. Approximately 80 olive baboons (P. c. anubis)
skulls, aged from infancy through adulthood,
extensively described and analyzed elsewhere
(Oyen, ’74; Oyen et al., ’78) are also considered. Serial placement of individual skulls
AM. J. PHYS. ANTHROP. (1979) 51: 83-96.
was determined on the basis of dental eruption sequence and attrition status (Krogman,
’30; Schultz, ’35; Bramblett, ’69).
The nature of the bone surface in the brow
region of each of the skulls was noted; samples
of bone were then removed from the supraorbital region of the non-hominid skulls and prepared and analyzed using standard light microscopy and scanning electron microscopy
Figures la,b-3a,b show variations of a surface pattern t h a t we observed in the supraorbital region of several monkey, ape and fossil
hominid skulls. This trait, described as “vermiculate bone” by Tappen (‘731, was found
along portions of the supraorbital margin in
the Gibraltar child, Skhul V, Skhul IX, Tabun
I, and Broken Hill skulls; Tappen (‘73, ’78) has
described the trait in the brow region of numerous Neanderthal specimens. We encountered variations of the pattern in the supraorbital region of many of the macaque and chimpanzee skulls considered during this analysis.
The vermiculate pattern is absent or virtually
’ Supported in part by a grant from the Office of Univeraity Research, Texas A&M University, and by NIH Training Grant
indiscernible of the Pech de 1'Aze infant and
the Gibraltar adult, and the trait was virtually unrecognizable on several of the adult macaque or chimpanzee skulls examined.
On Rhodesian Man, Skhul IX, La Chapelleaux-Saints and La Quina 5, and Tabun I the
worm-track pattern covers most of the supraorbital torus; the trait extends onto t h e floor
of the superciliary sulcus in Rhodesian Man
and Skhul IX. Discontinuous patches can be
observed on both sides of the frontozygomatic
suture in Rhodesian Man, whereas the pattern
spreads in a continuous fashion across the suture and down onto the frontal process of the
zygomatic bone in La Quina 5 (Tappen, '73).
Slight traces of the pattern can be observed
along the anterior aspect of the supraorbital
margin of the Gibraltar child and Skhul V
fossils, though i t is possible t h a t some of surface pattern on the Skhul specimen had been
removed during its original restoration and
Though the limitations of cross-sectional
materials and the nature of the phenomena
involved make i t difficult to establish precise
developmental categories, certain generalized
observations can be made about the appearance and spatio-temporal occurrence of the
vermiculate pattern. Table 1 provides an approximate schematic representation of the
trait as it was observed in the supraorbital region of the chimpanzee, macaque and fossil
hominid skulls. On skulls in which pairs of
molars and/or permanent incisors are actively
erupting through the alveolar margin the vermiculate pattern is distinct (figs. 1, 3). During
eruption the pattern commonly covers the supraorbital region; multiple layers of fine cancellous bone may extend posteriorly into the
superciliary sulcus and laterally and inferiorly onto the anterolateral aspect of the frontal
process of the zygomatic bone. This distinct,
penetrating pattern was either totally absent
or limited to small, discontinuous patches on
Browridge surface compared with approximate stages of dental development
Approximate dental
Deciduous second molar
dm2in occlusion
First permanent molar
(MI) erupting
MI in occlusion
First permanent incisor
(1') erupting
Second permanent molar
1'. M'in occlusion
Third permanent molars
M3in occlusion
Brow surface
Single layer of
fine cancellous
bone (fcb)
Smooth, little or
no vermiculate
pattern ivp)
Penetrating layers
of fcb; vp
fcb; vp superficial
Penetrating layers of
fcb; vp pronounced
Extensive layers of
fcb; vp pronounced
fcb; superficial vp
Penetrating layers of
fcb; vp pronounced
fcb, extensive
superficial vp
fcb, limited vp
fcb consolidated
Macaque Chimpanzees
Gibraltar child
Pech de I' Ace
La Quina 5
Rhodesian man,
Tabun I, La
Skhul V, IV
Gibraltar adult
the 26 non-hominid skulls in which all erupting teeth were in occlusion. The vermiculate
pattern on this latter group of skulls is somewhat reduced, obscured, and less penetrating
as a result of lamellar compaction (Enlow, '68,
'75); the modified trait tends to be limited to
the anterior aspect of the orbital margin and/
or confined to patchy traces along the lateral
orbital margin. On several adult skulls the
vermiculate pattern was indiscernible; on
three macaques and five chimpanzees, however, the vermiculate pattern, in a somewhat
modified version is present. While the vermiculate pattern on skulls in which erupted
teeth are in occlusion is altered by consolidated or semi-consolidated fine cancellous
bone, presence of this modified trait was not
limited to these skulls. The otherwise penetrating vermiculate pattern seen on skulls
with erupting teeth frequently shows evidence of lamellar compaction, especially in
the posterior aspect of the brow region (figs.
1, 3).
Histologic sections from the supraorbital region of immature macaque and chimpanzee
skulls (figs. 3c, 4a,b) show t h a t the characteristic vermiculate surface pattern and the
browridges result from repeated depositions of
woven and parallel-fibered nonlamellar fine
cancellous bone (Enlow, '66) on the outer
table. Portions of the outer table that are
closer to the neurocranium and/or the diploe
tend to be less porous, more dense, and more
distinctly layered. Bone of the outer table that
forms the floor of the superciliary sulcus
grades into the compact primary bone of the
vault. The coarse cancellous diploe is composed of lamellar and non-lamellar primary
vascular bone, and in adult skulls traces of inner circumferential bone (Enlow, '66) are evident. The inner table (orbital roof) consists of
primary vascular bone, with primary vascular
canals (primary osteons). Primary osteons are
also found in the outer table.
The osteological traits that have been described in macaques, chimpanzees and fossil
hominid skulls closely resemble characteristics we have encountered in our ongoing
analyses of craniofacial growth in another
species, Papio cynocephalus anubis (Oyen,
'74; Oyen et al., '78). In olive baboons, the portion of t h e outer table that forms the supraor-
bital torus is comprised of bone tissue that is
rapidly deposited in fine cancellous form, then
slowly consolidated into compact bone. Periods of rapid deposition tend to coincide with
active eruption of the molars, incisors, and canines. These growth stages, during which the
vermiculate pattern is readily discernible in
the brow region seem to alternate with periods
of bone consolidation and surface remodeling,
during which the browridge may show traces
of the vermiculate pattern or may be relatively smooth and compact. The periods of
compaction tend to occur between eruptive
phases, with onset as one pair of teeth reaches
the occlusal plane, and termination or dimunition coinciding with subsequent eruption of
molars, canines or incisors. As with the macaques and chimpanzees, the vermiculate pattern persists into adulthoods in the baboons;
the trait is present, though in a somewhat
modified form on approximately one-third of
t h e adult males (Oyen, '74, '77; Oyen et al.,
The pattern we have observed in adult
skulls, and immature ones for that matter, are
mute testimony that fine cancellous bone had
been deposited and had not undergone total lamellar compaction a t the time of death of each
specimen. In the words of Enlow ('68) presence
of this type of bone "provides an indication of
the past nature of growth in that particular
region at the specific time of formation."
Thus, persistence of the vermiculate trait into
adulthood could result from fine cancellous
bone having been deposited, perhaps in coordination with eruption of the third permanent
molars, continued mesial drift (as seen in
adult male baboons following eruption of the
molars and canines; Oyen et al., '78) or postocclusal expansion of the muscles of mastication, followed by an incomplete phase of consolidation. Alternatively, because the brow
surface on many of the skulls show signs of
antemortem remodelling, it is possible that
the vermiculate pattern seen on many adult
skulls re-emerged, so to speak, as a result of
differential resorption of previously consolidated or semiconsolidated fine cancellous
bone. A third possibility is that the adult vermiculate pattern resulted from growth processes not associated with changes in the masticatory complex.
Of these possibilities we suggest that the
last option is least likely to be correct (and
most difficult to verify), and we speculate that
the vermiculate pattern in adults is perhaps
best understood in terms of the first two possi- supraorbital ridges do occur, the outer table of
bilities. Until it has been more clearly demon- the frontal bone is subject to modification bestrated precisely what governs bone growth cause of mechanical interrelationships with
process, however we can only speculate why chewing activity (Moss and Young, '60). In
the vermiculate pattern appears when i t does. other words, while the phylogenetic occurIt is important to note, moreover, t h a t given rence of browridges may be affected by the
the present state of our knowledge, presence neurocranial and orbital functional complexes
of the vermiculate pattern in adults does not (Moss and Young, '601, the ontogenesis of the
refute our original thesis that browridge for- frontal bone, especially the outer table overlymation is related to growth-related changes in ing the supraorbital region in species with
browridges, is also heavily influenced by the
the masticatory system.
We have described a surface pattern that is muscles of mastication (Moss and Young, '60;
common to the supraorbital region of mon- Washburn, '47).
Boule ('17) and Tappen ('73) offer a conkeys, apes, and fossil hominids. We have
shown that this feature is present as brow- trasting interpretation of the evolutionary
ridges are formed through the accretion and and structural-functional significance of
remodeling of fine cancellous bone, and we browridges, exemplifying those who hold t h a t
have provided evidence that suggests that the browridges in Neanderthals are an adaptive
deposition-consolidation of fine cancellous response to a need for protection from heavy
bone, the process of browridge formation, fluc- blows landing above the eyes (Tappen, '73,
tuates in accordance with dental eruption '78). Specifically, Tappen ('73) maintains that
the presence of the vermiculate pattern, along
Based on this information, we infer t h a t with the absence of weathering cracks in the
browridges in Neanderthals and other large- supraorbital region (Tappen, '78) indicates
browed hominids were produced by growth that Neanderthal browridges are not associprocesses t h a t were developmentally and ated with normal mechanical forces such as
functionally very closely attuned to changes chewing exertion, and t h a t the vermiculate
in the masticatory system. Previous investi- bone, whose orientation does not lend itself to
gators have offered numerous interpretations the occurence of split-lines, would be well
of the origins, and structural, functional, and suited to absorbing impact and preventing
evolutionary significance of browridges. Stud- secondary cracking (Tappen, '73, '78). He also
ies by Toldt ('14),Weidenreich ('46), Wash- notes that the vermiculate pattern is not
burn ('471, Biegert ('63), Endo ('66, '67, '701, characteristic of ape browridges (Tappen, '78).
Our evidence shows that a vermiculate patEhara ('69, '721, and Ehara and Seiler ('701, in
particular have shown that in addition to tern (fine cancellous bone) appears to be
being affected by neurocranial and orbital size common to several different primates, and
and shape (Moss and Young, '601, skeletal por- that its deposition and subsequent assimilations of the supraorbital region develop from a tion in browridges of Neanderthals, chimstrengthening of the bony structures caused panzees, macaques, and baboons may be assoby the pulling actions of the temporalis mus- ciated with changes in the masticatory apparatus. Furthermore, recent work by Buckculature (Ehara and Seiler, '70).
A slightly different, but complementary land-Wright ('77) questioning the reliability
view of browridge formation has been offered of split-line techniques (Tappen, '53, '71, '76,
by Weidenreich ('411,Biegert ('571, Moss and for example) for analyzing the structural orYoung, ('60), Dutterloo and Enlow ('70), and ganization of bone and determining its transEnlow and McNamara ('731, who have vari- mission of force, places constraints on the very
ously documented the effects of neurocranial basis for Tappen's interpretations of the funcand orbital expansion on skull configuration tional significance of the vermiculate pattern
and development of the frontal bone. Most of and its role in browridge formation in Neanthese investigators share, to some degree, the derthals.
We have assessed browridge formation in
view that "the presence or absence of supraorbital ridges is a reflection of the spatial rela- Neanderthals, monkeys, and apes; based upon
tionship between two functionally unrelated surface features, spatiotemporal parameters,
cephalic components, t h e orbit and the brain trabecular organization, and microanatomy,
case, both of which are served by the frontal supraorbital region morphogenesis in these
bone" (Moss and Young, '60). They also ac- primates is apparently related to development
knowledge, however, that in species in which of the masticatory system. However, full un-
derstanding of the interrelationships between
browridge formation and growth of the masticatory system requires that we determine precisely the actual control mechanisms which
govern these developmental activities. If
browridges can be unified phylogenetically,
the task remains to ask ontogenetic questions
which can experimentally elucidate underlying processes; to paraphrase Enlow (‘731, we
sometimes confuse what happens with how it
happens and are thereby deluded into believing that we understand and can account for
t h e entire growth process. This confusion has
contributed to the situation which precipitated Howell’s (‘74) request for a “period of
quiet analysis,” in which we may develop,
through re-evaluation and synthesis of new
information and prevailing hypotheses, a
more precise and unified rationale for browridge development. In closing we suggest that
a n approach which incorporates a concern for
exact identification of osteological tissues and
growth processes (Enlow, ’66, ’68, ’75) with
dynamic, functional perspectives of craniofacial biomechanics and development
(Carlson and van Gerven, ’77; Hylander,
’75a,b; Walker, ’78, for example) will eventually enable us to understand craniofacial
morphogenesis i n ontogenetic, and then phylogenetic terms.
We wish to express our thanks t o Doctor J.
Mungai, Department of Human Anatomy,
University Nairobi; Doctor Peter Andrew,
British Museum (N.H.), London; J. L. Heim,
Musee de l’Homme, Paris; and Mr. C. PowellCotton, Quex P a r k , Birchington who so
generously made available the skeletal collections under their care for this study. Also, we
would like to thank Doctor Milford Wolpoff,
who provided both skeletal materials and
advice; and Mrs. Lucille Schultz and Mr. John
Purcell, without whose technical assistance
this project would have been far more difficult.
We are particularly indebted to Doctors A.
C. Walker, H. B. Sarles, and D. H. Enlow for
the kindness, encouragement, and stimulation they have provided, and to H. L. Oyen,
without whose steadfast support this project
would never have been undertaken.
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l a Vermiculate (‘‘worm-track’) surface pattern created by deposition of fine cancellous bone (f.c.b.1 on the right supraorbital ridge of a macaque (specimen 1483) in
which the second permanent molars were moving into the occlusal plane. Posteriorly, patches of unconsolidated f.c.b. are visible in the midst of compact cortical
bone. X 4.
b Vermiculate pattern encountered on the supraorbital region of a chimpanzee of
comparable age (specimen UM146). X 4.
0. J. Oyen, R. W. Rice and M. S. Cannon
2a Diminished yet identifiable vermiculate surface pattern on the supraorbital ridge
of Tabun I, a fully adult heavy-browed hominid. x 2.
b Vermiculate pattern along the right supraorbital ridge of the Broken Hill (Rhode-
sian Man) specimen. Irregularities in the surface pattern appear to have been
caused by cortical remodeling prior to death. x 2.
0. J . Oyen, R. W. Kice and M. S. Cannun
A, fine cancellous bone (vermiculate pattern) on the
outer table
B, coarse cancellous bone of the diploe
C, primary vascular bone of the orbital roof
D, region of endosteal remodelling
E, transitional zone between fine cancellous bone and
layered compact bone of outer table
F, laminated compact bone a t posterior aspect of ridge
3a,b Scanning electron micrographs of sections from t h e right supraorbital ridge of
(a) macaque (specimen 1483) and Ib) chimpanzee (specimen UM146). X20.
Polarized light micrograph of a section directly adjacent to the cut surface seen
in figure 3a. X 45.
0. J. Qyeo, R. W. Rice and M. S. Cannon
4a,b Polarized light micrographs of the (A) anterior aspect and (B) posterior aspect of
the right supraorbital ridge from a section in close proximity to t h e cut surface of
the specimen in figure 3b (chimpanzee UM146). The fine cancellous bone of the
outer table (A) is non-lamellar, while t h e diploe (B) consist of lamellar bone. Evidence of endosteal remodeling in region D appears as compacted circumferential
bone, and periosteal remodeling is seen around E and F, where fine cancellous
(non-lamellar) bone has been consolidated into distinct layers parallel with the
free surface. X 60.
W. Rice and M. S. Cannon
0. J. Oyen, R.
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structure, neanderthal, primate, function, extant, browridge
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