AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 82:267-274 (1990)
Expression of the Entoconulid (Sixth Cusp) on Mandibular Molar Teeth of an Australian Aboriginal Population GRANT TOWNSEND, HIROWKI YAMADA, AND PATRICIA SMITH Department of Dentistry, The University of Adelaide, Adelaide, South Australia 5000 (G.T.);The First Department of Anatomy, School of Dentistry, Aichi-Gakuin University, Nagoya 464, Japan (H.Y.); and The Department of Anatomy and Embryology, Hadassah Medical School, The Hebrew Uniuersity, Jerusalem, Israel 91010 (P.S.)
KEY WORDS Genetics
Dental morphology, Australian Aboriginals,
ABSTRACT
The expression and genetic basis of the entoconulid (sixth cusp) on mandibular molars were examined in a geographically isolated group of aboriginals from Yuendumu in the Northern Territory of Australia. Four grades of trait expression, ranging from trace to small, medium, and large cusps, were defined on dental casts of 399 subjects. Frequencies of occurrence were among the highest reported in human populations. Approximately 80%of dm2s showed the trait, whereas frequencies in the permanent dentition ranged from around 50% on M2 to 70% on M1 and 80% on M3. The degree of expression increased distally along the molar series, with only 3% of dm2s showing large cusps compared with 25% of M3s. Fluctuating asymmetry was highest for M2 and lowest for dm2. No strong evidence for sexual dimorphism in occurrence or degree of expression was found. Based on a quasi-continuous threshold model, a genetic contribution t o entoconulid variability was observed that was strongest for M1. Significant associations were noted between entoconulid expression on mandibular molars and metaconule expression on maxillary molars, indicating that similar developmental mechanisms may influence these traits. The entoconulid and the metaconule both provide additional bulk on the distal occlusal surface of molar teeth, an area subjected to early wear during mastication in aboriginals.
Comparisons of the occurrence of dental crown traits, such as extra cusps or altered groove patterns, between different human populations have provided useful information about biological affinities and migratory patterns (Sofaer et al., 1986; Turner, 1986a,b). Furthermore, detailed assessments of the expression of these characters in the dentition are assuming more importance in forensic investigations, particularly in those countries where dental caries experience is decreasing (Dahlberg, 1985). This study presents data relating to the frequency of occurrence and de ee of expression of the entoconulid (sixt cusp) on mandibular molars in a geo aphically isolated group of Australian boriginals. To clarify the genetic basis of the trait, its expression was compared between deciduous
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1990 WILEY-LISS, INC.
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and permanent teeth in individuals, as well as between related individuals. The entoconulid, or sixth cusp, sometimes termed tuberculum sextum, is located on the distal marginal ridge area of the occlusal surface of mandibular molars, between the distal cusp (hypoconulid) and the distolingual cusp (entoconid). This feature has been described in several families of primates, especially pongids, as well as in early hominid fossils (Kirveskari, 1974). In modern human PO ulations, its frequency varies considerab y, being rare in Caucasians and Negroes, but more common in Mongoloids
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Received April 18,1988; accepted September 13,1988. Address re rint requests to Dr. Grant Townsend, Department ofDentistry, !'he University ofAdelaide, Adelaide,South Australia 5000.
268
G. TOWNSEND ET AL
and Melanesians (Bailit et al., 1968; Hanihara, 1976; Mayhall et al., 1982). Few detailed reports of the entoconulid in Australian Aboriginal groups are available, although Hanihara (1976) remarked on its high fre uency in aboriginals from Yuendumu i n a e Northern Territory ofAustralia, and similar findings were also reported for an aboriginal PO ulation from Broadbeach in Queensland by 8mith et al. (1981).
Data for this investigation were obtained from dental models collected during a longitudinal growth study of the dentition and craniofacial structures of aboriginals living at Yuendumu, located about 285 km northwest of Alice Springs in the Northern Territory of Australia. Descriptions of Yuendumu and its people, who are predominantly members of the Walbiri tribe, have been given reviously (Barrett et al., 1965; Brown and arrett, 1973; Brown, 1974). The Yuendumu Aboriginals provide sev-
g
and their caries experience was very low (Barrett and Williamson, 19721, thereby minimizing problems of classification associated with missing teeth or dental restorations. Although some teeth were excluded from analysis because of excessive attrition, the availability of earlier serial dental models for many subjects enabled recordings to be made for most erupted teeth. In fact, all except four of the models examined had been obtained from individuals less than 20 years Of tfkification of the entoconulid (sixth cusp) followed the definitions and standard plaque prepared by Turner et al. (1969). Four grades of trait expression were defined ranging from trace through small, medium, and large cusps. The “trace” category (1) included on1 those cuspules located between the istal and distolingual cusps bounded by two distinct parallel grooves running over the distal marginal ridge. The other grades of entoconulid expression were scored relative to the size of the distal cusp of the particular tooth under examination being classified as either smaller than (21, equal to (31, or larger than (4)the distal cusp in overall size (Fig. 1).
B
Fig. 1. Entoconulids (sixth cusps) on permanent mandibular left first molar (grade 3) and second molar (grade 4) of a n Australian Aboriginal male.
269
ENTOCONULID EXPRESSION IN ABORIGINALS
Five-cusped permanent second molars presented the eatest difficulty in classification, with a ecision needed as to whether the fifth cusp represented a true distal cusp or an entoconulid on an otherwise 4-cusped tooth. In these instances, the position of the cusp and the ex ression of the entoconulid on the other mo ar teeth on the same side both were taken into consideration. In 21 subjects, when the cusp was clearly distolingually positioned in relation to the central groove and when other molar teeth also
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TABLE 1. Frequency of occurrence of the entoconulid on mandibular molars of Australian Aboriginals
Tooth
Sex
n
Grade of expression (percentage) 1 2 3
0
Deciduous second molar Right M 70 18.6 F 47 23.4 M & F 117 20.5 Left M 59 20.3 F 41 22.0 M & F 100 21.0 Permanent first molar Right M 178 33.1 F 138 34.8 M & F 31ti 33.9 Left M 174 31.6 F 139 36.0 M & F 313 33.5 Permanent second molar Right' M 143 50.3 F 128 50.8 M & F 271 50.6 Left M 146 47.9 F 122 45.9 M & F 268 47.0 Permanent third molar Right M 45 31.1 F 58 20.7 M & F 103 25.2 Left M 44 18.2 F 54 20.4 M&F 98 19.4
4
0.0 0.0 0.0 0.0 0.0 0.0
74.3 74.5 '74.4 '74.6 75.6 75.0
1.4 2.1 1.7 5.1 2.4 1.0
5.7 0.0 3.4 0.0 0.0 3.0
5.1 2.9 4.1 5.7 3.6 4.8
51.1 51.4 51.3 50.6 46.8 48.9
5.ti
5.1 8.0 6.3 5.2 5.0 5.1
0.0 0.8 0.4 0.7 1.6 1.1
26.6 18.0 22.5 25.3 17.2 21.6
12.6 8.6 10.7 11.6 10.7 11.2
10.5 21.9
0.0 0.0 0.0 0.0 0.0 0.0
31.1 43.1 i37.9 43.2 42.6 42.9
17.8 6.9 11.7 15.9 13.0 14.3
20.0 29.3 25.2 22.7 24.1 23.5
~~
2.9 4.4 6.9 8.6 7.7
15.9
14.4 24.6 19.0
'Significant association between sex and gradeofexpression a t P < 0.05.
showed similar definite expression, a classification of an entoconulid was made. Occasionally double entoconulids were identified, and in these instances the total cuspal area was taken into consideration when classifying the degree of expression. A preliminary eriod was spent when all three authors efined and standardized scoring methodology. All teeth then were scored twice by two of us (GT and HY), with a reliability of 92%.When the double-determination procedure indicated discrepancies in classification, a third determination was made, and these corrected data then were included to determine trait frequencies for teeth on both sides in males and females. Associations between sides and sexes were tested by chi-square analysis. For enetic analysis, the individual count met od of Scott (1980) was ap lied. A condensed presence-absence classiRcation was used when assessing associations within the dentition and between relatives. The frequency of trait expression was compared between siblings of individuals showing the trait and siblings of individuals from the general population. Associations between sibling pairs for trait expression were also determined following the method of Berry (1978).
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RESULTS
Table 1 presents the frequencies of occurrence of the entoconulid in mandibular molars of Aboriginal males and females. Aproximately 80%of deciduous second molars dm2) showed the trait, most displaying small cusps. In the ermanent dentition, the frequency of indivi uals showing the character ranged from about 50% on second molars (M2), to around 70% on first molars (Ml) and 80% on third molars (M3). The de ee of Y expression of entoconulid showed a C efinite pattern along the molar series, becoming more pronounced from dm2 through M1 and M2 to M3. Only about 3% of dm2s showed extreme entoconulid expression, whereas
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TABLE 2. Asymmetry in the presence-absence expression of the entoconulid'
Left dm2
Right
Absent Present
19 0
Absent M1 M2
M3
dm2
92 10
16 1
71
'Associations between sides for all teeth significant P
114 8
< 0.01
1
Present M1 M2
M3
11 183
3 54
11
113
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G. TOWNSEND ET AL
around 25% of M3s displayed large cusps. Frequencies of occurrence were similar in males and females for all teeth, with only one comparison (right M2) yielding a significant association between sex and degree of expression. Associations between trait ex ression for right and left sides are indicatec r in Table 2, with data condensed to indicate either the presence or absence of the entoconulid. Initial analyses failed to demonstrate any systematic differences in asymmetry between the sexes, and so data for males and females were combined. Associations between sides for all molars were significant, indicating that the trait tended to occur bilaterally. Only one example of the trait being present unilaterally was noted in dm2s, whereas 19 cases (7.7%) were noted for M2. When the various grades of ex ression were considered, four examples o unilateral expression of grade 4 cusp were noted on M2, one example on M3, and one example of unilateral grade 3 on M1. No differences in trait expression greater than one grade were noted between opposite dm2s. When subjects classified as bilaterally absent were excluded from the analysis to overcome the possibility of bias associated with differences in total trait frequency between molar teeth (Saunders and Mayhall, 1982a), M2 showed the highest frequency of presence-absence asymmetry (14.4%)while dm2 showed the least (1.4%). Data for entoconulid expression in different mandibular molars of the same individuals are given in Table 3. Generally, if the trait was a parent on dm2, it was also present on t e other molar teeth, although exceptions were noted in 20 of 69 comparisons between dm2 and M2. Correlations between adjacent molar teeth for the entoconulid were generally higher than those between teeth that were farther apart (Table 4). The strongest correlation was between dm2 and M1 (0.531,whereas the correlation between M1 and M3 for entoconulid expression was low (0.08). Comparisons of the frequency of occurrence of the entoconulid between siblings of individuals showing the trait and siblings of individuals from the general population are even in Table 5. Preliminary analyses did not disclose any systematic differences between the sexes, and so combined results are given. Siblings of individuals with the trait displayed the character more frequently
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T A B L E 3. Expression o f the entoconulid in different mandibular molars of the same individuals M1'
dm2
Absent Present
Absent M2l
15 11
M3
M1
2 4
7 86
13 20
Present M2 M3 5 49
3 18
'Significant association between dm2 and M I , and dm2 and M2 a t
P < 0.01.
T A B L E 4. Correlations between molar teeth for entoconulid expression (phi-coefficients)'
dm2 M1 M2 M3
dm2
MI
M2
M3
-
0.53
0.36 0.26
0.20 0.08 0.24
-
-
-
'Phi-coefficients calculated following H ays (1973).
T A B L E 5. Frequency o f the entoconulid i n siblings o f individuals showing the trait compared with siblings o f individuals f r o m the general population
Tooth
Siblings of
n
dm2
General population Affected individuals General population Affected individuals General population Affected individuals General population Affected individuals
47 29 106 99 80 62 34 21
M1 M2
M3
Expression (8) Absent Present 14.9 3.4 30.2 18.2 42.6 38.7 20.6 19.0
85.1 96.6 69.8 81.8 67.5 61.3
19.4 81.0
than siblings of individuals from the general population, the trend being strongest for M1 (81.8% compared with 69.8%). The frequency of occurrence of the entoconulid in siblings of those individuals who showed the more marked cuspal forms (categories 3 and 4) was further increased for all teeth, being most marked for M2 (77.4% compared with 61.3%). Furthermore, when the occurrence of the trait was considered in sibling pairs, M1 yielded a significant association, corres onding to a phi-coefficient of 0.30 (Taile 6). DISCUSSION
The entoconulid (cusp 6) was very commonly found on mandibular molars of the Yuendumu aboriginals. In fact, the observed fre uencies are among the highest reported for uman populations, exceeding those of
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ENTOCONULID EXPRESSION IN ABORIGINALS TABLE 6. Expression of the entoconulid in Aboriginal sibling pairs Sibling 1
Sibling 2
12 12
1
Absent Present
2
12 16
0 4
0 22
13 55
17 26
2 15
'Significant association between siblings a t P < 0.01, phi-coefficient = 0.30.
Pol esians, Melanesians, Japanese, Inuit, a n r h e r i c a n Blacks, similar to reported frequencies in American Indian groups who show a so-called Sinodont pattern of dental features (Turner, 1985,1986b).The contrast between Australian Aboriginals and Caucasians in Table 7 is striking. Smith et al. (1981) also reported high frequencies for the entoconulid in aboriginal skeletal remains from Broadbeach; 65% on M1,42%on M2, and 27% on M3. It therefore appears that the entoconulid is an im ortant feature of the Australian aborigina dentition. The Yuendumu and Broadbeach groups also show similar trends for other dental crown features. For example, metaconules and Carabelli trait are very common on maxillary molars, whereas seventh cusps and protostylids are rare on mandibular molars. This pattern of expression seems likely to represent a characteristic Australian dental com lex, distinct from either the Mongoloid or aucasoid patterns previously described (Hanihara, 1967; Mayhall et al., 1982). Within the Yuendumu grou , there was no strong evidence for sexual imorphism in either occurrence or degree of expression of the entoconulid. Similar findings were noted in relation to metaconule expression in this group (Townsend et al., 19861, but these results contrast with findings for Carabelli trait, which showed definite sexual dimorphism in Yuendumu Aboriginals (Townsend and Brown, 1981). Presumably the pattern of dimorphism for different dental crown traits can vary within a population. The frequency of occurrence of the entoconulid was highest on dm2, although few examples of large accessory cusps were noted on this tooth, most exam les being classified as smaller than the &a1 cusp (hypoconulid). In the ermanent dentition, the attern of prevaence was M3>M1> M2. n contrast, mean size of the trait followed the trend noted by Harris (1979) in Melanesians, that is, M3>M2>Ml, in accor-
P
cp
B
!
f
TABLE 7. Percentage frequencies of the entoconulid on mandibular molars in several ethnic mourn
Pooulation
dm2
M1
Japanese' American Blacks' Inuit' Caucasians2 South African" Negro Kalahari San:' New Britians4 (Melanesians) Polynesians' Australian Aboriginals"
36.9 12.0 37.7 1.7
54.4 79.3
M2
M3
25.3 6.5 50.0 2.4 5.5
0.5 4.3
4.3 20.4
15.9 32.5
13.2 9.7
30.8 24.2
54.5 66.3
30.0 51.2
50.0 71.6
'Hanihara (1976). 'Saunders and Mayhall (1982h) "Grine (1981). 4Turner and Swindler (1978). 'SSuzuki and Sakai 11973). 'Present study.
dance with the pattern predicted by field theory (Dahlberg, 1945). Axelsson and Kirveskari (1979) suggested that lower frequencies of the entoconulid on M2 compared with M1 are found in populations in which some reduction in molar cusp number has occurred. They noted that the entoconulid was more common on M1 than M2 in Icelanders, and similar trends have been reported in Melanesians (Turner and Swindler, 1978) and Polynesians (Suzuki and Sakai, 1973). Molar size sequence of mandibular molars in Yuendumu Aboriginals is similar to that of other contemporary populations (Townsend and Brown, 19831, and so the present results are not unexpected. However, the lower frequency of the entoconulid noted on M2 compared with other molars might also relate to our system of classification which tended, if anything, to underestimate the true frequency of entoconulid on M2, especially on 4-cusped teeth. Because of our conservative approach, it is likely that some entoconulids, particularly
272
G. TOWNSEND ET AL.
on M2, were considered to be distal cusps in our sample. As Harris (1977) has pointed out, the ossible bifurcation or trifurcation of either t e hypoconulid or the entoconulid can further com licate classification, and this may have in luenced our frequency calculations too, as well as contributing to some of the instances in which asymmetric expression was recorded. Smith et al. (1987) have postulated that the directionality in frequency shown by dental traits along the molar series is related to ontogenetic history. Having compared the expression of several dental features on dm2 and M1 in four different ethnic groups, they found that trait frequency varied between the grou s, presumably reflecting their genetic bac ground, but the pattern of expression between dm2 and M1 for each articular trait was similar in all groups. !'hey proosed that those traits present on dm2 in Righer frequencies than M1 develop early, whereas those more fre uent on M1 appear later during crown morp ogenesis. The entoconulid appeared to be more frequent on M1 than dm2 in their study, but some caution is needed in inter reting this result because of the small num er of individuals who actually showed the trait. Saunders and Mayhall (1982b) also reported a slightly higher frequency of the entoconulid on M1 than dm2 in a Caucasian sample, but again very few individuals displayed the trait. In the present study, we have found a higher frequency of occurrence of the entoconulid on dm2 than M1, although its degree of expression increased distally. It would seem that both the degree of expression of the trait and its frequency of occurrence need to be considered when attempting to formulate theories to explain directionality in the molar teeth. As we have suggested previously (Townsend et al., 1986), the similarity in expression of metaconules on maxillary molars and entoconulids on mandibular molars, together with their analogous locations, makes it tempting to speculate that similar developmental mechanisms may influence expression of both these traits. Indeed, when associations in expression of these two characters were considered within individuals, significant correlations were noted for dm2, M1, and M2, values bein 0.25, 0.18, and 0.16, respectively. Althoug these values are not high, they are of similar magnitude to those re orted by Scott (1978) for Carabelli trait an8 protostylids. Scott suggested that
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the association between Carabelli trait and protostylids might reflect a long-term developmental relationship in hominoid phylogeny. A similar association could also apply between the entoconulid and metaconule. Both the entoconulid and metaconule provide additional bulk on the distal occlusal surface of molar teeth, an area that is subjected to early wear in aboriginals. It seems reasonable to suggest that a high frequency of these traits in individuals who exert considerable masticatory force could be a selective advantage. The results of the genetic analysis confirm that there is a genetic basis to the entoconulid expression, but the heritability does not seem to be high. This is consistent with the findings of Scott and Potter (19841, who estimated that the heritability of the entoconulid was 0.19 in a sample of American twins. Interestingly, Mizoguchi (1977) obtained an estimate of 1.63for the heritability of the entoconulid in a study of Japanese twins. He attributed this overestimation t o either sam ling bias or possibly dominance variance. evertheless, in general it seems that nongenetic, environmental factors are likely to contribute significantly to observed phenotypic variation in crown form, as has also been shown for crown size variables (Townsend, 1980; Potter et al., 1983). The entoconulid, like several other dental morphological traits, appears to fit the criteria of a quasi-continuous variable, showing a continuous range of expression with a threshold below which it is undetectable (Harris, 1977). The quasi-continuous model assumes an underlying scale of continuous variation related to the expression of the character, termed liability by Falconer (19651, that results from a combination of genetic and environmental factors. It seems that the genetic component of entoconulid variability is strongest on M1 in aboriginals, although the extremely hi h trait frequency for dm2 is a complicating actor in our analysis. As most individuals display the trait on dm2, comparisons between related and nonrelated individuals are not particularly illuminating. Kolakowski et al. (1980) noted significant major gene and common sibling environmental effects for Carabelli trait by ap lying a complex segregation analysis to I fata obtained from a large number of families living on the Solomon Islands. More recently, Nichol (1989) has also applied segregation
rs
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ENTOCONULID EXPRESSION IN ABORIGINALS
analysis to family data in an attempt to clarify the mode of inheritance of a number of dental crown traits. Single-gene models rovided the best fit for some features, w ile others conformed to a polygenic model. In the latter instance, transmissibility estimates were low, averaging 0.36. Nichol concluded that both major genes and the environment have important roles in the development of dental crown morphology. More studies of this type are required to enable meaningful statistical testing of genetic models; they should be based on adequate samples of related individuals and include considerations of trait expression in both deciduous and permanent teeth. Our understanding of the genetic basis of dental traits needs to improve further in line with their increasing application in both anthropological and forensic areas.
K
ACKNOWLEDGMENT
The dental casts were collected by T. Brown and the late M.J. Barrett with the support of Grant 02034 from the National Institutes of Health, Bethesda, Mar land. Currently the research is supported y the National Health and Medical Research Council, Canberra.
i
LITERATURE CITED Axelsson G and Kirveskari P (1979) Sixth and seventh cusp on lower molar teeth of Icelanders. Am. J. Phys. Anthropol. 51:79-82. Bailit HL, De Witt SJ, and Leigh RA (1968)The size and morphology of the Nasioi dentition. Am. J. Phys. Anthropol. 28271-287. Barrett MJ and Williamson JJ (1972) Oral health of Australian Aborigines: Survey methods and prevalence of dental caries. Aust. Dent. J . 17:37-50. Barrett MJ, Brown T, and Fanning EA (1965) A longterm study of the dental and craniofacial characteristics of a tribe of Central Australian Aborigines. Aust. Dent. J . 10:63-68. Berry AC (1978) Anthropological and family studies on minor variants of the dental crown. In PM Butler and KA Joysey (eds.): Development, Function and Evolution of Teeth. London: Academic Press, pp. 80-98. Brown T (1974) Dental research in Australia and its practical applications: The Australian Aborigine. Int. Dent. J . 24:299-309. Brown T and Barrett MJ (1973) Dental and craniofacial growth studies of Australian Aborigines. In RL Kirk (ed.): The Human Biology of Aborigines in Cape York. Australian Aboriginal Studies No. 44. Canberra: Australian Institute of Aboriginal Studies, pp. 69-80. Dahlberg AA (1945) The changing dentition of man. J. Am. Dent. Assoc. 32:67&690. Dahlberg AA (1985) Ontogeny and dental genetics in forensic problems. Forensic Sci. Int. 30:163-176. Falconer DS (1965)The inheritance of liability to certain
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diseases, estimated by the incidence among relatives. Ann. Hum. Genet. 29:51-76. Grine FE (1981) Occlusal morphology of the mandibular ermanent molars of the South African Negro and the alahari San (Bushman). Ann. South African Museum 86: 157-215. Hanihara K (1967) Racial characteristics in the dentition. J . Dent. Res. [Suppl.] 46:923-926. Hanihara K (1976) Statistical and Comparative Studies of the Australian Aboriginal Dentition. Bulletin No. 11. The University Museum. Tokyo: The University of Tokyo. Harris EF (1977) Anthropologic and Genetic Aspects of the Dental Morphology of Solomon Islanders, Melanesia. Ph.D. Dissertation, Arizona State University. Ann Arbor: University Microfilms International. Harris EF (1979) Morphogenetic and genetic patterning within accessory molar cusps. Am. J. Phys. Anthrop. 50:446 (Abstract). Hays WL (1973) Statistics for the Social Sciences. 2nd Ed. New York: Holt, Rinehart and Winston Inc., pp. 743-745. Kirveskari P (1974) MorDholo&al traits in the oermanent dentition of 1ivingSkol;Lapps. Proc. Finn'. Dent. SOC.70, Suppl. 11. Kolakowski D. Harris EF and Bailit HL (1980) Comalex segregation'analysis of Carabelli's trait in a Melanesian population. Am. J. Phys. Anthropol. 53:301-308. Mayhall JT, Saunders SR, and Belier PL (1982) The dental morphology of North American Whites: a reapraisal. In B Kurten (ed.): Teeth: Form, Function and volution. New York: Columbia University Press, pp, 245-258. Mizoguchi Y (1977) Genetic variability of tooth crown characters: Analysis by the tetrachoric correlation method. Bull. Natl. Sci. Mus. Series D (Anthrop.) 3:3742. Nichol CR (1989)Complex segregation analysis of dental morphological variants. Am. J. Phys. Anthrop. 78:3759. Potter RHY, Rice JP, Dahlberg AA, and Dahlberg T (1983)Dental size traits within families: Path analysis for first molar and lateral incisor. Am. J. Phys. AnthroPOI. 61:283-289. Saunders SR and Mayhall JT (1982a) Fluctuating asymmetry of dental morphological traits: new interpretations. Hum. Biol. 54:789-799. Saunders SR and Mayhall JT (1982b) Developmental patterns of human dental morphological traits. Arch. Oral Biol. 27:45-49. Scott GR (1978) The relationship between Carabelli's trait and the protostylid. J. Dent. Res. 57570. Scott GR (1980)Population variation of Carabelli's trait. Hum. Biol. 52:63-78. Scott GR and Potter RHY (1984) An analysis of tooth crown morphology in American twins. Anthropologie 22:223-231. Smith P, Brown T, and Wood WB (1981) Tooth size and morphology in a recent Australian Aboriginal population from Broadbeach, South East Queensland. Am. J. Phys. Anthropol. 5:423-432. Smith P, Koyoumdjisky-KayeE, Kalderon W, and Stern D (1987) Directionality of dental trait frequency between human second deciduous and first permanent molars. Arch. Oral Biol. 32:5-9. Sofaer JA, Smith P, and Kaye E (1986) Affinities between contemoorarv and skeletal Jewish and nonJewish groups' based on tooth morphology. Am. J. Phys. Anthropol. 70:265-275.
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Suzuki M and Sakai T (1973)Occlusal surface pattern of the lower molars and the second deciduous molar among living Polynesians. Am. J . Phys. Anthropol. 39:305-315. Townsend GC (1980)Heritability of deciduous tooth size in Australian Aboriginals. Am. J. Phys. Anthropol. 52:297-300. Townsend GC and Brown T (1981)The Carabelli trait in Australian Aboriginal dentition. Arch. Oral Biol. 26t809-814. Townsend GC and Brown T (1983) Molar size sequence in Australian Aboriginals. Am. J. Phys. Anthropol. 60:69-74. Townsend GC, Yamada H, and Smith P (1986) The metaconule in Australian Aboriginals: an accessory tubercle on maxillary molar teeth. Hum. Biol. 58:851-862.
Turner CG(1985)Thedental search for Native American origins. In R Kirk and E Szathmary(eds.):Out ofAsia: Peopling the Americas and the Pacific. Canberra: Journal of Pacific History, pp. 31-78. Turner CG (1986a) Dentochronological separation estimates for Pacific Rim populations. Science 232: 1140-1142. Turner CG (198613) The first Americans: The dental evidence. Natl. Geogr. Res. 2:37-46. Turner CGand Swindler DR(1978)Thedentition ofNew Britain West Nakanai Melanesians. VIII. Peopling of the Pacific. Am. J . Phys. Anthropol. 49:361-371. Turner CG, Scott GR, and Rose TA (1969) Mandibular Molar Entoconulid Pla ue and Definitions of Variation. Department of An&ropology, Arizona State University.
Expression of the Entoconulid (Sixth Cusp) on Mandibular Molar Teeth of an Australian Aboriginal Population GRANT TOWNSEND, HIROWKI YAMADA, AND PATRICIA SMITH Department of Dentistry, The University of Adelaide, Adelaide, South Australia 5000 (G.T.);The First Department of Anatomy, School of Dentistry, Aichi-Gakuin University, Nagoya 464, Japan (H.Y.); and The Department of Anatomy and Embryology, Hadassah Medical School, The Hebrew Uniuersity, Jerusalem, Israel 91010 (P.S.)
KEY WORDS Genetics
Dental morphology, Australian Aboriginals,
ABSTRACT
The expression and genetic basis of the entoconulid (sixth cusp) on mandibular molars were examined in a geographically isolated group of aboriginals from Yuendumu in the Northern Territory of Australia. Four grades of trait expression, ranging from trace to small, medium, and large cusps, were defined on dental casts of 399 subjects. Frequencies of occurrence were among the highest reported in human populations. Approximately 80%of dm2s showed the trait, whereas frequencies in the permanent dentition ranged from around 50% on M2 to 70% on M1 and 80% on M3. The degree of expression increased distally along the molar series, with only 3% of dm2s showing large cusps compared with 25% of M3s. Fluctuating asymmetry was highest for M2 and lowest for dm2. No strong evidence for sexual dimorphism in occurrence or degree of expression was found. Based on a quasi-continuous threshold model, a genetic contribution t o entoconulid variability was observed that was strongest for M1. Significant associations were noted between entoconulid expression on mandibular molars and metaconule expression on maxillary molars, indicating that similar developmental mechanisms may influence these traits. The entoconulid and the metaconule both provide additional bulk on the distal occlusal surface of molar teeth, an area subjected to early wear during mastication in aboriginals.
Comparisons of the occurrence of dental crown traits, such as extra cusps or altered groove patterns, between different human populations have provided useful information about biological affinities and migratory patterns (Sofaer et al., 1986; Turner, 1986a,b). Furthermore, detailed assessments of the expression of these characters in the dentition are assuming more importance in forensic investigations, particularly in those countries where dental caries experience is decreasing (Dahlberg, 1985). This study presents data relating to the frequency of occurrence and de ee of expression of the entoconulid (sixt cusp) on mandibular molars in a geo aphically isolated group of Australian boriginals. To clarify the genetic basis of the trait, its expression was compared between deciduous
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1990 WILEY-LISS, INC.
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and permanent teeth in individuals, as well as between related individuals. The entoconulid, or sixth cusp, sometimes termed tuberculum sextum, is located on the distal marginal ridge area of the occlusal surface of mandibular molars, between the distal cusp (hypoconulid) and the distolingual cusp (entoconid). This feature has been described in several families of primates, especially pongids, as well as in early hominid fossils (Kirveskari, 1974). In modern human PO ulations, its frequency varies considerab y, being rare in Caucasians and Negroes, but more common in Mongoloids
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Received April 18,1988; accepted September 13,1988. Address re rint requests to Dr. Grant Townsend, Department ofDentistry, !'he University ofAdelaide, Adelaide,South Australia 5000.
268
G. TOWNSEND ET AL
and Melanesians (Bailit et al., 1968; Hanihara, 1976; Mayhall et al., 1982). Few detailed reports of the entoconulid in Australian Aboriginal groups are available, although Hanihara (1976) remarked on its high fre uency in aboriginals from Yuendumu i n a e Northern Territory ofAustralia, and similar findings were also reported for an aboriginal PO ulation from Broadbeach in Queensland by 8mith et al. (1981).
Data for this investigation were obtained from dental models collected during a longitudinal growth study of the dentition and craniofacial structures of aboriginals living at Yuendumu, located about 285 km northwest of Alice Springs in the Northern Territory of Australia. Descriptions of Yuendumu and its people, who are predominantly members of the Walbiri tribe, have been given reviously (Barrett et al., 1965; Brown and arrett, 1973; Brown, 1974). The Yuendumu Aboriginals provide sev-
g
and their caries experience was very low (Barrett and Williamson, 19721, thereby minimizing problems of classification associated with missing teeth or dental restorations. Although some teeth were excluded from analysis because of excessive attrition, the availability of earlier serial dental models for many subjects enabled recordings to be made for most erupted teeth. In fact, all except four of the models examined had been obtained from individuals less than 20 years Of tfkification of the entoconulid (sixth cusp) followed the definitions and standard plaque prepared by Turner et al. (1969). Four grades of trait expression were defined ranging from trace through small, medium, and large cusps. The “trace” category (1) included on1 those cuspules located between the istal and distolingual cusps bounded by two distinct parallel grooves running over the distal marginal ridge. The other grades of entoconulid expression were scored relative to the size of the distal cusp of the particular tooth under examination being classified as either smaller than (21, equal to (31, or larger than (4)the distal cusp in overall size (Fig. 1).
B
Fig. 1. Entoconulids (sixth cusps) on permanent mandibular left first molar (grade 3) and second molar (grade 4) of a n Australian Aboriginal male.
269
ENTOCONULID EXPRESSION IN ABORIGINALS
Five-cusped permanent second molars presented the eatest difficulty in classification, with a ecision needed as to whether the fifth cusp represented a true distal cusp or an entoconulid on an otherwise 4-cusped tooth. In these instances, the position of the cusp and the ex ression of the entoconulid on the other mo ar teeth on the same side both were taken into consideration. In 21 subjects, when the cusp was clearly distolingually positioned in relation to the central groove and when other molar teeth also
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TABLE 1. Frequency of occurrence of the entoconulid on mandibular molars of Australian Aboriginals
Tooth
Sex
n
Grade of expression (percentage) 1 2 3
0
Deciduous second molar Right M 70 18.6 F 47 23.4 M & F 117 20.5 Left M 59 20.3 F 41 22.0 M & F 100 21.0 Permanent first molar Right M 178 33.1 F 138 34.8 M & F 31ti 33.9 Left M 174 31.6 F 139 36.0 M & F 313 33.5 Permanent second molar Right' M 143 50.3 F 128 50.8 M & F 271 50.6 Left M 146 47.9 F 122 45.9 M & F 268 47.0 Permanent third molar Right M 45 31.1 F 58 20.7 M & F 103 25.2 Left M 44 18.2 F 54 20.4 M&F 98 19.4
4
0.0 0.0 0.0 0.0 0.0 0.0
74.3 74.5 '74.4 '74.6 75.6 75.0
1.4 2.1 1.7 5.1 2.4 1.0
5.7 0.0 3.4 0.0 0.0 3.0
5.1 2.9 4.1 5.7 3.6 4.8
51.1 51.4 51.3 50.6 46.8 48.9
5.ti
5.1 8.0 6.3 5.2 5.0 5.1
0.0 0.8 0.4 0.7 1.6 1.1
26.6 18.0 22.5 25.3 17.2 21.6
12.6 8.6 10.7 11.6 10.7 11.2
10.5 21.9
0.0 0.0 0.0 0.0 0.0 0.0
31.1 43.1 i37.9 43.2 42.6 42.9
17.8 6.9 11.7 15.9 13.0 14.3
20.0 29.3 25.2 22.7 24.1 23.5
~~
2.9 4.4 6.9 8.6 7.7
15.9
14.4 24.6 19.0
'Significant association between sex and gradeofexpression a t P < 0.05.
showed similar definite expression, a classification of an entoconulid was made. Occasionally double entoconulids were identified, and in these instances the total cuspal area was taken into consideration when classifying the degree of expression. A preliminary eriod was spent when all three authors efined and standardized scoring methodology. All teeth then were scored twice by two of us (GT and HY), with a reliability of 92%.When the double-determination procedure indicated discrepancies in classification, a third determination was made, and these corrected data then were included to determine trait frequencies for teeth on both sides in males and females. Associations between sides and sexes were tested by chi-square analysis. For enetic analysis, the individual count met od of Scott (1980) was ap lied. A condensed presence-absence classiRcation was used when assessing associations within the dentition and between relatives. The frequency of trait expression was compared between siblings of individuals showing the trait and siblings of individuals from the general population. Associations between sibling pairs for trait expression were also determined following the method of Berry (1978).
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RESULTS
Table 1 presents the frequencies of occurrence of the entoconulid in mandibular molars of Aboriginal males and females. Aproximately 80%of deciduous second molars dm2) showed the trait, most displaying small cusps. In the ermanent dentition, the frequency of indivi uals showing the character ranged from about 50% on second molars (M2), to around 70% on first molars (Ml) and 80% on third molars (M3). The de ee of Y expression of entoconulid showed a C efinite pattern along the molar series, becoming more pronounced from dm2 through M1 and M2 to M3. Only about 3% of dm2s showed extreme entoconulid expression, whereas
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TABLE 2. Asymmetry in the presence-absence expression of the entoconulid'
Left dm2
Right
Absent Present
19 0
Absent M1 M2
M3
dm2
92 10
16 1
71
'Associations between sides for all teeth significant P
114 8
< 0.01
1
Present M1 M2
M3
11 183
3 54
11
113
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G. TOWNSEND ET AL
around 25% of M3s displayed large cusps. Frequencies of occurrence were similar in males and females for all teeth, with only one comparison (right M2) yielding a significant association between sex and degree of expression. Associations between trait ex ression for right and left sides are indicatec r in Table 2, with data condensed to indicate either the presence or absence of the entoconulid. Initial analyses failed to demonstrate any systematic differences in asymmetry between the sexes, and so data for males and females were combined. Associations between sides for all molars were significant, indicating that the trait tended to occur bilaterally. Only one example of the trait being present unilaterally was noted in dm2s, whereas 19 cases (7.7%) were noted for M2. When the various grades of ex ression were considered, four examples o unilateral expression of grade 4 cusp were noted on M2, one example on M3, and one example of unilateral grade 3 on M1. No differences in trait expression greater than one grade were noted between opposite dm2s. When subjects classified as bilaterally absent were excluded from the analysis to overcome the possibility of bias associated with differences in total trait frequency between molar teeth (Saunders and Mayhall, 1982a), M2 showed the highest frequency of presence-absence asymmetry (14.4%)while dm2 showed the least (1.4%). Data for entoconulid expression in different mandibular molars of the same individuals are given in Table 3. Generally, if the trait was a parent on dm2, it was also present on t e other molar teeth, although exceptions were noted in 20 of 69 comparisons between dm2 and M2. Correlations between adjacent molar teeth for the entoconulid were generally higher than those between teeth that were farther apart (Table 4). The strongest correlation was between dm2 and M1 (0.531,whereas the correlation between M1 and M3 for entoconulid expression was low (0.08). Comparisons of the frequency of occurrence of the entoconulid between siblings of individuals showing the trait and siblings of individuals from the general population are even in Table 5. Preliminary analyses did not disclose any systematic differences between the sexes, and so combined results are given. Siblings of individuals with the trait displayed the character more frequently
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T A B L E 3. Expression o f the entoconulid in different mandibular molars of the same individuals M1'
dm2
Absent Present
Absent M2l
15 11
M3
M1
2 4
7 86
13 20
Present M2 M3 5 49
3 18
'Significant association between dm2 and M I , and dm2 and M2 a t
P < 0.01.
T A B L E 4. Correlations between molar teeth for entoconulid expression (phi-coefficients)'
dm2 M1 M2 M3
dm2
MI
M2
M3
-
0.53
0.36 0.26
0.20 0.08 0.24
-
-
-
'Phi-coefficients calculated following H ays (1973).
T A B L E 5. Frequency o f the entoconulid i n siblings o f individuals showing the trait compared with siblings o f individuals f r o m the general population
Tooth
Siblings of
n
dm2
General population Affected individuals General population Affected individuals General population Affected individuals General population Affected individuals
47 29 106 99 80 62 34 21
M1 M2
M3
Expression (8) Absent Present 14.9 3.4 30.2 18.2 42.6 38.7 20.6 19.0
85.1 96.6 69.8 81.8 67.5 61.3
19.4 81.0
than siblings of individuals from the general population, the trend being strongest for M1 (81.8% compared with 69.8%). The frequency of occurrence of the entoconulid in siblings of those individuals who showed the more marked cuspal forms (categories 3 and 4) was further increased for all teeth, being most marked for M2 (77.4% compared with 61.3%). Furthermore, when the occurrence of the trait was considered in sibling pairs, M1 yielded a significant association, corres onding to a phi-coefficient of 0.30 (Taile 6). DISCUSSION
The entoconulid (cusp 6) was very commonly found on mandibular molars of the Yuendumu aboriginals. In fact, the observed fre uencies are among the highest reported for uman populations, exceeding those of
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ENTOCONULID EXPRESSION IN ABORIGINALS TABLE 6. Expression of the entoconulid in Aboriginal sibling pairs Sibling 1
Sibling 2
12 12
1
Absent Present
2
12 16
0 4
0 22
13 55
17 26
2 15
'Significant association between siblings a t P < 0.01, phi-coefficient = 0.30.
Pol esians, Melanesians, Japanese, Inuit, a n r h e r i c a n Blacks, similar to reported frequencies in American Indian groups who show a so-called Sinodont pattern of dental features (Turner, 1985,1986b).The contrast between Australian Aboriginals and Caucasians in Table 7 is striking. Smith et al. (1981) also reported high frequencies for the entoconulid in aboriginal skeletal remains from Broadbeach; 65% on M1,42%on M2, and 27% on M3. It therefore appears that the entoconulid is an im ortant feature of the Australian aborigina dentition. The Yuendumu and Broadbeach groups also show similar trends for other dental crown features. For example, metaconules and Carabelli trait are very common on maxillary molars, whereas seventh cusps and protostylids are rare on mandibular molars. This pattern of expression seems likely to represent a characteristic Australian dental com lex, distinct from either the Mongoloid or aucasoid patterns previously described (Hanihara, 1967; Mayhall et al., 1982). Within the Yuendumu grou , there was no strong evidence for sexual imorphism in either occurrence or degree of expression of the entoconulid. Similar findings were noted in relation to metaconule expression in this group (Townsend et al., 19861, but these results contrast with findings for Carabelli trait, which showed definite sexual dimorphism in Yuendumu Aboriginals (Townsend and Brown, 1981). Presumably the pattern of dimorphism for different dental crown traits can vary within a population. The frequency of occurrence of the entoconulid was highest on dm2, although few examples of large accessory cusps were noted on this tooth, most exam les being classified as smaller than the &a1 cusp (hypoconulid). In the ermanent dentition, the attern of prevaence was M3>M1> M2. n contrast, mean size of the trait followed the trend noted by Harris (1979) in Melanesians, that is, M3>M2>Ml, in accor-
P
cp
B
!
f
TABLE 7. Percentage frequencies of the entoconulid on mandibular molars in several ethnic mourn
Pooulation
dm2
M1
Japanese' American Blacks' Inuit' Caucasians2 South African" Negro Kalahari San:' New Britians4 (Melanesians) Polynesians' Australian Aboriginals"
36.9 12.0 37.7 1.7
54.4 79.3
M2
M3
25.3 6.5 50.0 2.4 5.5
0.5 4.3
4.3 20.4
15.9 32.5
13.2 9.7
30.8 24.2
54.5 66.3
30.0 51.2
50.0 71.6
'Hanihara (1976). 'Saunders and Mayhall (1982h) "Grine (1981). 4Turner and Swindler (1978). 'SSuzuki and Sakai 11973). 'Present study.
dance with the pattern predicted by field theory (Dahlberg, 1945). Axelsson and Kirveskari (1979) suggested that lower frequencies of the entoconulid on M2 compared with M1 are found in populations in which some reduction in molar cusp number has occurred. They noted that the entoconulid was more common on M1 than M2 in Icelanders, and similar trends have been reported in Melanesians (Turner and Swindler, 1978) and Polynesians (Suzuki and Sakai, 1973). Molar size sequence of mandibular molars in Yuendumu Aboriginals is similar to that of other contemporary populations (Townsend and Brown, 19831, and so the present results are not unexpected. However, the lower frequency of the entoconulid noted on M2 compared with other molars might also relate to our system of classification which tended, if anything, to underestimate the true frequency of entoconulid on M2, especially on 4-cusped teeth. Because of our conservative approach, it is likely that some entoconulids, particularly
272
G. TOWNSEND ET AL.
on M2, were considered to be distal cusps in our sample. As Harris (1977) has pointed out, the ossible bifurcation or trifurcation of either t e hypoconulid or the entoconulid can further com licate classification, and this may have in luenced our frequency calculations too, as well as contributing to some of the instances in which asymmetric expression was recorded. Smith et al. (1987) have postulated that the directionality in frequency shown by dental traits along the molar series is related to ontogenetic history. Having compared the expression of several dental features on dm2 and M1 in four different ethnic groups, they found that trait frequency varied between the grou s, presumably reflecting their genetic bac ground, but the pattern of expression between dm2 and M1 for each articular trait was similar in all groups. !'hey proosed that those traits present on dm2 in Righer frequencies than M1 develop early, whereas those more fre uent on M1 appear later during crown morp ogenesis. The entoconulid appeared to be more frequent on M1 than dm2 in their study, but some caution is needed in inter reting this result because of the small num er of individuals who actually showed the trait. Saunders and Mayhall (1982b) also reported a slightly higher frequency of the entoconulid on M1 than dm2 in a Caucasian sample, but again very few individuals displayed the trait. In the present study, we have found a higher frequency of occurrence of the entoconulid on dm2 than M1, although its degree of expression increased distally. It would seem that both the degree of expression of the trait and its frequency of occurrence need to be considered when attempting to formulate theories to explain directionality in the molar teeth. As we have suggested previously (Townsend et al., 1986), the similarity in expression of metaconules on maxillary molars and entoconulids on mandibular molars, together with their analogous locations, makes it tempting to speculate that similar developmental mechanisms may influence expression of both these traits. Indeed, when associations in expression of these two characters were considered within individuals, significant correlations were noted for dm2, M1, and M2, values bein 0.25, 0.18, and 0.16, respectively. Althoug these values are not high, they are of similar magnitude to those re orted by Scott (1978) for Carabelli trait an8 protostylids. Scott suggested that
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t
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the association between Carabelli trait and protostylids might reflect a long-term developmental relationship in hominoid phylogeny. A similar association could also apply between the entoconulid and metaconule. Both the entoconulid and metaconule provide additional bulk on the distal occlusal surface of molar teeth, an area that is subjected to early wear in aboriginals. It seems reasonable to suggest that a high frequency of these traits in individuals who exert considerable masticatory force could be a selective advantage. The results of the genetic analysis confirm that there is a genetic basis to the entoconulid expression, but the heritability does not seem to be high. This is consistent with the findings of Scott and Potter (19841, who estimated that the heritability of the entoconulid was 0.19 in a sample of American twins. Interestingly, Mizoguchi (1977) obtained an estimate of 1.63for the heritability of the entoconulid in a study of Japanese twins. He attributed this overestimation t o either sam ling bias or possibly dominance variance. evertheless, in general it seems that nongenetic, environmental factors are likely to contribute significantly to observed phenotypic variation in crown form, as has also been shown for crown size variables (Townsend, 1980; Potter et al., 1983). The entoconulid, like several other dental morphological traits, appears to fit the criteria of a quasi-continuous variable, showing a continuous range of expression with a threshold below which it is undetectable (Harris, 1977). The quasi-continuous model assumes an underlying scale of continuous variation related to the expression of the character, termed liability by Falconer (19651, that results from a combination of genetic and environmental factors. It seems that the genetic component of entoconulid variability is strongest on M1 in aboriginals, although the extremely hi h trait frequency for dm2 is a complicating actor in our analysis. As most individuals display the trait on dm2, comparisons between related and nonrelated individuals are not particularly illuminating. Kolakowski et al. (1980) noted significant major gene and common sibling environmental effects for Carabelli trait by ap lying a complex segregation analysis to I fata obtained from a large number of families living on the Solomon Islands. More recently, Nichol (1989) has also applied segregation
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ENTOCONULID EXPRESSION IN ABORIGINALS
analysis to family data in an attempt to clarify the mode of inheritance of a number of dental crown traits. Single-gene models rovided the best fit for some features, w ile others conformed to a polygenic model. In the latter instance, transmissibility estimates were low, averaging 0.36. Nichol concluded that both major genes and the environment have important roles in the development of dental crown morphology. More studies of this type are required to enable meaningful statistical testing of genetic models; they should be based on adequate samples of related individuals and include considerations of trait expression in both deciduous and permanent teeth. Our understanding of the genetic basis of dental traits needs to improve further in line with their increasing application in both anthropological and forensic areas.
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ACKNOWLEDGMENT
The dental casts were collected by T. Brown and the late M.J. Barrett with the support of Grant 02034 from the National Institutes of Health, Bethesda, Mar land. Currently the research is supported y the National Health and Medical Research Council, Canberra.
i
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