Genetic and Environmental Contributions to Covariation Between DHEA and Testosterone in Adolescent Twins

Behavior Genetics

Volumn 45, Issue 3, 2015, Pages 324-340

  Van Hulle, Carol A ^a   Moore, Mollie N ^a   Shirtcliff, Elizabeth A ^b   Lemery Chalfant, Kathryn ^c   Goldsmith, H Hill ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b IOWA STATE UNIVERSITY   (United States)

^c ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Adolescents; Behavior genetics; DHEA; Puberty; Testosterone; Twins

Indexed keywords

PRASTERONE; TESTOSTERONE;

ADOLESCENT; BEHAVIOR GENETICS; CHEMISTRY; CHILD; DIZYGOTIC TWINS; ENVIRONMENT; FEMALE; GENETICS; HUMAN; MALE; METABOLISM; MONOZYGOTIC TWINS; MULTIVARIATE ANALYSIS; PHENOTYPE; PUBERTY; SALIVA; SAMPLE SIZE; SEXUAL MATURATION; TWINS;

ADOLESCENT; CHILD; DEHYDROEPIANDROSTERONE; ENVIRONMENT; FEMALE; GENETICS, BEHAVIORAL; HUMANS; MALE; MULTIVARIATE ANALYSIS; PHENOTYPE; PUBERTY; SALIVA; SAMPLE SIZE; SEXUAL MATURATION; TESTOSTERONE; TWINS, DIZYGOTIC; TWINS, MONOZYGOTIC;

EID: 84939954344     PISSN: 00018244     EISSN: 15733297     Source Type: Journal    
DOI: 10.1007/s10519-015-9709-7     Document Type: Article

References (84)

1. Akamine Y, Kato K, Ibayashi H (1980) Studies on changes in the concentration of serum adrenal androgens in pubertal twins. Acta Endocrinol 93(3):356–364
2. Boker S, Neale M, Maes H, Wilde M, Spiegel M, Brick T et al (2011) OpenMx: an open source extended structural equation modeling framework. Psychometrika 76(2):306–317. doi:10.1007/s11336-010-9200-6
3. Booth A, Shelley G, Mazur A, Tharp G, Kittok R (1989) Testosterone, and winning and losing in human competition. Horm Behav 23(4):556–571
4. Booth A, Johnson DR, Granger DA, Crouter AC, McHale S (2003) Testosterone and child and adolescent adjustment: the moderating role of parent-child relationships. Dev Psychol 39(1):85–98. doi:10.1037//0012-1649.39.1.85
5. Bordini B, Rosenfield RL (2011) Normal pubertal development: part I: the endocrine basis of puberty. Pediatr Rev 32(6):223–229. doi:10.1542/pir.32-6-223
6. Brooks-Gunn J (1988) Antecedents and consequences of variation in girls’ maturational timing. J Adolesc Health Care 9(5):365–373
7. Ceballos N, Alabsi M (2006) Dehydroepiandrosterone sulfate, cortisol, mood state and smoking cessation: relationship to relapse status at 4-week follow-up. Pharmacol Biochem Behav 85(1):23–28. doi:10.1016/j.pbb.2006.06.021
8. Compagnone NA, Mellon SH (1998) Dehydroepiandrosterone: a potential signaling molecule for neocortical organization during development. Proc Natl Acad Sci 95(8):4678–4683
9. Dick D, Rose R, Pulkkinen L, Kaprio J (2001) Measuring puberty and understanding its impact: a longitudinal study of adolescent twins. J Youth Adolesc 30(4):385–399
10. Dorn L, Susman E (2002) Puberty script: assessment of physical development in boys and girls. Cincinnati Children’s Hospital Medical Center, Cincinnati
11. Dorn L, Dahl R, Woodward HR, Biro FM (2006) Defining the boundaries of early adolescence: a user’s guide to assessing pubertal status and pubertal timing in research with adolescents. Appl Dev Sci 101(1):30–56
12. Doughty D, Rodgers JL (2000) Behavior genetic modeling of menarche in US females. In: Rodgers JL, Rowe D, Miller WB (eds) Genetic influences on human fertility and sexuality. Kluwer Academic Publishers, New York, pp 169–181
13. Ellis BJ (2004) Timing of pubertal maturation in girls: an integrated life history approach. Psychol Bull 130(6):920–958. doi:10.1037/0033-2909.130.6.920
14. Ellis BJ, Shirtcliff EA, Boyce WT, Deardorff J, Essex MJ (2011) Quality of early family relationships and the timing and tempo of puberty: effects depend on biological sensitivity to context. Dev Psychopathol 23(01):85–99. doi:10.1017/S0954579410000660
15. Finkelstein JW, D’Arcangelo MR, Susman EJ, Chinchilli VM, Kunselman SJ, Schwab J et al (1999) Self-assessment of physical sexual maturation in boys and girls with delayed puberty. J Adolesc Health 25(6):379–381
16. Forget-Dubois N, Peruuse D, Turecki G, Billette J, Rouleau G, Malo M, Tremblay RE (2003) Diagnosing zygosity in infant twins: physical similarity, genotyping, and chorionicity. Twin Research 6:479–485
17. Galsworthy M, Dionne G, Dale P, Plomin R (2000) Sex differences in early verbal and non-verbal cognitive development. Dev Sci 3:206–215
18. Ge X, Natsuaki M, Neiderhiser JM, Reiss D (2007) Genetic and environmental influences on pubertal timing: results from two national sibling studies. J Res Adolesc 17(4):767–788
19. Goel N, Bale TL (2008) Organizational and activational effects of testosterone on masculinization of female physiological and behavioral stress responses. Endocrinology 149(12):6399–6405. doi:10.1210/en.2008-0433
20. Goldsmith HH (1991) A zygosity questionnaire for young twins: a research note. Behav Genet 21(3):257–269. doi:10.1007/BF01065819
21. Granger DA, Schwartz EB, Booth A, Curran M, Zakaria D (1999) Assessing dehydroepiandrosterone in saliva: a simple radioimmunoassay for use in studies of children, adolescents and adults. Psychoneuroendocrinology 24(5):567–579. doi:10.1016/S0306-4530(99)00013-X
22. Granger DA, Shirtcliff EA, Zahn-Waxler C, Usher B, Klimes-Dougan B, Hastings P (2003) Salivary testosterone diurnal variation and psychopathology in adolescent males and females: individual differences and developmental effects. Dev Psychopathol 15(02):431–439. doi:10.1017/S0954579403000233
23. Granger DA, Shirtcliff EA, Booth A, Kivlighan KT, Schwartz EB (2004) The “trouble” with salivary testosterone. Psychoneuroendocrinology 29(10):1229–1240
24. Grumbach MM (2002) The neuroendocrinology of human puberty revisited. Horm Res 57(Suppl 2):2–14
25. Halpern CT, Udry JR, Campbell B, Suchindran C, Mason GA (1994) Testosterone and religiosity as predictors of sexual attitudes and activity among adolescent males: a biosocial model. J Biosoc Sci 26(2):217–234
26. Halpern CT, Udry JR, Suchindran C (1997) Testosterone predicts initiation of coitus in adolescent females. Psychosom Med 59(2):161–171
27. Harden KP, Kretsch N, Tackett JL, Tucker-Drob EM (2014) Genetic and environmental influences on testosterone in adolescents: evidence for sex differences: genetic influences on testosterone. Dev Psychobiol 9(4):558–565. doi:10.1002/dev.21207
28. Harris J, Vernon PA, Boomsma DI (1998) The heritability of testosterone: a study of Dutch adolescent twins and their parents. Behav Genet 28(3):165–171
29. Hermans EJ, Putman P, Baas JM, Koppeschaar HP, van Honk J (2006) A single administration of testosterone reduces fear-potentiated startle in humans. Biol Psychiatry 59(9):872–874. doi:10.1016/j.biopsych.2005.11.015
30. Hibel LC, Granger DA, Cicchetti D, Rogosch F (2007) Salivary biomarker levels and diurnal variation: associations with medications prescribed to control children’s problem behavior. Child Dev 78(3):927–937
31. Hoekstra RA, Bartels M, Boomsma DI (2006) Heritability of testosterone in 12 year old twins and its relation to pubertal development. Twin Res Hum Genet 9(4):558–565
32. Huang B, Biro FM, Dorn LD (2009) Determination of relative timing of pubertal maturation through ordinal logistic modeling: evaluation of growth and timing parameters. J Adolesc Health 45(4):383–388. doi:10.1016/j.jadohealth.2009.02.013
33. Ibanez L, Ferrer A, Marcos MV, Hierro FR, de Zegher F (2000) Early puberty: rapid progression and reduced final height in girls with low birth weight. Pediatrics 106(5):e72
34. Jaffee SR, Price TS (2007) Gene–environment correlations: a review of the evidence and implications for prevention of mental illness. Mol Psychiatry. doi:10.1038/sj.mp.4001950
35. Johnson MM, Dismukes AR, Fleury E, Shirtcliff EA (2014) Psychopathy’s influence on the coupling between hypothalamic-pituitary-adrenal and -gonadal axes among incarcerated adolescents. Dev Psychobiol 56(3):448–458
36. Kaprio J, Rimpelä A, Winter T, Viken RJ, Rimpelä M, Rose RJ (1995) Common genetic influences on BMI and age at menarche. Hum Biol 67:739–753
37. Kauffman AS, Navarro VM, Kim J, Clifton DK, Steiner RA (2009) Sex differences in the regulation of Kiss1/NKB neurons in juvenile mice: implications for the timing of puberty. AJP 297(5):E1212–E1221. doi:10.1152/ajpendo.00461.2009
38. Koenis MMG, Brouwer RM, van Baal GCM, van Soelen ILC, Peper JS, van Leeuwen M et al (2013) Longitudinal study of hormonal and physical development in young twins. J Clin Endocrinol Metab 98(3):E518–E527. doi:10.1210/jc.2012-3361
39. Kuijper EAM, Lambalk CB, Boomsma DI, van der Sluis S, Blankenstein MA, de Geus EJC, Posthuma D (2007) Heritability of reproductive hormones in adult male twins. Hum Reprod 22(8):2153–2159. doi:10.1093/humrep/dem145
40. Lee M-S, Yang J-W, Ko Y-H, Han C, Kim S-H, Lee M-S et al (2008) Effects of methylphenidate and bupropion on DHEA-S and cortisol plasma levels in attention-deficit hyperactivity disorder. Child Psychiatry Hum Dev 39(2):201–209. doi:10.1007/s10578-007-0081-6
41. Luke B, Witter FR, Abbey H, Feng T, Namnoum AB, Paige DM, Johnson TR (1991) Gestational age-specific birthweights of twins versus singletons. Acta Genet Med Gemellol 40(1):69–76
42. Malina R, Ryan RC, Bonci CM (1994) Age at menarche in athletes and their mothers and sisters. Ann Hum Biol 21:417–422
43. Marceau K, Dorn LD, Susman EJ (2012) Stress and puberty-related hormone reactivity, negative emotionality, and parent–adolescent relationships. Psychoneuroendocrinology 37(8):1286–1298. doi:10.1016/j.psyneuen.2012.01.001
44. Marceau K, Ruttle PL, Shirtcliff EA, Hastings PD, Klimes-Dougan B, Zahn-Waxler C (2013) Within-person coupling of changes in cortisol, testosterone, and DHEA across the day in adolescents: coupling of diurnal hormone changes. Dev Psychobiol. doi:10.1002/dev.21173
45. Marceau K, Shirtcliff EA, Hastings PD, Klimes-Dougan B, Zahn-Waxler C, Dorn LD, Susman EJ (2014) Within-adolescent coupled changes in cortisol with DHEA and testosterone in response to three stressors during adolescence. Psychoneuroendocrinology 41:33–45. doi:10.1016/j.psyneuen.2013.12.002
46. Matchock RL, Dorn LD, Susman EJ (2007) Diurnal and seasonal cortisol, Testosterone, and DHEA rhythms in boys and girls during puberty. Chronobiol Int 24(5):969–990. doi:10.1080/07420520701649471
47. Meaney MJ, McEwen BS (1986) Testosterone implants into the amygdala during the neonatal period masculinize the social play of juvenile female rats. Brain Res 398(2):324–328
48. Meikle AW, Stringham JD, Bishop D, West D (1986) Quantitating genetic and nongenetic factors influencing androgen production and learning rates in men. J Clin Endocrinol Metab 67(1):104–109
49. Meyer JM, Eaves LJ, Heath AC, Martin NG (1991) Estimating genetic influences on the age-at-menarche. Am J Med Genet 39:148–154
50. Mustanski BS, Viken RJ, Kaprio J, Pulkkinen L, Rose RJ (2004) Genetic and environmental influences on pubertal development: longitudinal data from Finnish twins at ages 11 and 14. Dev Psychol 40(6):1188–1198
51. Neale M, Cardon L (1992) Methodology for genetic studies of twins and families. Kluwer Academic Publishers, Dordrecht
52. Op de Macks ZA, Moor BG, Overgaauw S, Güroğlu B, Dahl RE, Crone EA (2011) Testosterone levels correspond with increased ventral striatum activation in response to monetary rewards in adolescents. Dev Cogn Neurosci 1(4):506–516. doi:10.1016/j.dcn.2011.06.003
53. OpenMx (2012) (Version 1.3.2). Retrieved from http://openmx.psyc.virginia.edu. Accessed 2/4/2013
54. Parker LN (1991) Adrenarche. Endocrinol Metab Clin North Am 20:71–83
55. Petersen AC, Crockett L, Richards M, Boxer A (1988) A self-report measure of pubertal status: reliability, validity, and initial norms. J Youth Adolesc 17(2):117–133. doi:10.1007/BF01537962
56. Purcell S (2002) Variance components models for gene-environment interaction in twin analysis. Twin Res 5(6):554–571. doi:10.1375/136905202762342026
57. Rathouz PJ, Van Hulle CA, Rodgers JL, Waldman ID, Lahey BB (2008) Specification, testing, and interpretation of gene-by-measured-environment interaction models in the presence of gene–environment correlation. Behav Genet 38(3):301–315. doi:10.1007/s10519-008-9193-4
58. Rejeski WJ, Gagne M, Parker PE, Koritnik DR (1989) Acute stress reactivity from contested dominance in dominant and submissive males. Behav Med (Washington, D.C.) 15(3):118–124. doi:10.1080/08964289.1989.9934574
59. Rice T, Sprecher DL, Borecki IB, Mitchell LE, Laskarzewski PM, Rao DC (1993) Cincinnati myocardial infarction and hormone family study: family resemblance for testosterone in random and MI families. Am J Med Genet 47(4):542–549. doi:10.1002/ajmg.1320470421
60. Rutter M, Redshaw J (1991) Annotation: growing up as a twin: twin-singleton differences in psychological development. J Child Psychol Psychiatry 32(6):885–895
61. Ruttle PL, Shirtcliff EA, Armstrong JM, Klein MH, Essex MJ (2013) Neuroendocrine coupling across adolescence and the longitudinal influence of early life stress: Neuroendocrine Coupling. Dev Psychobiol. doi:10.1002/dev.21138
62. Saenger P, Dimartino-Nardi J (2001) Premature adrenarche. J Endocrinol Invest 24(9):724–733
63. Schmidt NL, Van Hulle CA, Brooker RJ, Meyer LR, Lemery-Chalfant K, Goldsmith HH (2012) Wisconsin twin research: early development, childhood psychopathology, autism, and sensory over-responsivity. Twin Res Hum Genet 16(01):376–384. doi:10.1017/thg.2012.105
64. Schulz KM, Molenda-Figueira HA, Sisk CL (2009) Back to the future: the organizational–activational hypothesis adapted to puberty and adolescence. Horm Behav 55(5):597–604. doi:10.1016/j.yhbeh.2009.03.010
65. Shirtcliff EA (2005) Neuroendocrine and neural contributions to pubertal development, normative adolescent development and affect-related behavior problems. Paper presented at the Workshop on the Science of Adolescence Health and Development, National Academy of Science
66. Shirtcliff EA, Ruttle P (2010) Immunological and nueroendocrine dysregulation following early deprivation and stress. In: Brisch KH (ed) Attachment and early disorders of development. Kletta-Cotta, Stuttgart
67. Shirtcliff EA, Dahl R, Pollak SD (2009) Pubertal development: correspondence between hormonal and physical development. Child Dev 80(2):327–337
68. Sklar CA, Kaplan SL, Grumbach MM (1980) Evidence for dissociation between adrenarche and gonadarche: studies in patients with idiopathic precocious puberty, gonadal dysgenesis, isolated gonadotropin deficiency, and constitutionally delayed growth and adolescence. J Clin Endocrinol Metab 51(3):548–556. doi:10.1210/jcem-51-3-548
69. Slap GB, Khalid N, Paikoff RL, Brooks-Gunn J, Warren MP (1994) Evolving self-image, pubertal manifestations, and pubertal hormones: preliminary findings in young adolescent girls. J Adolesc Health 15(4):327–335. doi:10.1016/1054-139X(94)90606-8
70. Spellacy W, Handler A, Ferre CF (1990) A case-control study of 1,253 twin pregnancies from a 1982-1987 perinatal data base. Obstet Gynecol 75(2):168–171
71. Terasawa E (1994) Steroid modulation of pulsatile LHRH release in the rhesus monkey. Horm Behav 28(4):406–416. doi:10.1006/hbeh.1994.1037
72. Terasawa E (1995) Control of luteinizing hormone-releasing hormone pulse generation in nonhuman primates. Cell Mol Neurobiol 15(1):141–164. doi:10.1007/BF02069563
73. Treloar SA, Martin N (1990) Age at menarche as a fitness trait: non-additive genetic variance detected in a large twin sample. Am J Hum Genet 47:137–148
74. Van den Akker OB, Stein GS, Neale MC, Murray RM (1987) Interview guide for the Hamilton Depression Rating Scale, Seasonal genetic and environmental variation in menstrual cycle: histories of Affective Disorder version (SIGH-SAD). Acta Genet Med Gemellol (Roma) 36:541–548
75. Van den Berg SM, Boomsma DI (2007) The familial clustering of age at menarche in extended twin families. Behav Genet 37(5):661–667. doi:10.1007/s10519-007-9161-4
76. Van den Berg SM, Setiawan A, Bartels M, Polderman TJC, van der Vaart AW, Boomsma DI (2006) Individual differences in puberty onset in girls: bayesian estimation of heritabilities and genetic correlations. Behav Genet 36(2):261–270. doi:10.1007/s10519-005-9022-y
77. Van den Oord EJCG, Koot HM, Boomsma DI, Verhulst FC, Orlebeke JF (1995) A twin-singleton comparison of problem behavior in 2-3-year-olds. J Child Psychol Psychiatry 36(3):449–458. doi:10.1111/j.1469-7610.1995.tb01302.x
78. Van Niekerk JK, Huppert FA, Herbert J (2001) Salivary cortisol and DHEA: association with measures of cognition and well-being in normal older men, and effects of three months of DHEA supplementation. Psychoneuroendocrinology 26(6):591–612. doi:10.1016/S0306-4530(01)00014-2
79. Van Weissenbruch MM, Delemarre-van de Waal HA (2006) Early influences on the tempo of puberty. Horm Res 65(3):105–111. doi:10.1159/000091514
80. Wehkalampi K, Hovi P, Dunkel L, Strang-Karlsson S, Jarvenpaa AL, Eriksson JG, Kajantie E (2011) Advanced pubertal growth spurt in subjects born preterm: the Helsinkin study of very low birth weight adults. Clin Endocrinol Metab 96(2):525–533
81. Wirth MM, Schultheiss OC (2007) Basal testosterone moderates responses to anger faces in humans. Physiol Behav 90(2–3):496–505. doi:10.1016/j.physbeh.2006.10.016
82. Wolf OT, Kirschbaum C (1999) Action of dehydroepiandrosterone and its sulfate in the central nervous system: effects on cognition and emotion in animals and humans. Brain Res Rev 30(3):264–288
83. Yen SS, Laughlin GA (1998) Aging and the adrenal cortex. Exp Gerontol 33(7–8):897–910. doi:10.1016/S0531-5565(98)00046-1
84. Zilioli S, Watson NV (2014) Testosterone across successive competitions: evidence for a “winner effect” in humans? Psychoneuroendocrinology 47:1–9. doi:10.1016/j.psyneuen.2014.05.001