Selective Pressures and Dental Evolution in Hominids PATRICIA SMITH Laboratory of Physical Anthropology, Department of Anatomy and Embryology, Hebrew University Hadassah Schools of Medicine and Dental Medicine, Hadassah P.O.B. I 1 72 Jerusalem, Israel

KEY WORDS Dentition . Evolution Neanderthal - Upper Paleolithic Attrition . Selection

ABSTRACT Inter-group differences in tooth size and attrition scores in fossil hominids from the late Riss, Wurm 1-11 and Wurm 111-IV were compared to determine: (1) the extent and timing of reduction in tooth size; (2) the relation of such reduction to decreased functional demands made on the dentition, as esti- mated by the severity of attrition. The largest reduction in tooth size was found to take place between the Riss and Wurm 1-11 groups, and to affect anterior teeth as well as posterior teeth. It is suggested that the differences between these con- clusions and those reached by Brace ('67) are a function of the samples used. Similarly the observed reduction in tooth size was not associated with any con- comitant reduction in functional demands made on the dentition, but appears to have outstripped them, as demonstrated by the increased severity of attrition found in the later smaller-toothed groups.

Reduction in tooth size is one of many trends characteristic of hominid evolution (LeGros Clark, '64) and generally attributed to the relaxation of selective pressures favor- ing large teeth as functional demands made on the dentition decreased. The presumed re- duction in functional demands has been at- tributed to dietary change and improved tool technology, the latter acting directly by sub- suming functions previously carried out by the teeth, as well as indirectly, through per- mitting a wider choice of foodstuffs. For Dahlberg ('63) this trend was well under way in the Middle Pleistocene, and accelerated by the introduction of fire which provided another method of altering the physical con- sistency of food utilized. Brace ('67) and Brose and Walpoff ('71) have on the contrary pro- posed that selective pressures favoring large anterior teeth remained high until a much later time. Brace ('67: p. 814) writes that Neanderthal incisors "were used for more than just eating" He suggests that during this period, but especially in the Upper Paleolithic "a variety of specialised tools ap- peared which reduced the hitherto increasing- ly important manipulative role played by the front teeth" (p. 815).

AM. J. PHYS. ANTHROP., 47: 453-458.

This hypothesis was based on calculation of anterior teeth area in specimens from Choukoutien, Krapina, and PPedmost. Using these specimens as representative of Homo erectus, Homo neanderthalensis and Upper Paleolithic Homo sapiens, Brace ('67) found no reduction in tooth area between the first two, but a big decrease in tooth size between Homo neanderthalensis and Upper Paleolithic Homo sapiens.

However, although a study was undertaken by Brose and Walpoff ('71) to examine the as- sociation between tooth size and tool types, no attention has been given to ascertaining a re- lationship between temporal trends in tooth size and functional demands made on the den- tition. These vary with the abrasive nature of the diet or other non-dietary activities involv- ing the teeth (Smith, '72; Molnar, '72). The severity of the resultant attrition is then dependent on age, tooth size and hardness. The attrition can be graded to provide an esti- mate of the severity of functional demands, which are excessive when so severe that the crown of the tooth is completely worn down and the pulp chamber exposed, resulting in dental abscess formation and tooth loss (fig. 1).

453

454 PATRICIA SMITH

Fig 1 Periapical abscess resulting from infection of the dental pulp, expmed by attrition

In the present study I have compared tooth size and attrition scores in fossil horninids from Riss. Wurm 1-11 and Wurm 111-IV sites to determine (1) the differences present in tooth size between the three groups and so the ext,ent and timing of t,erriporal trends in i ts re- duction, and (%) the relationship of the ob. served decrease in tooth size to the reduction of functional demands made on the teeth as shown by attrition scores.

MATERLALS AND METHODS

For this st,udy I examined the jaws and teeth of 105 fossil horninids from Arago, Lazaret, Malarnaud, Montmaurin, Krapina, Tabun, Amud, Skhul, Quafzeh, Gibraltar, Sac- copastore, Hortus, La E'errasie, La Quina, Spy, Engis, La Chapelle aux Saints, Marillac, Combe-Grenal, Monsempron, Ein Gev, Ha- dera, Cro-Magnon, Grimaldi, Isturitz, Farin- court, La Madelaine and Espugo.

All teeth were scored for degree of attrition. using a &point scale for varying degrees of severity. I then measured the niesiodistal and buccolingual diamet,ers of all t,eet.h graded through 1-3, i.e., unworn to moderately worn, and recorded the locality and, where possible, the etiology of dental abscesses and missing t,eeth. When the teeth were present in the socket,, the differential diagnosis of abscesses (trauma, periodont.al disease, caries or attr i- tion) was simple. For the etiology of missing teeth, in addition to the possibilities con- sidered above, must be added impacted or con- genitally missing teeth. For these identifica- tions, I relied on the condition of the adjacent teeth. Thus, in jaws where the teet,h present were healthy, the absence of t,hird molars, sec ond premolars or lower central incisors is

most probably congenital, as for exilmple, 111

the child from Gibraltar and Malarnaiid When the adjacent ttxeth are severely worn, but caiies free and there is little periodontal diseaw (ns in the adult spc'cim Gibraltar) then attrition may tic assumed to be the probable cause of tooth loss

To this sample 1 added published data on 46 specimens from Eh ririgsdorf (Srh walbc, '1 ?), Mauer and Stemhelm (Howell, ' G O ) , Shanidar (Stewart, '58. '61, '63) Circeo (Sergi, '64 arid Sergi and Ascemi, '56), Arcy-sur Cure ( 1 , c w ) i

Gouhran, '58), T x Moustier (Dieck, '231, .Jersey (Keith and Knowles, '1 l),Orhoz and Sipka (VIPck, '691, Subalyuk (Szabo, '361, Kulna (Jelinek, '67), Chanctxladc ('tallois, '461, Roc de Sers (Martin, '27), S t Gerniain (Blanchard e t al., '721, Briiniquel (Gcnct Var ciir and Miquel, '671, Predrnost (Matiegka, '34) and Dolni Vestonice (Jelinek, '53)

All specimens were classified by period :is Riss and Riss Wurm, Wurm I and TI, or Wurm IT1 and I V , using the clnbsifiration adopttd 1)y Oakley r t a1 ('71, '75) The only exception wnh Krapina, whirh, i n V I V W of the controversy burrounding the precise age of the skeletal re mains, I classified on morphological gruiinds a s Riss-Wurm (Smith, '77) Ttie mean va1ui.s of nwsiodistal and buccolingual diameters of teeth from specimens in rach period were computed and compared using one way analy- sis of variance (ANOVA MIDAS statistical package, University of Tvfichigan)

Since the severity of attrition is age depen- dent (Miles, 'ti3, Smith, '72), I calrulated mean attrition scores using adult specimens only to reduce the possibility of agr' dif fwences of specimens influciiring at Lrition scores h r t t i e r subdivisions of age w t w r i o t

SE1,ECTIVE PRESSURES AND DENTAL EVOLUTION 455

attempted since most estimates of age in adult fossils do not, appear to show marked in- tersite differences (Vallois, '37, '60). I further calculated the number and percent,age of adults with missing teeth.

RESULTS

The mean values calculated for teeth mea- surements arc! given in table l. They show re- duction in size through time for both dimen- sions of all teeth, with most of the reduction taking place between the Riss and Wurm 1-11 groups. That is, teeth in the "Neanderthal" gronp resemble those of the Upper Paleolithic Wiirin 111-IV more than they resemble the earlier Riss and Kiss- Wurm Iiominidx. The validity of the statistically significant dif-

ferences found, listed in the same table, is limited, especially for the anterior teeth, by the small size of the Riss sample. On the other hand, since the individual teeth measure- ments rather than the sum total of the entire tooth row, were used, I was able to utilize teeth from specimens in which only some teeth were suitable for measuring. This ac- counts for the differences in number of mea- surements taken on the various teeth.

The mean attrition scores show an inverse correlation with tooth size. They are low in the Riss group, escalate in the Wurm 1-11 group and remain high in the Wurm 111-IV sample. In all periods attrition is more severe in the anterior teeth than in the posterior teeth (figs. 2, 3). The percentage of individ-

T4BLE 1

blfsto~lzst~il und huccoliriguul diurnetfrs of teeth by period

M? M2 M1 Pm2

No x S D No Y S1) No x SD No X SD Perlld

Mandl ble 13 1277" 1 0 24 1 1 4 5 0 8 18 1 1 33 0 8 I1 1163 O H 23 1091 0 7 18 1108 0 8

Maxilla 8 1102 L O

LO 1069 O H 12 1033 0 8 H 12 3.1 0 t i

21 1239 0 8 12 1229 0 8

H I M Wiirol 1 I I Wurm 111 I V H i w W u r i n I 11 Wurni LJI-IV

13 12 44 ' I 0 2fi 11 60 n 7 18 11 1 3 ' 1 0 1% 11 13 O R 26 11) 79 0 9 18 109'3 O H

19 12.28 I 0.8

21 11 75 0.8 32 11.75 0.9

17 11.43 1.0 30 11.13 0.7 22 11.13 0.6

13 8.07 0.5 MD 25 7.55 0.6 16 7.44 0.5 12 9.62 l P 0.8 BL 25 9.103 0.7 15 8.58 0.4

RIBS Wurm 1 I1 Wurm 111 IV It188

Wurni I 11 Wurrn 111 JV

10 10.35 2.0 14 9 53 0.7 H 9 6 5 1 0

10 1204 1 6 15 11.98 0 9 A 11 89 09

8 1183'z 1 0 27 11 23 0 6

8 1202 0 5 2% 12 16 0 7 13 1231 0 5

13 in80 0 7

15 8.07 0.8 MD 19 7.18 0.5 7 7.08 0.5

15 10.70 0.7 BL 21 10.23 0.6 9 9.75 0.5

F m l 12 I1

No x SI) X SD No x SIJ

Maiidi ble 12 801' 0 6 22 7 9 2 ' O R 12 722 ( 1 8 11 868 0 7 21 8 5 4 0 8 12 8 5 0 0 8

Maxil la 8 911" 0 6

23 R3HJ 0 4 11 781 0 6 7 1O17I2 0 6

23 9 4 1 ' 0 7 11 8 7 3 0 6

Rlsn Wurn4 i 11 W u m i 111 I V R I S Y

Wurni I 11 Wurm I11 1V

15 8-52 I 2 0.6 23 7.7J 0.4 1% 7.34 0.5 15 9.27 0.2 23 8.91' 0.7 12 8.40 0.4

5 6.93 0.5 17 6.60 0.5 1'7 6.58 0.5 4 7.90 0.6

19 7.44 3 0.6 20 6.97 0.4

2 14 10 3

15 14

6.2 0.1 MD 5.76 0.6 5.75 0.6

6.90 0.4 6.39 0.4

7.93 1 2 0.1 BL

El49 Wiirm 1-11 Wurrn 111 1V Hiss Wurrn 1-11 Wurrn 111-IV

9 8.57 0.8 26 7.86 0.6 11 7.40 0.5 9 11.07 ' J 0.X

26 10.37 0.6 11 9.52 0.6

12 8.46' 0.6 15 8.05' 0.5 7 7.02 1.0

10 8.69 0.7 19 7.90 0.7 7 6.83 0.4

6 13 12 5

16 12

10.29 0.4 MI) 9.89 0.6 9.29 0.9 8.90 I 0.7 BL 8.14' 0.5 7.61 0.3

I 0' L>lg.jilii.ant ditfrrerwe p s: 0 5 txtncen Pin8 and Wurm 1 11. 'Significant diS1erenc.r p ' 0.5 Letween Risu nnd Wurm 111 IV.

Significant difSereni:e p .-: 0.5 twtwwn W ~ i v i n 1.11 and Wurni 111-IV

456 PATRICIA SMITH

M E A N A T T R I T I O N SCORES IN THE M A X I L L A

...... ...... ...... ...... ...... ...... ...... ...... ...... ........ 3 2m ........ ....... ......

....... ......... ........... ......... ........ ......... 1 *:::::: . . . , i I i i I i ............. ........... ............... ............ :::::: . , . . :::::: ....... :::::: .......... ............. ............. M'

...... ...... ...... ...... ...... ...... ...... ...... ...... ...... ...... ...... ...... ...... ...... ....... ......... ...... ...... ...... ........ ........... . . . ...... ......... ............ ....... ; . .; :::::: .................. :::::::, " ; : y; i:i:ii .j iijF ......... ............. .... ,:::::::: ................ ............ .......... .......... ... .: ...... .....

~ ............ M' M ' Pm' C

Fig. 2 Histogram of mean attrition scores in the maxillary teeth of adult specimens from the Riss Wurm Wurm 1-11 and Wurm Ill-IV.

M E A N ATTRITION SCORES I N T H E M A N D I B L E

Fig 3 Histogram of mean attrition scores in the mandibular teeth of adult specimens from the Riss Wurm Wurm 1-11 and Wurm 111-IV.

uals afflicted by periapical abscess formation and tooth loss, diagnosed as due to severe a t - trition, shows a similar increase throughout time (table 2). In addition, abscesses due to

periodontal disease were found in two Wurm 1-11 individuals, one from Marillac and one from Skhul. The Circeo 1 cranium is eden- tulous, with much alveolar resorption. Here

SELECTlVE PRESSURES AND DENTAL EVOLUTION 457

TAB1.E 2

Distribution ofspecimens with dental abscesses and ante mortem tooth loss in adult specimens examined

No. of adult No. with Nu wilh Period specimens examined abbcesseg looth loss

Kiss and Kiss Wurm 15 1 (6.7W 1 (6.7X) Wurm 1-11 50 11 (22%) 8 (16%) Wurm 111-IV 34 15 (44.1%) 8 (23.5%)

no attempt was made to diagnose the cause of booth loss and so the specimen was excluded from the calculations shown in table 2.

DISCIJSSION

This study incorporates new data from fossil hominids recently discovered (Hortus, Arago, Qafzeh, Ein Gev, Hadera, Tabun), so that the sample sizes used are larger than those used by earlier investigators. In mea- suring most of the specimens myself, and ex- cluding severely worn teeth from the calcu- lations, I have tried to minimize biases introduced by differences in measuring tech- niques as well as those due to measuring teeth of various stages of wear.

As the attrition scores show, teeth in the three periods show considerable differences in attrition scores, so that if measurements taken on severely worn teeth are used: a false value for tooth size would be obtained. Also, as previously stated, Krapina was excluded from the Wurm 1-11 sample. Using the groupings so defined, a continual trend towards reduction in tooth size was found for the three periods investigated. The difference between these results and those reached by Brace ('67) ap- pear to be due to his using Krapina as repre- sentative of the Wiirm 1-11 group, although they differ considerably from all the other known Wiirm 1-11 hominids (Smith, '77) and a t least some of the material may be late Riss (Oakley et al., '71). Jelinek ('76) also assigns the Krapina specimens to the Riss-Wiirm in- terglacial.

The observed reduction in tooth size re- corded here was not associated with reduction in functional demands made on the dentition as estimated by the severity of attrition. The increased frequency of dental abscesses and tooth loss caused by attrition in the Wiirm 1-11 and Wiirm 111-IV groups indicates that, on the contrary, the functional load born by these teeth was excessive in both these periods. I t seems that the trend towards reduction in

tooth size was well underway by the latter part of the Middle Pleistocene and was not af- fected by dietary differences a t this time. This suggests that teeth in the later smaller toothed groups were being used for the same purposes a s those of t h e la te Middle Pleistocene groups.

ACKNOWLEDGMENTS

This study was supported by grants from the Wenner-Gren Foundation and the Joint Research Fund of the Hebrew University- Hadassah School of Dental Medicine founded by the Alpha Omega Fraternity and the Hadassah Medical Organization. For assist- ance in the analysis of the data I am indebted to G. Walker and C. Kowalski, University of Michigan Dental School. For permission to ex- amine the specimens in their care I would like to thank L. Y. Rachmani, Rockefeller Museum, Jerusalem; I. Crnolatac, Norodne Museum, Zagreb; R. Gessain, Musee de L'Homme Paris; J. Piveteau, J. Lehmann and B. Vandermeersch, Faculte des Sciences, Uni- versite de Paris, Paris; L. Balout, Institut de Paleontologie Humaine, Paris; H. de Lumley and M. A. de Lumley, Faculte des Sciences, Universite de Marseilles, Marseilles; M. Bar- ral, Musee d'Anthropologie Prehistorique, Monaco; T. Molleson, Natural History Mu- seum, London, and F. Twiesselmann, Institut royal des Sciences naturelles de Belgique, In- stitut de Paleontologie, Universite de Liege.

LITERATURE CITED

Blanchard, R., D. Peyrony and H. V. Vallois 1972 Le gise- ment et le aquelette de Saint Germain La Riviere. Arch de l'institut de Palbnt. Humaine: Mem. 34, Masson et Cie, Paris.

Brace, C. L. 1967 Environment, tooth form and size in the Pleistocene. J. Dent. Res.. 46: 809-816.

Brose, D. S., and M. H. Wolpoff 1971 Early Upper Paleolithic Man and Late Middle Paleolithic Twls. Amer. Anthrop., 73: 1156-1194.

Coon, C. S. 1962 The Origin of Races. Arthur Knopf, New York.

458 PATRICIA SMITH

Dahlberg, A. A. 1963 Dental evolution and culture. Hum. Biol., 35: 237-249.

Diek, W. 1923 Das Gebiss des diluvialen Homo mous- teriensis Hauseri und seine Rekonstruktion. Odon- tologisk Tidskraft, 3: 196-209.

Genet-Varcin, E., and M. Miquel 1967 Contribution a I'etude du squelette magdalenien de 1'Abri Lafaye a Bru- niquel. Anthropologie, 71: 467-478.

Howell, F. C. 1960 European and Northwest African Middle Pleistocene Hominids. Current Anthropology, 1: 195-232.

HrdliEka, A. 1930 The skeletal remains of early man, Smithson. Misc. Collns, 83.

Jelinek, J. 1953 The fossil man of nolni Vgstonice Czekoslovakia Anthropozoikum (Prague), 3: 37-91.

1967 Der Fund eines Neandertaler Kiekers (Kulna 1) aus der Kulna-Hohle in Mahren. Anthropolo- pie (Brno), 5: 3-19,

1976 A contribution to the origin of Homo sapiens. J. Human Evolution 5: 497-500.

Keith, A,, and F. S. H.Knowles 1911 A description of Paleolithic Man From Jersey. J. Anat. Physiol., 46: 12- 27.

LeGros Clark, W. E. 1955 The Fossil Evidence for Human Evolution (Second ed.) U. of Chicago Press, Chicago and London.

Leroi-Gouhran, A. 1958 Etude des restes humaines fossiles provenant des Grottes d'Arcy-Sur-Cure. Annls. Palhnt . , 44: 87-148.

Martin, H. 1923 L'homme fossile de la Quina. Arch. de Morph. Gen et Exper., Paris, 260 pp.

Caracteres des squelettes humains quaternaires de la Vallee du Roc (Charentel, Bull. Mem. Soc. Anthrop. Paris, 8: 103.129.

Matiegka, H. 1934 Homo PrBdmostensis, C h k a Aka- demie Ved A Umeni, Prague.

McCown, T., and A. Keith 1939 Mount Carmel. Vol. 2. Oxford University Press.

Miles, A. E. W. 1963 The dentition in the assessment of individual age in the dentition. p. 191-210. In: Dental An- thropology. D. Brothwell, ed. Pergamon Press, London, England.

Molnar, S. 1972 Tooth wear and culture: A survey of tooth functions among some prehistoric populations. Current Anthropology, 13: 511-526.

1975 Catalogue of Fossil Hominids, Par t 111. British Museum Pub. London, England.

Schwalbe, G. 1914 Uber Einen Bei Ehringsdorf in der Nahe von Weimar Gefundenen Unterkiefer des Homo primigenius. Anat. Anz., 47: 337-345.

Sergi, S. 1954 La mandibola neandertaliana. Circeo 11, Riv. Antrop., 41: 305-344.

Sergi, S.. and A. Ascenzi 1956 La mandibola neanderta- liana Circeo 111, Riv. Antrop., 42: 337-403.

Smith, P. 1972 Diet and nutrition in the Natufians. Am. J. Phys. Anthrop., 37: 233-238.

1976 Dental pathology in fossil hominids. Cur- rent Anthropology, 17: 149-151.

Regional variation in tooth size and pathology in fossil hominids. Am. J. Phys. Anthrop., 47: 459-466.

Stewart, T. D. 1958 Restoration and study of the Shanidar I Neanderthal skeleton in Bagdad Iraq. Year Book of the Amer. Philosoph. SOC., pp. 274-278.

The skull of Shanidar 11, Sumer, 17. 97 106.

Shanidar Skeletons, IV andVI. Sumer, 19: 8-25.

Szabo, J. 1935 L'homme Mousterien de la Grotte Mussolini (Hongrie). Etude de la Mandibule, Bull, M$m. SOC. Anthrop., Paris, 6: 23-30.

1937 La d u r k de la vie chez l'homme fossile. LAnthropologie (Paris), 50: 165-202.

Vital Statistics in Prehistoric Populations as Determined from Archeological Data pp. 181-222. In: The Application of Quantitative Methods in Archeology, Heizer, R. F. and S. F. Cook, eda. Viking Fund Pub. no. 28.

Vandermeersch. B. 1972 Recentes dkouvertes des squelettes humains a'Qafzeh (Israel). In: The Origin of Homo sapiens. F. Bordes, ed. UNESCO pub. Paris.

VIEek, E. 1969 Neandertaler der Tschechoslowakei. Academia: Verlag der Tschechoslowakischer Akademie der Wissenschaften Prag.

Oakley, K. P., B. G. Campbell and T. I . Molleson

1961

1963

Vallois, H. V.

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