On genetic variation in menarche and age at first sexual intercourse A critique of the Belsky Draper hypothesis

Transcription

1 Evolution and Human Behavior 23 (2002) On genetic variation in menarche and age at first sexual intercourse A critique of the Belsky Draper hypothesis David C. Rowe School of Family and Consumer Sciences, Campus Box , University of Arizona, Tucson, AZ 85721, USA Received 25 February 2002; accepted 15 April 2002 Abstract The association of age of menarche, nonvirginity status, and age of first sexual intercourse was investigated in teenage, female twins (mean age, 17 years) in the National Longitudinal Study of Adolescent Health (Add Health). The sample sizes were all relatively small, so complex biometric models were not fit to twin covariance matrices; rather, rough estimators of genetic effects were used. Accordingly, all three characteristics were influenced by genetic variation, with higher heritabilities on nonvirginity status and age of menarche than on age of first sex. In MZ twins, the phenotypic (i.e., on individuals) correlation between menarcheal age and age of first sexual intercourse was.27. The association of menarcheal age in identical (MZ) Twin 1 and sexual onset age in MZ Twin 2, and vice versa, was.25. The genetic correlation between them, r g, was roughly estimated to be.72. These findings weaken a conditional adaptation interpretation of this association as proposed by Belsky and Draper, suggesting instead that heritable individual differences may give rise to this association. D 2002 Elsevier Science Inc. All rights reserved. Keywords: Add Health; Menarche; Sexual intercourse; Conditional adaptation 1. Introduction A debate exists between certain developmental theorists and behavioral geneticists over the relative role of conditional adaptations vs. heritable variation in life history address: dcr091@ag.arizona.edu (D.C. Rowe) /02/$ see front matter D 2002 Elsevier Science Inc. All rights reserved. PII: S (02)

2 366 D.C. Rowe / Evolution and Human Behavior 23 (2002) traits (Rowe, 2000b; Rowe, Vaszonyi, & Figueredo, 1997). The former theorists have made the counterintuitive prediction that early menarche is due to father absence (Draper & Harpending, 1982), or to less sensitive and less nurturing experiences in the family (Belsky, 2000; Belsky, Steinberg, & Draper, 1991). Belsky et al. (1991) regarded family treatments as answering how father absence might promote an earlier pubertal maturation in females. Families without fathers, or with stepfathers, are often poor, and discipline more harshly and physically than other families do. According to these theorists, girls from such families are also sexually precocious and promiscuous. The family effects imply a correlation between menarcheal age and the age of first sexual intercourse. On the other hand, both sides in this debate recognize possible genetic confounds. One is that the age of menarche is heritable (Belsky, 2000; Rowe, 2000a). Less widely appreciated is that parenting behaviors are heritable (Losoya, Callor, Rowe, & Goldsmith, 1997; Rowe, 1981), as are the onset of sexual intercourse and other aspects of sexual behavior (Dunne et al., 1997; Martin, Eaves, & Eysenck, 1977; Rodgers & Doughty, 2000; Segal, 1993). In light of this evidence of heritability, Belsky (2000) modified his position to suggest that only some children may be susceptible to environmental influences, whereas other children are genetically fixed in their behavioral repertoire. This compromise, however, is empirically supported neither for age of menarche nor for precocious sex. In this article, I estimate the heritability of age of menarche, nonvirginity status, and age of first sexual intercourse using the twins in the National Longitudinal Study of Adolescent Health (Add Health). Twins were used to control for age differences within sibling pairs. Because of small sample sizes, biometrical models were not fit to the twin covariances; rather, rough and simple estimators were used. In any case, larger studies than this one have established the heritability of menarcheal age and age of onset of sexual intercourse; these findings are not in doubt. The unique contribution of this study is to examine genetic and environmental components of the correlation of menarcheal age and age of first sexual intercourse. Phenotypic correlations are ordinarily calculated on individuals. Thus, on all the Twin 1s in the sample, some correlation may exist between menarcheal age and age of sexual intercourse. Imagine that this correlation was.30. It could represent either effects of genes in common to menarche and sex, or environmental influences shared by the two characteristics. To discover which is true, a second correlation is computed, called a cross-trait, cross-twin correlation. In one case, the correlation is between age of menarche for Twin 1 and the age of first sex for Twin 2. A second cross-correlation exists with the roles of Twins 1 and 2 reversed. How are these correlations to be interpreted? Consider a case in which the MZ twin cross-trait, cross-twin correlation equals the phenotypic correlation, i.e., r MZ phenotypic =.30, r MZ cross =.30. This is an example of a genetic effect. Because of their shared genes, a correlation computed on two MZ twins has the same value as one computed on one MZ twin. In this example, the values of the DZ twin correlations would be phenotypic,.30, and cross-trait, crosstwin,.15. The cross-correlation is less because DZ twins share 50% of their genes, not the 100% that MZ twins share.

3 D.C. Rowe / Evolution and Human Behavior 23 (2002) Method 2.1. Sample These data came from Waves 1 2 of the Add Health. The Add Health Wave 1 was collected in 1994 and, except for specific subgroups, it was a nationally representative survey of US adolescents (see details in Udry & Bearman, 1998); the data set is publicly available. Black children of highly educated parents were oversampled. Wave 2 was collected in 1995, with an interval of about 1 year between Waves 1 and 2. Within each wave, the twins were often interviewed on different days, and interviewers may have changed between waves. In Wave 2, the average age of the adolescents was 17 years. African American respondents were excluded because their ages of menarche were the least accurate. Their reports were badly telescoped such that older respondents gave an older age of menarche than did younger respondents (r.30). Ideally, chronological age should correlate zero with age of menarche. Twins were identified through self-report on an in-school questionnaire completed by about 90,000 adolescents that preceded Wave 1, and by investigating school rosters. The majority of same-sex twins were diagnosed as either monozygotic (MZ, N = 247 pairs) or dizygotic (DZ, N = 200) on the basis of their self-reports of confusability of appearance. The confusability scale developed for the Add Health study had four items: (1) When you were young children, did you and NAME look very much alike, like two peas in a pod, or did you just look like members of the same family? ; (2) Are strangers confused about which of you is which? ; (3) Are your teachers ever confused? ; and (4) Are family members ever confused?. Each item had a 1 or 0 score, with 1 indicating greater confusability of appearance. A score was computed, which is the average of Twin 1 s and Twin 2 s response to the four items, times 100. Inspection of the histogram distribution indicated that a score of 60 was the best threshold on which to separate MZ and DZ twins. The majority of twins were assigned using this confusability score. Confusability of appearance scales have been found to have greater than.90 agreement with zygosity determination on the basis of DNA evidence (Spitz et al., 1996). Eighty-nine twin pairs of uncertain diagnosis were classified by their match on DNA genetic markers (47 DZ, 42 MZ). Twins were diagnosed as MZ if they were the same for five or more genetic makers, and as DZ if they were different at one or more markers. Zygosity determination could not be ascertained for an additional 43 twin pairs. For the present analyses, these undecided (UD) twin pairs were omitted. In the sample of female twin pairs, 106 pairs were diagnosed as MZ and 76 pairs as DZ Measures Age of menarche In Waves 1 2, the female respondents reported their age of menarche to the nearest year. In the arbitrarily chosen Twin 1, the Waves 1 2 retest correlation was.75 ( P <.0001);

4 368 D.C. Rowe / Evolution and Human Behavior 23 (2002) comparably, in arbitrarily chosen Twin 2, it was.77 ( P <.0001). In both Twins 1 and 2, the mean menarcheal age in Wave 2 (12.40 and years, respectively) was greater than in Wave 1 (12.15 and years), though neither change was statistically significant (t = 1.14, P=.25; t = 1.18, P=.24). Thus, the mean changed about 3 months between waves. Ninety percent of the changes was 0 or 1 year. Given the moderate retest correlations and small absolute changes, the menarcheal age was taken as the average of the Waves 1 and 2 values Sexual intercourse In Wave 2, virgins were scored as 0; respondents reporting one or more acts of sexual intercourse were scored as 1. Thirty-seven percent of female respondents was a nonvirgin Age of first sexual intercourse In Wave 2, respondents reported retrospectively on their age of first sexual intercourse. Although there is no ideal way to treat virgins in these data, virgins were given as a score their current age, which avoids creating a lump score that extremely biases the shape of the distribution (i.e., if all virgins were to be assigned a single score). The earliest age of first intercourse was 10.2 years. 3. Results Table 1 presents the twin correlations. All three outcomes, menarcheal age, nonvirginity status, and age of first sexual intercourse, had greater MZ twin than DZ twin correlations, as expected under a hypothesis of genetic variation. A Z score test of the difference of two correlations was conducted to evaluate the statistical significance of this difference. Menarcheal age and nonvirginity status MZ twin correlations statistically exceeded the DZ twin correlations, whereas there was a trend in the same direction for age of first intercourse (P=.08). Thus, the conditions for an association between variables to be genetically influenced were established. Virginity status was uncorrelated with age of menarche. Table 2 shows the correlations that are critical to an analysis of the origin of the association between menarcheal age and age of first sexual intercourse. The correlations on MZ twins supported a genetic hypothesis Table 1 Twin correlations for age of menarche, ever had sex, and age at first sexual intercourse Variable r MZ N/Pairs r DZ N/Pairs Z P Age of menarche <.05 Ever had sex <.05 Age at sex <.08 a All correlations, P <.01. Confidence intervals not given because calculating proper intervals require biometric model fitting. a One-tailed test.

5 D.C. Rowe / Evolution and Human Behavior 23 (2002) Table 2 Genetic mediation of the association between age of sexual intercourse and age of menarche Full sample At least one nonvirgin twin Association r MZ r DZ r MZ r DZ Phenotypic Twin 1.28* (98).02 (76).26 (56).16 (36) Phenotypic Twin 2.25* (106).06 (76).25 (52).16 (37) Twin 1 age of sex with Twin 2 age of menarche.23* (103).10 (74).20 (49).22 (35) Twin 2 age of sex with Twin 1 age of menarche.26* (99).04 (76).23 (49).13 (36) N values in parentheses. * P <.02. in that the phenotypic correlation was of about the same magnitude as the cross-twin, crosstrait one. In the full sample, the average MZ twin phenotypic correlation was.27; the average cross-trait, cross-twin correlation was.25. The confidence interval for the former was.21.33; for the latter cross-correlation, it was In a worst case scenario, the phenotypic correlation could equal.33 and the cross-correlation.20, allowing for considerable nongenetic influences on the association between menarcheal age and age of sex. In the smaller sample of MZ twin pairs, at least one of whom is a nonvirgin twin, there is even more sampling variation. Nonetheless, the phenotypic and cross-correlations were of similar magnitudes. The results were less clear for the DZ twin pairs. In the full sample, all the DZ twin correlations were close to zero. As one would expect at least for a phenotypic correlation between age of sex and age of menarche, this result is challenging. Inspection of scatterplots reveals no obvious outliers. The findings were better patterned for those DZ twins at least one of whom was a nonvirgin. Their phenotypic correlation was.16. The crosscorrelations were ambiguous because one was negative and the other positive. Because of the small sample size, none of these DZ twin correlations attained statistical significance. 4. Discussion In this study, a comparison of MZ and DZ twin correlations revealed that genetic effects contributed to the variance (i.e., individual differences) in menarcheal age, nonvirginity status, and age of first sexual intercourse among teenagers with a mean age of 17 years. A rough estimate of heritability is twice the difference of the MZ and DZ twin correlations (i.e., h 2 =2[r MZ r DZ ]; Rowe, 1994). Using this estimator, the heritabilities in this sample were: age of menarche,.50; nonvirginity status,.56; age of first sexual intercourse,.28. The age of menarche heritability estimate is close to that obtained by Doughty and Rodgers (2000) using a comparison of full and half-siblings, as h 2 = Given the small sample sizes, my heritability estimates would have large confidence intervals. The main question was whether the phenotypic correlation of menarcheal age and age of first sexual intercourse had a genetic basis. In MZ twins, there was a phenotypic correlation of.27 between menarcheal age and age of first sexual intercourse such that females who had an

6 370 D.C. Rowe / Evolution and Human Behavior 23 (2002) earlier menarche also tended to have an earlier age of first sex. The interpretation of the phenotypic correlation depended on the value of the cross-trait, cross-twin correlation, e.g., menarcheal age in Twin 1 correlated with age of first sex in Twin 2. The MZ twin cross-trait, cross-twin correlation of.25 about equaled the phenotypic correlation on individuals,.27. The mathematical expectation for the phenotypic correlation (r p ) and for the MZ twin crosstrait, cross twin correlation (r c ) is (Eq. (1)): r p ¼ r c ¼ h m h sex r g ð1þ where h m is the square root of the heritability of menarcheal age, h sex is the square root of the heritability of age of first sexual intercourse, and r g is the correlation of the genes influencing the two characteristics. Solving the equation for r g yields the following result, with a wide confidence interval (Eq. (2)): r g ¼ :72 ¼ :27=ð:53 :71Þ: ð2þ Thus, the origin of the phenotypic correlation may be a.72 genetic correlation between menarcheal age and age of first sexual intercourse. Other genes, which influence just one of the characteristics, would cause r g to be less than 1.0. There are several possible interpretations for this genetic correlation: (1) physiological, (2) assortative mating, and (3) reactive heritability. The most straightforward interpretation is that age of first sex and menarcheal development share some common physiological pathways that are genetically determined. Comings, Muhleman, Johnson, and MacMurray (2002) advanced this hypothesis for a polymorphism in the X-linked androgen receptor gene. They found that fathers carrying the AR risk alleles were more likely to abandon a marriage. Those same alleles, when passed onto a daughter, were associated with her having an earlier age of menarche and behavioral problems. A second explanation, which is not inconsistent with the first, is that the genetic correlation arises from assortative mating. In this case, the physiological pathways to precocious sex and early menarche would be distinct, but the genes become correlated because early maturing girls tend to mate at a young age with impulsive, sensation-seeking men, i.e., Mealey s (1995) primary psychopaths. Over generations, a correlation would build up between genes affecting the two characteristics such that a girl who carried risk alleles for early menarcheal age would also inherit risk alleles for a younger first sexual intercourse. Finally, a third hypothesis is that boys are attracted to girls showing secondary sexual characteristics; but while this is certainly true, it seems unlikely that this reactive heritability would create equal phenotypic and cross-correlations. After all, nearly all girls in the sample were postmenarcheal and had their secondary sexual traits in full display; yet about two thirds of them was still a virgin. I know of no evidence that girls who have early sex are physically distinct from other girls, and even if so, whether the effect would be strong enough to explain much variance. Several limitations reduce the confidence that can be placed in the findings of this study. First, about two thirds of the adolescent girls was a virgin. No method exists that can account for missing data on nonvirginity adequately. The solution used here, scoring virgins as their ages, guarantees that twins are alike when both twins are virgins. It may exaggerate twins

7 D.C. Rowe / Evolution and Human Behavior 23 (2002) resemblance to one another. Second, the sample sizes were small. Therefore, the correlation coefficient had wide confidence intervals. The MZ twin phenotypic and cross-trait, cross-twin correlations appear to be alike, but this could be coincidental. It would take a larger sample to know what these values are more precisely. Third, the findings for DZ twins were inconsistent because in the full sample, the DZ correlations were about zero. Their low correlations might be interpreted as showing epistasis, i.e., gene gene interactions shared only by MZ twins. However, there is no reason to expect that all the genetic variations are nonadditive; this puzzle can be resolved only through a replication study. Acknowledgments The Add Health was designed by J. Richard Udry and Peter Bearman and funded by grant P01-HD31921 from the National Institute of Child Health and Human Development. Data sets can be obtained by contacting the Carolina Population Center, 123 West Franklin Street, Chapel Hill, NC , USA, or by ing addhealth@unc.edu. References Belsky, J. (2000). Conditional and alternative reproductive strategies: individual differences in susceptibility to rearing experiences. In: J. L. Rodgers, D. C. Rowe, & W. B. Miller (Eds.), Genetic influences on human fertility and sexuality: Theoretical and empirical contributions from the biological and behavioral sciences ( pp ). Boston: Kluwer Academic Publishing. Belsky, J., Steinberg, L., & Draper, P. (1991). Childhood experience, interpersonal development, and reproductive strategy: An evolutionary theory of socialization. Child Development, 62, Comings, D. E., Muhleman, D., Johnson, J. P., & MacMurray, J. P. (2002). Parent daughter transmission of the androgen receptor (AR) gene as an explanation of the effect of father absence on age of menarche. Submitted for publication. Doughty, D., & Rodgers, J. L. (2000). Behavior genetic modeling of menarche in US females. In: J. L. Rodgers, D. C. Rodgers, & W. B. Miller (Eds.), Genetic influences on human fertility and sexuality: Theoretical and empirical contributions from the biological and behavioral sciences ( pp ). Boston: Kluwer Academic Publishing. Draper, P., & Harpending, H. (1982). Father absence and reproductive strategy: An evolutionary perspective. Journal of Anthropological Research, 38, Dunne, M. P., Martin, N. G., Statham, D. J., Slutske, W. S., Dinwiddie, S. H., Bucholz, K. K., Madden, P. A., & Heath, A. C. (1997). Genetic and environmental contributions to variance in age at first sexual intercourse. Psychological Science, 8, 1 6. Losoya, S. H., Callor, S., Rowe, D. C., & Goldsmith, H. H. (1997). The origins of familial similarity in parenting: A study of twins and adoptive siblings. Developmental Psychology, 33, Martin, N. G., Eaves, L. J., & Eysenck, H. J. (1977). Genetical, environmental, and personality factors influencing the age of first sexual intercourse in twins. Journal of Biosocial Science, 9, Mealey, L. (1995). The sociobiology of sociopathy: An integrated evolutionary model. Behavioral and Brain Sciences, 18, Rodgers, J. L., & Doughty, D. (2000). Genetic and environmental influences on fertility expectations and outcomes using NLSY kinship data. In: J. L. Rodgers, D. C. Rowe, & W. B. Miller (Eds.), Genetic influences on human fertility and sexuality: Theoretical and empirical contributions from the biological and behavioral sciences ( pp ). Boston: Kluwer Academic Publishing.

8 372 D.C. Rowe / Evolution and Human Behavior 23 (2002) Rowe, D. C. (1981). Environmental and genetic influences on dimensions of perceived parenting: A twin study. Developmental Psychology, 17, Rowe, D. C. (1994). The limits of family influence: Genes, experience, and behavior. New York: Guilford Press. Rowe, D. C. (2000a). Environmental and genetic influences on pubertal development: evolutionary life history traits? In: J. L. Rodgers, D. C. Rowe, & W. B. Miller (Eds.), Genetic influences on human fertility and sexuality: Theoretical and empirical contributions from the biological and behavioral sciences ( pp ). Boston: Kluwer Academic Publishing. Rowe, D. C. (2000b). Death hope and sex: steps to an evolutionary ecology of mind and morality by J.S. Chisholm. Evolution and Human Behavior, 21, Rowe, D. C., Vazsonyi, A. T., & Figueredo, A. J. (1997). Mating-effort in adolescence: Conditional or alternative strategy. Personality and Individual Differences, 23, Segal, N. (1993). Heritable and environmental variables affect reproduction-related behaviors, but not ultimate reproductive success. Personality and Individual Differences, 14, Spitz, E., Moutier, R., Reed, T., Busnel, M. C., Marchaland, C., Roubertoux, P. L., & Carlier, M. (1996). Comparative diagnoses of twin zygosity by SSLP variant analysis, questionnaire, and dermatoglyphic analysis. Behavior Genetics, 26, Udry, J. R., & Bearman, P. S. (1998). New methods for new research on adolescent sexual behavior. In: R. Jessor (Ed.), New perspectives on adolescent risk behavior ( pp ). New York: Cambridge University Press.