Inbreeding Effects on Bilateral Asymmetry of Dermatoglyphic Patterns

AMERICAN JOURNAL. OF PHYSICAL ANTHROPOLOGY 81:77-89 (1990)

Inbreeding Effects on Bilateral Asymmetry of Dermatoglyphic Patterns

ARINDAM MUKHERJEE Department of Anthropology, university of Calcutta, Calcutta 700019, India

KEY WORDS Inbreeding, Asymmetry, Dermatoglyphics

ABSTRACT Bilateral correlations are higher and bilateral variances within individuals smaller in the samples of inbred individuals than in matched control groups of the same sex for pattern intensities on fingers in four series of data and also for pattern intensities on palms, toes, and soles and the palmer main line indices in the data collected from a Muslim population of West Bengal. This trend is not apparent in two series of data from the Yanadi tribe, in which the inbred and noninbred samples are not controlled for random variation of genes and environment. Increased variances between individuals and changes in means and distributions of the traits in the inbred samples of the matched data indicate some influence of homozygosity of genes for the traits on their asymmetry. The reduced variability of asymmetry of the traits in the inbred cannot be explained by homozygosity of genes for either directional or absolute asymmetry. One possible explanation is that heterozygotes for these dermatoglyphic traits are more responsive to environmental stress than homozygotes andlor increased selection in the homozygotes against genetic disorders associated with dermatoglyphic asymmetry may reduce the variability of such asymmetry.

Genetic influences on right-left differences or relationships of dermatoglyphic traits are not yet satisfactorily understood. Although Holt (1954) found no evidence for inheritance of right (R) minus left (L) differences of finger ridge-counts in twins and families, later studies on larger series of data (Singh 1970; Mi and Rashad 1977; Martin et al., 1982; Loesch and Martin 1982) have indicated significant, though very small, he- reditary components for both directional (R- L) and absolute (1R-L1) asymmetries of the trait. However, the results of these studies are not consistent between sexes, between fingers, between different types of relatives, and between the two types of asymmetry. Again, the suggestion of a small heritability of directional asymmetry of pattern elements (triradii) of loops and whorls (Bener 1979; Bener and Erk 1979) remains incom- plete due to significant negative correlations between sibs for some fingers and absence of significant father-offspring correlations for loop elements. Pons (1961) also obtained small sibpair and mother-offspring correla-

tions for main line index on palms, but correlations between monozygotic twins and between fathers and offspring are not significant.

Further evidence for a genetic background of dermatoglyphic asymmetry comes from racial, rather than geographical, differences between populations in respect of d A 2 , a measure of absolute asymmetry (Jantz 19751, and variance of R-L difference of finger ridge-count (Jantz 1979; Malhotra and Sengupta, 1985) as well as of bilateral correlations for a-b ridge-count on palms (Jantz and Webb 1982). Jantz points out that the value of l/A2 is greater in populations which have intermediate values of mean total finger ridge-count (TFRC) than in those which have high or low means. This suggests the possibility of an increased bilateral asymme-

Received June 16,1986; revision accepted February 15,1989. Arindam Mukherjee is now at Department of Anthropology,

The Pennsylvania State University, 409 Carpenter Building, University Park, PA 16802.

@ 1990 WILEY-LISS, INC.

78 A. MUKHERJEE

try of a dermatoglyphic trait in individuals who are heterozygous for genes determining that trait, irrespective of separate genes for asymmetry, if any. In the case of ab count, however, the minimum asymmetry tended to coincide with the mean of the trait in the sample as one would expect in the case of canalization (Jantz and Webb, 1980). The present study examines the hypothesis that the degree of heterozygosity influences the variation in asymmetry of five dermatoglyphic traits. For this purpose, it compares some measures of asymmetry of each trait between two groups of individuals of the same sex who differ in their average coeffi- cient of inbreeding, f, which measures the proportion of homozygous loci above that expected in random mating.

The study of the effects of homozygosity in humans is limited. Several of these limitations have been reduced in the present study, where possible, to obtain meaningful results. The inbreeding effect in a population as an evolutionary condition can be neither removed nor separated from homozygosity effects in random inbreeding. These can, however, reasonably be assumed to affect similarly the two grou s from the same endogamous population. sp econdly, random differences in gene frequency and environmental influence between the compared groups of highly inbred (IN; average f 3 0.0625) and apparently noninbred (NI; 0 < f < 0.0039) individuals are largely removed in four series of data (A-D) from three endogamous populations (Table 1). These are minimized

TABLE 1. Details o f six series (A-F) of dermatoglyphic data f rom males and/or females o f different Indian populations: numbers o f noninbred (NI) and inbred (IN) indiuiduals with different coefficients o f autosomal

inbreeding ( f ) with numbers of sibs studied from different families in each series'

Inbreeding No. of sibships level with the following Sample cn Relationship No. of sibs size Population

series isex) NI IN of parents 1 2 3 4 5 6 NI IN

A. Sheik Muslim Rurdwan dist. West Bengal Mukherjee, A, 1986' (Male)

B. Mala Chittoor dist., Andhra Pradesh Reddy, 1978' (Male)

C. Pokanati Reddy Chittoor dist., Andhra Pradesh Ghosh. 1980' (Male)

D. - do - (Female)

E. Yanadi Chittoor & Nellore dist. Andhra Pradesh Vasulu, 1977-782 (Male)

F. - do - (Female)

0.00

0.00

0.00

0.00

0.00

0.00

0.0195 0.0625

0.0781 0.0937

0.0625

0.0625

0.1250

0.0625

0.1250

0.03125 0.0625 0.0664 0.1250

0.03125 0.0625 0.0664 0.1250 0.1328

36 1

MBD 8 FSD 1 MSD 3 FBD 7 MBD 2 MRD 1

85 MBD 30 FSD 15

MBD FSD U:N

157 18 16 44

72 MBD 15 FSD 8 U:N 40

102

1 19 1

U:N 1 91 1

16 2

U:N 1 IJ:N 1

11 3 1

5 1

2

71 1

18 3 9

1

30 15

157 18 16 44

72 12 8

40 102

1 22

1 1

1 1 20

2 1

91

1

'NR:MRD = mother's brother's daughter: MSD = mother's sister's daughter; FRD = father's brother's daughter: FSD = father's sister's daughter; U:N = unc1e:niece. SData collected by.

INBREEDING EFFECTS ON DERMATOGLYPHIC 79

effects on phenotypic variance (V,) of anthropometric and physiometric traits in man (Barrai et al., 1964; Lakshmanudu, 1982; Martin et al., 1973; Mukherjee, 1984; Muk- herjee and Lakshmanudu, 1980; Neel et al., 1970; Schork, 1964; Schreider, 1967; Schull, 1958, 1962; Schull and Neel, 1965) are not consistent with a linear increase off. The increase of Vp is not always significant; but the expected increase of V, is also not large enough to show significance in the available sample sizes (Morton, 1958; Neel et al., 1970; Schork, 1964; Schull and Neel, 1965; Slatis and Hoene, 1961). A part of the irregular results can also be explained by unmatched, mixed or biased samples, and lack of adequate data for high inbreedinglevels, i.e., f 3 0.0625 (e.g., Barrai et al., 1964; Barbosa and Krieger, 1979; Krieger, 1969; Morton, 1958). Even then, in most of the published data, including that from a few endogamous populations of India (Mukherjee, 19841, the Vp increases in high inbreeding (f 2 0.0625) as the mean decreases, but the Vp decreases as the mean increases in low f (0 < f < 0.0625) from its value in NI (f = 0). This has been attributed to the overwhelming influence of enhanced selection in low inbreeding. Be- sides selection, epistasis can cause nonlin- earity in effects of inbreeding (Kempthorn, 1957; Crow and Kimura, 1970band epistasis has not been excluded for dermatoglyphic traits.

To circumvent the problems that I have enumerated, in the present study, the great- est possible difference between f has been ensured between the IN and NI groups of data from each population to increase the probability of homozygosity of specific genes in the IN group and to reduce complications due to a nonlinear model. However, it has not been possible to obtain sufficient data from individuals with exactly equal values of high f except in series B. Consequently, the data for different levels of high f (>0.0625) have been compared with that for the NI groups (f < 0.0039) and not between themselves, in the initial stage. Within these limitations, the phenotypic variances between individuals CV,) are compared between corresponding IN and NI groups to observe increased homozygosity of specific genes for the traits in the IN groups, indications for which have also been obtained in the data earlier (A. Mukherjee, 1985, 1989; D.P. Mukherjee, 1984; D.P. Mukherjee et al., 1980; Mukher- jee and Ghosh, 1981; Sabarni and Mukher- jee, 1976).

to the maximum possible extent in the data for all five traits in series A by comparing close IN and NI relatives who share the same environment (see Materials and Methods). In addition, the reliability of the results for one of the traits is verified in three other series (B-D) of matched IN and NI data. Still further, two additional series (E and F) of data available from the two sexes of another population, in which the IN and NI groups are not adequately matched, are used as negative checks. Increased sampling devia- tions or significant differences in the opposite direction in these two series (E and F) would strengthen the evidence for homozygosity effects, if any, obtained from the rest of the data (series A and D).

Thirdly, although large samples of matched data from IN and NI groups are required for realizing the limited possibility of increased homozygosity a t specific loci in the human range of f, such large samples are technically unrealistic. Therefore, data from several populations are analysed to compen- sate for this deficiency. The data available from females are not adequate for observing additional effects of X-linked inbreeding. But this does not pose a serious problem, as there is evidence for only negligble influence, if any, of X-linked genes on the selected traits (Loesch 1971,1974; Mukherjee, 1966; Pons 1961). In any case, the present study is limited to the effects of homozygosity of autosomal genes.

The probability of increase of homozygosity with inbreeding may not be always real- ized for specific loci (Jenkins et al., 1985) and linear progress of homozygosity is inter- rupted by adaptive processes for certain en- zymes (Lerner, 1954; Johnson, 1974). The homozygosity effect of inbreeding is less un- certain for multifactorial traits such as dermatoglyphic patterns, but a system of additive and nonadditive genes at different loci may pose difficulties for estimation of homozygosity (Barrai et al., 1964). For example, the genetic variance, V,, would increase at a rate f only if the genes are all additive, but at a greater rate for recessive genes with a wide range of frequencies (Mather, 1949; Falconer, 1964; Slatis and Hoene, 1961) as would be the case if environmental variance also increases with inbreeding (Niswander and Chung, 1965). Again, VG would decrease with inbreeding if there are dominant genes with low frequencies (Wright, 1952; Reid, 19731.

Most of the available data on inbreeding

80 A. MUKHEFLJEE

MATERIALS AND METHODS The samples

The four endogamous populations from which four series (A-D) of matched data and two series (E and F) of relatively uncontrolled data regarding the IN and NI individuals are derived, are characterized by traditional preference for consanguineous marriages, which are concentrated in a few families or local sections of the populations with small effective sizes. The individuals with the highest f (20.0625) in the populations are identified by tracing the consanguineous relationship between their parents in pedigrees up to the fourth antecedent generation; those without parental consan- guinity within the range (0 < f < 0.0039) are considered as NI (f = 0). These values off do not consider random inbreeding, which cannot be high and is equally probable in the IN and NI groups of the matched series.

In a Muslim population (series A) it was possible to obtain data from consanguine- ously related IN and NI males who lived in the same households and cultivated potatoes and paddy in commonly owned land. The noninbred sample in this series include 15 fathers, 5 sons, 13 father’s brothers, 11 mother’s brothers, 3 stepbrothers, 25 father’s brother’s sons, and 10 mother’s sister’s sons of the inbred males as controls. Four- teen of these noninbred relatives are related to an inbred male in two different ways. But as this sort of comparison is limited, it was necessary to increase the sample size by including multiple sibs in both IN and NI groups (Table 11, combining different degrees o f f and including an offspring of second cousins, both of which were products of first cousins that occurred in a large pedi- gree showing several IN and NI relatives.

Dermatoglyphic data from IN and NI groups in the Mala and Reddy populations (Table 1, series B-D) were collected by other workers from the same kindred in localities, though for some married women (series D) this type of control might not have been so efficient. But no such control for even genetic homogeneity could be exercised in the Ya- nadi data collected for a different purpose (T.S. Vasulu, personal communication). The last two series of data are also analysed to observe the interference of random differences between IN and NI groups. The gene- alogical relationships traced through male propositi or their fathers have been recorded except for the Yanadi data (Table 1). As all

these populations follow the rule of exogamy of the paternal lineage (Mukherjee, 19711, all types of cousin marriages are encoun- tered in the muslim populations and only cross cousin marriages in the others.

Choice of traits The basic materials for this analysis in-

clude complete dermal prints taken with printers’ ink on white paper or cellotape (for toe prints). The dermatoglyphic traits studied are pattern intensities measured by the number of triradii on 1) fingers (trNF), 2) palms (trNP), 3) toes (trNT), and 4) soles (trNS) following Mukherjee (1966); and ridge inclination on palms measured by 5) main line index (MLI) following Cummins and Midlo (1943). They are chosen for their moderate to high heritability (Barnicot et al., 1972; Loesch, 1971,1974; Mukherjee, 1966; Pons 1961; Reed et al., 1975) and utility in representing different dermatoglyphic ar- eas. The scope of the paper is, however, limited to overall ridge configuration, and results of studies on ridge counts and other traits will be reported separately.

Analysis Bilateral (righaeft) interclass correla-

tions, rRL, is used as a negative measure of variation of asymmetry (Jantz and Webb, 1982). But it also depends to some extent on the variance of the trait between individuals (Angus, 1982) which would increase with homozygosity of the involved genes. There- fore, to find out whether IN-NI difference of rRL depends exclusively on the difference of VB or also on the bilateral difference within individuals, V,, the total variance of each side is analysed (AOV) into its VB and Vw components as shown in Table 2.

The increase of homozygosity for each trait in the inbred group is verified by referring to earlier reports of inbreeding effects on means and distributions in these data (A. Mukherjee, 1985, 1989; D.P. Mukherjee,

TABLE 2. Analysis of total uariance’

Variance ss df MS

Within Z 2: (X, - Z,Xij/2)2 N-n SS,/N-n Between 2,$iZid,,/2 - Z PiXi./N)2 n- l SSb/n-l Total Pj&(Xij ~ X,X$,,/Nj2 N-l SS,/N-1

li = 1, 2 = left and right side, respectively, or the number of observations and j = 1, 2 , 3, . . . , n. = number of individuals (or groups). X is the ith observation on thejth individual;N is the total number oibbservations (in this case = 2n, where n is the number of individuals in each population sample).


1984; D.P. Mukherjee et al., 1980) and by examining the differences between IN-NI in V,. Furthermore, variance of (R-L) asymmetry, is compared between corresponding IN and NI groups of individuals in each series of data to assess its respective contribution to rRL and Vw.

One-tailed Z tests are applied to differences of rRL, and F tests i& differences of variances between IN and NI groups in order to judge the significance of those differences. Due to inherent limitations of sample size, various degrees of control for homogeneity and other complications, already pointed out, the consistency of the results over different series of matched data have also been considered as evidence of the reliability of trends.

Correction for mean and sibship size The comparison of V, and Vw between IN

and NI groups is made in three stages: 1) overall analysis of the observed scores of traits, 2) reanalysis of standardized scores (mean = 0, S.D. = 1) to remove the effects of mean on variances, and 3) reanalysis of standardized scores using single sibs (drawn at random) where necessary, to remove error due to variable sibship size. The results of all

these stages are presented together for a critical appraisal of the effects of mean differences and variable sibship sizes.

RESULTS Bilateral correlations

The bilateral correlation rRL, for each of the five traits (Table 3) is significantly higher in the inbred group than in corresponding NI group in each of the four series of data (A-D) for matched comparison. The two series (E and F) of the Yanadi data, which are not adequately controlled for random variations show, in contrast, a fluctuation of rRL values in the IN and NI groups in most of the comparisons. There is an indication of nonlinear increase of rRL with f in its high range (f.0.0625) in Reddy males and females (series C and D). But it is not possible to verify this in the present study.

Analysis of variance The total variance CV,) of each trait on

single hands or feet, as the case may be, appears to increase in the IN groups in the majority of matched Comparisons (Table 4). The IN-NI difference is not consistent, however, especially for traits on palms and soles in both observed and standardized values of

TABLE 3. Intraclass bilateral correlation (r) wi th S.E. fo r number o f triradii (trN) on fingers (F), pa lms (P), toes (T)3 and soles 6) and for palmar m a i n line index (MLI) i n inbred ( IN) and noninbred (NI) males or females in four

series ( A - 0 ) o f matched data and two series (E and F) o f relatively uncontrolled data f r o m four populations

IN NI Z Data series Trait f n r SE n r SE IN-NI

Muslim A. Male trNF 0.0675 108 0.87 0.02 142 0.76 0.04 2.61**

trNP trNT

P Reddy C . Male trNF 0.0625

0.1250 0.0978

D. Female trNF 0.0625 0.1250 0.1042

Yanadi E. Male trNF 0.06391

trNP MT.1

108 108 106 108

90

68 88

156 40 80

120

50 50 50

0.58 0.88 0.81 0.59

0.89

0.84 0.77 0.80 0.94 0.83 0.88

0.70 0.59 0.61

0.06 0.02 0.03 0.06

0.02

0.04 0.04 0.03 0.02 0.03 0.02

0.07 0.09 0.09

142 0.35 138 0.81 142 0.70 142 0.26

170 0.79

314 0.57

146 0.67

204 0.73 204 0.40 204 0.51

0.07 0.03 0.04 0.08

0.03

0.04

0.05

0.03 0.06 0.05

2.30* 3.19** zoo* 3.09**

2.77**

4.21*** 3.05** 4.57*** 5.03*** 2.66** 4.53***

-0.38 1.57 0.90

F. Female trNF 0.06687 50 0.71 0.07 182 0.83 0.02 -1.83* trNP 50 0.08 0.14 182 0.33 0.07 -1.60 MLI 50 0.62 0.09 180 0.40 0.06 1.84*

* P < 0.05. **P < 0.01. ***P < 0.001

82 A. MUKHERTEE

TABLE 4. Comparison of total uariance (VJ of the observed scores (I) and standardized scores with mean = 0 and S.D. = 1 (II) of the number of triradii (trN) on fingers (F), palms (P), toes (TI, and soles (S) and of main line index on palms (MLI), considering single limbs, between inbred (IN) and noninbred (Nl) individuals in six series

o f data from four populations

df vt (1) vt (11) Data series Trait IN NI IN NI IN NI

Muslim A. Male trNF 107 141 3.23 3.01 1.00 0.83

trNP 107 141 1.41 1.01 0.93 1.03 trNT 107 137 4.34 2.60 1.04 0.99 trNS 105 141 1.60 1.61 1.02 0.99 MLI 107 141 4.21 4.87 1.00 0.99

B. Male trNF 89 169 3.63 3.28 1 .oo 1.00 Mala

P. Reddy C. Male trNF 155 313 5.03 2.10 1.00 1.03 f = 0.0625 67 5.16 1.03 f = 0.125 87 4.97 0.88 D. Female trNF 119 145 5.30 1.46 0.90 1.02 f = 0.0625 39 7.48 1.03 f = 0.125 79 4.19 1.03

Yanadi E. Male trNF 49 203 4.72 3.10 1.04 0.98

MLI 49 203 7.51 6.07 1.03 1.01 F. Female trNF 49 181 2.32 3.31 1.01 1.02

trNP 49 181 0.62 0.64 0.87 0.98 MLI 49 179 5.44 5.47 1.01 1.00

trNP 49 203 0.69 1.06 0.96 1.04

the trait. The VB component of this variance is significantly greater than the V, component except for trNP in the inbred females of series F of the Yanadi data. The Vfl, ratio (F) exceeds in the IN groups in most cases (Table 5). The V, andV, components ofV, are also separately compared between corresponding IN and NI groups of different series of data.

Variance between individuals There is a general trend of increase ofVB in

the IN groups in the matched series of data (Tables 6 , 7) despite sampling fluctuations, although the magnitude of this increase be- comes considerably smaller when the influences of mean differences are removed (Table 7) . The correction of possible errors due to variable sibship size does not alter this general trend.

Bilateral variance within individuals Also, Vw tends to be smaller in the IN

groups than in corresponding NI groups in the four series of controlled data when the influence of means are removed (Table 8). The IN-NI differences are significant at P = 0.05, except for the two palmer traits (trNP and MLI). The reduction of the bilateral

variance of trNT and trNS in the Muslim data remain significant at P = 0.05, even in the smaller sample consisting of single sibs from different families.

Variances of asymmetries There is no consistent trend of IN-NI dif-

ference in the means of R-L differences (Table 9), although in the majority of the matched comparisons (in series A-D), the variance declines in the offspring of first cousins (0.0625 d f d 0.0675). Thus, the decrease of bilateral variance (V,) in the IN groups for each trait may reflect the decrease of variances of asymmetries but not the decrease of mean asymmetry of either type.

DISCUSSION

The most striking results of the present analysis are the increase of bilateral correlations (rRL and the decrease of bilateral variances (Vw) of the five dermatoglyphic traits in the high inbreeding classes, when random variations of alleles and envircnment are adequately controlled. This means that the sources (genetic and/or epigenetic) of bilateral correlations and bilateral variances for these traits must be related to homozygosity

83 INBREEDING EFFECTS ON DERMATOGLYPHIC

TABLE 5. F-ratio o f variance between individuals (V,) to bilateral uariance within individuals (Vw) of both observed scores (I) and standardized scores with mean = 0 and S.D. = I (II) for different dermatoglyphcc traits

in the inbred (IN) and noninbred (NI) individuals of the four series (A-D) o f matched data and two series ( E and F) of relatively uncontrolled data

I IN I1

Data series Trait f F NI:F 1N:F NI:F

Muslim A. Male trNF 0.0675 9.02 7.90 8.90 2.45

trNP 4.20 2.61 3.03 3.40' trNT 16.52 9.27 19.02 7.05 trNS 9.77 5.73 15.50 5.51 MLI 3.58 2.60 4.13 3.47

B. Male t rNF 0.0625 15.66 8.34 16.77 8.90 Mala

CP Reddv C. Malk t rNF 0.0625 11.00 11.48

0.1250 7.95 14.03 0.0978 9.21 4.16 18.41 4.34

D. Female trNF 0.0625 33.76 9.85 0.1250 9.63 36.66 0.1042 15.18 5.04 13.06 5.12

E. Male t rNF 0.06391 12.93 6.25 6.59 6.35 trNP 3.70 3.26 4.54 3.30 MLI 3.81 2.96 5.94 4.24

F. Female trNF 0.06687 5.66 11.89 6.07 12.49l trNP 1.12 1.97* 1.12 2.10' MLI 4.15 2.26 7.75 2.32

Yanadi

'Indicates greater VB/VW in the NI group than in the IN.

TABLE 6. Variance between individuals (V,) in inbred (IN) and noninbred (NI) groups for some dermatoglyphic traits in four series ( A - 0 ) o f matched data and two series ( E and F) o f uncontrolled data, with variance ratio F

between IN and NI groups

IN NI (f = 0.00) F-ratio Population Trait f df VB df VB IN/NI NI/IN

Muslim A. male t rNF

trNP trNT trNS MLI

B. Male trNF

C. Male t rNF

Mala

P. Reddy

D. Female

0.0675

0.0625

0.1250 0.0625 0.0978 0.1250 0.0625 0.1042

53 53 53 52 53

44

43 33 77 .39 19 59

5.86 70 5.37 2.93 70 2.57 8.26 68 4.73 2.31 70 1.46 6.62 70 7.05

6.76 84 5.83

8.74 156 1.53 9.35 156 1.53 9.03 156 1.53 7.51 71 2.42

14.18 71 2.42 9.87 71 2.42

1.09 1.14 1.75* 1.58*

1.06

1.16

5.71** 6.11** 5.90** 3.10** 6.86** 4.08**

Yanadi E. Male trNF 0.06391 24 8.62 101 5.32 1.62

t rNP 24 1.08 101 1.62 1.50 MLI 24 11.76 101 9.06 I .30

F. Female t rNF 0.06687 24 3.89 90 6.08 I .56 trNP 24 0.65 90 0.84 1.29 MLI 24 8.65 89 7.58 1.14

*,*"P-ratio: * P < 0.05; **P< 0.001.

84 A. MUKHERJEE

TABLE 7. Variance between individuals (V,) of standardized scores (mean = 0, S.D. = 1) o f number of triradii (trN) on fingers (F), palms (P), toes (T), and soles (S) and of palmar main line index (MLI) in inbred (IN) and

noninbred (NI) of matched (A-0) and relatively uncontrolled data (E and F)'

IN NI F-ratio Population Trait df VB df v, IN/NI NI/IN

Muslim A. Male I

Mala

P. Reddy B. Male

C. Male D. Female

E. Male Yanadi

F. Female

I1

I1 I1

I

I1

I

I1

trNF trNP trNT trNS MLI trNF trNP trNT trNS MLI

t rNF

trNF trNF

trNF trNP MLI t rNF trNP MLI t rNF trNP MLI trNF trNP MLI

53 53 53 52 53 33 33 33 32 33

44

77 59

24 24 24 22 22 22 24 24 24 21 21 21

1.78 70 1.40 70 1.96 68

1.61 70 1.71 49 1.57 49 1.86 48 1.79 49 1.62 49

1.81 84

1.88 156 1.66 71

1.78 101 1.55 101 1.73 101 1.70 101 2.40 101 1.81 101 1.71 90 0.92 90 1.75 89 1.76 90 1.39 90 1.75 89

1.91 70

1.17 1.52* 1.59 1.73 1.13 1.66 1.15 1.53 1.05 1.80 1.57 1.00 1.75 1.06 1.63 1.10 1.57 1.03

1.79 1.01

1.67 1.13

.14

.05

1.70

1.69 1.59 1.62 1.69 1.59 1.62 1.88 1.33 1.40 1.88 1.33 1.40

1.02

1.05

1.07 1.01 1.51 1.12

1.03

1.10 1.45

1.07 1.25

1.05 1.25

'Analysis based on multiple sibs (I) supplemented by that on single sibs (11) *P < 0.05.

of individuals. It is extremely unlikely that occurrence of genes for asymmetry or of those controlling developmental processes, if any, differ in the same direction between matched samples of IN and NI individuals in the four series of data from three different populations. Differences of the variances for these traits between IN and NI groups of individuals appear to be compounded in the change of correlations and bilateral variations on inbreeding.

There is evidence that these overall measures of variation of asymmetry decrease with the increased homozygosity of specific genes for the traits under study. A general trend of increase of VB of different traits in high inbreeding can be noticed in the matched comparisons of IN and NI groups, notwithstanding small sample fluctuations. The magnitude of this increase, though small appears to approach the expected rate (0 of increase of V, for additive genes, when the mean differences are controlled. The low significance and sampling fluctuations that

are observed for IN-NI differences in VB do not in any way contraindicate the homozygosity of additive genes in view of the small amount of expected increase, and the limited sizes of the samples. The results do not suggest any significant amount of V, related to f underlying the increase of VB in the IN groups.

It is possible that homozygosity of some genes with nonadditive effects also contrib- ute to the further increase of VB in the IN groups in the data not controlled for means. In fact, consistent increase of the mean trNF in the IN groups of all six series of the present data and also another sample, and a significant decrease of mean trNT and trNS in the IN males of the Muslim population (series A) observed earlier (Mukherjee, 1985, 1989) suggest recessive effects of genes also. However, no systematic change of mean trNP or mean MLI on inbreeding has been observed in the data series A, E and F. The increased homozygosity of the genes for all these traits in the inbred groups is most


TABLE 8. Bilateral variances within individuals (V,) of standardized scores (mean = 0, S.D. = I) of number of triradii (trN) of fingers (F), palms (P), toes (T), and soles (S) and of palmar main line index (MLI) in inbred (IN)

and noninbred (NI) individuals in four series (A-0) of matched data and two series (E and F) of relatively uncontrolled data'

Population

A. Male Muslim

Mala

P. Reddy B. Male

C. Male

D. Female

Yanadi E. Male

F. Female

Trait IN

f df V...

I

I1

I1

I1

I1

I

I1

I

I1

t rNF trNP trNT trNS MLI t rNF trNP trNT trNS MLI

t rNF

trNF

trNF

trNF trNP MLI t rNF trNP MLI t rNF trNP MLI t rNF trNP

-

MLI 22 0.22

0.0675 54 0.20 54 0.46 54 0.10 53 0.12 54 0.39 34 0.26 34 0.44 34 0.12 33 0.18 34 0.36

0.0625 45 0.11

0.0625 0.1250 0.0978

34 0.13 44 0.16 78 0.14

0.0625 20 0.05 0.1250 40 0.19 0.1042 60 0.13

0.06391 25 0.27 25 0.34 25 0.29 23 0.25 23 0.35 23 0.25

0.06687 25 0.28 25 0.82 25 0.23 22 0.29 22 1.29

NI df VW

71 0.48 71 0.47 69 0.26 ~ ~~

71 0.30 71 0.44 50 0.17 50 0.45 49 0.23 50 0.37 50 0.44

85 0.20

157 0.39 157 0.39 157 0.39 72 0.33 72 0.33 72 0.33

102 0.27 102 0.48 102 0.38 102 0.27 102 0.48 102 0.38 91 0.15 91 0.63 90 0.60 91 0.15

F-ratio NI/IN IN/NI

2.40*** 1.02 2.50*** 2.50*** 1.13

1.02 1.92* 2.06** 1.22

1.82**

3.00*** 2.44*** 2.78*** 6.60*** 1.74" 2.54***

1 .oo 1.41

1.53

1.30

1.93* 2.61**

~

91 0.63 2 n6* -. . . ~~

~~ ~~ . 90 0.60 2.73**

'Analyses based on samples including multiple sibs (I) and single sibs (11). *P < 0.05. **P < 0.01. ***P < 0.001.

TABLE 9. Comparison of mean (Mi and variance (V) of directional (R-L) asymmetry of the number of triradii (trN) on fingers (F), palms (Pi, toes (T)> and soles IS) and of main line index on palms (MLI)

between inbred (IN) and noninbred (NI) groups of indiuiduals in different series of data

M k S.E. V F-ratio Data series Trait I N NI I N NI NI/IN IN/NI

Muslim A. Male

Mala

P. Reddy B. Male

C. Male D. Female

E. Male Yanadi

F. Female

t rNF t rNP trNT trNS MLI

t rNF

trNF t rNF

t rNF t rNF MLI t rNF t rNP MLI

0.22 t 0.15 -0.02 k 0.13

0.04 k 0.14 0.06 t 0.10 0.93 t 0.23

0.00 t 0.13

0.63 k 0.14 0.05 t 0.14

0.04 + 0.23 0.00 + 0.15 1.44 k 0.39

-0.04 k 0.23 -0.24 k 0.21

1.36 k 0.29

0.07 k 0.14 0.07 t 0.11

-0.06 * 0.12 0.09 k 0.12 1.71 k 0.02

0.01 * 0.13

-0.12 * 0.10 0.15 + 0.11

0.22 zk 0.13 0.06 + 0.10 1.33 * 0.20 0.11 k 0.10 0.21 k 0.09 0.82 k 0.26

1.21 1.45 0.98 0.94 1 .OO 1.01 0.58 0.95 2.84 4.05

0.80 1.38

1.54 1.60 1.25 0.92

1.28 1.64 0.56 0.98 3.85 1.78 1.32 1.00 1.06 0.80 2.15 5.95

1.20

1.01 1.64* 1.43'

1.72*

1.04

1.04

1.36

1.28 1.75*

2.16* 1.32 1.32

2.77*

*P < 0.05.

86 A. MUKHERJEE

clearly indicated by increased frequencies of extreme values and reduced frequencies of some intermediate values. For example, the frequencies of low values (below 12) of trNF in the IN and NI groups are, respectively, 29.6% and 23.9% in Muslim males (series A), 34.7% and 32.5% in Mala males (series B), and 34.2% and 31.8% in Reddy males (series C). Again the frequencies of trNF above 15 are 38.9% and 33.8% in the IN and NI groups of series A, 42.2% and 29.4%, respectively, in series B and 43.0% and 18.5%, respectively, in series C. Thus, homozygosity of genes for certain dermatoglyphic traits appears to have reduced the variability of bilateral expression of those traits.

This does not exclude the possibility that a general increase of homozygosity of genes other than those determining specific dermatoglyphic traits would also influence the bilateral variance and variation of asymmetry of those traits. The finding of increased asymmetry of finger ridge-count and pattern counts and that of their variances with heterozygosity in a majority of four serological loci-MN, Ss, Cc(Rh), and Duffy-among the Ashkenazi Jews (Kobyliansky and Livshits, 1986) may suggest such a possibility but does not provide unequivocal evidence for it, especially because genomic homozygosityl heterozygosity cannot be predicted from a few loci (Chakraborty, 1981; Mitton and Pierce, 1980) unless there is a large amount of linkage disequilibrium or large f values due to inbreeding or small population sizes. Furthermore, there are indications that fluctuating asymmetry for different traits in an individual are uncorrelated (Soul6 and Couzin-Roudy, 1982), which argues against general genomic heterozygosityhomozy- gosity being responsible for it.

The results of the present study are supported by investigations of other traits in plants and animals as well as results on human dermatoglyphic traits (Adams and Shank, 1959; Bradshaw, 1965; Pfahler and Linshens, 1979; Leary et al., 1984; McAn- drew et al., 1982; Kobyliansky and Livshits, 1986; Clark et al., 1986). On the other hand, there is wide support for the opposite result-namely, reduced fluctuating asymmetry in heterozygotes (reviewed in Mitton and Grant, 1984; Palmer and Strobeck, 1986; Allendorfand Leary, 1986). This is generally explained by the concept of genetic and developmental homeostasis (Lerner, 1954; Waddington, 1948). The relationship between homozygosity and reduced variability

of dermatoglyphic asymmetry remains to be elucidated fully. Two explanations of the observed phenomenon are proposed here as possibilities: 1) A genotype-environment interaction may form part of the epigenetic influence on the expression of dermatoglyphic traits on two sides of the body. 2) an increased intensity of selection against congenital malformations and other recessive disorders, which are associated with dermatoglyphic asymmetry (Adams and Nis- wander, 1967; Polani and Polani, 1969; Woolf and Gianas, 1976) may lead to a reduction in the variability of such asymmetries in the inbred individuals.

It is possible to think of a greater homeostatic ability of a heterozygous system of genes to respond to developmental stresses than that of a homozygous system of loci. It is possible that if heterozygotes are more ecosensitive they would more easily respond to changes in environment and thus show greater variability in growth and stature (Wolanski, 1975, 1977). This means one could expect a greater Vp with VE in heterozygotes. But this is not to say that the increase of variance of stature with inbreeding will be overshadowed by increased variance in noninbred, as stature is a highly heritable trait, just as the increase in V, in the inbred of the present data does not overshadow the increase of V, and V, in them.

A possible mechanism for the variable bilateral expression in heterozygotes could be the inactivation of certain autosomal alleles in some cells, as postulated for sex-linked genes, for fingerprint patterns (Parsons, 1964). There is evidence that inactivation of some genes but not others on the X-chromosome as well as autosomes are the result of different segments of DNA being methylated at different times (see Adams and Burdon, 1985; Cantoni and Razin, 1985; Holliday, 1987). This could possibly explain the increased asymmetry in some traits with inbreeding like tooth size (Bailit et al., 1970; Niswander and Chung, 1965) but not in dermatoglyphic patterns.

The second hypothesis postulating a “piggy back selection for dermatoglyphic asymmetry presupposes a selection pressure against homozygotes for deleterious genes. Although the hypothesis lacks direct confir- mation, the present evidence for a more marked inbreeding effect on the variability of asymmetry than on the variability of the dermatoglyphic traits themselves (V,) justi- fies consideration of such indirect effects of


general homozygosity on the asymmetry of pattern intensities. The two hypotheses are not mutually exclusive.

A reduced variability and mean of total asymmetry may, of course, result from a completely dominant gene or genes with low frequencies (P < 0.3). But this is incompati- ble with the absence of a greater sibpair correlation than parent-offspring correlations for asymmetries and lack of any clear indication of reduced mean of either type of asymmetry in the inbred groups for any of the traits.

There are indications that stress can in- duce gross malformations (Ford and Bull, 1926; Wilson, 1973; Pleet et al., 1981) as well as fluctuating asymmetry (Siegel and Doyle, 1975; Doyle and Johnston, 1977; Siegel et al., 1977; Sciulli et al., 1979; Harris and Nweeia, 1980) in a number of organisms, including humans. It would seem from their distribution that malformations and fluctuating asymmetry lie on a continuum (Valentine et al., 1973; see also Soule and Couzin-Roudy, 1982). There is also indication that stressors are nonspecific in that one cannot predict the kind or amount of malformation or asymmetry from the kind of stressor (DiBennardo and Bailit, 1978; Sciulli et al., 1979) and the physiological (Selye, 1973) and molecular mechanism (Schlesinger et al., 1982; Nover, 1984; Atkinson and Walden, 1985; Lind- quist, 1986) of stress combat are very similar for widely different agents that cause stress. Heat shock (or stress) proteins (hsps) that are produced in all organisms in response to a wide variety of stressors seem to have a homeostatic function and protect against major malformations (Mitchell and Peter- son, 1982; Walsh et al., 1985; Webster et al., 1985; Lindquist, 1986) and thus also asymmetry. It should be profitable to study (Mukherjee, 1988b) the production of hsps in homozygotes and heterozygotes under different regimes of stress to clarify the relationship between developmental homeostasis and zygosity at the molecular level.

ACKNOWLEDGMENTS

This work is supported by a NET fellow- ship awarded by the University Grants Com- mission, New Delhi. The author is thankful to T.S. Vasulu for the use of unpublished Yanadi data; D.P. Mukherjee, P.C. Reddy, and G.C. Ghosh for the use of Mala and Pokanati Reddy data sets; and to D.P. Mukherjee, P.P. Majumdar, and R.B. Eck-

hardt, and three anonymous referees for suggestions and comments during prepara- tion and revision of this paper.

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Inbreeding Effects on Bilateral Asymmetry of Dermatoglyphic Patterns