Heritability of Permanent Tooth Size GRAKT C TOWNSEND A N D TASMAN BROWN Thtr C'rlwcr\lty of Addardt,, Adc~lardr~, South A u ~ t r a l r a5000
K E Y WORDS Heritability
. Genetics .
Tooth size
Australian
Aboriginals
ABSTRACT
The aim of this investigation was to quantify the relative contributions of genetic and environmental influences to t h e observed variability of permanent tooth size in a group of Australian Aboriginals. Tooth size data were obtained from dental casts of Aboriginals living at Yuendumu in the Northern Territory of Australia. The custom of polygyny practised by these people enabled the analysis of associations between full-siblings and half-siblings. Phenotypic variability of tooth size was partitioned into four variance cumponents; between sides, between fathers, between mothers and between offspring. From these components. t h e relative genetic and environmental contributions were quantified and heritability estimates for tooth size derived. Additional estimates of heritability were obtained by regression analysis from a small sample of parent-offspring data. Results of t h e analyses suggested t h a t about 64% of t h e total variability of permanent tooth size could be attributed to genetic factors, while a further 6!K was due t o common environment. Although t h e findings confirm a relatively strong genetic component, they emphasise the importance of non-genetic influences in the determination of tooth size variability.
Tooth size, which exhibits a continuous range of variation, appears to conform to a polygenic model of inheritance (Bailit, '75; Harris, '75; Townsend and Brown, '78a). The variation in phenotypic expression of quantitative characters can be expressed in terms of genetic and environmental components; that is Vp = Vti VE, where Vp = total phenotypic variance, VL; = genetic variance, and VE = environmental variance. However, t h e relative importance of these contributors t o variability of tooth size is still unclear. The heritability of a character refers to the portion of t h e variation i n a population t h a t is due to genetic differences between individuals. It may be estimated from various types of family data, for example data obtained from twins? full-siblings, half-siblings or parents and offspring. Heritabilities tend to be overestimated when derived from twin or full-sibling data because of common environmental effects. On t h e other hand, paternal half-sibling data a r e less likely to be influenced by common environment and consequently they provide more reliable estimates of heritabilities.
+
AM. d P H Y S AWTHROP. (1978)49: 497-504
In this instance. heritability is expressed as t h e proportion of t h e total phenotypic variance due to additive genetic factors and it is generally denoted by the symbol h'; t h a t is, h = VAIVp, where VA = additive genetic variance and Vp is defined as above. Very few authors have reported heritabilities for permanent tooth size. Osborne et al. ('58) were amongst t h e first to compare phenotypic tooth size variability within and between related individuals although numerical estimates of heritabilities were not reported. Their analysis of twin data suggested a strong component of genetic variability for t h e mesiodistal size of anterior permanent teeth. By using a cross-twin analysis, they also provided evidence t h a t genetic factors may affect tooth size individually as well as collectively within t h e dentition. Goose ('71) estimated heritabilities for t h e mesiodistal diameters of maxillary permanent incisors and canines i n British families. The values derived from parent-offspring regressions were generally h i g h , around 0.60. Alvesalo a n d Tigerstedt ('74) analyzed data from full-sib-
49 7
498
GRANT C. TOWNSEND AND TASMAN BROWN
lings and provided heritability estimates for tooth size in a population living on t h e island of Hailuoto off t h e coast of Finland. They also calculated values for Swedes using the twin data of Lundstrom ('48). Although t h e findings of this study indicated t h a t t h e genetic contribution to tooth size variability was high, t h e authors recognized the limitations inherent in studies of this nature - "Because of t h e lack of valid human data about the extent of maternal influence or common environment on tooth size, i t is impossible to get any reliable estimate of t h e magnitude of total genetic variance of tooth sizes.'' Furthermore, Smith and Bailit ('771, in a review of genetic studies of dental occlusion, pointed out t h a t in t h e strict sense: heritability has not been determined for any traits of dental occlusion despite t h e fact t h a t it is t h e only estimate of real value in studies of human genetics. The present investigation is concerned with genetic aspects of permanent tooth size in a small population of Australian Aboriginals geographically isolated in t h e Northern Territory of Australia. The custom of polygyny practised by these people provided a rare opportunity for analyzing data derived from groups of full-siblings and half-siblings. METHODS
Measurements of mesiodistal and bucco lingual tooth diameters of t h e permanent teeth, excluding third molars, were recorded from dental casts collected as part of a longitudinal growth study of the Aboriginals living a t Yuendumu. Descriptions of Yuendumu, its inhabitants and their marriage patterns, together with t h e methods of tooth measurement have been reported previously (Brown a n d B a r r e t t , '71; Townsend a n d Brown, '78a,b). The sample for the-present study consisted of 124 male offspring from 40 fathers and 68 mothers, and 103 female offspring from 38 fathers and 57 mothers. The number of offspring from each mother varied from one to five. Data from male and female offspring were pooled for the genetic analysis after applying a correction factor, described below, to compensate for t h e sex dimorphism in tooth size. A further sample of 22 parents, 20 of whom were females, and 41 offspring provided a limited pool of 2-generation data. A previous report referred to t h e genealogical records of Yuendumu families t h a t were used to form t h e sibling groupings in this study (Townsend and Brown, '78a).
In the first stage of t h e data analysis, nested analysis of variance was used to partition tooth size variability into four components: between right and left sides, u.$ between fathers (T:, between mothers (T h, and between offspring, (r 8.The technique, which allows for unequal family sizes, was carried out according to Sokal and Rohlf ('69). Intraclass correlations for full-siblings, r F S , and half-siblings, r H s ,were then derived from t h e above components of variance as follows: rFS=(u$+ub)/u+;
+
r H S = u $/u
where
;+
u+ = (1
11;
+ h + 6. (1
fT
Standard errors of the intraclass correlations were calculated by t h e method of Falconer ('63). Heritabilities for t h e various measures of tooth size were estimated from t h e intraclass correlations in two alternative ways: twice t h e correlation between full-siblings and four times t h e correlation between half-siblings. Standard errors of the heritability estimates between full-siblings and half-siblings were also derived, being calculated as twice or four times t h e standard errors of t h e respective intraclass correlations. Finally, the relative contributions of genetic and environmental factors were interpreted from estimates of t h e variance components. Phenotypic variance was taken to be the sum of t h e four observed components: V p (100%)= u + = u h +
ui. + u + w &
Assuming the dominance variance to be small, t h e additive genetic variance, VA, common environmental variance, VEC, and withinfamily environmental variance, VEW, were then estimated from the variance components and expressed as percentages of Vp according to Falconer ('64): vA=4U$ VEC = (7 - u
b
6;
vgw=U&-zu;.
Although heritabilities were derived for all tooth size variables, the findings were summarized as weighted mean values, calculated on t h e basis of t h e degrees of freedom derived from t h e nested analysis of variance. Weighted means were derived similarly for the percentage contributions of VA, VECand VEWto t h e total variability. The above stages of the genetic analysis were carried out on tooth measurement d a t a pooled from male and female offspring. In
499
HERITABILITY OF PERMANENT TOOTH SIZE
order to justify a mixed-sibling form of analysis, t h e nested analysis of variance was first applied to t h e data for males and females separately. Comparisons of tooth size heritabilities derived from either full-sibling or half-sibling data did not reveal any syst e m a t i c t r e n d for heritabilities t o differ markedly between sexes. I n t h e males weighted mean values of h L calculated from full-sibling data were 0.89 t 0.11 and 0.91 0.11 for mesiodistal and buccolingual dimensions respectively. For the full-sibling female group t h e weighted means were 0.81 t 0.12 and 0.80 -+ 0.13. Heritabilities calculated from half-sibling data for the same dimensions were 0.84 0.47 and 0.99 4 0.47 in 0.60 i n males and 0.06 .t 0.66 and 0.56 females. The numerical values of heritabilities were on average lower in t h e two groups of female subjects and moreover, estimates
*
*
*
derived from half-sibling data were accompanied by large standard errors. However, sex differences in heritabilities were not statistically significant for either full-sibling or halfsibling comparisons. A previous finding t h a t sex differences in interclass correlations based on full-sibling data were numerically small and non-significant provided further support for t h e approach adopted in t h e present study (Townsend and Brown, '78a). Accordingly, t h e tooth measurements from males and females were combined to provide more extensive data for a mixed-sibling analysis. The standard errors of t h e estimated parameters were reduced substantially compared with those obtained from a separate analysis of male and female data. Previous studies have demonstrated t h a t all tooth dimensions, except the mesiodistal diameter of third molars, are significantly
TABLE 1
Values of uariance components derived from nested analysis of variance ofAboriginal tooth size data Variance components
Tooth Sides (n&
Mesiodistal Maxilla I1 I2 C P1 P2 M1 M2 Mandible I1 I2 C P1 P2 M1 M2
Buccolingual Maxilla 11 I2 C P1 P2
M1 M2 Mandible 11 12 C P1 P2 M1 M2
0.003 0.001 0.001 0.000 -0.001 0.001 0.001
0.077 0.083 0.024 0.063 0.046 0.016 0.079
0.044 0.001 0.060 0.024 0.030 0.111 0.077
0.183 0.329 0.173 0.115 0.097 0.165 0.232
0.000 0.002 0.002
0.020 0.015 0.026 0.023 0.058 0.014 0.038
0.037 0.044 0.040 0.054 0.021 0.081 0.100
0.092 0.108 0.105 0.154 0.161 0.232 0.302
-0.002 - 0.002 0.000 -0.002
0.059 0.073 0.080 0.041 0.053 0.021 0.037
0.059 0.019 0.014 0.088 0.080 0.155 0.166
0.143 0.217 0.233 0.177 0.171 0.181 0.236
-0.001 -0.002 -0.002 --0.001 -0.002 -0.001 0.001
0.021 0.035 0.044 0.057 0.055 0.071 0.066
0 054 0.023 0.050 0.103 0.062 0.075 0.074
0.122 0.133 0.136 0.157 0.186 0.177 0.181
~
~
~
0.000 -0.003 0.003 -0.002
0.000 0.000 0.000
500
GRANT C. TOWNSEND AND TASMAN BROWN TABLE 2
Heritahi1Lt.y estimates, h', and standard errors, SE, for permanent tooth size in Australian Aboriginals deiiued f r o m full-sibling correlations ' Mesindistal
BuccollnRu~l
Tooth hZ
SE
h'
SE
0.80 0.41 0.65 0.87 0.88 0.87 0.80
0.08 0.09 0.08 0.08 0.08 0.08 0.09
0.91 0.60 0.58 0.88 0.85 0.93
0.08 0.09 0.09 0.08 0.08 0.08 0.08
0.77 0.69 0.76 0.67 0.67 0.57 0.63
0.08 0.08 0.08 0.08 0.09 0.08 0.09
0.77 0.61 0.82 1.01 0.78 0.91 0.87
0.08 0.09 0.08 0.07 0.08 0.08 0.08
Maxilla
I1 I2 C P1 P2 M1 M2 Mandible 11 I2 C P1 P2 M1 M2 Weighted mean I
IS
0.72?0.08
0.85
0.812 0.08
h' calculated as twice t h e full~sihlingintrarlass correlation, t h a t h' = 2 r F S .
TABLE 3
Heritability estimates, h2, and standard errors, SE, for permanent tooth size i n Australian Ahorigznals derived f r o m h a l f ~ s i b l i n gcorrelations ' Mesindistal
Tooth
Maxilla I1 I2
c:
P1 P2 M1 M2
__
Buccolingunl
_______
h?
SE
h'
SE
1.02 0.81 0.36 1.25 1.06 0.22 0.82
0.28 0.25 0.32 0.27 0.29 0.34 0.32
0.91 0.94 0.54 0.70 -0.27 0.34
0.30 0.27 0.26 0.33 0.32 0.36 0.39
0.54 0.34 0.59 0.39 0.98 0.17 0.35
0.31 0.31 0.30 0.31 0.28 0.30 0.34
0.43 0.74 0.77 0.72 0.73 0.88 0.82
0.31 0.28 0.31 0.33 0.31 0.30 0.33
RESULTS
0.98
Mandibular
11 12 C P1 P2 M1 M2 Weighted mean
tion of equality of means between t h e groups considered, a correction factor was applied t o eliminate this sex difference in tooth size. This correction factor, equivalent to the absolute difference in mean values for each dimension between t h e sexes, was added to t h e individual female values, following the method of Alvesalo and Tigerstedt ('74). Some subjects, not included in t h e separate analyses of t h e males and females, were added to t h e pooled data, for example subjects who had sibling relatives of t h e opposite sex only. The combined analysis included 261 offspring derived from 67 fathers and 115 mothers. The number of wives for each husband varied from one to four, while the number of offspring from each mother ranged from one to eight. The availability of a small sample of twogeneration data enabled additional estimates of heritabilities to be made from t h e regressions of offspring on parent. The sex correction factor referred t o above was again applied to t h e data for females. The method outlined by Falconer ('63) was followed to calculate the regression coefficients for mesiodistal and buccolingual tooth dimensions. By using weighting coefficients as described by Kempthorne and Tandon ('531, allowance was made for families of different size. The heritability values were computed as twice t h e value of b , t h e regression of offspring on single parent; t h a t is, h' = 2b.
0.632 0.30
0.662 0.31
h' calculated as four tirnrs t h e half~aihhngintraclass correlation. t h a t I S . h' :4 7 ~ s . I
greater in Aboriginal males than females (Barrett et al., '63; Townsend and Brown, '78b). Because t h e calculation of intraclass correlation coefficients involves t h e assump-
The values of t h e variance components derived from t h e analysis of mesiodistal and buccolingual tooth dimensions are presented in table 1. Variability attributable t o side differences, mi, was small and non-significant for all teeth. Percentage contributions of cr; were in all instances less than 1.1%. Heritability estimates and their standard errors derived from full-sibling and half-sibling data, males and females combined, are shown in tables 2 and 3. Weighted mean values are included t o summarize results. Mean heritabilities in full-siblings were 0.72 f 0.08 for mesiodistal dimensions, and 0.81 i 0.08 for buccolingual dimensions. Mean values were lower in t h e half-siblings, being 0.63 +0.30 and 0.66 k 0.31 respectively. Contributions of genetic and environmental components to the total phenotypic variance were derived from t h e variance components shown in table 1by t h e method outlined previ-
501
HERITABILITY OF PERMANENT TOOTH SIZE
ously. For example, referring to t h e four components of variability for t h e mesiodistal dimension of t h e mandibular central incisor shown in table 1, t h e calculations were as follows: Vp(100%)=
CT;
+ T $ t ~h + ~6 = 0.149.
The percentage contributions of t h e four components a r e Ox, 13%.25% and 62% respectively. Since V A = 4 u $, t h e additive genetic variance was calculated to account for 52%of t h e observed variability. Common environmental ~ u - u ;-, contributed 12%, variance, V E = and within-family environment, VEW= (78 2tr $, contributed 36%. These calculations were carried out for each tooth and t h e results a r e summarized in table 4 which presents t h e contributions to phenotypic variance in the form of weighted means obtained from t h e values for individual teeth. The weighted mean percentage contributions shown in table 4 suggest t h a t additive genetic variance accounted for about 64% of total phenotypic variability, common environment contributed about 6X, and within-family environment t h e remaining 30%. Table 5 presents heritability estimates and standard errors derived from regressions of offspring on parent and calculated by the method of Falconer ('63). The weighted mean heritabilities were 0.64 0.35 for mesiodistal dimensions and 0.57 0.37 for buccolingual dimensions. Estimates of mean heritability values for permanent tooth size derived from full-sibling, half-sibling and parent-offspring data are summarized in table 6. The relatively large standard errors associated with estimates based on half-sibling and parent-offspring data were due to t h e small sample sizes available. From these results it appears t h a t about 64% of t h e total variability in permanent tooth size can be attributed to additive genetic effects operating in t h e population under observation.
tf
*
*
DISCUSSION
Although it is generally assumed t h a t tooth size is under strong genetic control, few estimates of heritability for this metric character have been reported for human populations. Furthermore, heritability estimates t h a t are available have generally been derived from either full-sibling or twin data. Values obtained from this type of data tend to overestimate t h e contribution of genetic factors to t h e
'TABLE 4
Weighted mean. estimates o f t h e percentage contrrbulions to phenotypic variu bility of tooth size VarianrP cornponrrrt,
Tooth dimension
Additive
Common environment
genetic V4
Mesiodistal Buccolingual
Both
VEC
Within family cnvironmmt VEW
x, 4 8
8 63 66 64
% 33 26 30
6
TABLE 5
Heritability estimates, h', and standard errors, SE, for p e r manent tooth size i n Australian Aboriginals, derived f r o m regression of offspring on parents. (Mean uulues f o r right and left side t m t h prrsrntedj Mesiodistal
Biiccolingual
Tnoth
Maxilla I1 I2
C P1 P2 M1 M2 Mandible I1 12
C P1 P2 M1 M2 Weighted mean
h'
SE
hi
SE
0.27 0.50 0.35 0.73 0.83 0.26 0.77
0.36 0 27 0 37 0.30 0.38 036 0 25
0.14 0.33 0.78 0.90 0.79 0.16 0.45
0.39 0.28 0.51 0.30 0.27 0.38 0.35
0.35 0.21 0.85 154 1.15 0.57 0.61
0.32 0.27 0.36 0.44 042 0.31 0 47
0.06 0.35 0.47 0.85 0.81 0.93 0.99
0.31 0.23 0.35 0.37 0.33 0.49 0.49
0.64? 0.35
0.5750.37
TABLE 6
S u m m a r y o f estimates of mean heritability values for permanent tooth size, with standard errors, derived f r o m genetic analyses Relationship
Mesicdistal
Buccolingual
Half-sibling Full -sibling Parent-offspring
0 . 6 3 t 0.30 0.72+0.08 0.64T 0.35
0.66k0.31 0.81 0.08 0.5750.37
_____
*
-
observed variability because of common environmental influences. The assumption of polygenic inheritance is implicit in t h e present analysis but t h e possibility t h a t other genetic models may be applied to tooth size d a t a is acknowledged. However, most evidence suggests that a polygenic
502
GRANT C. TOWNSEND AND TASMAN BROWN
model is likely for t h e inheritance of tooth size. Although t h e validity of linear models for partitioning variance components has been questioned by some (Lewontin, '74; Feldman and Lewontin, '751, t h e use of nested analysis of variance in t h e present study enabled a comprehensive survey of t h e available fullsibling and half-sibling data. Different values for t h e genetic parameters might be expected with other models and assumptions, however the present findings have provided estimates of heritability in its narrow sense and indicated t h e importance of common environmental effects in determining tooth size variability. Inbreeding in a population, resulting from the mating of related individuals, leads to changes in genotypic frequencies. High levels of inbreeding, such as expected in small isolated communities, can alter the variance components within and between families. Boettcher ('75), on t h e basis of serological information, has estimated t h a t the coefficient of inbreeding is of the order of 0.05 for the Yuendumu population. White and Parsons ('76) have estimated t h e average level of inbreeding in a traditionally structured group of Australian Aboriginals living in northeastern Arnhem Land in the Northern Territory to be 0.02. As far a s could be ascertained, no offspring of first cousin marriages were included in the present study. Under these circumstances t h e effects of inbreeding on estimates of genetic variance would undoubtedly be very small. For this reason mathematical expressions taking inbreeding into account were not included in the genetic analysis. The results of this study do not confirm t h e hypothesis t h a t genetic factors may account for up to 90% of t h e total variability in tooth size (Garn et al., '65). Heritability values derived from the various types of family d a t a suggest t h a t t h e contribution of additive genetic variance is less in Australian Aboriginals - around 64%on average. Alvesalo and Tigerstedt ('74) reported heritability estimates for permanent tooth size in Finns derived from the analysis of full-sibling data. Heritability values averaged 0.54 0.23 for mesiodistal dimensions and 0.68 0.27 for buccolingual dimensions. Although t h e s e values a r e slightly less than those calculated for t h e Yuendumu Aboriginals, it should be emphasized t h a t heritability values refer to
* *
particular populations living under specific environmental conditions. Comparisons of heritability values derived from different populations must therefore be made with care. It has been suggested t h a t t h e earlier developing teeth in each tooth class display higher heritabilities than the later developing members (Alvesalo and Tigerstedt, '74; Sofaer et al., '71). Furthermore, Sofaer et al. ('72) reported t h a t additive genetic variance contributed less to tooth size variability for t h e later developing teeth. This observation led these authors to propose t h a t the increased morphological variability observed in t h e later developing teeth within a tooth class is likely to result from a relatively larger environmental component of variance. Although t h e results of t h e present study suggest t h a t a similar division of variance exists in t h e Aboriginal dentition, t h e evidence is by no means conclusive. The interpretation of heritability estimat.es based on half-sibling data was difficult because they ranged in value considerably. Estimates derived from t h e full-sibling data were generally higher for t h e earlier developing tooth, but several exceptions were noted. Further investigation is required to clarify this point. The variance due to common environment, V F , ~was , estimated to account for about 6%of t h e total variance of permanent tooth size. There was some evidence t h a t common environment influenced tooth size variability more for buccolingual dimensions than for mesiodistal. V E C was estimated to account for about 8%of t h e buccolingual variability compared with 4% for mesiodistal dimensions. This result could account for the observed tendency of phenotypic correlations between fullsiblings based on buccolingual dimensions t o be greater t h a n those derived from mesiodistal dimensions. It also supports the findings of Sofaer et al. ('71) who compared correlations for both dimensions between sibling and parent-offspring pairs in two Melanesian tribes. They found no differences between t h e two types of correlations for mesiodistal dimensions but noted t h a t correlations between siblings for buccolingual dimensions were generally higher than those between parentoffspring pairs. They suggested t h a t dominance and common environmental influences might account for these differences. Common environmental effects may be prenatal or postnatal. Most studies in experimen-
HERITABILITY OF PERMANENT TOOTH SIZE
tal animals have emphasized t h e importance of prenatal effects (Paynter and Grainger, '56; Holloway et al., '61). It seems t h a t prenatal factors are also likely to be important in influencing t h e human dentition, particularly with respect to tooth size as calcification of the crowns of all primary and permanent teeth, except t h e third molars, begins within t h e period extending from about three months in utero until three years postnatal. Bailit and Sung ('68) investigated the role of maternal effects on t h e developing dentition in Caucasians using maternal age, birth order and birth weight as indicators of intra-uterine environmental conditions. Birth weight and maternal age were both shown to have a statistically significant correlation with dental development. The importance of birth weight on dental development was also noted in a large sample of Japanese children (Bailit et a]., ' 6 8 ) . Furthermore, Keene ('71) found t h a t low birth weight was associated with a reduction in permanent tooth size in a study of caries-free naval recruits. Bader ('65) found t h a t t h e common environmental variance, which h e also termed maternal effect, for molar tooth widths in mice ranged from 16.8% to 25.0%of t h e total variance. While the mean value of 6% estimated for V E in ~ this study is less, t h e importance of t h e maternal effect in human tooth size variation warrants further investigation. The value of estimating heritabilities from quantitative characters has been queried by some (Feldman and L,ewontin, '75). Certainly heritabilities derived from full-sibling d a t a have limited application due t o t h e compounding effects of common environment. However, estimates derived from half-siblings give a direct insight into t h e contribution of additive genetic effects to observed variability. Quantification of these parameters is worthwhile, not only to increase t h e understanding of tooth size variability and its determinants, but also because this type of information is relevant to studies of human evolution, a field in which dental observations often provide useful data. Tooth size variability appears to have a strong genetic component, but environmental factors are also of importance. Further family studies designed to elucidate the contribution and nature of these components are needed. Segregation and linkage analyses may indicate t h e presence of major genes, t h a t is,
503
genes with large effects within t h e normal range of variability and as Smith and Bailit ('77) have indicated, t h e investigation of major genes of this type, once identified, could have far-reaching implications. ACKNOWLEDGMENTS
The growth study which has provided data for this investigation was supported by Research Grant DE 02034 from the National Institute of Dental Research, Bethesda, Maryland and by grants from The University of Adelaide and t h e Australian Jnstitute of Aboriginal Studies, Canberra. Our late colleague, M. J. Barrett, of The University of Adelaide, obtained t h e dental casts used in t h e study. The analysis of data was carried out during t h e tenure of a Postgraduate Research Scholarship awarded by t h e National Health and Medical Research Council of Australia. We acknowledge t h e assistance of Doctor G. Mayo, Department of Genetics, The University of Adelaide, who provided very helpful comments on t h e study methods. LITERATURE CITED Alvesalo, L., and P. M. A. Tigerstedt 1974 Heritab~litiesof human tooth dimensions. Hereditas, 77: 311-318. Bader, R. S. 1965 Heritability of dental characters in the house mouse. Evolution, 19: 378-384. Bailit, H. L. 1975 Dental variation among populations. Dent. Clin. N.Amer., 19: 125-139. Bailit, H. L., J. D. Niswander and C. J. MacLean 1968 The relationship among several prenatal factors and variation in the nermanent dentition in Jananese children. Growth, 32 '331 345 Bailit, H L , and B Sung 1968 Maternal effects on the de veloping dentition. Arch. Oral Biol., 13: 155-161. Barrett, M. J., T. Brown and M. R. Macdonald 1963 Dental observations on Australian Aborigines: mesiodistal crown diameters of permanent teeth. Aust. Dent. J., 8: 150-155. Boettcher, B. 1975 Personal communication. Brown, T., and M. J . Barrett 1971 Growth in Central Australian Aborigines: stature. Med. J. Aust., 2: 29-33. Falconer, D. S. 1963 Quantitative Inheritance. In: Methodology in Mammalian Genetics. W. J. Burdette, ed. Holden-Day, San Francisco, pp. 193-216. 1964 Introduction to Quantitative Genetics. Oliver and Boyd, Edinburgh, pp. 165-185. Feldman, M. W., and R. C. Lewontin 1975 The heritability hang-up. Science, 190: 1163-1168. Garn, S. M., A. B. Lewis and R. S. Kerewsky 1965 Genetic, nutritional, and maturational correlates of dental development. J. Dent. Res., 44: 228-242. Goose, D. H. 1971 The inheritance of tooth size in British families. In: Dental Morphology and Evolution. A. A. Dahlberg, ed. The University of Chicago Press, Chicago and London, pp. 263-270. Harris, J. E. 1975 Genetic factors in the growth of t h e bead. Dent. Clin. PIT. Amer.. 19: 151-160.
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GRANT C. TOWNSEND AND TASMAN BROWN
Holloway, P. J.. J. H. Shaw and E. A. Sweeney 1961 Effects of various sucrose-casein ratios i n purified diets on t h e teeth and supporting structures of rats. Arch. Oral Biol.. 3: 185-200. Keene, H. J. 1971 Epidemiologic study of tooth size variability i n caries-free naval recruits. J. Dent. Res., 50: 1331-1345. Kempthorne, O., and 0 . B. Tandon 1953 The estimation of heritability by regression of offspring on parent. Biometrics. 9: 90-100. Lewontin, H. C. 1974 The analysis of variance and t h e analysis of causes. Am. J. Hum. Genet., 26: 400-411. Lundstrom, A. 1948 Tooth Size and Occlusion in Twins. S. Karger. Basle. Osborne. R. H., S. L. Horowitz and F. V. DeGeorge 1958 Genetic variation in tooth dimensions: a twin study of permanent anterior teeth. Am. J. Hum. Genet., 10: 350-356. Paynter, K. J.. and R. M. Grainger 1956 The relation of nutrition t o t h e morphology andsize of r a t molar teeth. .J. Can. Dent. Assoc.. 22: 519-531. Smith, R. J.. and H. L. Bailit 1977 Problems and methods in
research on the genetics of dental occlusion. Angle Orthodont.. 47: 65-77. Sofaer, J. A,, H. L. Bailit and C. J. MacLean 1971 A developmental basis for differential tooth reduction during hominid evolution. Evolution, 25: 509-517. Sofaer, *J. A.. C. J . MacLean and H. L. Bailit 1972 Heredity and morphological variation in early and late developing human teeth of the same morphological class. Arch. Oral Biol., 17: 811-816. Sokal, R. R., and F. J. Rohlf 1969 Biometry. W. H. Freeman and Co., San Francisco, pp. 274-279. Townsend. G. C . , and T. Brown 1978a Inheritance of tooth size in Australian Aboriginals. Am. J. Phys. Anthrop., 48: 305-314. 1978h Tooth size characteristics of Australian Aborigines. Occasional papers i n Human Biology. Aust. Inst. Abor. Stud., Canberra, in press. White, N. G., and P. A. Parsons 1976 Population genetic, social. linguistic and topographical relationships i n north-eastern Arnhem Land, Australia. Nature, 261: 223-225.
K E Y WORDS Heritability
. Genetics .
Tooth size
Australian
Aboriginals
ABSTRACT
The aim of this investigation was to quantify the relative contributions of genetic and environmental influences to t h e observed variability of permanent tooth size in a group of Australian Aboriginals. Tooth size data were obtained from dental casts of Aboriginals living at Yuendumu in the Northern Territory of Australia. The custom of polygyny practised by these people enabled the analysis of associations between full-siblings and half-siblings. Phenotypic variability of tooth size was partitioned into four variance cumponents; between sides, between fathers, between mothers and between offspring. From these components. t h e relative genetic and environmental contributions were quantified and heritability estimates for tooth size derived. Additional estimates of heritability were obtained by regression analysis from a small sample of parent-offspring data. Results of t h e analyses suggested t h a t about 64% of t h e total variability of permanent tooth size could be attributed to genetic factors, while a further 6!K was due t o common environment. Although t h e findings confirm a relatively strong genetic component, they emphasise the importance of non-genetic influences in the determination of tooth size variability.
Tooth size, which exhibits a continuous range of variation, appears to conform to a polygenic model of inheritance (Bailit, '75; Harris, '75; Townsend and Brown, '78a). The variation in phenotypic expression of quantitative characters can be expressed in terms of genetic and environmental components; that is Vp = Vti VE, where Vp = total phenotypic variance, VL; = genetic variance, and VE = environmental variance. However, t h e relative importance of these contributors t o variability of tooth size is still unclear. The heritability of a character refers to the portion of t h e variation i n a population t h a t is due to genetic differences between individuals. It may be estimated from various types of family data, for example data obtained from twins? full-siblings, half-siblings or parents and offspring. Heritabilities tend to be overestimated when derived from twin or full-sibling data because of common environmental effects. On t h e other hand, paternal half-sibling data a r e less likely to be influenced by common environment and consequently they provide more reliable estimates of heritabilities.
+
AM. d P H Y S AWTHROP. (1978)49: 497-504
In this instance. heritability is expressed as t h e proportion of t h e total phenotypic variance due to additive genetic factors and it is generally denoted by the symbol h'; t h a t is, h = VAIVp, where VA = additive genetic variance and Vp is defined as above. Very few authors have reported heritabilities for permanent tooth size. Osborne et al. ('58) were amongst t h e first to compare phenotypic tooth size variability within and between related individuals although numerical estimates of heritabilities were not reported. Their analysis of twin data suggested a strong component of genetic variability for t h e mesiodistal size of anterior permanent teeth. By using a cross-twin analysis, they also provided evidence t h a t genetic factors may affect tooth size individually as well as collectively within t h e dentition. Goose ('71) estimated heritabilities for t h e mesiodistal diameters of maxillary permanent incisors and canines i n British families. The values derived from parent-offspring regressions were generally h i g h , around 0.60. Alvesalo a n d Tigerstedt ('74) analyzed data from full-sib-
49 7
498
GRANT C. TOWNSEND AND TASMAN BROWN
lings and provided heritability estimates for tooth size in a population living on t h e island of Hailuoto off t h e coast of Finland. They also calculated values for Swedes using the twin data of Lundstrom ('48). Although t h e findings of this study indicated t h a t t h e genetic contribution to tooth size variability was high, t h e authors recognized the limitations inherent in studies of this nature - "Because of t h e lack of valid human data about the extent of maternal influence or common environment on tooth size, i t is impossible to get any reliable estimate of t h e magnitude of total genetic variance of tooth sizes.'' Furthermore, Smith and Bailit ('771, in a review of genetic studies of dental occlusion, pointed out t h a t in t h e strict sense: heritability has not been determined for any traits of dental occlusion despite t h e fact t h a t it is t h e only estimate of real value in studies of human genetics. The present investigation is concerned with genetic aspects of permanent tooth size in a small population of Australian Aboriginals geographically isolated in t h e Northern Territory of Australia. The custom of polygyny practised by these people provided a rare opportunity for analyzing data derived from groups of full-siblings and half-siblings. METHODS
Measurements of mesiodistal and bucco lingual tooth diameters of t h e permanent teeth, excluding third molars, were recorded from dental casts collected as part of a longitudinal growth study of the Aboriginals living a t Yuendumu. Descriptions of Yuendumu, its inhabitants and their marriage patterns, together with t h e methods of tooth measurement have been reported previously (Brown a n d B a r r e t t , '71; Townsend a n d Brown, '78a,b). The sample for the-present study consisted of 124 male offspring from 40 fathers and 68 mothers, and 103 female offspring from 38 fathers and 57 mothers. The number of offspring from each mother varied from one to five. Data from male and female offspring were pooled for the genetic analysis after applying a correction factor, described below, to compensate for t h e sex dimorphism in tooth size. A further sample of 22 parents, 20 of whom were females, and 41 offspring provided a limited pool of 2-generation data. A previous report referred to t h e genealogical records of Yuendumu families t h a t were used to form t h e sibling groupings in this study (Townsend and Brown, '78a).
In the first stage of t h e data analysis, nested analysis of variance was used to partition tooth size variability into four components: between right and left sides, u.$ between fathers (T:, between mothers (T h, and between offspring, (r 8.The technique, which allows for unequal family sizes, was carried out according to Sokal and Rohlf ('69). Intraclass correlations for full-siblings, r F S , and half-siblings, r H s ,were then derived from t h e above components of variance as follows: rFS=(u$+ub)/u+;
+
r H S = u $/u
where
;+
u+ = (1
11;
+ h + 6. (1
fT
Standard errors of the intraclass correlations were calculated by t h e method of Falconer ('63). Heritabilities for t h e various measures of tooth size were estimated from t h e intraclass correlations in two alternative ways: twice t h e correlation between full-siblings and four times t h e correlation between half-siblings. Standard errors of the heritability estimates between full-siblings and half-siblings were also derived, being calculated as twice or four times t h e standard errors of t h e respective intraclass correlations. Finally, the relative contributions of genetic and environmental factors were interpreted from estimates of t h e variance components. Phenotypic variance was taken to be the sum of t h e four observed components: V p (100%)= u + = u h +
ui. + u + w &
Assuming the dominance variance to be small, t h e additive genetic variance, VA, common environmental variance, VEC, and withinfamily environmental variance, VEW, were then estimated from the variance components and expressed as percentages of Vp according to Falconer ('64): vA=4U$ VEC = (7 - u
b
6;
vgw=U&-zu;.
Although heritabilities were derived for all tooth size variables, the findings were summarized as weighted mean values, calculated on t h e basis of t h e degrees of freedom derived from t h e nested analysis of variance. Weighted means were derived similarly for the percentage contributions of VA, VECand VEWto t h e total variability. The above stages of the genetic analysis were carried out on tooth measurement d a t a pooled from male and female offspring. In
499
HERITABILITY OF PERMANENT TOOTH SIZE
order to justify a mixed-sibling form of analysis, t h e nested analysis of variance was first applied to t h e data for males and females separately. Comparisons of tooth size heritabilities derived from either full-sibling or half-sibling data did not reveal any syst e m a t i c t r e n d for heritabilities t o differ markedly between sexes. I n t h e males weighted mean values of h L calculated from full-sibling data were 0.89 t 0.11 and 0.91 0.11 for mesiodistal and buccolingual dimensions respectively. For the full-sibling female group t h e weighted means were 0.81 t 0.12 and 0.80 -+ 0.13. Heritabilities calculated from half-sibling data for the same dimensions were 0.84 0.47 and 0.99 4 0.47 in 0.60 i n males and 0.06 .t 0.66 and 0.56 females. The numerical values of heritabilities were on average lower in t h e two groups of female subjects and moreover, estimates
*
*
*
derived from half-sibling data were accompanied by large standard errors. However, sex differences in heritabilities were not statistically significant for either full-sibling or halfsibling comparisons. A previous finding t h a t sex differences in interclass correlations based on full-sibling data were numerically small and non-significant provided further support for t h e approach adopted in t h e present study (Townsend and Brown, '78a). Accordingly, t h e tooth measurements from males and females were combined to provide more extensive data for a mixed-sibling analysis. The standard errors of t h e estimated parameters were reduced substantially compared with those obtained from a separate analysis of male and female data. Previous studies have demonstrated t h a t all tooth dimensions, except the mesiodistal diameter of third molars, are significantly
TABLE 1
Values of uariance components derived from nested analysis of variance ofAboriginal tooth size data Variance components
Tooth Sides (n&
Mesiodistal Maxilla I1 I2 C P1 P2 M1 M2 Mandible I1 I2 C P1 P2 M1 M2
Buccolingual Maxilla 11 I2 C P1 P2
M1 M2 Mandible 11 12 C P1 P2 M1 M2
0.003 0.001 0.001 0.000 -0.001 0.001 0.001
0.077 0.083 0.024 0.063 0.046 0.016 0.079
0.044 0.001 0.060 0.024 0.030 0.111 0.077
0.183 0.329 0.173 0.115 0.097 0.165 0.232
0.000 0.002 0.002
0.020 0.015 0.026 0.023 0.058 0.014 0.038
0.037 0.044 0.040 0.054 0.021 0.081 0.100
0.092 0.108 0.105 0.154 0.161 0.232 0.302
-0.002 - 0.002 0.000 -0.002
0.059 0.073 0.080 0.041 0.053 0.021 0.037
0.059 0.019 0.014 0.088 0.080 0.155 0.166
0.143 0.217 0.233 0.177 0.171 0.181 0.236
-0.001 -0.002 -0.002 --0.001 -0.002 -0.001 0.001
0.021 0.035 0.044 0.057 0.055 0.071 0.066
0 054 0.023 0.050 0.103 0.062 0.075 0.074
0.122 0.133 0.136 0.157 0.186 0.177 0.181
~
~
~
0.000 -0.003 0.003 -0.002
0.000 0.000 0.000
500
GRANT C. TOWNSEND AND TASMAN BROWN TABLE 2
Heritahi1Lt.y estimates, h', and standard errors, SE, for permanent tooth size in Australian Aboriginals deiiued f r o m full-sibling correlations ' Mesindistal
BuccollnRu~l
Tooth hZ
SE
h'
SE
0.80 0.41 0.65 0.87 0.88 0.87 0.80
0.08 0.09 0.08 0.08 0.08 0.08 0.09
0.91 0.60 0.58 0.88 0.85 0.93
0.08 0.09 0.09 0.08 0.08 0.08 0.08
0.77 0.69 0.76 0.67 0.67 0.57 0.63
0.08 0.08 0.08 0.08 0.09 0.08 0.09
0.77 0.61 0.82 1.01 0.78 0.91 0.87
0.08 0.09 0.08 0.07 0.08 0.08 0.08
Maxilla
I1 I2 C P1 P2 M1 M2 Mandible 11 I2 C P1 P2 M1 M2 Weighted mean I
IS
0.72?0.08
0.85
0.812 0.08
h' calculated as twice t h e full~sihlingintrarlass correlation, t h a t h' = 2 r F S .
TABLE 3
Heritability estimates, h2, and standard errors, SE, for permanent tooth size i n Australian Ahorigznals derived f r o m h a l f ~ s i b l i n gcorrelations ' Mesindistal
Tooth
Maxilla I1 I2
c:
P1 P2 M1 M2
__
Buccolingunl
_______
h?
SE
h'
SE
1.02 0.81 0.36 1.25 1.06 0.22 0.82
0.28 0.25 0.32 0.27 0.29 0.34 0.32
0.91 0.94 0.54 0.70 -0.27 0.34
0.30 0.27 0.26 0.33 0.32 0.36 0.39
0.54 0.34 0.59 0.39 0.98 0.17 0.35
0.31 0.31 0.30 0.31 0.28 0.30 0.34
0.43 0.74 0.77 0.72 0.73 0.88 0.82
0.31 0.28 0.31 0.33 0.31 0.30 0.33
RESULTS
0.98
Mandibular
11 12 C P1 P2 M1 M2 Weighted mean
tion of equality of means between t h e groups considered, a correction factor was applied t o eliminate this sex difference in tooth size. This correction factor, equivalent to the absolute difference in mean values for each dimension between t h e sexes, was added to t h e individual female values, following the method of Alvesalo and Tigerstedt ('74). Some subjects, not included in t h e separate analyses of t h e males and females, were added to t h e pooled data, for example subjects who had sibling relatives of t h e opposite sex only. The combined analysis included 261 offspring derived from 67 fathers and 115 mothers. The number of wives for each husband varied from one to four, while the number of offspring from each mother ranged from one to eight. The availability of a small sample of twogeneration data enabled additional estimates of heritabilities to be made from t h e regressions of offspring on parent. The sex correction factor referred t o above was again applied to t h e data for females. The method outlined by Falconer ('63) was followed to calculate the regression coefficients for mesiodistal and buccolingual tooth dimensions. By using weighting coefficients as described by Kempthorne and Tandon ('531, allowance was made for families of different size. The heritability values were computed as twice t h e value of b , t h e regression of offspring on single parent; t h a t is, h' = 2b.
0.632 0.30
0.662 0.31
h' calculated as four tirnrs t h e half~aihhngintraclass correlation. t h a t I S . h' :4 7 ~ s . I
greater in Aboriginal males than females (Barrett et al., '63; Townsend and Brown, '78b). Because t h e calculation of intraclass correlation coefficients involves t h e assump-
The values of t h e variance components derived from t h e analysis of mesiodistal and buccolingual tooth dimensions are presented in table 1. Variability attributable t o side differences, mi, was small and non-significant for all teeth. Percentage contributions of cr; were in all instances less than 1.1%. Heritability estimates and their standard errors derived from full-sibling and half-sibling data, males and females combined, are shown in tables 2 and 3. Weighted mean values are included t o summarize results. Mean heritabilities in full-siblings were 0.72 f 0.08 for mesiodistal dimensions, and 0.81 i 0.08 for buccolingual dimensions. Mean values were lower in t h e half-siblings, being 0.63 +0.30 and 0.66 k 0.31 respectively. Contributions of genetic and environmental components to the total phenotypic variance were derived from t h e variance components shown in table 1by t h e method outlined previ-
501
HERITABILITY OF PERMANENT TOOTH SIZE
ously. For example, referring to t h e four components of variability for t h e mesiodistal dimension of t h e mandibular central incisor shown in table 1, t h e calculations were as follows: Vp(100%)=
CT;
+ T $ t ~h + ~6 = 0.149.
The percentage contributions of t h e four components a r e Ox, 13%.25% and 62% respectively. Since V A = 4 u $, t h e additive genetic variance was calculated to account for 52%of t h e observed variability. Common environmental ~ u - u ;-, contributed 12%, variance, V E = and within-family environment, VEW= (78 2tr $, contributed 36%. These calculations were carried out for each tooth and t h e results a r e summarized in table 4 which presents t h e contributions to phenotypic variance in the form of weighted means obtained from t h e values for individual teeth. The weighted mean percentage contributions shown in table 4 suggest t h a t additive genetic variance accounted for about 64% of total phenotypic variability, common environment contributed about 6X, and within-family environment t h e remaining 30%. Table 5 presents heritability estimates and standard errors derived from regressions of offspring on parent and calculated by the method of Falconer ('63). The weighted mean heritabilities were 0.64 0.35 for mesiodistal dimensions and 0.57 0.37 for buccolingual dimensions. Estimates of mean heritability values for permanent tooth size derived from full-sibling, half-sibling and parent-offspring data are summarized in table 6. The relatively large standard errors associated with estimates based on half-sibling and parent-offspring data were due to t h e small sample sizes available. From these results it appears t h a t about 64% of t h e total variability in permanent tooth size can be attributed to additive genetic effects operating in t h e population under observation.
tf
*
*
DISCUSSION
Although it is generally assumed t h a t tooth size is under strong genetic control, few estimates of heritability for this metric character have been reported for human populations. Furthermore, heritability estimates t h a t are available have generally been derived from either full-sibling or twin data. Values obtained from this type of data tend to overestimate t h e contribution of genetic factors to t h e
'TABLE 4
Weighted mean. estimates o f t h e percentage contrrbulions to phenotypic variu bility of tooth size VarianrP cornponrrrt,
Tooth dimension
Additive
Common environment
genetic V4
Mesiodistal Buccolingual
Both
VEC
Within family cnvironmmt VEW
x, 4 8
8 63 66 64
% 33 26 30
6
TABLE 5
Heritability estimates, h', and standard errors, SE, for p e r manent tooth size i n Australian Aboriginals, derived f r o m regression of offspring on parents. (Mean uulues f o r right and left side t m t h prrsrntedj Mesiodistal
Biiccolingual
Tnoth
Maxilla I1 I2
C P1 P2 M1 M2 Mandible I1 12
C P1 P2 M1 M2 Weighted mean
h'
SE
hi
SE
0.27 0.50 0.35 0.73 0.83 0.26 0.77
0.36 0 27 0 37 0.30 0.38 036 0 25
0.14 0.33 0.78 0.90 0.79 0.16 0.45
0.39 0.28 0.51 0.30 0.27 0.38 0.35
0.35 0.21 0.85 154 1.15 0.57 0.61
0.32 0.27 0.36 0.44 042 0.31 0 47
0.06 0.35 0.47 0.85 0.81 0.93 0.99
0.31 0.23 0.35 0.37 0.33 0.49 0.49
0.64? 0.35
0.5750.37
TABLE 6
S u m m a r y o f estimates of mean heritability values for permanent tooth size, with standard errors, derived f r o m genetic analyses Relationship
Mesicdistal
Buccolingual
Half-sibling Full -sibling Parent-offspring
0 . 6 3 t 0.30 0.72+0.08 0.64T 0.35
0.66k0.31 0.81 0.08 0.5750.37
_____
*
-
observed variability because of common environmental influences. The assumption of polygenic inheritance is implicit in t h e present analysis but t h e possibility t h a t other genetic models may be applied to tooth size d a t a is acknowledged. However, most evidence suggests that a polygenic
502
GRANT C. TOWNSEND AND TASMAN BROWN
model is likely for t h e inheritance of tooth size. Although t h e validity of linear models for partitioning variance components has been questioned by some (Lewontin, '74; Feldman and Lewontin, '751, t h e use of nested analysis of variance in t h e present study enabled a comprehensive survey of t h e available fullsibling and half-sibling data. Different values for t h e genetic parameters might be expected with other models and assumptions, however the present findings have provided estimates of heritability in its narrow sense and indicated t h e importance of common environmental effects in determining tooth size variability. Inbreeding in a population, resulting from the mating of related individuals, leads to changes in genotypic frequencies. High levels of inbreeding, such as expected in small isolated communities, can alter the variance components within and between families. Boettcher ('75), on t h e basis of serological information, has estimated t h a t the coefficient of inbreeding is of the order of 0.05 for the Yuendumu population. White and Parsons ('76) have estimated t h e average level of inbreeding in a traditionally structured group of Australian Aboriginals living in northeastern Arnhem Land in the Northern Territory to be 0.02. As far a s could be ascertained, no offspring of first cousin marriages were included in the present study. Under these circumstances t h e effects of inbreeding on estimates of genetic variance would undoubtedly be very small. For this reason mathematical expressions taking inbreeding into account were not included in the genetic analysis. The results of this study do not confirm t h e hypothesis t h a t genetic factors may account for up to 90% of t h e total variability in tooth size (Garn et al., '65). Heritability values derived from the various types of family d a t a suggest t h a t t h e contribution of additive genetic variance is less in Australian Aboriginals - around 64%on average. Alvesalo and Tigerstedt ('74) reported heritability estimates for permanent tooth size in Finns derived from the analysis of full-sibling data. Heritability values averaged 0.54 0.23 for mesiodistal dimensions and 0.68 0.27 for buccolingual dimensions. Although t h e s e values a r e slightly less than those calculated for t h e Yuendumu Aboriginals, it should be emphasized t h a t heritability values refer to
* *
particular populations living under specific environmental conditions. Comparisons of heritability values derived from different populations must therefore be made with care. It has been suggested t h a t t h e earlier developing teeth in each tooth class display higher heritabilities than the later developing members (Alvesalo and Tigerstedt, '74; Sofaer et al., '71). Furthermore, Sofaer et al. ('72) reported t h a t additive genetic variance contributed less to tooth size variability for t h e later developing teeth. This observation led these authors to propose t h a t the increased morphological variability observed in t h e later developing teeth within a tooth class is likely to result from a relatively larger environmental component of variance. Although t h e results of t h e present study suggest t h a t a similar division of variance exists in t h e Aboriginal dentition, t h e evidence is by no means conclusive. The interpretation of heritability estimat.es based on half-sibling data was difficult because they ranged in value considerably. Estimates derived from t h e full-sibling data were generally higher for t h e earlier developing tooth, but several exceptions were noted. Further investigation is required to clarify this point. The variance due to common environment, V F , ~was , estimated to account for about 6%of t h e total variance of permanent tooth size. There was some evidence t h a t common environment influenced tooth size variability more for buccolingual dimensions than for mesiodistal. V E C was estimated to account for about 8%of t h e buccolingual variability compared with 4% for mesiodistal dimensions. This result could account for the observed tendency of phenotypic correlations between fullsiblings based on buccolingual dimensions t o be greater t h a n those derived from mesiodistal dimensions. It also supports the findings of Sofaer et al. ('71) who compared correlations for both dimensions between sibling and parent-offspring pairs in two Melanesian tribes. They found no differences between t h e two types of correlations for mesiodistal dimensions but noted t h a t correlations between siblings for buccolingual dimensions were generally higher than those between parentoffspring pairs. They suggested t h a t dominance and common environmental influences might account for these differences. Common environmental effects may be prenatal or postnatal. Most studies in experimen-
HERITABILITY OF PERMANENT TOOTH SIZE
tal animals have emphasized t h e importance of prenatal effects (Paynter and Grainger, '56; Holloway et al., '61). It seems t h a t prenatal factors are also likely to be important in influencing t h e human dentition, particularly with respect to tooth size as calcification of the crowns of all primary and permanent teeth, except t h e third molars, begins within t h e period extending from about three months in utero until three years postnatal. Bailit and Sung ('68) investigated the role of maternal effects on t h e developing dentition in Caucasians using maternal age, birth order and birth weight as indicators of intra-uterine environmental conditions. Birth weight and maternal age were both shown to have a statistically significant correlation with dental development. The importance of birth weight on dental development was also noted in a large sample of Japanese children (Bailit et a]., ' 6 8 ) . Furthermore, Keene ('71) found t h a t low birth weight was associated with a reduction in permanent tooth size in a study of caries-free naval recruits. Bader ('65) found t h a t t h e common environmental variance, which h e also termed maternal effect, for molar tooth widths in mice ranged from 16.8% to 25.0%of t h e total variance. While the mean value of 6% estimated for V E in ~ this study is less, t h e importance of t h e maternal effect in human tooth size variation warrants further investigation. The value of estimating heritabilities from quantitative characters has been queried by some (Feldman and L,ewontin, '75). Certainly heritabilities derived from full-sibling d a t a have limited application due t o t h e compounding effects of common environment. However, estimates derived from half-siblings give a direct insight into t h e contribution of additive genetic effects to observed variability. Quantification of these parameters is worthwhile, not only to increase t h e understanding of tooth size variability and its determinants, but also because this type of information is relevant to studies of human evolution, a field in which dental observations often provide useful data. Tooth size variability appears to have a strong genetic component, but environmental factors are also of importance. Further family studies designed to elucidate the contribution and nature of these components are needed. Segregation and linkage analyses may indicate t h e presence of major genes, t h a t is,
503
genes with large effects within t h e normal range of variability and as Smith and Bailit ('77) have indicated, t h e investigation of major genes of this type, once identified, could have far-reaching implications. ACKNOWLEDGMENTS
The growth study which has provided data for this investigation was supported by Research Grant DE 02034 from the National Institute of Dental Research, Bethesda, Maryland and by grants from The University of Adelaide and t h e Australian Jnstitute of Aboriginal Studies, Canberra. Our late colleague, M. J. Barrett, of The University of Adelaide, obtained t h e dental casts used in t h e study. The analysis of data was carried out during t h e tenure of a Postgraduate Research Scholarship awarded by t h e National Health and Medical Research Council of Australia. We acknowledge t h e assistance of Doctor G. Mayo, Department of Genetics, The University of Adelaide, who provided very helpful comments on t h e study methods. LITERATURE CITED Alvesalo, L., and P. M. A. Tigerstedt 1974 Heritab~litiesof human tooth dimensions. Hereditas, 77: 311-318. Bader, R. S. 1965 Heritability of dental characters in the house mouse. Evolution, 19: 378-384. Bailit, H. L. 1975 Dental variation among populations. Dent. Clin. N.Amer., 19: 125-139. Bailit, H. L., J. D. Niswander and C. J. MacLean 1968 The relationship among several prenatal factors and variation in the nermanent dentition in Jananese children. Growth, 32 '331 345 Bailit, H L , and B Sung 1968 Maternal effects on the de veloping dentition. Arch. Oral Biol., 13: 155-161. Barrett, M. J., T. Brown and M. R. Macdonald 1963 Dental observations on Australian Aborigines: mesiodistal crown diameters of permanent teeth. Aust. Dent. J., 8: 150-155. Boettcher, B. 1975 Personal communication. Brown, T., and M. J . Barrett 1971 Growth in Central Australian Aborigines: stature. Med. J. Aust., 2: 29-33. Falconer, D. S. 1963 Quantitative Inheritance. In: Methodology in Mammalian Genetics. W. J. Burdette, ed. Holden-Day, San Francisco, pp. 193-216. 1964 Introduction to Quantitative Genetics. Oliver and Boyd, Edinburgh, pp. 165-185. Feldman, M. W., and R. C. Lewontin 1975 The heritability hang-up. Science, 190: 1163-1168. Garn, S. M., A. B. Lewis and R. S. Kerewsky 1965 Genetic, nutritional, and maturational correlates of dental development. J. Dent. Res., 44: 228-242. Goose, D. H. 1971 The inheritance of tooth size in British families. In: Dental Morphology and Evolution. A. A. Dahlberg, ed. The University of Chicago Press, Chicago and London, pp. 263-270. Harris, J. E. 1975 Genetic factors in the growth of t h e bead. Dent. Clin. PIT. Amer.. 19: 151-160.
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