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Evolution of the base of the brain in highly encephalised human species
Supplementary Information
Markus Bastir, Antonio Rosas, Philipp Gunz, Angel Peña-Melian, Giorgio Manzi, Katerina
Harvati, Robert Kruszynski, Chris Stringer, Jean-Jacques Hublin
Supplementary Figures S1-S2
Supplementary Table S1
Supplementary Discussion
Supplementary References
2
Supplementary Figures
Supplementary Figure S1: Landmarks and semilandmarks. On the endocranial surface
of the modern human mean configuration. True 3D landmarks in blue (count 1- 27),
semilandmarks in yellow (on the left); right part: labeled landmarks defined in
Supplementary Table S1. Numbers correspond to counts in Supplementary Table S1.
3
Supplementary Figure S2: Shape change in Midpleistocene-H.sapiens and Midpleistocene-
Neanderthal evolution. Comparisons between landmarks from the Midpleistocene Broken Hill cranium
with Neanderthal and modern human mean shapes, illustrating evolutionary patterns of encephalisation
between Middle Pleistocene and later large-brained human species. Left column: Broken Hill specimen;
middle column: modern human mean shape; right column: Neanderthal mean shape. a) shows Broken
Hill warped onto a modern human endocranium. b) Broken Hill into H. sapiens mean shape, c) Broken
Hill into Neanderthal mean shape. d, e, f show lateral views, g, h, i frontal views and j, k, l show inferior
views. Note that the thin plate spline transformations in b) and c) are very similar in pattern when
compared with corresponding grid transformations between early Homo-modern humans and early
Homo-Neanderthals. The magnitude of the transformations is less, however. H. sapiens shows relative
enlargement of the temporal lobes (e, k) and middle cranial fossae, and a backwards shift of the central
cranial base accompanied by an enlargement of the cribriform plate and olfactory bulbs (k). The anterior
cranial fossa at the base of the lateral prefrontal cortex is medio-laterally widened. In Neanderthals (c)
medio-lateral widening of the anterior cranial fossa is also observed, but different in shape than in
modern humans. Neanderthals (c, l) show the forward shift of the central base relative to the lateral one
that underlines absence of relative temporal lobe elongation and absence of height increase (f). A slight
widening at the anterior parts of the temporal lobes and middle cranial fossae does occur. Cribriform
expansion is less pronounced (l). This overall similarity supports the morphological interpretations
discussed in the main text based on evolutionary large-scale comparisons between early Homo and later
large-brained human species.
4
Supplementary Table S1. Endocranial landmark definitions. (Counts match with
Supplementary Figure S1.)
count landmark definitions
1 Fm. caecum
2 left anterior cribriform antero-lateral border of
cribriform plate
3 left posterior cribriform foramen of posterior sphenoid
vessels
4 posterior midcribriform in the midline
5 posterior sphenoid at the level of the orbital canals
6 pituitary
7 dorsum sellae
8 basion
9 opisthion
10 left spheno-parietal junction
[limit between anterior cranial
fossa [ACF] and middle cranial
fossa [MCF].
in the centre of the triangle of
the frontal, greater sphenoid
and parietal
11 left petro-parietal junction [limit
between MCF and posterior
cranial fossa [PCF].
pyramidal base
12 left internal acoustic porus antero-lateral vertex
13 left petrosal apex
14 left fm. ovale medial
15 left fm. rotundum medial
16 left ant MCF point
17 left orbital foramen antero-lateral vertex
18 right anterior cribriform antero-lateral border of
5
cribriform plate
19 right posterior cribriform foramen of posterior sphenoid
vessels
20 right spheno-parietal junction
[ACF-MCF limit]
centre of fusion between frontal,
greater sphenoid wing and
parietal
21 right petro-parietal junction
[MCF-PCF limit]
pyramidal base
22 right internal acoustic porus antero-lateral vertex
23 right petrosal apex
24 right fm. ovale medial
25 right fm. rotundum medial
26 right ant. MCF point
27 right orbital foramen antero-lateral vertex
28 left porion
29 left articular tubercle (TMJ)
30 right porion
31 right articular tubercle (TMJ)
32 hormion
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Supplementary Discussion
Integration between the anterior cranial base and the face
Originally Enlow and collaborators60
suggested in their counterpart analysis that, in
order to keep a functional and structural balance in the craniofacial system,
functionally relevant structures should be expected to correspond among their
adjacent craniofacial components (growth counterparts). For example, on clinical
orthodontic radiographs, Enlow found the length of the frontal lobes to correspond
with that of the anterior cranial fossae which in turn matched the length of the face
attached below and the mandibular corpus. Similarly, the length of the temporal lobes
would correspond to the length of the middle cranial fossae, which correspond to the
breadths of the mandibular ramus and the pharynx. On such a 2D-basis Lieberman61
suggested the hypothesis, applying Enlows60,62
schemes to human evolution, that
changes in midline anterior cranial base length should be related to changes in midline
facial projection (thus explaining the autapomorphic conditions of facial projection in
modern humans and Neanderthals. However, Spoor and collaborators13
rejected that
hypothesis on the basis of better measurements, by showing that sphenoid length in
the midline did not differ between humans of greater or lesser facial projection in the
way, Lieberman61
had suggested.
Then, further research by Lieberman and collaborators2 has shown that the relative
length of the anterior cranial base in modern humans is approximately 15-20% longer
than in archaic humans, despite their retracted face. This led to the hypothesis6 that
increase in anterior cranial base length would cause the face to rotate and to become
reduced thereby30,63
.
7
One major problem with these models is that the 2D nature of the data does not
account for off-midline structures32
. But integration between midline cranial base and
facial morphology is rather low compared with lateral basicranial structures64-65
.
However, so far no developmental model on these integration mechanisms has been
elaborated and tested, which requires comparative ontogenetic 3D analysis. And while
a developmental mechanism linking midline base flexion with facial rotation can be
imagined66
, a testable developmental mechanism linking facial rotation with facial
reduction in a way relevant to Neanderthal or modern human evolution is currently
not available.
Also, endocranial and external basicranial surfaces belong to different functional
matrices67-69
. The endocranial surface is separated by diplöe from the external cranial
base surface, thus permitting certain independent morphogenetic processes. The
discrepancies between evolutionary increase of endocranial length and decreased
external facial projection (i.e. length) in modern humans challenge the very basis of
the counterpart principles with respect to the face65,72
. Following the logic of the
counterpart principles would lead one to expect increased facial projection caused by
increased anterior cranial base length. But this is not the case.
Instead, evolution of facial projection and size seems much more related to
respiration73-75
, energetics76
and mastication77
than to anterior basicranial morphology
or cribriform plate and olfactory bulb size.
In addition, long standing research of Trinkaus78
suggests that autapomorphic
Neanderthal midfacial prognathism is a morphological phenomenon located off the
midsagittal plane, adding further complexity to this problem by exemplifying the need
8
for simultaneous 3D analysis of ontogenetic facial and basicranial data. Trinkaus’s78
suggestion fits well, however, with recent integration analyses that identified low
levels of integration between the midline base and facial morphology32,65,79
.
For these reasons it is difficult to think of a simple developmental model according to
which the size of the cribriform (not its sagittal orientation80
) would interact with the
morphology and projection of the face. And, certainly, testing such a model will
require a data set very different from the present one. Taking all the evidence
discussed above together, it seems safest to assume that the size of the cribriform
plate itself is mostly driven by the size of the adjacent and jointly developing olfactory
bulbs and the number of its cells9,11,41
. Certainly, more research is necessary to clarify
these problems.
Supplementary References
60 Enlow, D. H., Moyers, R. E., Hunter, W. S.and McNamara Jr., J. A. A procedure
for the analysis of intrinsic facial form and growth. Am. J. Orthod. 56, 6-23
(1969).
61 Lieberman, D. E. Sphenoid shortening and the evolution of modern human
cranial shape. Nature 393, 158-162 (1998).
62 Enlow, D. H. Facial Growth. 3rd edn, (W. B. Saunders Company, 1990).
63 McCarthy, R.and Lieberman, D. E. Posterior Maxillary (PM) Plane and Anterior
Cranial Architecture in Primates. The Anatomical Record 264, 247-260 (2001).
9
64 Bastir, M.and Rosas, A. Hierarchical nature of morphological integration and
modularity in the human posterior face. Am. J. Phys. Anthropol. 128, 26-34,
doi:DOI: 10.1002/ajpa.2019 (2005).
65 Bastir, M.and Rosas, A. Correlated variation between the lateral basicranium
and the face: A geometric morphometric study in different human groups.
Arch. Or. Biol. 51, 814-824 (2006).
66 Biegert, J. Der Formwandel des Primatenschädels und seine Beziehungen zur
ontogenetischen Entwicklung und den phylogenetischen Spezialisationen der
Kopforgane. Ggbrs. Morphol. Jahrb. 98, 77-199 (1957).
67 Moss, M. in Vistas in Orthodontics (Eds B Kraus and R Reidel) 85-98 (Lea and
Febiger, 1962).
68 Moss, M. The functional matrix hypothesis revisited. 1. The role of
mechanotransduction. Am. J. Orthod. Dent. Orthop. 112, 8-11 (1997).
69 Moss, M. The functional matrix hypothesis revisited. 2. The role of an osseous
connected cellular network. Am. J. Orthod. Dent. Orthop 112, 221-226 (1997).
70 Moss, M. The functional matrix hypothesis revisited. 3. The genomic thesis. Am.
J. Orthod. Dent. Orthop 112, 338-342 (1997).
71 Moss, M. The functional matrix hypothesis revisited. 4. The epigenetic
antithesis and the resolving synthesis. Am. J. Orthod. Dent. Orthop 112, 410-
417 (1997).
72 Bastir, M., Rosas, A.and O'Higgins, P. Craniofacial levels and the morphological
maturation of the human skull. J. Anat. 209, 637-654 (2006).
10
73 Bastir, M., Godoy, P.and Rosas, A. Common features of sexual dimorphism in
the cranial airways of different human populations. Am. J. Phys. Anthropol.,
146:414 (2011).
74 Bastir, M.and Rosas, A. Nasal form and function in Midpleistocene human
facial evolution. A first approach. Am. J. Phys. Anthropol. 144, 83 (2011).
75 Trinkaus, E. Neanderthal faces were not long; modern human faces are short.
Proc. Natl. Acad. Sci. USA 100, 8142-8145 (2003).
76 Yokley, T. Ecogeographic variation in human nasal passages. Am. J. Phys.
Anthropol. 138, 11-22 (2009).
77 O'Connor, C. F., Franciscus, R. G.and Holton, N. E. Bite force production
capability and efficiency in Neanderthals and modern humans. Am. J. Phys.
Anthropol. 127, 129-151 (2005).
78 Trinkaus, E. The Neanderthal face: Evolutionary and functional perspectives on
a recent hominid face. J. Hum. Evol. 16, 429-443 (1987).
79 Gkantidis, N.and Halazonetis, D. J. Morphological integration between the
cranial base and the face in children and adults. J. Anat. 218, 426-438,
doi:10.1111/j.1469-7580.2011.01346.x (2011).
80 Enlow, D. H.and Azuma, M. in Morphogenesis and Malformation of the Face
and the Brain Vol. 11 No. 7 The National Foundation - March of Dimes. Birth
Defects Original Article Series eds D. Bergsma, J. Langman, & N. W. Paul) pp.
217-230 (1975).