a multivariate study of evolutionary change in the hominid cranial vault and some evolution rates

Alan Bilsborough

De#artment of Physical Anthro@ology, Uniunsiry of Cambridge, Downing Strsct, Cambridge, England

Received 2 April 1972

A Multivariate Study of Evolutionary Change in the Hominid Cranial Vault and Some Evolution Rates

Multivariate analysis is used to describe the total morphological pattern of the hominid cranial vault, and to obtain distancea between samples of Plio-Pleistocene Hominidae. Such techniques provide a means of quantifying phyletic change within a lineage, and therefore ruefully complement the traditional Linncan nomenclature. When divided by elapsed time, the multivariate distancol between groups provide a measure of the rate of evolution of a character complex, and such data are given for the hominid cranial vault over the Quaternary as a whole, and for more detailed changes within Upper Pleistocene H. sapimr. The evolutionary significance of the observed rates, and their impli- cations for the construction of phyletic schemes, arc discussed.

1. lntrodmtion

The great increase in hominid cranial dimensions during the Pleistocene provides one of the most spectacular evolutionary trends of any mammalian phylum, and hominid taxa are differentiated largely upon neurocranial proportions. Changes in the site

of the cranial vault mainly reflect the progressive increase in cranial capacity (and therefore brain size) characteristic of Quaternary Hominidae, whilst changes in the external shape of the neurocranium are partly a result of differences in endocranial proportions and partly due to the effects of splanchnocranial changes-especially those of the masticatory apparatus-upon the braincase. Although it is not possible to infer mental abilities from endocranial size and morphology, it is informative to compare changes in neurocranial proportions with the evidence of intellectual status and social organization revealed by the archaeological record.

Most studies of neurocranial change have been based upon the univariate analysis of either cranial dimensions or changes in cranial capacity. However, there is general recognition that it is desirable to compare the total morphological pattern of a structure (Clark, 1962) rather than a series of isolated dimensions, since the latter approach results in much loss of information (Bronowski & Long, 1952) and may lead to erroneous conclusions (Weiner & Campbell, 1964). The availability of computers makes it prac- ticable to quantify total morphological pattern by means of multivariate statistical analysis, thereby deriving a measure of the morphological distance between groups on the basis of their overall similarity.

Of the various statistics available, Mahalanobis’ Da possesses optimal properties, and its positive square root (D) may be used as a measure of the divergence between the original variables. Da rejects redundant information which would otherwise distort the separation achieved, and expresses the distances between groups in units of common within-group variability. Since natural selection operates directly upon the phenotypic variability present within populations, this is a meaningful unit to adopt in evolutionary studies, and Lerman (1965) has suggested the use of D, when divided by time, as a measure of the rate of evolution between successive samples within a lineage. D may therefore be used to indicate both phenetic affinity and evolutionary velocity between

Journal of Human Evolution (1973) 2, 38743.

388 A. BILSBOROUGH

groups for a particular structure, and the patterns of change so derived provide a comple- mentary and in many respects more meaningful view of hominid evolution than that reflected by the conventional Linnean nomenclature.

The present paper reports a study using the multivariate techniques outlined above to describe morphological changes within the cranial vault of Plio-Pleistocene Hominidae.

2. Measurements

The cranial vault as defined here includes the squamous frontal, parietals, squamous temporals and occipital bones. The basicranial region has been largely excluded from the analysis because of its relationship to the vertebral column, and the fact that its morphology is principally determined by the requirements for the articulation and balancing of the skull in orthograde hominids. The basicranium is therefore relatively

invariant in Hominidae, most of the expansion in cranial capacity being reflected by changes in the vault itself. Of the various components of the cranial base, only the basioccipital has been included within the present study, owing to the absence of a satisfactory reference point from which to measure that part of the occipital contributing to the vault proper. The most obvious landmarks-basion and opisthion-themselves migrate according to the degree of truncal erectness of the specimens considered, and the spheno-occipital synchondrosis was therefore chosen as the anterior and inferior limit of the occipital.

In discussing changes in the cranial vault of hominids it is important to consider dimensions which are strictly comparable from one taxon to another (Clark, 1964). For this reason measurements other than the usual anthropometric ones were employed in an effort to provide greater definition of cranial changes. For example, dimensions of the frontal bone in the MSP have been measured not from the usual landmark (nasion) but from the point of inflection behind the supraorbital torus, since this latter structure adds appreciably to the size of the frontal in early hominids. Similarly, the cranial vaults of some Hominidae are provided with crests and tori, correlated with the masticatory and nuchal musculature, whereas the vault of Homo sajiens is not. To include these

‘ectocranial embellishments’ (Tobias) would appreciably distort the analysis and so far as possible they have been omitted.

The following characters were eventually chosen to describe the cranial vault (see also Figure 1) : (1) Horizontal length of the frontal eminence in the MSP. (2) Vertical height of the frontal eminence in the MSP. (3) Development of the frontal eminence in

Figure 1. Neanderthal neurocranium (La Chapelle-aux-Saints) to show characters used to describe cranial vault proportions in this study.

HOMINID CRANIAL VAULT EVOLUTION 389

the MSP (tape). (4) M’ ’ rmmum breadth of the braincase at the level of glabella. (5) Horizontal length of the parietal eminence in the MSP. (6) Vertical height of the parietal eminence in the MSP. (7) Development of the parietal eminence in the MSP (tape). (8) Vertical height of the parietal bone in the coronal plane. (9) Lateral expansion of the parietal bone in the coronal plane. (10) Development of the parietal bone in the coronal plane (tape). (11) Vertical height of the tempora1 bone. (12) Lateral expansion of the temporal bone. (13) Development of the temporal bone (tape). (14) Horizontal length of the occipital eminence in the MSP between the occipito-sphenoid suture and a vertical projection of lambda. (15) Vertical height of the occipital eminence in the MSP. (16) Development of the occipital eminence in the MSP (tape).

3. Phylogeny and Dpting

There is general agreement that hominid evolution throughout the Pleistocene was predominantly anagenetic (e.g. Weiner, 1958; Dobzhansky, 1963), and this view is adopted here. Of the several hominid taxa usually recognized, only the Austsalopithcus boisei/robustus lineage is considered to be cladistically distinct from other Hoxninidae, the remainder (A. africanus, Homo species) forming a single evolutionary lineage. The categories used to order specimens within this continuum are therefore arbitrary chrono- taxa and it is more meaningful to group specimens according to morphological, chronological and geographical criteria. On this basis the following groupings were recognized: A. boiwi (Olduvai hominid 5) dated at 1,750,OOO years ago; A. afsicanus, including material from Sterkfontein (Sts V) and Makapansgat (MLDl, MLD 37/38), dating from the late Pliocene or basal Pleistocene. A date of 2 million years has been suggested for the Plio-Pleistocene boundary (Oakley, 1969) and that figure is adopted here for the A. afticanus sample. This is a minimum date, and likeIy to be revised upwards as further data @pear.

The available H. erectus specimens span a relatively long period ( 2 700,000 years) throughout the Middle Pleistocene, and the taxon has therefore been divided into two groups-an early Middle Pleistocene sample and a late Middle Pleistocene one. The early group includes material from Java-the Trinil calotte and Sangiran specimens (calvarium II from the Trinil beds; IV from the Djetis beds)-and Olduvai hominid 9 (Chellean Man from Upper Bed II). A mean date of 700,000 years is assumed for the early H. emctus sample. The later sample comprises material from Pekin (skulls II, III, X-XII) considered to be equivalent to late Elster or early Holstein in European Quatern- ary chronology (Huang, 1960; Kahlke & Chow, 1961) and therefore dated at 300,000 years.

Although much fossil material of H. saP;mr is available from the Upper Pleistocene, morphological contrasts between the specimens are relatively slight, whilst the time intervals between geographically diverse samples are short (usually I: 50,000 years). Individual and polytypic variability are relatively more important in accounting for sample differences, whilst evolution rates calculated over short time spans may not be sustained for long periods. Data derived from Upper Pleistocene specimens are therefore not strictly comparable with those obtained between earlier Hominidae separated by much longer periods. However, late H. erectus and modern H. s. sapiens are sufficiently far apart to be comparable with the earlier segments of the lineage, whilst the various Upper Pleistocene samples provide information on short-term morphological changes within a single hominid chronospecies.

8

390 A. BILSBOROUGH

The following groupings within the chronotaxon H. sapiens were recognized: Holstein H. [email protected] (Steinheim, Swanscombe) dated at 250,000 years; H. s. soloensis (skulls I, IV, V, VI) dated at 50,000 years; European Neanderthals (Neandertal, Spy I and II, Gibraltar, La Chapelle, Le Moustier (Weinert reconstruction), La Ferrassie I, La Quina, Mt Circeo) dated at 50,000 years; Middle East Neanderthals (Tabun I, Skhul IV, V) dated at 40,000; H. s. rhodesiensis (Broken Hill) dated at 40,000 years; Upper Palaeolithic H. s. sapiens (Cromagnon I, II, Combe Capelle, Grotte des Enfants II; Engis, Brno I and II, Predmost III and IV) dated at 25,000 years. Detailed evidence in support of this dating scheme is in Bilsborough (1971).

Modern H. s. sapiens is represented by a sample (n = 17) of geographically diverse crania so as to encompass as much as possible of the polytypic variation characteristic of hominids whilst still retaining an appropriate sample size. The accuracy of a distance statistic depends upon the accuracy of both sample estimates, and since the fossil samples are small and discrimination as such is not the prime object of the analysis, a large modern series is unnecessary and undesirable for it would bias dispersion in multivariate space. Measurements of fossil hominids were taken upon casts. Comparison of arc and chord values with those published for the original specimens show that casting errors are slight (< 3 %) and unlikely to be significantly affecting the results when compared with limitations of dating and restricted sampling of early hominid populations.

Inspection of the original data was followed by multivariate analysis using the MAP and Orion 60 programmes based upon Gower’s Q-technique (Gower 1966a, 6). These compute not only the O2 values between all pairs of groups, but also canonical variates which enable one to depict the separation of the groups in a restricted number of dimensions and also indicate which of the original characters are contributing most to the observed separation (Seal, 1964; Bartlett 1965).

4. Results

The multivariate analysis derived ten variates (one less than the number of groups), of which the first accounted for 46.7 % of the original variance, the second 29.3 ‘A and the third 12.3 ‘A. The first three variates therefore encompass > 88 ‘A of the total variability, and the remainder may be neglected with little loss of information. Plots of the groups on variates I and II and I and III are shown in Figures 2 and 3, whilst Table 1 lists the scaled loadings of the original characters on these variates,

Canonical axes I and II provide relatively good separation between the groups, with the australopithecine taxa well isolated from the human material. The Middle Pleistocene specimens, and European Neanderthal sample are situated near the limit of the right-hand quadrants, the remaining Upper Pleistocene groups occupy the lower left quadrant with the Rhodesian skull isolated from the other specimens. The modern sample occupies an intermediate position, equidistant from the Mt Carmel and Pekin specimens, but closest to the Upper Palaeolithic material.

Maximum separation along variate I (28 units) is between the Solo group at the negative limit and the early H. erectus sample at the positive end. A. africanw is close to the Solo material, as is the Rhodesian skull, but the remaining samples are well separated. The Mt Carmel, Upper Palaeolithic and modern groups are all close together, as are the Holstein H. sapiens and late H. erectus samples. However, also overlapping with these two groups is the ‘Zinjanthropus’ cranium indicating that separation along the variate

HOMINILl CRANIAL VAULT EVOLUTION 391

Figure 2. Plot of hominid groups on canonical variates I and II. I, Modern H. s. sa+ns; 2, Upper Palaeolithic H. s. sapiens; 3, Middle East Neanderthals; 4, H. s. rlrodcrimris; 5, European Neanderthals; 6, H. s. solomis; 7, Holstein H. sapiens; 8, Pekin H. crectus; 9, Early H. srcctus; 10, A. afticaws; 11, A. boisei. Circles encompass 90% of intra-group variability.

-II

is not based upon neurocranial size, but upon some complex function of shape. The ordering of the specimens reveals no obvious chronological or phyletic sequence.

Separation along variate II is much more striking, with the two Australopithms taxa occupying what are essentially identical positions at the positive limit of the axis, and the human samples clustered about the negative portion. The early H. erectus sample is

Figure 3. Plot of hominid groups on canonical variates I and III Symbols as for Figure 2.

392 HOMINID CRANIAL VAULT EVOLUTION

Table 1 Scaled loadlags of hominid cranial vault dimensions on canonlad variates I-III

Character Axis I Axis II Scaled Scaled

Axis III Scaled

2 3 4 5 6 7 8 9

10 11 12 13 14 15 16

-22.436 - 12.245 -11.052 -56.154 -5.797 -7.471

38.242 -54.471 26.619 39.248 -4.752 -11.429

-32.585 16.301 53.098 15.774 24.264 18.550 15.482 - 15.472 - 12.574 9.368 - 42.647 25.187

39.252 - 18.358 21.325 -35.819 42.813 -33.391

24.920 -6.930 - 14.368 16.435 10.618 - 5.343 41.886 45.863 20.713 35.463 -77.212 11.345 40.184 88.893 42.574

9.887 13.125 11.275

closest to the australopithecines, although the remaining human groups do not follow a temporal sequence, revealing instead an overlapping spread with only the Rhodesian skull distinct at the limit of the variate.

The plot of axes I and III presents a different array, with the modern, Upper Palaeo- lithic and Mt Carmel samples forming a compact group at the positive limit of the axis whilst A. africanus, the Solo and Rhodesian specimens are spread over the left-hand quandrants. Early H. sapiens, the classic Neanderthals, A. robustus and late H. erect=

form a similar spread over the right hand ones, with the early H. erectus sample isolated in the bottom right quadrant. Once again, the ordering along axis III does not conform to a phyletic or chronological sequence. The early H. erectus and modern H. sapiens

samples are at opposite ends of the variate, with the intermediate groups forming a continuous spread. The Solo and Rhodesian specimens overlap with the early H. erectus

group, as does the later (Pekin) sample to some extent. The two australopithecine taxa are close together in the centre of the cluster, but the most noteworthy feature on this variate is the close proximity of the Middle East Neanderthal, Upper Palaeolithic and modern groups at one end of the axis.

The lack of any clear-cut evolutionary or temporal ordering of the groups indicates that the separation is effected not on the basis of cranial size but by some complex function of neuro-cranial shape, and inspection of the scaled loadings of the original characters in the variates confirms this view. None of the variates is discriminating on size alone since all contain both positive and negative loadings.

High scaled loadings on axis I are those for characters 2-4, 9, 10 and 13-l 5, indicating that discrimination is primarily based upon the proportions of the frontal, parietal and occipital areas. In particular, the shape and relative height of the frontal bone in the MSP and the parietals in the coronal plane (characters 2-3 and 9-10) are influencing the spread. Those groups with a high, domed frontal (i.e. 2 forms a high proportion of 3) will generally occupy the negative part of the variate, those with a lower, flatter, frontal region are spread along the positive portion. In a similar manner specimens with a relatively low, wide parietal region (i.e. 9 forms a high proportion of 10) are situated


along the positive side of the variate, those in which the biparietal arch is high and narrow are situated along the negative portion.

The relative importance of these regions explains the wide separation of the two Austzalopithecus taxa along the variate, since A. africanus has a relatively high, domed forehead and narrow biparietal arch, A. rob&us a low, flattened frontal and broad, laterally expanded parietal region. The two H. erectw samples are similarly separated, with the earlier material possessing a receding frontal and low parietal region, at the positive limit. The final Pleistocene groups, with the exception of the European Neander- thals, have high, relatively short frontals and vertically expanded parietals and therefore occupy the negative portion of the variate, an ordering reinforced by the loadings for variables 14 and 15 describing occipital dimensions. Those samples with a relatively long occipital region are shifted towards the positive side of the axis, those in which the occipital is shorter and higher are near the negative limit. These characters again discriminate between the two australopithecine species, and also separate the Middle and Upper Pleistocene human groups.

Separation along variate II is based principally upon the proportions of the occipital (characters 14 and 15) and frontal (character 3) regions. In general, the ordering of the groups reflects the overall size of the occipital area, with those taxa possessing a small occiput (both Australopithecus species) at the positive end of the axis, those with a large occipital (Upper Pleistocene Homo) at or near the negative limit. Characters 14 and 15 are of opposite sign, indicating that shape contrasts are also contributing to the separation, and those groups which possess a high value for (14) compared with (15) i.e. a relatively long occipital region, are shifted towards the negative end of the variate. This results in the Rhodesian specimen being well separated from the remaining groups at the negative limit of the axis. Similarly, those groups with high values for (3)) measuring the development of the, frontal region, are also displaced towards the negative part of the variate, whilst the australopithecines with small frontal areas, are well isolated at the positive end.

High loadings on variate III are shown by characters 3, 5, 8-10 and 15. Most of these describe parietal dimensions, and it is obvious that this region is dominating the discrimination afforded by the axis. The ordering of the groups and the presence of both positive and negative loadings indicate that separation is based upon parietal shape, particularly in the coronal plane, rather than gross size. Those groups with a relatively low, wide bi-parietal arch (e.g. Rhodesian and early H. erectus specimens) occupy the negative part of the variate, those in which the parietals are higher and relatively narrower (e.g. Upper Pleistocene groups) are spread along the positive portion, whilst those groups in which the vertical and horizontal diameters are approximately equal are situated about the centre of the variate. Other characters with high loadings include the vertical height of the occipital (15) and the development of the frontal eminence (3). Groups with high values for these characters are shifted towards the positive end of the variate; those with low values towards the negative limit, thereby accounting for the position of A. boisei on this axis, although in general the separation afforded by these dimensions reinforces that based upon parietal proportions.

Inspection of the character loadings thus reveals that the three major axes are discriminating mainly upon the basis of frontal and occipital development in the MAP., and parietal proportions in both the sagittal and coronal planes. The total separation of the groups, based upon their ordering on all ten canonical variates, is shown by the

Tab

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Mat

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of

D d

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M

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H

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(Rh

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rica

nus

bose

i

Mod

ern

H

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sa

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pper

P

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H.

s. s

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Mid

dle

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Lat

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H.

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9.68

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11

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703)

18

40

($8?

)

(412

97)

12.7

9 (4

.265

) 22

.18

(3.1

69)

23.7

8 (1

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) 23

.31

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16.4

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09.5

33)

8.92

(3

5.17

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15.3

8 (6

1.51

6)

13.1

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) 13

.80

(5.5

43)

23.0

0

19.7

9

21.9

1

17.2

5 (1

72.5

46)

8.85

(8

8.49

0)

15.6

8 (1

56.8

30)

13.7

4 (6

.541

) 14

.37

(5.5

28)

21.9

6

18.0

6

20.2

9 30

44

21.5

1 27

.64

- 12.1

9 (1

21.9

32)

10.6

0 (1

06.0

40)

20.6

2 (9

.819

) 17

.69

(6.8

04)

26.9

5 (4

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) 25

.21

-

13.6

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8.74

22

.02

(4.3

69)

(11.

014)

13

.15

20.0

1 (5

.259

) (8

.004

) 12

.61

29.5

5 (1

.940

) (4

.546

) 30

.31

18.9

2

-

10.1

9 -

(20.

376)

16

.13

12.9

0 (3

.585

) (3

.226

) 26

.48

24.4

8 30

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(2.3

09)

20.4

3 17

.87

18.9

5 21

.66

-


matrix of D distances (Table 2), and in addition evolution rates-expressed in D units per hundred thousand years (u.p.h.)-are given for the successive segments of the hominid lineage. Alternative rates have been calculated between the various Upper Pleistocene samples in order to compare detailed patterns of morphological velocity between groups whose precise phyletic relationships are controversial. The data so derived provide a more meaningful basis for the assessment of evolutionary relationships than a simple measure of phenetic affinity which does not take into account the temporal ordering of the specimens.

Maximum separation in multivariate space (30.4 D units) is between A. b&i and the Rhodesian skull, whilst the minimum distance (5.4 units) is that between the Middle East Neanderthals and Upper Palaeolithic H. s. sa#iens. Apart from the segment A. africanus-early H. emtus successive groups within the lineage are generally closer to one another than to other groups, indicating a trend for neurocranial expansion within the genus Homo, without any marked reversab in cranial evolution.

The A. africanus and A. boisei specimens are > 21 D units apart, corresponding to their separation along variate I. This reflects the considerable differences in cranial proportions between the two taxa. The robust australopithecine vault is lower, with a poorly developed frontal region compared with A. afticanus, the biparietal arch is lower, longer and more laterally flared, and the occipital region is longer and not as developed vertically. These are fundamental contrasts in the shape of the neurocranium rather than mere size differences, and confirm the taxonomic separation of the forms based primarily upon dental and spIanchnocrania1 contrasts.

The A. africanus and early H. erectus samples are 30 D units apart, resulting in a high overall phyletic rate of 2.309 u.p.h. during the Lower Pleistocene. This represents a general increase in most cranial dimensions, but particularly in the length and lateral expansion of the frontal, the length, height and lateral development of the parietal region, and the antero-posterior development of the occipital. A considerable proportion of this can no doubt be explained as an allometric consequence of an increase in overall body size, but the magnitude of the differences -and the consequent high evolution rate-are sufficient to indicate selection for greater cranial capacity additional to the size dependent component.

By contrast, the distance between the two H. erectus samples is much lower but the evolution rate (3.226 u.p.h.) is even higher than that of the preceding segment because of the much shorter time interval involved. The two groups are, in fact, very similar in many characters, and although there is a general increase in most dimensions, changes in shape are relatively minor. The Pekin material has a higher, more expanded frontal region, and the parietals are slightly longer and higher than in the earlier sample, but the proportions of the H. erectus neurocranium remained remarkably constant throughout the Middle Pleistocene, and the figure essentially represents an increase in neurocranial size.

A similar distance separates the late H. erectus and modem samples, and the evolution rate is 4.265 u.p.h. calculated over the Upper Pleistocene as a whole. In this instance the figure reflects differences in neurocranial proportions rather than size, since changes in gross cranial capacity during the later Quaternary are relatively minor. Major contrasts in vault shape include the higher, expanded frontal of the modern skull, the higher broader bi-parietal arch, more rounded occipital with absence of marked nuchal torus, and the laterally expanded squamous temporals.

396 A. BILSBOROUCH

Evolutionary change within H. sapiens is reflected by the separation of the Upper Pleistocene groups, although polytypism is also contributing to the distances obtained, particularly those between penecontemporaneous samples from different continents.

The early H. sapiens specimens are IO.19 D units away from the Pekin material, which represents-assuming strict phyletic continuity-an evolution rate of 20.376 u.p.h. towards the end of the Middle Pleistocene. This separation results primarily from shape contrasts, since the mean values for the sagittal and coronal arc measurements do not differ greatly between the two groups. However, the frontal bone is considerably higher and set at a different angle to that of H. erectus; the parietal region is similarly much higher whilst the temporal bulges laterally, and there is a considerable increase in the horizontal and vertical dimensions of the occipital bone, although the arc length is, in fact, less than that of the preceding group due to the disappearance of the nuchal torus.

The distance between the Holstein H. sapiens specimens and the Solo material is slightly greater than that between the latter group and the Pekin sample. Both distances result in high evolution rates (Il.014 u.p.h. and 8.004 u.p.h. respectively). These distances emphasise the peculiar cranial morphology of the Solo specimens, and the minimum distance between the Javanese material and another group (early H. s. sapiens) is > 15 units. There are marked contrasts in cranial proportions between the Holstein H. sapiens and Solo specimens, making a derivation from populations resembling the former group unlikely. The frontal region is much lower in the Solo material, the parietal arch is longer, lower and wider; the temporal curves medially above porion rather than bulging laterally, and the occipital is much reduced. In fact, the cranial vault of the Solo group is basically H. erector-like in many of its dimensions, the main contrasts with the Pekin sample being a shorter, laterally expanded frontal and a much longer parietal segment. Whilst emphasising the distinctive cranial morphology of the Solo group, the multivariate analysis suggests a derivation from a late H. erectus population rather than one morphologically similar to the early H. sapiens group.

The classic Neanderthal sample is 8.74 D units from the early H. sapiens specimens and somewhat further from late H. erectus. The proximity of the Holstein and early Wiirm groups is rather unexpected in view of the traditional view that the classic Nean- derthals are too specialised in their cranial morphology to be derived from specimens such as Steinheim and Swanscombe. In fact, a rate of only 4.369 u.p.h. results if the early H. sapiens group is considered ancestral, whilst a rate of 5.259 u.p.h. is necessary for derivation from the earlier Pekin sample. The main contrasts between the European Holstein and Wtirm samples are an increase in frontal breadth, a slight lowering and lateral expansion of the parietal and temporal regions and a somewhat greater vertical development of the occipital. These changes are relatively minor compared with those necessary to transform the late H. erectus calvarium into that of the classic Neanderthals. The Neanderthal skull is much larger in almost every dimension, but especially in the parietal region which is expanded in both sagittal and coronal planes, and in the orien- tation of the occipital.

The whole neurocranium of the European Neanderthals is generally longer than that of the preceding groups, but the total morphological pattern of the early H. sapiens cranial vault approximates to the classic proportions much more closely than does the late H. erectus sample.

The Neanderthal sample is separated from the approximately contemporary Soko material by > 13 units, a distance which reflects the marked contrasts in cranial

HOMINID CRANJiAL VAULT EVOLUTION 397

proportions between the two groups. The Rhodesian skull is similarly well separated from the European Neanderthals, corresponding to their dispersed positions along canonical variates I and III. This is due to the greater size of the frontal region in the African specimen, its much lower parietal vault, and the contrasts in occipital proportions. The marked dispersion of these penecontemporaneous groups suggests considerable polytypic variability in cranial vault dimensions among Late Pleistocene populations, and further evidence for this is provided by the relative positions of other groups. The Rhodesian skull is, in fact, much closer to the Solo material than to the European Nean- derthals, whilst its derivation from late H. erectus is morphologically much more economical than evolution from populations resembling the Holstein H. sapiens specimens.

The Middle East Neanderthals are well separated and approximately equidistant from both the Rhodesian and Solo specimens, and much closer (< 9 units) to the Euro- pean Neanderthal sample. The distances mainly reflect the shorter, higher, more expanded frontal region and smaller occipital of the Mt Carmel material-parietal dimensions do not differ greatly between the three groups. The separation between the European and Middle Eastern groups results in a rate of 88.490 u.p.h. if the known classic material is posited ancestral to the Carmel population. This is much higher than in other segments, and it is therefore likely that the separation reflects geographical and individual variation rather than phyletic change. However, it is possible that both the European and Middle Eastern Neanderthals share a common ancestry in mid-Eem, and present evidence indicates that such ancestral populations resembled the ‘classic’ Nean- derthals rather than the Cannel specimens. A rate of only 22.121 u.p.h. is necessary to derive the Palestinean material from mid-Eem populations morphologically identical to the known classic Neanderthals, and such a figure appears more consistent with the data since it approximates to those rates between other Upper Pleistocene samples separated by comparable periods of time.

The Upper Palaeolithic H. s. sapiens group is only 5.4 D units from the Middle East Neanderthals, representing a general increase in most dimensions but particularly in the development of the frontal region, the curvature and height of the parietal arch and the length of the occipital area. These are mainly size differences rather than contrasts in shape, and may therefore merely reflect sampling error. However, a phyletic rate of c. O-36 u.p.h. results-a very low figure in view of the short time interval (15,000 years) separating the two groups, but essentially identical to that (35.178 u.p.h.) required to derive the cranial vault of the Upper Palaeolithic sample directly from that of the early Wtirm European Neanderthals. Thus analysis of the cranial vault indicates that when the chronology of the groups is taken into account, derivation of late Pleistocene H. s. sapiens from the European Neanderthals is as morphologically economical as positing the Middle East Neanderthals ancestral.

A similarly low rate of 30.22 u.p.h. results between the Upper Palaeolithic and modern specimens, and the D distance is well within the range of those obtained between modern samples (Weiner & Campbell, 1964). It represents a general decrease in most parameters, more marked in the parietal and occipital regions than elsewhere, but no fundamental changes in shape are involved. Evolution of the modern cranial vault directly from the Middle East Neanderthals requires a somewhat lower rate but the time span is longer, whilst derivation from the ‘classic’ Neanderthals results in a rate of 22.7 u.p.h.-not an excessive figure calculated over 50,000 years and comparable to that obtained between the late Middle/early Upper Pleistocene groups separated by a similar time interval.

398 A. BILSBOROUGH

Considerably higher rates than those above are needed to transform either the Rhode- sian or Solo cranial vault into that of modern H. s. sapiens, implying morphological changes much more rapid, for example, than those between the late H. erectus and early H. sapiens samples. Multivariate analysis of the cranial vault therefore indicates a derivation for H. s. sapiens from populations such as the European or Middle Eastern Neanderthals, rather than directly from other late Pleistocene groups.

The separation of A. africanus and the modern sample results in an overall evolution rate in cranial dimensions of 1.189 u.p.h. throughout the Pleistocene. The early H. erectus group is almost as far away from the modern sample, and the average rate from the early Middle Pleistocene onwards is 3.169 u.p.h. The later H. erectus material is much nearer to the modern sample but the distances, together with the great separation of A. africanus and early H. erectus, indicate a marked reversal in evolutionary trends during the Lower and Middle Pleistocene. This results not from any marked diminution in gross cranial size, but from changes in cranial proportions.

The expansion in cranial capacity between A. africanus and early H. erectus is primarily accomplished by an increase in the antero-posterior and lateral dimensions of the cranial vault, and there is much less increase in the vertical dimensions of the cranial bones. The neurocranium of early H. erectus is long and relatively low, thereby contrasting with both A. africanus and modern H. s. sagiens which possess a relatively higher, vertically expanded cranial vault. The main changes in cranial parameters during the later Middle and Upper Pleistocene involve an increase in vertical dimensions, and in shape A. africanus and H. s. sapiens resemble one another more closely than either does early H. erectus. It is these changes in cranial vault proportions, superimposed upon the general increase in cranial size, which account for the great separation between early Middle Pleistocene and modern hominids.

5. Discussion

Given the distinctive nature of human adaptation and the genetic consequences of this, it is probable that throughout much of the Pleistocene hominid evolution was reticulate in pattern, with gene flow between adjacent populations. Consideration of hunter- gatherer economies and the mating patterns of human communities renders it highly improbable that any population was isolated for an appreciable period, and the various evolution rates considered above-particularly those between Upper Pleistocene groups- should not be construed as mutually exclusive alternatives. Rather they represent an attempt to derive the most economical evolutionary network, assuming that the contri- bution of each of several possibly ancestral groups to the gene pool of a descendent population is directly proportional to the degree of morphological resemblance to that descendent population.

The analysis of cranial vault dimensions resulted in considerable separation of the Australopithecus species, reflecting the marked differences in cranial proportions between the two forms. The frontal region of the robust specimen is much lower and generally less developed, with a more marked post-orbital constriction, the parietals are longer, depressed, and more laterahy flared, whilst the occipital is longer, lower and flatter than in the gracile australopithecines. The low cranial vault of A. boisei compared with A. afficanus is mainly responsible for the separation of the two taxa along canonical variate I, and the contrast is most conveniently expressed by the supra-orbital height


index (Clark, 1950). The Olduvai specimen has an index of 52we11 within the pongid range-whilst that of A. ufricanur (Sts. 5) has variously been estimated at between 61 and 74 (Tobias, 1967) i.e. within the range of modern human crania. However, as Tobias notes, the low vault of the ‘Zinjanthropus’ skull does not imply a lack of cerebral expansion-in fact the Olduvai specimen has a greater cranial capacity than A. afrricntu.

The Olduvai hominid 5 skull has an estimated capacity of 530 cc whilst a recent examination of the more complete A. africanus specimens (Holloway, 1970) yielded a mean capacity of 442 cc-considerably lower than previous estimations. Comparison of australopithecine endocasts indicates that the main differences between the gracile and robust forms are the greater length and lateral expansion of the parietal area in the latter group (Tobias, 1967). This corresponds to the greater size of the parietal region noted in the multivariate analysis. The low vault of the robust australopithecine cranium is a consequence of a shallower, broader biparietal arch and a neurocranium which is hafted to the facial skeleton at a lower level than in A. africanus (Tobias, 1967). For this latter reason frontal development (as measured by characters 4 and 5) is much less in the Olduvai specimen than in A. afticanus.

Thus the discrimination between the two australopithecine samples provided by the cranial analysis reflects fundamental differences in the proportions and structure of the cranial vault not explicable by size difference alone, and confirms the taxonomic dis- tinctiveness of the groups indicated by other complexes, e.g. the face and masticatory apparatus.

The analysis also revealed marked changes in cranial dimensions between A. afiicanus and early H. erectus. These result from a doubling in cranial capacity during the Lower and early Middle Pleistocene-from 440 cc to more than 900 cc. As noted above, a proportion of this is probably an allometric consequence of greater body size, but the magnitude of the increase is such that there must also have been selection for increased cranial capacity.

This expansion is accomplished by a large increase in horizontal dimensions, particularly of the frontal and occipital regions, together with a lateral expansion of the cranial base, but with little vertical development of the neurocranium. Parietal expansion is less marked than that of the other areas, and because of the great increase in occipital dimensions, the ratio of parietal arc:occipital arc is lower than that of either A. afkanus or modern H. s. sa@ns, where there has been a secondary increase in parietal dimensions (Tobias, 1967). The differential increase in horizontal and vertical diameters results in a neurocranium which contrasts in shape with that of A. afianw, and which suggests a change in the growth patterns of the various components of the cranial vault.

There is some evidence to indicate when these changes occurred. The material recovered from Beds I and II, Olduvai Gorge, during the last ten years, although only provisionally described, provides a series of fossil hominids covering the period 1.85- c. O-7 million years. Olduvai hominid 7 (the type of H. habilis) from Lower Bed I has a biparietal volume substantially larger than that of the South African australopithecines, and presumably, a total cranial capacity correspondingly greater (Tobias, 1964). The recently described penecontemporareous specimen from DKI (Leakey, Clarke & Leakey, 1971) has a comparable endocranial capacity and provides more complete data on skull proportions. After allowing for distortion, the cranial vault is more platycephalic and the occipital more protruberant than in A. ufricanus, but less so than in H. erectus.

400 A. BILSBOROUGH

Other remains (hominids 13-16) from around the fauna1 break in Bed II-tentatively dated at 1.3-1.0 million years-also possess a relatively large cranial capacity (> 600 cc) (Leakey & Leakey, 1964), and a cranium which in shape and construction is intermediate between that of A. africanus and H. erectus. The later specimens from Upper Bed II (Olduvai hominid 9) and from the Far East show a further increase in cranial capacity (800-1000 cc) together with an elongated and distinctly more robust cranium.

Thus the presence of large brained, lightly-built crania in the later Villafranchian deposits at Olduvai suggests that cranial capacity was increasing throughout the Lower Pleistocene as a result of selection for greater intelligence and intellectual ability. The greater robusticity of the cranium and further increase in cranial capacity in late Lower/ early Middle Pleistocene H. erectus are probably simple consequences of the increase in overall body size which occurred at this time, possibly due to altered selection pressures resulting from a shift in dietary niche, from a predominantly vegetarian to an increasingly omniverous one. Such an explantion would also account for the change in cranial proportions between A. africanus, H. habilis and H. erectus. If this theory is correct, the differences in cranial shape and robusticity are allometrically determined, and there is therefore no need to posit several phyletic lines of hominids in the Lower and Middle Pleistocene on the basis of these differences, as Leakey (1966) has done.

Between the early and late samples of H. erectus there is a general increase in the height of the bones of the cranial vault, particularly in the frontal regions. The parietals show a general, although slight, increase in all dimensions and there is a further development of the occipital These changes correspond to the gradual ‘rolling up’ or kyphosis of the neurocranium during hominid phylogeny, as noted by Weidenreich (195 1) and Biegert (1963).

This process is continued into the early Upper Pleistocene. The early H. sapiens

material shows further vertical expansion of the frontal and occipital together with marked expansion of the parietal region in both sagittal and coronal planes, whilst the lateral expansion of the cranial vault results in the maximum breadth being about the temporo-parietal structure, not at the level of porion as in H. erectus. Whilst thus showing a number of contrasts with the Pekin material in the proportions of the cranial vault, the early H. sapienr specimens are only IO.19 D units away-little more than the Mt Carmel sample is from the modern series. There is therefore no reason to reject the known late specimens of H. erectus from the ancestry of early H. sapiens, and the derived rate of change--20.376 u.p.h.-is not unduly high.

Moreover, the proximity of the early H. sajiens specimens to the classic Neanderthals (8.74 D units) indicates similarity in cranial proportions, and there is no justification for regarding Steinheim and Swanscombe as evidence of a ‘prae-sapiens’ lineage (Vallois, 1954, 1958). These results are broadly in agreement with those reached by Weiner & Campbell (1964) who provide a more extensive discussion of the early sapiens material.

Although it is reasonable to derive the European classic Neanderthals from the Holstein specimens, a similar ancestry for either the Rhodesian or Solo specimens is less likely in view of their wide separation in the discriminant analysis. They are somewhat closer to the late H. erectus sample, and whilst the distances emphasise their distinctive cranial morphology, a derivation from late polytypic erectus populations is the most likely hypothesis. This is in agreement with Weidenreich’s (1943, 1951) views, and the muiti- variate analysis of cranial dimensions also supports Weidenreich’s contention that these specimens should not be regarded as ‘tropical Neanderthals’. The Rhodesian skull is

HOMINID CRANLtL VAULT EVOLUTION 401

12.19 D units from the classic sample, the Solo specimens are 13.64 units away. The fact that these distances are almost as great as the corresponding distances of the fossil groups from the modern sample emphasises their diversity, and provides further evidence that throughout much of the Middle and Upper Pleistocene there was considerable morphological variability in neurocranial proportions owing to relatively isolated phyletic development from locally differentiated basal H. erectur populations.

The Mt Carmel material is relatively well separated from the classic Neanderthals owing to its shorter, more rounded cranial vault and fuller frontal region and contrasts in occipital proportions. As noted above, derivation from the European Wiirm Neander- thals is improbable, but a morphologically similar, mid-Eemian ancestor-perhaps represented by remains such as Ehringsdorf and Krapina in Europe and Galilee and Shanidar in the Middle East-is much more likely. Such a scheme would accommodate the known fossil material from late H. erectus onwards without any marked reversals in evolutionary trends or differentiation into ‘generalized’ and ‘classic’ Neanderthals (Howell, 1957).

Livingstone (1969) has proposed a genetic model for changes in cranial dimensions (basi-bregmatic height and cranial length) assuming 4 and 8 loci, with equal and additive alleles at certain posited frequencies. With selection coefficients comparable to those known to affect metrical traits in modern populations, Livingstone shows that with even a relatively small number of genes determining the traits in question, the changes in mean value from the classic Neanderthals to the Upper Palaeolithic population could have occurred within 20,000 years. Although in the absence of definite knowledge concerning the genetic basis of cranial morphology, it remains something of an academic exercise, the study is interesting in suggesting that directional selection of moderate intensity can effect relatively rapid changes in metrical characters. There thus seems no cogent reason to consider the European Wiirm Neanderthals as ‘aberrant’ (Boule & Vallois, 1957) (Ivanhoe, 1970; Wright, 1971), orgeneticallyisolated (Howell, 1951,1952) because of their cranial proportions, although they are almost certainly too late in time to be directly ancestral to the Middle Eastern specimens.

The only significant contrast between the Mt Carmel material and the late Pleistocene and modern H. s. sapiens is a further increase in height and expansion of the frontal region. The remaining differences are trivial ones of size, and the human cranial vault had reached essentially modern proportions by middle-Wiirm times.

Previous studies of evolution rates in hominids have been concerned almost exclusively with changes in cranial dimensions. Haldane (1949) advocated the use of darwins (a change by a factor e per million years) as a measure of the rate of evolution, and provided as an example the rate of change in the ratio of cranial length: height from Sinant/zr@uc (Pekin H. erectus) to modern Man. Other studies are those of Kurten (1959), Bone (1962) and Campbell (1963), all of whom discuss changes in cranial capacity. Kurten and Campbell used the cube root of cranial capacity as their data, Bone appears to have used cranial capacity itself. All three express the rate of change in darwins, although as Campbell notes, it is difficult to derive Kurten and Bone’s results using Haldane’s formula, and all are based upon a short Pleistocene chronology leading to spuriously high evolution rates.

Campbell’s data are the most comprehensive and indicate a fairly rapid (280 milli- darwin) increase in cranial capacity during the (too short) Lower Pleistocene, rising to 357 md during the Middle Pleistocene (early-late H. erectus) and reaching a peak of

402 A. BILSBOROUGH

375 md in the late Middle/early Upper Pleistocene (late H. erectus-early H. sapiens), thereafter dropping to almost zero (early-modern H. sapiens). Recent determinations of australopithecine cranial capacity (Holloway, 1970) indicate that the figure given by Campbell for A. africanus (500 cc) is too high, but this apart the data are in broad agreement with those of the present study when the chronologies are adjusted.

The two sets of results are not comparable in detail, since Campbell’s study is a univariate one, using the natural logarithm of the cube root of cranial capacity as a measure of proportional change in cranial size, whereas the present study is multivariate and uses several linear dimensions to measure both size and shape. Two skulls may have the same cranial capacity (and therefore show no change in Campbell’s study) and yet be well separated in multidimensional space if they are of different shape i.e. the linear dimensions are contributing differentially to the total size of the two crania. Whilst the distances between Lower and Middle Pleistocene hominid groups are based upon a combination of size and shape contrasts, cranial evolution during the Upper Pleistocene involves predominantly shape changes and size differences are trivial. The use of multivariate analysis to describe changes in cranial proportions therefore has considerable advantages, and studies which incorporate such techniques provide more extensive information than those based upon simple univariate statistics or some measure of overall size such as endocranial capacity.

6. Conclusions

Multivariate statistical techniques provide a valuable adjunct to the traditional Linnean nomenclature for describing evolutionary change within Hominidae, and when used in conjunction with an absolute chronology the distances so derived provide an estimate of the rate of morphological change between successive groups.

The data presented here show that throughout the Lower Pleistocene there were considerable changes in cranial vault morphology, partly an allometric consequence of increased body size, partly due to selection for increased brain size, presumably reflecting greater behavioural complexity. The rate of change, although substantial, is not as high as in later periods because of the long time intervals between samples. During the Middle Pleistocene there were extremely rapid changes in neurocranial dimensions, reflecting a general increase in cranial capacity, but with little change of shape. Cranial evolution during the Upper Pleistocene, however, involves a reproportioning of the vault, but little alteration in gross capacity. Neurocranial changes among late Pleistocene groups are complex, and probably reflect a predominantly reticulate pattern of evolution, combining in situ genetic change with gene flow between contiguous populations. The data as a whole support a predominantly monophyletic view of hominid evolution.

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a multivariate study of evolutionary change in the hominid cranial vault and some evolution rates

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