the mauer mandible and the evolutionary significance of homo heidelbergensis

THE MAUER MANDIBLE AND THE EVOLUTIONARY SIGNIFICANCE

OF HOMO HEIDELBERGENSIS

ANTONIO R O S A S & JOSE M. BERM-t~DEZ DE CASTRO

ROSAS A. & BERMIJDEZ DE CASTRO J.M. 1998. The Mauer mandible and the evolutionary significance of Homo heidelbergensis. [La mandibule de Mauer et la signification ~volutive de Homo heidelbergensis]. GEOBIOS, 31, 5: 687-697. Villeurbanne, le 31.10.1998.

Manuscrit d~pos~ le 16.06.1997; accept6 d~finitivement le 23.10.1997.

ABSTRACT - The significance of the species H. heidelbergensis is discussed by means of the comparison of the holotype of this species -the Mauer mandible- with a large set of Homo fossils. It is argued that the primitive appearance of the Mauer mandible occurs along with unequivocal indications of Neandertal apomorphies. The BL dimensions of the incisors and morphology of premolars as well as the variables related to the position of the mental foramen and retromolar space definitely indicate that Mauer should be classified as a member of the evolutionary lineage which evolved into classic Neandertals. We conclude that the Mauer mandible represents a population forming part of the Neandertals evolutionary lineage. Therefore, the name H. heidelbergensis cannot be used to denote the last common ancestor to Neandertals and Modern humans. It is proposed that the taxon H. heidelbergensis should be used only to name a European Middle Pleistocene chronospecies of the Neandertal evolutionary lineage.

KEYWORDS: MAUER, MANDIBLE, TEETH, HOMO HEIDELBERGENSIS, NEANDERTAL TRAIT.

RI~SUMt~ - La signification de l'esp~ce H. heidelbergensis est discut~e par la comparaison de l'holotype de cette esp~- ce, la mandibule de Mauer, avec un important ensemble de fossiles d'Homo. I1 est propos5 que l 'apparence de gran- de massivit~ de la mandibule de Mauer se trouve associ~e h des caract~res qui sont tr~s typiques des N~andertaliens. Par exemple, les dimensions BL des incisives et la morphologie des pr~molaires, ainsi que les variables li~es h la position du trou mentonnier et l'espace r~tromolaire, indiquent net tement que Mauer doit 6tre class~ comme un membre de la lign~e 5volutive europ~enne qui ~voluait vers les NSandertaliens. Nous sommes arrives/t la conclusion que le nom H. heidelbergensis ne peut pas ~tre employ~ pour d~signer le dernier anc6tre com- mun des N~andertaliens et des hommes modernes. Nous proposons que le nom H. heidelbergensis soit utilis~ pour une chrono-esp~ce du P15istoc~ne moyen europ~en de la branche ~volutive des N~andertaliens.

MOTS-CLI~S: MAUER, MANDtBULE, DENTS, HOMO HEIDELBERGENSIS, CARACTERE NEANDERTALIEN.

I N T R O D U C T I O N

The s igni f icance of Homo heidelbergensis h a s become a cen t ra l i ssue in the phylogene t ica l ly - b a s e d t a x o n o m y of Midd le -La te Ple is tocene hominids. T h e recogni t ion t h a t t axonomic d ive r s i ty in h u m a n e v o l u t i o n w a s b e i n g u n d e r e s t i m a t e d (Ta t t e r sa l 1986; 1992), t oge t he r w i t h the discove- ry of s ign i f ican t new fossils (Gabun i a & Vekua 1995; Carbone l l et al. 1995; H u a n g et al. 1995), is s t i m u l a t i n g a r ich deba t e on Ple is tocene homin id t a x o n o m y (Wood 1992a,b; S t r i nge r 1996; Ber- mfidez de Cas t ro et al. 1997). Tradi t ional ly , evolu- t ion of Homo h a s been perce ived by m e a n s of an anagene t i c mode l in which H. habilis g r a d u a l l y evolved into m o d e r n h u m a n s t h r o u g h o u t a long

i n t e r m e d i a t e p h a s e n a m e d H. erectus. However , a f t e r a u t o a p o m o r p h i c t r a i t s we re recogn i sed in the As ian Ple is tocene homin id s (Andrews 1984; S t r i nge r 1984; Wood 1984), H. erectus h a s become inc reas ing ly accepted as a d is t inc t species f rom the one t h a t gave or igin to m o d e r n h u m a n s (Righ tmi re 1990; Wood 1992a).

The removing of H. erectus f rom the ances t ry of N e a n d e r t a l s and m o d e r n h u m a n s , r e su l t ed in the use of the n o m e n Homo heidelbergensis for the re la t ive ly p r imi t ive Euro-Afr ican Middle Pleisto- cene species, which defines the p u t a t i v e common a n c e s t r y of n e a n d e r t a l s and m o d e r n h u m a n s (Rightmire 1990; S t r i nge r 1993). According to Righ tmi re (1996), Afr ican spec imens f rom Broken

688

Specimen & samples

Ramus MEN- M3- FOR- I-FOR Breadth CON LIN M3

Mauer 51 134,3 36,9 38,7 41

A. afarensis AL288 117,3 53,1 31,2 AL266 59 31,9 AL400 52,6 33,9 AL188-2 59,3 AL277-1 38,8

H. habilis OH13 16,9 53 25,7 ER1501 50,8 ER1802 30,3

H. ergaster ER992 49,8 28,4 49,4 34,7 ER730 WT15000 39,4 123 32,5 ER3230 35

If. erectus Lantian 39,8 Zhoukou. K1 47,8 38 Zhoukou. HI 40,9 118,5 23 32,8 Zhoukou. GII 40,8 130,7 20,6 53,9 31,8 Sangiran 9 53,4 35,5 Sangiran 53,6 29,9 Sangiran 27,4

North Africa Middle Pleistocene Tighenif I 27,9 51,9 34 Tighenif 2 44,1 121,9 18,3 48,5 31,9 Tighenif 3 47,6 143,3 33,2 50,9 43,3

East Africa Middle Pleistocene BK67 48,9 133,2 33,3 47,2 30,8 BK8518 55,1 25,6 OH22 30,7 45,5

Specimen & samples

Ramus MEN- M3- FOR- I-FOR Breadth CON LIN M3

Europe Middle Pleistocene (H. heidelbergensis) Arago II 49 130,1 32,4 35,4 39,8 Arago XIII 43 142 32,6 44,9 45,3 Mont 39,4 123,4 23,7 41,7 36,2

Atapuerca SH sample AT-950 42,2 123,7 35,9 33,9 36,4 AT-505 38,6 115 27,8 32,4 36,5 AT-605 47,7 139,3 39,9 35,6 38,3 AT-607 38 117,2 24,8 35,6 35 AT-300 125,7 31,7 38,2 36,9

Neandertals (H. neanderthalensis) Amud 39 136,3 32,2 35 42,9 La Ferrassie 43,3 142,6 37 35 37,6 Vindij a 226 41,6 126,7 33,6 34,2 30,8 Tabun I 37,7 123 33 38,7 29,8 Tabun II 39,3 134,7 33,3 38,7 43,4 Circeo III 42 32,5 39 41,8 La Quina I 44,2 Kebara 34,5 36,3 43,5 St Cesaire 136,4 35,9 38,6 38,3 Shanidar 4 33,3 44 38

Upper Pleistocene Abri Patu 118 18 44,7 30,1 Combe Capelle 121,8 24,5 34,6 37,1 Skhul V 131 29 44,6 33,4 Qafzeh IX 124,5 21,7 44,3 34,1 Pavlov 133,6 26,1 44,5 27 Predmost 36,8 136,3 28,9 38,8 35 Kostienski 116,6 25,1 41,7 29,3 Oberl 42,5 137,9 28,9 42,7 30,2 Ober2 36,8 117,2 20,3 38,3 33,2 Brno3 36,9 119,5 23,2 38,4 26,4 Dolniv3 35,5 117,1 20,6 39,8 26,5 Cromagnon 44,4 29,4 Chancelade 42 136

TABLE 1 - Mandibular variables and fossil samples used in the analysis. See text for definition of distances. Variables mandibu- laires et dchantillons fossiles utilisds lors de l'analyse. Voir le texte pour la ddfinition des distances.

Hill and Bodo, as well as the European ones from Petralona and Arago, among others, are similar enough to be grouped together. The specific nomem H. heidelbergensis is used to define the combina- tion of archaic and modern traits not present in H. erectus, neandertals and modern humans which supposedly characterizes the Afro-European hypodigm. Recently, however, the identification of neandertal apomorphic traits in the Middle Pleistocene European samples (see Rosas 1997 for references) has weakened the concept of H. heidelbergensis as the common ancestor (Stringer 1996). In this context, and the Mauer mandible being the holotype of the species H. heidelbergensis (SCHOETENSACK, 1908), a re-evaluation of its morphology is necessa- ry for understanding the affinities of the H. heidelbergensis taxon, and therefore the relationships between Middle Pleistocene hominids with neandertals and modern humans. The main aim of this study is to check whether or not the Mauer mandible exhibits Neandertal apomorphic traits.

MATERIAL AND METHODS

Bone structure and dentition of the Mauer mandible has been subject of a detailed comparative study. To this end, a large set of dental and mandibular samples of fossil and living hominids was employed (Tables 1, 2).

The morphological features of the mandible used in the study may be found in Rosas (1995), while metric variables are defined as distances between particular landmarks of the jaw (Fig. 1, Rosas 1995). The most relevant distances employed for the analysis of Mauer have been: I-FOR, distance between the infradental point and the mental foramen; FOR-M3, distance between the mental foramen and the M3; LIN-M3, distance from the M3 to the lingula of the mandible. The maximum length of the mandible, distance MEN-CON, was used to assess the size of the mandible and breadth of the ramus was measured as its minimum width. Continuous variables were compared by

6 8 9

Specimen/sample Reference

UR 501

OH7, OH13, OH16, OH24, 0H39

0H22

KNM-ER 730, 1802

KNM-ER 806, 820, 992

KNM-WT 15000

Sangi ran 9

Sangi ran B, Zhoukoudian

Dmanisi

Mauer

Krapina

Rabat

Thomas I

Cha teauneuf 2

Arcy2 and A9

Circeo 3 and 4

La Quina 9, Spy 1 and 2, Le Moustier, Subalyuk Ehr ingsdorf (adult and adolescent), Tabun

Ochoz

Monsempron b

Shan ida r

Aboriginals from Gran Canar ia (Canary Islands)

Bromage et al. 1995

Tobias 1991

Rightmire 1980

Leakey et al. 1978

Leakey & Wood 1973

Brown & Walker 1993

Jacob 1973

WoIpoff 1971

Rosas & Bermfidez de Castro, submit ted

Wolpoff 1971 and authors

Wolpoff 1979

Thoma & Vallois 1977

Sausse 1975

Tillier 1979

Leroi-Gourhan 1958

Borgognini 1983

de Lumley 1973

Vlcek 1969

Vallois 1952

Trinkaus 1978

Bermfidez de Castro 1985

TABLE 2 - List of hominid fossils used in the comparative analysis of the dental var iables . Liste des hominid~s fossiles utilis~s dans l'analyse comparative des variables dentaires.

CONI Triangular toms, anterior margin ~ ., LIN /

Ante rio r bo rdy._...~--~) "~ ~'~1" I of theramus / ~ / / / I

,

MEN ~ J

FIGURE 1 - Main morphological t r a i t s and l andmarks employed in this study. Distances between landmarks are used as var iables (double arrow). FOR: menta l foramen; LIN: Lingula; M3: the postero-lingual corner of the M3 alveoli; MEN: menton point; I: inf radenta l point; CON: the uppermost point of the condyle. Prineipaux caract~res morphologiques et rep~res utilis~s dans cette gtude. Les distances mesurges entre les points rep~res sont indiqudes par des doubles fl~ches. FOR: foramen mentionner; Lin: lingula; M3: point postgro-lingual de l'alv4ole; MEN: point mentionner; I: point infradental; CON: point supgrieur du condyle.

means of box-and-whisker plots in which the rec- tangular box length is equal to the inter-quartile range and which is divided into two parts at the median. The line is drawn to the highest and lowest observations in the group (range). Fossil specimens have been grouped under specific names in cases where there is a general agree- ment while a chrono-geographic concept was used in cases where taxonomy is unclear (Tabl. I).

In previous papers (Berm~dez de Castro 1993, Rosas & Bermfldez de Castro, submitted) we have shown that tooth shape analyses represents a powerful tool to establish relationships between different hominids. In order to made this kind of analysis first we have obtained the crown area (CA). This variable was calculated from the mesiodistal (MD) and buccolingual (BL) dimensions of the teeth (CA= MD x BL). The MD and BL dimensions of the Mauer, Atapuerca-SH, Arago, Mont- maurin (mandible), Lazaret, Tighenif, Hortus, Malarnaud, Macassargues, La Ferrassie 2, and La Quina 5 original specimens were recorded by JMBC to the nearest 0.i mm following the tech- nique proposed in Lefevre (1973). The data of other specimens and samples were taken from the litera- ture (Tabl. I).

690

Furthermore, in order to analyse the relative pro- portions of the Mauer teeth with regard to other specimens and samples, we have processed the data as follows.

Firstly, let us to obtain the value of the expression:

MAU X,/((MAU X~+SI XJ)I/2), (1)

where X~ (i=1 ......... n) is the value which takes each one of the n variables analysed in Mauer and in the S~ (i--1 ........ n) specimens or samples. Then, let us to calculate the average of the values obtained for all the variables used in the comparison between Mauer and each one of the S~:

n MAU X/((MAU XJ+S~ X~)l/2) - - ( 2 )

i=1 n

The expression (2) is named "average dental ratio" (ADR). The variance of the distribution of all MAU XJ((MAU X~+S1 X~)1/2) values represents the so-called WF distance (F) between Mauer and one of the specimens or samples (e.g. $1). This mult ivariate shape distance was first proposed by Bermfidez de Castro (1993).

Let us illustrate, by means of a bivariate scatter- gram, the ADR (e.g. in the X-axis) for all Si vs. the value of the expression (2) (y-axis) for each ~3. Obviously, the expressions (1) and (2) take the value 1 when S~ =Mauer; tha t is to say, when we compare the Mauer specimen with himself. In this way, the point representing Mauer will be in the line X=Y. Regarding the comparison between Mauer and the other S~, the greater the difference between the expression (1) and (2) for certain X~ the greater the distance of the the S~ to the line X=Y for this ~3.

If all points representing the different Si for certain Xi are close to the line X=Y, the correlation index (r) between the ADR values and the values for this variable in all S~ would be approaching 1. In contrast, the greater the dispersion of these points the lesser the correlation index. In the first case, this means tha t the variable does not show significant variations in the S~ with regard to our reference. In evolutionary terms, this case could imply important changes in size of the variable without significant changes in shape in relation to our reference. The second possibility needs a dee- per analysis, since we could detect systematic shape changes in some Si. In the bivariate scat- tergram obtained for any of the XJ, when a Si is located on the left of the X=Y line it implies tha t this S~ shows a proportionally lesser value than Mauer for the XJ at issue, and vice v e r s a when a S~ is placed on the right of the X=Y line.

In order to include the greatest number of specimens in this analysis, we have used the MD and BL dimensions of the lower (L) I2, C, P3, P4, M1, and M2. Thus, Si includes the Atapuerca-SH, Neandertal , Zhoukoudian, and Gran Canar ia samples (which are represented by their corres- ponding mean values for each variable), as well as the specimens OH 7, KNM ER 992, KNM WT 15.000, Tighenif 3, and Dmanisi.

RESULTS

MANDIBULAR TRAITS

Teeth and jaw of neandertals exhibit a set of apomorphic traits as part of its derived craniofacial pattern. In the mandible, the presence of a retromolar space and the mental foramen located at the level of the M1 have largely been considered the most noticeable Neandertal features (Stringer et al 1984; Rosas 1987; Condemi 1991). Conventionally, it has been said a mandible has a retromolar space when, observed in lateral view, it presents a gap between the M3 and the anterior border of the ascending ramus (Wolpoff 1975; Stringer et al. 1984; Franciscus & Trinkaus 1995). According to our observations, however, there are mandibles with a conspicuously developed retromolar space but with no gap between the M3 and the anterior border of the ramus is present. This is the case of the Mauer mandible. This specimen shows that the presence of a retromolar space in a mandible depends on two different factors. On one hand, the breadth of the ramus, particularly the position of the anterior border of the ramus. And, on the other hand, the position of the relieves of the internal aspect of the ramus such as the tr iangular torus and the lingula. That is, the presence of a retromolar space depends on the relationship between the M3 and the position of the structures of the ramus. Thus, the fact that a gap is visible in lateral view, is mainly related to the position of the anterior margin of the ramus. To our view, a proper retromolar space means the presence of a "space" behind the M3. It is clear that the maximum expression of a retromolar space is found in classic neandertals and this occurs together with a gap between the M3 and the anterior margin of the ramus. However, the presence of a space behind the M3 also occurs without such a gap between the M3 and the ramus. In this regard, a large variation is detected in the European Middle Pleistocene mandibles and this is particularly well-illustrated in the Atapuerca-SH sample (Rosas 1997). Figure 2 shows the Mauer mandible, together with Arago II, as having the broadest ramus of the hominid fossil record (Tabl. 1). However, in spite of their wide ramus, a large space behind the M3 is present in both mandibles.

26

H, ergaslet

H, erectus

Tighenif

East Africa MP

Mauer

H, heidelbergensfs

Atapuerca BH

Neandertals

Upper Pleistocene

Neolithios

30 Rarnus Breadth 34 38 42 46 50

I

I I

I I

i f i

5 4

691

14

A. afaransis

H, habilis

H. ergastet

H, erectus

Tighenif

Es! Africa MP

Mauer

H. he]delbergensie

Atapuerca SH

Neandertals

Upper Pleistocene

Neolithics

18

I

-Distance M3-LIN 22 26 30 34 38

t I I I

I

I I

I

I I I

I

I II

I I I

I o

I P P

42

0.24

H. ergaster

H, af~ctds

Tighenif

East Africa MP

Mauer

H, heide/bergensis

Atapuerca SH

Neandedals

Upper Pletstocene

Neolithics

Ramus Breadth/Size 0.28 0.32 0.36

i I

I I I

I I

~t I I 1

t I I I i I I I

0.40

t:IGURE 2 - Box-and-Whisker plot for the ramus breadth (above) and ramus breadth corrected by maximum length of the mandible (below) SH: Sima de los Huesos; MP: Middle Pleistocene. Dispersion des largeurs de la branche montante (en haut) et du quotient de ces valeurs par la Iongueur maximum de la branehe horizontale (en bas).

All the European Middle Pleistocene mandibles (Mauer, Atapuerca-SH, Arago) may be characteri- sed by having the s tructures of the internal side of the ramus displaced backwards with regard to the last molar. This circumstance has been measured by means of the distance M3-LIN (Tabl. 1), which records the relative position of the M3 and the in ternal s t ructures of the ramus. Figure 3 shows the dispersion of values of the distance M3- L I N in the analysed samples. It can be seen tha t neander ta ls occupy an extreme position, clearly i l lustrat ing the separat ion between the M3 and the s tructures of the ramus. The Atapuerca-SH sample also shows high values but a large variation in this distance is detected, similarly to other samples of H. h e i d e l b e r g e n s i s . Mauer clearly falls in an extreme position, only comparable to some n e a n d e r t a l s and some specimens from the Atapuerca-SH sample. This circumstance is bet- ter perceived when the distance is s tandardised by the size of the mandible (Fig. 3). Mauer is

0,12

A. afaransis

H, habilis

H. ergestar

H. erectus

Tighenif

East africa MP

Mauer

H, heibeibergensis

Atapuerca SH

Neandertals

Upper Pleistocene

Neolifhics

Distance MS-M IN/size 0.16 0,20 0.24 0,28

I I I

I

]

I I I

I I I I-{

I P--.4

i i

0,32

FIGURE 3 - Box-and-Whisker plot for the M3-LIN distance (above) and M3-LIN distance corrected by maximum length of the mandible (below). SH: Sima de los Huesos; MP: Middle Pleistocene. Dispersion des longeurs M3-LIN (en haut) et du quotient de ces valeurs par la longueur maximum de [a branehe horizontale (en bas).

again clearly associated with the European Mid- Pleistocene samples and neandertals , and can be distinguished from any other hominid sample.

The other feature that is commonly accepted as a Neandertal apomorphy, the backward position of the mental foramen, has been evaluated by means of two variables: distance between the mental foramen and the M3 (FOR-M3) and distance between the foramen and the Incision (I-FOR) (Fig 4). Figure 4 distinguishes two main groups of hominid samples. One group includes samples with a large FOR-M3 distance, with A u s t r a l o p i t h e c u s , early H o m o and African samples as the most represen- tatives. The other group includes European samples and modern humans. On its part, Mauer clearly lies with the European samples, and is fair- ly different from the African Middle Pleistocene samples such as Baringo and Olduvai IV (OH22). The FOR-M3 distance clearly i l lustrates how Mauer is closely associated with the European Middle Pleistocene specimens, Atapuerca-SH

692

30

A. afaraneis

H. h,~brlis

H. ergasfet

H. erectus

T i g h e n i f

Eas t A f r i ca M P

M a t l e r

H heidelbergensis

A t a p u e r c a S H

N e a n d e r t a l s

U p p e r P l e i s t o c e n e

N e o l i t h i c s

3 4 3 8 I I

D i s t a n c e F O R - M 3 42 4 6 50 54 58

i !

r - - r q

I

J IP

I I

I

I

I I I

I I I

i I I 14

1 I I I I I I I I

24

A. afarensts

H. habrlis

H. ergastet

H, crectus

T i g h e n i f

Eas t A f r i ca M P

M a u e r

H. heidelb~rgenei~

A t a p u e r e a S H

N e a n d e r t a l s

U p p e r P l e i s t o c e n e

Neo l i t h i c s

D i s t a n c e I - F O R 2 8 32 3 6 4 0 44 i i i i i

H I I i

I I i

I II

I I

I I I

I

I I

i- I I I

I I I I 1

6 2

48 52

FIGURE 4 - Box-and-Whisker plot for the FOR-M3 distance (above) and I -FOR distance (below). SH: Sima de los Huesos; MP: Middle Pleistocene. Dispersion des longueurs FOR-M3 (en haut) et I-FOR (en bas).

sample, neandertals as well as modern humans, both Upper Pleistocene and Neolithic. In a similar way, the distance I-FOR also accounts for the derived condition of the European samples. Thus, the distance I-FOR is particularly large in these mandibles as a consequence of the backward position of the foramen and, perhaps, the enlargement of the anterior part of the mandible, directly related to the expansion of the anterior dentition. Mauer, once again, shares with the European Middle Pleistocene samples a feature directly related to the so-called Neandertal apomorphies, and is like- wise conspicuously different from the African Middle Pleistocene samples. Finally, the Tighenif sample also shows a large I-FOR distance but this is a direct consequence of the large size of these mandibles.

DENTAL TRAITS

Table 2 presents the values of the expression (2), the ADR values, as well as the values of the WF

shape distance. The results of this last analysis indicates that the neandertals sample is the nearest to the Mauer mandible, followed by the modern h u m a n sample, Tighenif 3 and the Atapuerca-SH hominids. Other specimens and samples, especially Dmanisi and ER 992, are long- distanced from Mauer. The correlation index between the ADR values for all Si and the values for each Xi in these Si are also shown in table 2. In all cases, except for the BL dimension of the LI2 and LM1 the null hypothesis H0:r=0 is rejected.

In the whole dental sample the r values are very high for the MD dimensions, and changes in shape of some specimens and samples with regard to our reference are not expected. The r values for the BL dimensions are somewhat lower than those obtained with the MD dimensions. For this reason, further analyses are based only on the BL dimensions.

The analysis of the BL dimension of the LI2 offers clear results (Fig. 5a). In relation to Mauer, most specimens and samples are placed in two distinct regions of the bivariate morphological space. On the one hand, the specimens OH 7, KNM ER 992, and Dmanisi, as well as the Zhoukoudian sample crowd together round a line parallel, considerably distant and on the left of the X=Y line. On the other, the neander ta l s and Atapuerca-SH samples, as well as WT 15000 approach the X=Y line. Finally, Tighenif 3 and the modern human sample are located halfway between these two groups.

Figure 5b shows the results for the analysis of the BL dimension of the LC. The Atapuerca-SH and neandertals samples are near the X=Y line, whereas the Zhoukoudian and modern h u m a n samples, as well as OH 7, ER 992 and WT 15000 are located in a line parallel and on the left of the X=Y line. Dmanisi is also placed on the left of the X=Y line, but it is considerably far ther from this line.

Figures 6a and b present the results of the analysis of the BL dimension of the LP3 and LP4 res- pectively. It is remarkable tha t the Mauer mandible and the neandertal sample show a similar situation for the relative BL dimensions of both premolars. For the LP3, we ought to pay attention to the position of OH 7, on the left and far from the X=Y line, and the position of ER 992, on the right and also far from the X=Y line. Other specimens and samples are on the right side and not far from this line. For the LP4, the Atapuerca-SH hominids, as well as OH 7, WT 15000, and the modern sample are near the X=Y line, whereas Dmanisi, Tighenif 3, the Zhoukoudian sample, and especially ER 992 are on the right and far from this line.

1.1 1.11

1.09

1.06.

1.04.

1,01 -

.99.

693

1.05-

1.03-

• 1,07 DMA / '

992 • 1,05-

• • ; a - - l O ~ o 1,02-

oTG3 ~ S H 1

.97 J MAU

• NEA .95-

: , X , . . . . . . . . • .92 i .9

.95 .97 1 1,02 I..05 1.07 AVERAGE DENTAL RATIO

• C A N

.96 , .9 ,92 ., 1.08

t " • DMA . ~

I

2HO ~ ASH

992 • e J O N E A

. ~ • TGa

.93 i 1.03 1.05 AVERAGE DENTAL RATIO

FIGURE 5 - Bivariate scar te rgram showing the position of the different specimens and samples with respect to Mauer for the BL dimension of the I2 (left) and the BL dimension of the canine (right). See text for fur ther discussion. ASH: Atapuerca-SH; CAN: Aboriginals from Gran Canar ia (Canary Islands); DMA: Dmanisi; MAU: Mauer; NEA: Neandertals ; TG3: Tighenif 3; ~HO: Zhoukoudian. Diagramme de dispersion des diffgrents spdcimens par rapport & Mauer pour la dimension BL de I2 (gauche) et de la canine (droite).

1,08 1

l°°I 1.04 1

1.02-1

1 ~ N E A .98 ,

.g6-

,o4.

.g2- j ,9= Qgg2

.88 9' ' ' ' ', ' i ' ' ,9 . 3 .95 .98 1 1 03 1 05 1.08

AVERAGE DENTAL RATIO

1 E

.98

.95-

.93 •

.9 .9

oASH• ~ N

NA~,/ • DMA • TG3

Y . ' F . . . . i ' i ' ' .93 95 ,98 1 1 03 1 05 1.08

AVERAGE DENTAL RATIO

FIGURE 6 - Bivar ia te scar t te rgram showing the position of the different specimens and samples with respect to Mauer for the BL dimension of the P3 (left) and the BL dimension of the P4(right). See text for fur ther discussion. ASH: Atapuerca-SH; CAN: Aboriginals from Gran Canar ia (Canary Islands); DMA: Dmanisi; MAU: Mauer; NEA: Neandertals ; TG3: Tighenif 3; ZHO: Zhoukoudian. Diagramme de dispersion des diffdrents spgcimens par rapport & Mauer pour la dimension BL de P3 (gauche) et de P4 (droite).

The analysis of the BL dimension of the LM1 gives interesting results (Fig. 7a). The place of the OH7, KNM ER 992, and KNM WT 15000 specimens indicates a relative smaller BL dimension of the LM1 in these fossils in relation to Mauer. In contrast, Dmanisi and the modern human samples exhibit a relative large BL diameter of the LM1. The neandertals, Atapuerca-SH, and Zhoukoudian samples, as well as Tighenif 3 are near the X=Y line. With regard to the LM2, no clear trends are observed for the BL dimension in our analysis (Fig. 7b). In this case, the Mauer mandible shows remarkable diffe- rences with regard to the Atapuerca-SH hominids and the neandertals.

Concerning morphology, the dental t rai ts of the Mauer mandible are similar to those of other European Middle and early Upper Pleistocene hominids (Bermfidez de Castro 1988). The morphology of the P3 is particularly attractive. This premolar exhibits a great morphological variability of both the crown and root (Wood et al. 1988; Tobias 1991). In Mauer, the crown of the P3 is relatively symmetrical in comparison with H. habilis s.s., H. ergaster, Asian H. erectus, and specimens such as those of Tighenif and Rabat. Furthermore, the crown of the Mauer P3 shows a small, inflated, and centrally positioned lingual cusp. This tooth presents a single root, and lacks

694

1.03-

1.01

.9g- g •

.97-

.95

.93 .9

992

o° NAR / MAU

~E) TM

2.A I I I I ' I I

,93 .95 98 1 1.03 1 05 AVERAGE DENTAL RATIO

CN~

I

1.08

1,1

1.07

1.05-

~ 1.02- ~a

1

.97

.95-

,92 .9

ASH

NAR • N E A J

~ MAU

I I I I I I I

.93 .95 .98 1 1.03 1.05 1.08 AVERAGE DENTAL RATIO

FIGURE 7 - Bivariate scartergram showing the position of the different specimens and samples with respect to Mauer for the BL dimension of the M1 (left) and the BL dimension of the M2 (right). See text for further discussion. ASH: Atapuerca-SH; CAN: Aboriginals from Gran Canaria (Canary Islands); DMA: Dmanisi; MAU: Mauer; NEA: Neandertals; TG3: Tighenif 3; ZHO: Zhoukoudian. Diagramme de dispersion des diffdrents sp@cimens par rapport it Mauer pour la dimension BL de M1 (gauche) et de M2 (droite).

a buccal cingulum, which is also absent in the other postcanine teeth. In terms of these traits, the P3 of Mauer exhibits a morphology tha t can be considered characteristic of fossils such as Pontnewydd, Atapuerca-SH, Lezetxiki, Ehrins- dorf, Krapina, and Hortus.

DISCUSSION

The morphology of the Mauer mandible is gene- rally perceived as primitive, mainly because of its large ramus breadth and heavy appearance. The performed analysis have put into evidence, however, tha t Mauer may confidently be classified together with the European Middle Pleistocene samples. It was Howell (1960) who first recognised a significant difference between Mauer and other Middle Pleistocene samples from China and North Africa. Later on, Aguirre & de Lumley (1978) and Rosas (1987) also identified a close similarity of Mauer and other European specimens such as Arago II and XIII, and Atapuerca 1, but no "neandertal" derived traits were identified. In relation to that, the peculiar morphology of Mauer have offered some doubts about grouping this specimens together with other younger Mid- Pleistocene samples from Europe (Wolpoff 1980; Cook et al. 1982). The present analysis demons- trates tha t the Mauer mandible exhibits a set of characteristics which are the structural basis on which neandertal apomorphies will eventually be fully developed.

In relation to that, the Mauer mandible illus- trates how the evolutionary process tha t gives rise to neandertals was accomplished in several steps. Thus, the backward displacement of the

ramus during the evolution of the European Middle Pleistonece populations has taken place, firstly by displacing the anatomical structures of the ramus, and, in a second place, by the remodel- ling of the anterior border of the ramus. A major structural change of the mandible occurs before other more superficial processes defines the final morphology of the classic neandertals. Bearing in mind this twofold process, the structural basis of the neandertal mandible may be recognised from the early stages of the evolutionary process. The development of retromolar space as well as the position of the mental foramen must be unders- tood on this basis. Tr inkaus (1993), and Franciscus & Trinkaus (1995) have recently poin- ted out the mere presence of these features may be not a proper Neandertal apomorphy. Conve- rsely, a mandible, like Mauer, without the classic expression of the above mentioned features may display the complete morphological background of the neandertals.

The situation of the Mauer mandible with regard to the relative BL dimension of the LI2 is shared by the Atapuerca-SH and neandertal samples, as well as by WT 15000. The results reflect a fact lengthily discussed by Wolpoff (e.g. 1979 1980). This author suggested that an increase of the anterior dentition size, as measured by transverse breadth, characte- rised the evolution of the European Middle Pleistocene populations, and that this increase continued at least during the early Upper Pleistocene. It is noteworthy that the Nariokotome specimen exhibits the same situation. This may be either an individual variation within an African Lower Pleistocene population, or the expression of the above mentioned trend in the late H. ergaster.

695

ASH NEA WT 15.000 CAN ZHO TG3 DMA OH7 ER 992 R

MD 0.976 0.969 0.887 1.041 0.962 0.976 0.984 0.900 0.947 0.86* I2

BL 1.027 0.987 0.968 i.i00 1.054 1.026 1.077 1.020 1.054 0.39

MD 0.993 0.980 0.921 1.070 0.938 0.987 0.938 0.927 0.899 0.86* C

BL 1.023 0.994 0.968 1.084 0.994 0.932 1.046 0.942 0.983 0.81"

MD 1.012 1.012 0.936 1.087 0.970 0.958 0.953 0.895 0.936 0.97* P3

BL 1.005 1.000 0.923 1.071 0.957 0.937 0.962 0.942 0.891 0.86*

MD 1.020 0.987 0.909 1.034 0.914 0.955 0.955 0.806 0.931 0.93* P4

BL 1.034 1.005 0.953 1.051 0.934 0.948 0.963 0.924 0.906 0.90*

MD 1.017 0.991 0.954 1.017 0.951 0.966 0.943 0.878 0.987 0.85* M1

BL 1.032 1.009 1.004 1.023 0.965 0.965 0.937 0.949 1.023 0.57

MD 1.072 1.032 0.992 1.081 1.008 1.004 1.016 0.897 0.980 0.92* M2

BL 1.081 1.039 1.008 1.076 0.996 0.992 1.004 0.941 0.979 0.91"

ADR 1.024 1.000 0.952 1.061 0.970 0.971 0.982 0.918 0.960

TABLE 3 -Values of the expression MAU X j/((MAU Xj+S j X j)1/2), where MAU: Mauer; S j: ASH=Atapuerca-Sima de los Huesos; NEA= Neanderta ls ; WT 15.000; CAN= Aboriginals frmn Gran Canaria, Canary Islands; ZHO= Zhoukoudian; TG 3= Tighenif 3; DMA=Dmanisi; OH 7; KNM ER 992. ADR: Average Dental Ratio (see text); F: WF shape distance (see text). ADR and F for the mesiodistal (MD) and buccolingual (BL) dimensions of all teeth (12 variables). R: Correlation index between the ADR values for each S j and the values for each variable in these Sj (explication p. 690.

The modern human populations may have expe- rienced either an increase of the anterior teeth starting from a situation similar to that of early Homo and H. erectus, or a secondary reduction from a situation similar to that specimens such as WT 15000. Furthermore, the situation of the Mauer specimen for the relative BL dimension of the LC is shared only for the Atapuerca-SH hominids and the neandertals. It also reflects, although to a lesser degree, the above mentioned trend toward the expansion of the anterior dentition. In this case, WT 15000 has a LC proportionally lesser than that of the Mauer mandible.

The interpretat ion of the relative size of the Mauer mandibular premolars is complicated. The LP3 and LP4 of this specimen are relatively nar- row.as in H. habilis s.s. In contrast, the mandibular premolars of other Lower and Middle Pleistocene hominids are relatively broader than those of Mauer. From the evidence offered by other European Middle Pleistocene hominid samples, such as Arago and Abri Suard, we consider tha t the Mauer mandible shares with the neandertals a secondary reduction of the BL dimensions of the mandibular premolars.

As far as the relative BL dimension of the LM1 is concerned, the Middle Pleistocene hominids and the neandertals do not show significant depar- tures from the Mauer situation. It is not the same with other hominids. Thus, the BL narrowness of the mandibular molars in H. habilis s.s. has been noted by different authors (e.g. Wood 1992a). This

t ra i t is also observed in the African Lower Pleistocene specimens ER 992 and WT 15000. In a previous paper, we have discussed the big relative size of the LM1 in Dmanisi. We consider tha t this trai t probably represent an individual variation, which contributes decisively to the MI>M2 size sequence for the crown area observed in the Georgian specimen. Finally, we believe tha t the relative large BL dimension of the LM1 in modern humans represents a particular retention of the size of this tooth within the general reduction of all teeth.

The Mauer mandible is the holotype ofH. heidelbergensis, a species which in the Rightmire (1996)'s concept encloses an Afro-European Middle Pleistocene hypodigm supposedly representing the last common ancestor to modern humans and neandertals. The identification of neandertal apomorphies in the European Middle Pleistocene samples, nevertheless, is weakening the concept of H. heidelbergensis as the common ancestor of modern humans and neander ta ls (Stringer 1996). In this line, we do consider tha t the Mauer mandible cannot be the holotype of the of neandertals and modern humans common ancestral species. The fact of classifying Mauer together with other European Middle Pleistocene samples in which neandertal derived traits have been identified clearly inval idate the Afro- European concept. As mentioned, Mauer shows some of the morphological specialisation which defines the European lineage.

696

R e c e n t l y , s o m e a u t h o r s t e n d to u n i t e M i d d l e P l e i s t o c e n e h o m i n i d s f r o m E u r o p e a n d n e a n d e r - t a l s u n d e r t h e s a m e t a x o n o m i c n a m e H. neanderthalensis (STRINGER, 1996). To o u r view, a s s i g n i n g b o t h c l a s s i c n e a n d e r t a l s a n d E u r o p e a n M i d d l e P l e i s t o c e n e fo s s i l s to t h e s a m e s p e c i e s m a y gene - r a t e a l a r g e a m o u n t of con fus ion . F r o m a m o r p h o - l o g i c a l p o i n t of v iew, c l a s s i c n e a n d e r t a l s a n d M i d d l e P l e i s t o c e n e h o m i n i d s s e e m s u f f i c i e n t l y d i f f e r e n t to be d i s t i n g u i s h e d w i t h a d i f f e r e n t n o m e m . H. heidelbergensis s h o u l d b e e m p l o y e d to n a m e t h o s e E u r o p e a n M i d d l e P l e i s t o c e n e p o p u l a - t i o n s s h o w i n g a c o m b i n a t i o n of p r i m i t i v e t r a i t s a n d s o m e of t h e c l a s s i c n e a n d e r t a l a p o m o r p h i e s . T h e n a m e H. heidelbergensis m i g h t b e r e t a i n e d to d e n o t e a M i d d l e P l e i s t o c e n e c h r o n o s p e c i e s of t h e e u r o p e a n - n e a n d e r t a l l i n e a g e .

A c k n o w l e d g e m e n t s - We thank to Profs. H. and M.A. de Lumley for the easy access to the originals of Arago and their cast collection at the Laboratoire d'Anthropologie at the University of Aix-en-Provence (Marseille, France). We would like to thank Elena Nicolas and Emiliano Aguirre for their com- ments and discussion. We are also grateful to J.J. Hublin and the editorial board of the journal for their useful suggestions on the manuscript. This study was supported by a research grant from the Spanish Government (DICICYT PB 96-1026-C03-02 and Unidad Asociata Atapuerca).

R E F E R E N C E S

AGUIRRE E. & DE LUMLEY M.A. 1978 - Fossil man from Atapuerca , Spain: the i r bea r ing on h u m a n evolution in t he Midd le Ple is tocene . Journal of Human Evolution, 6: 681-738.

ANDREWS P. 1984 - An a l t e rna t ive in te rp re ta t ion of cha- rac te rs used to define Homo erectus. Courier Fors- chungs-Institut Senckenberg, 69: 167-175.

BERMtJDEZ DE CASTRO J.M. 1985 - La Denticihn de los Pobladores Prehis thr icos de las Is las Canar ias : estu- dio Antropolhgico. Ph. D. Thesis . U n i v e r s i d a d Complutense de Madr id (unpublished).

BERMI:IDEZ DE CASTRO J.M. 1988 - Denta l r emains from Atapuerca / Ibeas (Spain) II. Morphology. Journal of Human Evolution, 17: 279-304.

BERMf2DEZ DE CASTRO J.M. 1993 - The Atapue rca denta l remains . New evidence (1987-1991 excavations) and in te rpre ta t ions . Journal of Human Evolution, 24: 339-371.

BERMI~DEZ DE CASTRO J.M., ARSUAGA J.L., CARBONELL E., ROSAS A., MARTfNEZ I. & MOSQUERA M. 1997 - A horn- nid from the Lower Pleistocene of Atapuerca , Spain: Poss ib le Ances to r to N e a n d e r t a l s and Modern Humans . Science, 276: 1392-1395.

BORGOGNINI S.M. 1983 - A N e a n d e r t h a l lower molar from Fondo Ca t t i e (Magglie, Lecce). Journal of Human Evolution, 12: 383-401.

BROMAGE T.G., SCHRENK F. & ZONNEVEL F.W. 1995 - Paleoanthropology of the Malawi Rift: An early hominid mandible from the Chiwondo Beds, nor thern Malawi. Journal of Human Evolution, 28: 71-108.

BROWN B. & WALKER A. 1993 - The dent i t ion. In A. WALKER & R. LEAKEY (eds), The Nariokotome Homo erectus Skeleton: 161-192. H a r v a r d Univers i ty Press, Cambridge.

CARBONELL E., BERMI:IDEZ DE CASTRO J.M., ARSUAGA J.L., DIEZ C., ROSAS A., CUENCA-BEscos G., SALA R., MOSQUEBA M. • RODRIGUEZ X.P. 1995 - Lower Pleis- tocene hominids and ar tefac ts from Atapuerca-TD6 (Spain). Science 269: 826-829.

CONDEMI S. 1991 - Some considerat ions concerning Neander ta l features and the presence of Neander ta l s in the Near East . Rivista di Antropologia, 69: 27-38.

COOK J., STRINGER C.B., CURRANT A.P. & SCHWARCZ H.P. 1982 - A review of the chronology of the european Middle Pleis tocene Hominid record. YearBook of Physical Anthropology, 25: 19-65.

FRANCISCUS R.G. & TRINKAUS E. 1995 - Determinants of the retromolar space in Pleistocene Homo mandibles. Journal of Human Evolution, 28: 577-595.

GABUNIA L. & VEKUA A.K. 1995 - A Plio-Pleis tocene hominid from Dmanis i , Eas t Georgia, Caucasus. Nature, 373: 509-512.

HOWELL F.C. 1960 - European and Nor thwes t African Middle Pleis tocene hominids. Current Anthropology, 1: 195-232.

HUANG W., Gu Y., CIOCHON R., LARICK R., QIREN F., DE Vos J., SCmVARCZ H., RINK W. & YONGE C. 1995 - Ear ly Homo and associa ted ar tefac ts from Asia. Nature, 378: 275-278.

JACOB T. 1973 - Paleoanthropological discoveries in Indonesia wi th special reference to the finds of the las t two decades. Journal of Human Evolution, 2: 473-485.

LEAKEY R.E.F. & WOOD B.A. 1973 - New evidence for the genus Homo from Eas t Rudolf, Kenya (II). American Journal of Physical Anthropology, 39: 355-368.

LEAKEY R.E.F., LEAKEY M.G. & BEHERENSMEYER A.K. 1978 - The hominid catalogue. In M.G. LEAKEY & M.E. LEAKE¥ (eds), Koobi Fora Research Project, Volume 1: The Fossil Hominids and an Introduction to Their Context 1968-1974: 86-182. Clarendon Press, Oxford.

LEFEVRE J. 1973 - E tude odontologique des hommes de Muge. Bulletin et Mgmoire de la Socigtg d' Anthro- pologie de Paris, 12: 301-333.

LERoI-GoURHAN A. 1958 - E tude des res tes huma ins fossiles p rovenan t des grot tes d 'Arcy-Sur-Cure. Annales de Paldontologie, 44: 87-148.

LUMLEY M.A. de 1973 - Ant~n~ander ta l i ens et N~ander- ta l iens du Bass in M~di ter ran~en Occidental Euro- p~en. Etudes du Quaternaire, M~m. 2.

RIGHTMIRE G.P. 1980 - Middle Pleis tocene hominids from Olduvai Gorge, Nor the rn Tanzania . Amer ican Jour- nal of Physical Anthropology, 53: 225-241.

RIGHTMIRE G.P. 1990 - The evolution of Homo erectus. Univers i ty Press: Cambridge.

RIGHTMIRE G.P. 1996 - The h u m a n c ran ium from Bodo, Ethiopia: evidence for spec ia t ion in the Middle Pleistocene? Journal of Human Evolution, 31: 21-39.

RosAS A. 1987 - Two new m a n d i b u l a r f r agmen t s from Atapuerca / Ibeas (SH site). A r e - a s se s smen t of the affinities of the Ibeas mandib les sample. Journal of Human Evolution, 16: 417-427.

697

ROSAS A. 1995 - 17 New Mandibu la r specimens from the Atapuerca / Ibeas Middle Pleis tocene Hominids sample (1985-1992). Journal of Human Evolution, 28: 533-559.

ROSAS A. 1997 - A gradient of size and shape for the Atapuerca sample and Middle Pleistocene hominids variability. Journal of Human Evolution, 30:

RosAs A. & BERMIJDEZ DE CASTRO J.M. (submitted) - About the taxonomic affinities of the Dmanisi mandible (Georgia). American Journal of Physical Anthro- pology.

SAUSSE F. 1975 - Mandibule de la carri~re Thomas I (Casablanca). L'Anthropologie, 79: 81-112.

SCHOETENSACK O. 1908 - Der Unterkiefer des Homo heidelbergensis aus den Sanden yon Mauer bei Heide- lberg. Leipzig: W. Engelmann.

STRINGER C.B. 1984 - The definition of Homo erectus and the existence of the species in Africa and Europe. Courier Forschungs-Institut Senckenberg, 69: 131- 143.

STRINGER C.B. 1993 - New views on modern humans origins. In D.T. RASMUSSEN (ed.), The Origin and Evolu- tion of Humans and Humanness: 75-94. Jones and Bartlett : Boston.

STRINGER C.B. 1996 - Current issues in Modern H u m a n Origins. In W.E, MEIKLE F.C., HOWELL & N.G. JABLONSKI (eds), Contemporary Issues in Human Evo- lution. Memoir 21 California Academy of Sciences.

STRINGER C.B., HUBLIN J.J. & VANDERMEERSCH B. 1984 - The origin of anatomical ly modern humans in wes- te rn Europe. In The Origins of Modern Humans: A World Survey of the Fossil Evidence. Alan R. Liss, Inc. N.Y.: 51-135.

TATERSALL I. 1986 - Species recognition in human paleon- tology. Journal of Human Evolution, 15: 165-175.

TATERSALL I. 1992 - Species concepts and specis identifi- cat ion in h u m a n evolution. Journal of Human Evolution, 22: 341-349.

THOMA A. & VALLOIS H.V. 1977 - Les dents de l 'homme de Rabat. Bulletin et Mdmoires de la Societd d'Anthro- pologie de Paris,, 13: 31-58.

TILLIER A.M. 1979 - La dent i t ion de l 'enfant moust~rian Cha teauneu f 2 d~couvert ~ l 'Abri de Hauteroche (Charente). L'Anthropologie, 83: 417-438.

TOBL~S P.V. 1991 - Olduvai Gorge. Vol 4. The skulls, endocasts and teeth of Homo habilis. Cambridge Uni- versity Press: Cambridge.

TRINKAUS E. 1978 - Dental r emains from the Shan ida r Adult Neanderthals . Journal of Human Evolution, 7: 369-382.

TRINKAUS E. 1993 - Variabili ty in the position of the mand ibu la r menta l foramen and the identif icat ion of Neander ta l apomorphies. Rivista de Anthropologia, 71: 259-274.

VALLOIS H.V. 1952 - Les restes huma i ns du gisement Moust~rien de Monsempron. Annales de Paldonto- logie, 38: 100-120.

VLCEK E. 1969 - Neandertaler der Tschechoslowakei. Prague. Prague: Verlag der Tschechoslowakischen Akademiae der Wissenshaften.

WOLPOFF M.H. 1975 - Some aspects of h u m a n mandibular evolution. In J.A. McNAMARA (ed.), Determinants of Mandibular Form and Growth, 61 p. Ann Arbor, Michigan.

WOLPOFE M.H. 1971 - Metric Trends in Hominid Dental Evolution. Case Western Reserve Univers i ty Studies in Anthropology 2.

WOLPOFF M.H. 1979 - The Krapina dental remains. Ameri- can Journal of Physical Anthropology, 50: 67-114.

WOLPOFF M.H. 1980 - Paleoanthropology. New York: Alfred K. Knopf.

WOOD B.A. 1984 - Taxonomy a n d evolut ionary relationships of Homo erectus. Courier Forschungs-Institut Senckenberg, 171: 159-165. :.

WOOD B.A. 1992a - Origin and evolution of the genus Homo. Nature, 355: 783-790.

WOOD B 1992b - Early hominid species and speciation. Journal of Human Evolution, 22: 351-365.

WOOD B.A., ABBOTT S.A. & UYTTERSCHAUT H. 1988 - Analysis of the denta l morphology o f Plio-Pleisto- cene hominids IV. Mandibu la r postcanine morphology. Journal of Anatomy, 156: 107-139.

Ao ROSAS & J.M. B E R M ~ D E Z :DE CASTRO Departamento de Paleobiologla

Museo Nacional de Ciencias Naturales, CSIC Jos~ Gutierrez Abascal 2

E-28008 Madrid

the mauer mandible and the evolutionary significance of homo heidelbergensis

Documents