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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.

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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.

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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

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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

.

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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).

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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).

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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).