Abstract
To date, there has been relatively little work on gene-environment contributions to human sexuality, especially molecular analyses examining the potential contributions of specific polymorphisms in conjunction with life experiences. Using Wave III data from 717 heterozygous young adult sibling pairs included in the National Longitudinal Study of Adolescent Health, this article examined the combined contributions of attendance at religious services and three genetic polymorphisms (in the dopamine D4 receptor [DRD4]), dopamine D2 receptor [DRD2]), and the serotonin transporter promoter [5HTT]) to sensation seeking, a personality construct related to sexual behavior, and the number of vaginal sex partners participants had in the year before interview. Data analyses used an Allison mixed model approach to account for population stratification and correlated observations. DRD4 was unrelated to sensation seeking and to the number of sex partners in tests of both main effects and in interaction with religious attendance. Contrary to hypothesis, presence of the A1 DRD2 allele was associated with having had fewer sex partners in the past year. Associations between the 5HTT allele and sex partners varied by religious attendance, but again the patterns of associations were contrary to hypothesized relationships and were small in magnitude. These findings underscore the necessity of using more comprehensive multiple gene-multiple life experience approaches to investigations of complex behaviors such as sexual patterns.
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Allison, D. B., Heo, M., Kaplan, N., & Martin, E. R. (1999). Sibling-based tests of linkage and association for quantitative traits. American Journal of Human Genetics, 64, 1754–1764.
Allison, D. B., & Neale, M. C. (2001). Joint tests of linkage and association for quantitative traits. Theoretical Population Biology, 60, 239–251.
Bardo, M. T., Donohew, R. L., & Harrington, N. G. (1996). Psychobiology of novelty seeking and drug seeking behavior. Behavioral Brain Research, 77, 23–43.
Bau, C. H. D., Almeida, S., & Hutz, M. H. (2000). The TaqI A1 allele of the dopamine D2 receptor gene and alcoholism in Brazil: Association and interaction with stress and harm avoidance on severity prediction. American Journal of Medical Genetics, 96, 302–306.
Benjamin, J., Ebstein, R. P., & Belmaker, R. H. (Eds.). (2002). Molecular genetics and the human personality. Washington, DC: American Psychiatric Publishing.
Benjamin, J., Li, L., Patterson, C., Greenberg, B. D., Murphy, D. L., & Hamer, D. H. (1996). Population and familial association between the D4 dopamine receptor gene and measures of novelty seeking. Nature Genetics, 12, 81–84.
Benjamin J., Osher, Y., Kotler, M., Gritsenko, I., Nemanov, L., Belmaker, R. H., et al. (2000). Association between tridimensional personality questionnaire (TPQ) traits and three functional polymorphisms: Dopamine receptor D4 (DRD4), serotonin transporter promoter region (5-HTTLPR) and catechol O-methyltransferase (COMT). Molecular Psychiatry, 5, 96–100.
Bennett, A. J., Tsai, T., Hopkins, W. D., Lindell, S. G., Pierre, P. J., Champoux, M., et al. (1999). Early social rearing environment influences acquisition of a computerized joystick task in rhesus monkeys (Mucaca mulatta). American Journal of Primatology, 49, 33–34.
Berman, S. M., & Noble, E. P. (1997). D2 dopamine receptor (DRD2) gene and family stress: Interaction effects on cognitive functions in children. Behavior Genetics, 27, 33–43.
Berrettini, W. H., & Persico, A. M. (1996). Dopamine D2 receptor gene polymorphisms and vulnerability to substance abuse in African-Americans. Biological Psychiatry, 40, 144–147.
Brody, S. (2002). Age at first intercourse is inversely related to female cortisol stress reactivity. Psychoneuroendocrinology, 27, 933–943.
Cardon, L. R., & Palmer, L. J. (2003). Population stratification and spurious allelic association. Lancet, 361, 598–604.
Caspi, A., McClay, J., Moffitt, T. E., Mill, J., Martin, J., Craig, I. W. et al. (2002). Role of genotype in the cycle of violence in maltreated children. Science, 301, 851–854.
Caspi, A., Sugden, K., Moffitt, T. E., Taylor, A., Craig, I. W., Harrington, H., et al. (2003). Influence of life stress on depression: Moderation in the 5-HTT gene. Science, 301, 386–389.
Chang, F. M., Kidd, J. R., Livak, K. J., Pakstis, A. J. & Kidd, K. K. (1996). The world-wide distribution of allele frequencies at the human dopamine D4 receptor locus. Human Genetics, 98, 91–101.
Coccaro, E. F. (1992). Impulsive aggression and central serotonergic system function in humans: An example of a dimensional brain-behavior relationship. International Clinical Psychopharmacology, 7, 3–12.
Comings, D. E. (1998). Why different rules are required for polygenic inheritance: Lessons from studies of the DRD2 gene. Alcohol, 16, 61–70.
Comings, D. E., Muhleman, D., Ahn, C., Gysin, R., & Flanagan, S. D. (1994). The dopamine D2 receptor gene: A genetic risk factor in substance abuse. Drug and Alcohol Dependence, 34, 175– 180.
Dunne, M. P., Martin, N. G., Statham, D. J., Slutske, W. S., Dinwiddie, S. H., Bucholz, K. K. (1997). Genetic and environmental contributions to variance in age at first sexual intercourse. Psychological Science, 8, 211–216.
Ebstein, R. P., Nemanov, L., Klotz, I., Gritsendo, I., & Belmaker, R. H. (1997). Additional evidence for an association between the dopamine D4 receptor (D4DR) exon III repeat polymorphism and the human trait of novelty seeking. Molecular Psychiatry, 2, 472–477.
Ebstein, R. P., Novick, O., Umansky, R., Priel, B., Osher, Y., Blaine, D., et al. (1996). Dopamine D4 receptor (D4DR) exon III polymorphism associated with the human personality trait of novelty seeking. Nature Genetics, 12, 78–80.
Ekelund, J., Lichtermann, D., Jarvelin, M. R., & Peltonen, L. (1999). Association between novelty seeking and the type 4 dopamine receptor gene in a large Finnish cohort sample. American Journal of Psychiatry, 156, 1453–1459.
Ewens, W. J., & Spielman, R. S. (1995). The transmission/disequilibrium test: History, subdivision, and admixture. American Journal of Human Genetics, 57, 455–464.
Finkelstein, J. W., Susman, E. J., Chinchilli, V. M., DArcangelo, M. R., Kunselman, S. J., Schwab, J., et al. (1998). Effects of estrogen or testosterone on self-reported sexual responses and behaviors in hypogonadal adolescents. Journal of Clinical Endocrinology and Metabolism, 83, 2281–2285.
Flannery, D. J., Rowe, D. C., & Gulley, B. L. (1993). Impact of pubertal status, timing, and age on adolescent sexual experience and delinquency. Journal of Adolescent Research, 8, 21–40.
Gelernter, J., Kranzler, H., Coccaro, E., Siever, L., New, A., & Mulgrew, C. L. (1997). D4 dopamine-receptor (DRD4) alleles and novelty seeking in substance-dependent, personality-disorder, and control subjects. American Journal of Human Genetics, 61, 1144– 1152.
Gelernter, J., Kranzler, H., & Satel, S. A. (1999). No association between D2 dopamine receptor (DRD2) alleles or haplotypes and cocaine dependence in European- and African-Americans. Biological Psychiatry, 45, 340–345.
Goldman, D., Urbanek, M., Guenther, D., Robin, R., & Long, J. C. (1997). Linkage and association of a functional DRD2 variant [(Ser311Cys] and DRD2 markers to alcoholism, substance abuse and schizophrenia in Southwestern American Indians. American Journal of Medical Genetics, 74, 386–394.
Gottlieb, G. (2003). On making behavioral genetics truly developmental. Human Development, 46, 337–355.
Gottlieb, G., & Halpern, C. T. (2002). A relational view of causality in normal and abnormal development. Development and Psychopathology, 14, 421–435.
Guo, G., & Tong, Y. (2006). Age at first sexual intercourse, genes, and social and demographic context: Evidence from twins and the dopamine D4 receptor gene. Demography, in press.
Haberstick, B. C., Lessem, J. M., Hopfer, C. J., Smolen, A., Ehringer, M. A., Timberlake, D., et al. (2005). Monoamine oxidase A (MAOA) and antisocial behaviors in the presence of childhood and adolescent maltreatment. American Journal of Medical Menetics Part B (Neuropsychiatric Genetics), 135, 59–64.
Halpern, C. T., Campbell, B., Agnew, C. R., Thompson, V., & Udry, J. R. (2002). Associations between stress reactivity and sexual and non-sexual risk taking in adolescent males. Hormones and Behavior, 42, 387–398.
Halpern, C. T., Udry, J. R., Campbell, B., & Suchindran, C. (1993). Testosterone and pubertal development as predictors of sexual activity: A panel analysis of adolescent males. Psychosomatic Medicine, 55, 436–447.
Halpern, C. T., Udry, J. R., Campbell, B., Suchindran, C., & Mason, G. A. (1994). Testosterone and religiosity as predictors of sexual attitudes and activity among adolescent males: A biosocial model. Journal of Biosocial Science, 26, 217–234.
Halpern, C. T., Udry, J. R., & Suchindran, C. (1997). Testosterone predicts initiation of coitus in adolescent females. Psychosomatic Medicine, 59, 161–171.
Halpern, C. T., Udry, J. R., & Suchindran, C. (1998). Monthly measures of salivary testosterone predict sexual activity in adolescent males. Archives of Sexual Behavior, 27, 445–465.
Hamer, D. (2002). Genetics of sexual behavior. In J. Benjamin, R. P. Ebstein, & R. H. Belmaker (Eds.), (Molecular genetics and the human personality (pp. 257–272). Washington, DC: American Psychiatric Publishing.
Harris, K. M., Florey, F., Tabor, J., Bearman, P. S., Jones, J., & Udry, J. R. (2003). The National Longitudinal Study of Adolescent Health: Research design. Retrieved June 2, 2006, from University of North Carolina, Carolina Population Center Web site: http://www.cpc.unc.edu/projects/addhealth/design
Heils, A., Teufel, A., Petri, S., Stober, G., Riederer, P., Bengel, D., et al. (1996). Allelic variation of human transporter gene expression. Journal of Neurochemistry, 66, 2621–2624.
Hill, S. Y., Zezza, N., Wipprecht, G., Locke, J., & Neiswanger, K. (1999). Personality traits and dopamine receptors (D2 and D4): Linkage studies in families of alcoholics. American Journal of Medical Genetics, 88, 634–641.
Hillman, S. B., & Haskin, J. M. (2000). Personality and drug abstention in adolescents. Psychological Reports, 87, 1023–1026.
Horvath, P., & Zuckerman, M. (1993). Sensation seeking, risk appraisal, and risky behavior. Personality and Individual Differences, 14, 41–52.
Hull, E. M., Lorrain, D. S., Du, J., Matuszewich, L., Lumley, L. A., Putnam, S. K., et al. (1999). Hormone-neurotransmitter interactions in the control of sexual behavior. Behavioral Brain Research, 105, 105–116.
Johnston, T. D., & Edwards, L. (2002). Genes, interaction, and the development of behavior. Psychological Review, 109, 26– 34.
Jonsson, E. G., Nothen, M. M., Gustavsson, J. P., Neidt, H., Brene, S., Tylee, A., et al. (1997). Lack of evidence for allelic association between personality traits and dopamine D4 receptor gene polymorphism. American Journal of Psychiatry, 154, 697–699.
Joyce, J. N., & Meador-Woodruff, J. H. (1997). Linking the family of D2 receptors to neuronal circuits in human brain: Insights into schizophrenia. Neuropsychopharmacology, 16, 375– 384.
Kohler, H. P., & Christensen, K. (2000). Genetic influences on fertility behavior: Findings from a Danish twin study. In J. L. Rodgers, D. C. Rowe, & W. B. Miller (Eds.), Genetic influences on human fertility and sexuality (pp. 67–84). Boston: Kluwer.
Kono, Y., Yoneda, H., Sakai, T., Nonomura, Y., Inayama, Y., Koh, J., et al. (1997). Association between early-onset alcoholism and the dopamine D2 receptor gene. American Journal of Medical Genetics, 74, 179–182.
Koob, G. F., Ahmed, S. H., Boutrel, B., Chen, S. A., Kenny, P. J., Markou, A., et al. (2004). Neurobiological mechanisms in the transition from drug use to drug dependence. Neuroscience and Biobehavioral Reviews, 27, 739–749.
LeMarquand, D., Pihl, R. O., & Benkelfat, C. (1994). Serotonin and alcohol intake, abuse, and dependence: Clinical evidence. Biological Psychiatry, 36, 326–337.
Lesch, K. P., Bengel, D., Heils, A., Sabol, S. Z., Greenberg, B. D., & Petri, S. (1996). Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science, 274, 1527–1531.
Lesch, K. P., Greenberg, B. D., Higley, J. D., Bennett, A., & Murphy, D. L. (2002). Serotonin transporter, personality and behavior: Toward a dissection of gene-gene and gene-environment interaction. In J. Benjamin, R. P. Ebstein, & R. H. Belmaker (Eds.), (Molecular genetics and the human personality (pp. 109–135). Washington, DC: American Psychiatric Publishing.
Madrid, G. A., MacMurray, J., Lee, J. W., Anderson, B. A., & Comings, D. E. (2001). Stress as a mediating factor in the association between the DRD2 TaqI polymorphism and alcoholism. Alcohol, 23, 117–122.
Malhotra, A. K., Virkkunen, M., Rooney, W., Eggert, W., Linnoila, M., & Goldman, D. (1996). The association between the dopamine D4 receptor (D4DR) 16 amino acid repeat polymorphism and novelty seeking. Molecular Psychiatry, 1, 388–391.
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, 91– 97.
Melis, M. R., & Argiolas, A. (1995). Dopamine and sexual behavior. Neuroscience and Biobehavioral Reviews, 19, 19–38.
Miller, W. C., Ford, C. A., Morris, M., Handcock, M. S., Schmitz, J. L., Hobbs, M. M., et al. (2004). Prevalence of chlamydial and gonococcal among young adults in the United States. Journal of the American Medical Association, 291, 2229–2236.
Miller, L., & Gur, M. (2002). Religiousness and sexual responsibility in adolescent girls. Journal of Adolescent Health, 31, 401–406.
Miller, W. B., Pasta, D. J., MacMurray, J., Chiu, C., Wu, H., & Comings, D. E. (1999). Dopamine receptors are associated with age at first sexual intercourse. Journal of Biosocial Science, 31, 43–54.
Missale, C., Nash, S. R., Robinson, S. W., Jaber, M., & Caron, M. G. (1998). Dopamine receptors: From structure to function. Physiological Reviews, 78, 189–225.
Munafo, M. R., Clark, T. G., Moore, L. R., Payne, E., Walton, R., & Flint, J. (2003). Genetic polymorphisms and personality in health adults: A systematic review and meta-analysis. Molecular Psychiatry, 8, 471–484.
Noble, E. P. (2003). D2 dopamine receptor gene in psychiatric and neurologic disorders and its phenotypes. American Journal of Medical Genetics Part B (Neuropsychiatric Genetics), 116B, 103–125.
Noble E. P., Blum, K., Khalsa, M. E., Ritchie, T., Montgomery, A., Wood, R. C., et al. (1993). Allelic association of the D2 dopamine receptor gene with cocaine dependence. Drug and Alcohol Dependence, 33, 271–285.
Noble, E. P., Ozkaragoz, T. Z., Ritchie, T. L., Zhang, X., Belin, T. R., & Sparks, R. S. (1998). D2 and D4 dopamine receptor polymorphisms and personality. American Journal of Medical Genetics, 8, 257–267.
O’Hara, B. F., Smith, S. S., Bird, G., Persico, A. M., Suarez, B. K., Cutting, G. R., et al. (1993). Dopamine D2 receptor RFLPs, haplotypes and their association with substance use in Black and Caucasian research volunteers. Human Heredity, 43, 209–218.
Ono, Y., Manki, H., Yoshimura, K., Muramatsu, T., Mizushima, H., Higuchi, S., et al. (1997). Association between dopamine D4 receptor (D4DR) exon III polymorphism and novelty seeking in Japanese subjects. American Journal of Medical Genetics, 74, 501–503.
Owen, M. J., & Nemeroff, C. B. (1994). The role of serotonin in the pathophysiology of depression: Focus on the serotonin transporter. Clinical Chemistry, 40, 288–295.
Paterson, A. D., Sunohara, G. A., & Kennedy, J. L. (1999). Dopamine D4 receptor gene: Novelty or nonsense? Neuropsychopharmacology, 21, 3–16.
Pato, C. N., Macciardi, F., Pato, M. T., Verga, M., & Kennedy, J. L. (1993). Review of the putative association of dopamine D2 receptor and alcoholism: A meta-analysis. American Journal of Medical Genetics, 48, 78–82.
Poston, W. S., Ericsson, M., Linder, J., Haddock, C. K., Hanis, C. L., Nilsson, T., et al. (1998). D4 dopamine receptor gene exon III polymorphism and obesity risk. Eating & Weight Disorders: EWD, 3, 71–77.
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 (pp. 85–106). Boston: Kluwer.
Rodgers, J. L., Kohler, H. P., Kyvik, K. O., & Christensen, K. (2001). Behavior genetic modeling of human fertility: Findings from a contemporary Danish twin study. Demography, 38, 29–42.
Rodgers, J. L., Rowe, D. C., & Buster, M. (1999). Nature, nurture and first sexual intercourse in the USA: Fitting behavioral genetic models to NLSY kinship data. Journal of Biosocial Science, 31, 29–41.
Smolen, A., & Hewitt, J. K. (2000). DNA sampling, genotyping, and determination of zygosity. In L. Manhart (Ed.), Biomarkers in Wave III of the Add Health Study (pp. 42–57). Retrieved June 2, 2006, from University of North Carolina, Carolina Population Center Web site: http://www.cpc.unc.edu/projects/ addhealth/files/biomark.pdf
Stanton, B., Li, X., Cottrell, L., & Kaljee, L. (2001). Early initiation of sex, drug-related behaviors, and sensation-seeking among urban, low-income African-American adolescents. Journal of the National Medical Association, 93, 129–138.
Sullivan, P. F., Field, W. J., Kennedy, M. A., Mulder, R. T., Sellman, J. D., & Joyce, P. R. (1998). No association between novelty seeking and the type 4 dopamine receptor (DRD4) in two New Zealand samples. American Journal of Psychiatry, 155, 98– 101.
Tomitaka, M., Tomitaka, S., Otuka, Y., Kim, K., Matuki, H., & Sakamoto, K. (1999). Association between novelty seeking and dopamine receptor D4 (DRD4) exon III polymorphism in Japanese subject. American Journal of Medical Genetics (Neuropsychiatric Genetics), 88, 469–471.
Udry, J. R., Billy, J. O. G., Morris, N. M., Groff, T. R., & Raj, M. H. (1985). Serum androgenic hormones motivate sexual behavior in adolescent boys. Fertility and Sterility, 43, 90–94.
Udry, J. R., Talbert, L. M., & Morris, N. M. (1986). Biosocial foundations for adolescent female sexuality. Demography, 23, 217–230.
van Furth, W. R., Wolterink, G., & van Rhee, J. M. (1995). Regulation of masculine sexual behavior: Involvement of brain opioids and dopamine. Brain Research Reviews, 21, 162–184.
Van Tol, H. H., Wu, C. M., Guan, H. C., Ohara, K., Bunzow, J. R., & Civelli, O. (1992). Multiple dopamine D4 receptor variants in the human population. Nature, 358, 149–152.
Vandenbergh, D. J., Zonderman, A. B., Wang, J., Uhl, G. R., & Costa, P. T. (1997). No association between novelty seeking and dopamine D4 receptor (D4DR) exon III seven repeat alleles in Baltimore Longitudinal Study of Aging Participants. Molecular Psychiatry, 2, 417–419.
Weinstock, H., Berman, S., & Cates, W. (2004). Sexually transmitted diseases among American youth: Incidence and prevalence estimates, 2000. Perspectives on Sexual and Reproductive Health, 36, 6–10.
Whitehead, B. D., Wilcox, B. L., Rostosky, S. S., Randall, B., & Wright, M. L. C. (2001). Keeping the faith: The role of religion and faith communities in preventing teen pregnancy. Washington, DC: National Campaign to Prevent Teen Pregnancy.
Wong, A. H. C., Buckle, C. E., & Van Tol, H. H. M. (2000). Polymorphisms in dopamine receptors: What do they tell us? European Journal of Pharmacology, 410, 183–203.
Zuckerman, M. (1979). Sensation-seeking: Beyond the optimal level of arousal. New York: Wiley.
Zuckerman, M., & Cloninger, C. R. (1996). Relationships between Cloningers, Zuckerman's, and Eysenck’s dimensions of personality. Personality and Individual Differences, 21, 283–285.
Acknowledgments
Funding for this study is from the National Institute of Drug Abuse (Grant R01-DA14496, Denise Dion Halfors, principal investigator). This research uses data from Add Health, a program project designed by J. Richard Udry, Peter S. Bearman, and Kathleen Mullan Harris, and funded by the National Institute of Child Health and Human Development (a Grant P01-HD31921) with cooperative funding from 17 other agencies. Special acknowledgment is due Ronald R. Rindfuss and Barbara Entwisle for assistance in the original design. Persons interested in obtaining data files from Add Health should contact Add Health, Carolina Population Center, 123 W. Franklin Street, Chapel Hill, NC 27516-2524 (www.cpc.unc.edu/addhealth/contract.html).
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Halpern, C.T., Kaestle, C.E., Guo, G. et al. Gene-Environment Contributions to Young Adult Sexual Partnering. Arch Sex Behav 36, 543–554 (2007). https://doi.org/10.1007/s10508-006-9084-9
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DOI: https://doi.org/10.1007/s10508-006-9084-9