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Published in: BMC Medicine 1/2013

Open Access 01-12-2013 | Review

Evo-devo of human adolescence: beyond disease models of early puberty

Authors: Ze'ev Hochberg, Jay Belsky

Published in: BMC Medicine | Issue 1/2013

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Abstract

Despite substantial heritability in pubertal development, much variation remains to be explained, leaving room for the influence of environmental factors to adjust its phenotypic trajectory in the service of fitness goals. Utilizing evolutionary development biology (evo-devo), we examine adolescence as an evolutionary life-history stage in its developmental context. We show that the transition from the preceding stage of juvenility entails adaptive plasticity in response to energy resources, other environmental cues, social needs of adolescence and maturation toward youth and adulthood. Using the evolutionary theory of socialization, we show that familial psychosocial stress fosters a fast life history and reproductive strategy rather than early maturation being just a risk factor for aggression and delinquency. Here we explore implications of an evolutionary-developmental-endocrinological-anthropological framework for theory building, while illuminating new directions for research.
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Literature
1.
2.
go back to reference Hochberg Z: Evo Devo of Child Growth: Treatize on Child Growth and Human Evolution. 2012, New York: Wiley Hochberg Z: Evo Devo of Child Growth: Treatize on Child Growth and Human Evolution. 2012, New York: Wiley
3.
go back to reference Tinggaard J, Mieritz MG, Sorensen K, Mouritsen A, Hagen CP, Aksglaede L, Wohlfahrt-Veje C, Juul A: The physiology and timing of male puberty. Curr Opin Endocrinol Diabetes Obes. 2012, 19: 197-203.CrossRefPubMed Tinggaard J, Mieritz MG, Sorensen K, Mouritsen A, Hagen CP, Aksglaede L, Wohlfahrt-Veje C, Juul A: The physiology and timing of male puberty. Curr Opin Endocrinol Diabetes Obes. 2012, 19: 197-203.CrossRefPubMed
4.
go back to reference Aksglaede L, Olsen LW, Sorensen TI, Juul A: Forty years trends in timing of pubertal growth spurt in 157,000 Danish school children. PLoS One. 2008, 3: e2728-10.1371/journal.pone.0002728.CrossRefPubMedPubMedCentral Aksglaede L, Olsen LW, Sorensen TI, Juul A: Forty years trends in timing of pubertal growth spurt in 157,000 Danish school children. PLoS One. 2008, 3: e2728-10.1371/journal.pone.0002728.CrossRefPubMedPubMedCentral
5.
go back to reference Smith BH, Tompkins RL: Toward a life history of the hominidae. Annu Rev Anthropol. 1995, 24: 257-279. 10.1146/annurev.an.24.100195.001353.CrossRef Smith BH, Tompkins RL: Toward a life history of the hominidae. Annu Rev Anthropol. 1995, 24: 257-279. 10.1146/annurev.an.24.100195.001353.CrossRef
6.
go back to reference Sisk CL, Foster DL: The neural basis of puberty and adolescence. Nat Neurosci. 2004, 7: 1040-1047. 10.1038/nn1326.CrossRefPubMed Sisk CL, Foster DL: The neural basis of puberty and adolescence. Nat Neurosci. 2004, 7: 1040-1047. 10.1038/nn1326.CrossRefPubMed
8.
go back to reference Tardieu C: Short adolescence in early hominids: infantile and adolescent growth of the human femur. Am J Phys Anthropol. 1998, 107: 163-178. 10.1002/(SICI)1096-8644(199810)107:2<163::AID-AJPA3>3.0.CO;2-W.CrossRefPubMed Tardieu C: Short adolescence in early hominids: infantile and adolescent growth of the human femur. Am J Phys Anthropol. 1998, 107: 163-178. 10.1002/(SICI)1096-8644(199810)107:2<163::AID-AJPA3>3.0.CO;2-W.CrossRefPubMed
9.
go back to reference Howell N: Life Histories of the Dobe !Kung. 2010, Berkley: University of California Press Howell N: Life Histories of the Dobe !Kung. 2010, Berkley: University of California Press
10.
go back to reference Klein KO, Baron J, Colli MJ, McDonnell DP, Cutler GB: Estrogen levels in childhood determined by an ultrasensitive recombinant cell bioassay. J Clin Invest. 1994, 94: 2475-2480. 10.1172/JCI117616.CrossRefPubMedPubMedCentral Klein KO, Baron J, Colli MJ, McDonnell DP, Cutler GB: Estrogen levels in childhood determined by an ultrasensitive recombinant cell bioassay. J Clin Invest. 1994, 94: 2475-2480. 10.1172/JCI117616.CrossRefPubMedPubMedCentral
11.
go back to reference Ankarberg Lindgren C: Testosterone and 17beta-oestradiol secretion in children and adolescents. Assay development, levels for comparison and clinical applications. PhD Thesis. 2005, Goteborg University Ankarberg Lindgren C: Testosterone and 17beta-oestradiol secretion in children and adolescents. Assay development, levels for comparison and clinical applications. PhD Thesis. 2005, Goteborg University
12.
go back to reference Mead M: Coming of Age in Samoa. 2001, New York: Perrenial Classics, Originally published in 1928 by Williams Morrow and Company Mead M: Coming of Age in Samoa. 2001, New York: Perrenial Classics, Originally published in 1928 by Williams Morrow and Company
13.
go back to reference Locke JL, Bogin B: Language and life history: a new perspective on the development and evolution of human language. Behav Brain Sci. 2006, 29: 259-280. discussion 280-325PubMed Locke JL, Bogin B: Language and life history: a new perspective on the development and evolution of human language. Behav Brain Sci. 2006, 29: 259-280. discussion 280-325PubMed
14.
go back to reference Wingfield JC, Jacobs J, Hillgarth N: Ecological constraints and the evolution of hormone-behavior interrelationships. Ann N Y Acad Sci. 1997, 807: 22-41. 10.1111/j.1749-6632.1997.tb51911.x.CrossRefPubMed Wingfield JC, Jacobs J, Hillgarth N: Ecological constraints and the evolution of hormone-behavior interrelationships. Ann N Y Acad Sci. 1997, 807: 22-41. 10.1111/j.1749-6632.1997.tb51911.x.CrossRefPubMed
15.
go back to reference Campbell B: Adrenarche and the evolution of human life history. Am J Hum Biol. 2006, 18 (5): 569-589. 10.1002/ajhb.20528.CrossRefPubMed Campbell B: Adrenarche and the evolution of human life history. Am J Hum Biol. 2006, 18 (5): 569-589. 10.1002/ajhb.20528.CrossRefPubMed
16.
go back to reference Hochberg Z: Juvenility in the context of life history theory. Arch Dis Child. 2008, 93: 534-539. 10.1136/adc.2008.137570.CrossRefPubMed Hochberg Z: Juvenility in the context of life history theory. Arch Dis Child. 2008, 93: 534-539. 10.1136/adc.2008.137570.CrossRefPubMed
17.
go back to reference Del Giudice M: Sex, attachment, and the development of reproductive strategies. Behav Brain Sci. 2009, 32: 1-21. 10.1017/S0140525X09000016. discussion 21-67CrossRefPubMed Del Giudice M: Sex, attachment, and the development of reproductive strategies. Behav Brain Sci. 2009, 32: 1-21. 10.1017/S0140525X09000016. discussion 21-67CrossRefPubMed
18.
go back to reference White S: The child's entry into the age of reason. The five to seven year shift: the age of reason and responsibility. Edited by: Sameroff A, Haith, MM. 1996, Chicago: University of Chicago Press, 17-32. White S: The child's entry into the age of reason. The five to seven year shift: the age of reason and responsibility. Edited by: Sameroff A, Haith, MM. 1996, Chicago: University of Chicago Press, 17-32.
19.
go back to reference Weisfeld GE, Czilli T, Phillips KA, Gall JA, Lichtman CM: Possible olfaction-based mechanisms in human kin recognition and inbreeding avoidance. J Exp Child Psychol. 2003, 85: 279-295. 10.1016/S0022-0965(03)00061-4.CrossRefPubMed Weisfeld GE, Czilli T, Phillips KA, Gall JA, Lichtman CM: Possible olfaction-based mechanisms in human kin recognition and inbreeding avoidance. J Exp Child Psychol. 2003, 85: 279-295. 10.1016/S0022-0965(03)00061-4.CrossRefPubMed
20.
go back to reference Belsky J, Steinberg L, Draper P: Childhood experience, interpersonal development, and reproductive strategy: and evolutionary theory of socialization. Child Dev. 1991, 62: 647-670. 10.2307/1131166.CrossRefPubMed Belsky J, Steinberg L, Draper P: Childhood experience, interpersonal development, and reproductive strategy: and evolutionary theory of socialization. Child Dev. 1991, 62: 647-670. 10.2307/1131166.CrossRefPubMed
21.
go back to reference Zemel BS, Katz SH: The contribution of adrenal and gonadal androgens to the growth in height of adolescent males. Am J Phys Anthropol. 1986, 71: 459-466. 10.1002/ajpa.1330710409.CrossRefPubMed Zemel BS, Katz SH: The contribution of adrenal and gonadal androgens to the growth in height of adolescent males. Am J Phys Anthropol. 1986, 71: 459-466. 10.1002/ajpa.1330710409.CrossRefPubMed
22.
go back to reference Arlt W, Martens JW, Song M, Wang JT, Auchus RJ, Miller WL: Molecular evolution of adrenarche: structural and functional analysis of p450c17 from four primate species. Endocrinology. 2002, 143: 4665-4672. 10.1210/en.2002-220456.CrossRefPubMed Arlt W, Martens JW, Song M, Wang JT, Auchus RJ, Miller WL: Molecular evolution of adrenarche: structural and functional analysis of p450c17 from four primate species. Endocrinology. 2002, 143: 4665-4672. 10.1210/en.2002-220456.CrossRefPubMed
23.
go back to reference Palmert MR, Hayden DL, Mansfield MJ, Crigler JF, Crowley WF, Chandler DW, Boepple PA: The longitudinal study of adrenal maturation during gonadal suppression: evidence that adrenarche is a gradual process. J Clin Endocrinol Metab. 2001, 86: 4536-4542. 10.1210/jc.86.9.4536.CrossRefPubMed Palmert MR, Hayden DL, Mansfield MJ, Crigler JF, Crowley WF, Chandler DW, Boepple PA: The longitudinal study of adrenal maturation during gonadal suppression: evidence that adrenarche is a gradual process. J Clin Endocrinol Metab. 2001, 86: 4536-4542. 10.1210/jc.86.9.4536.CrossRefPubMed
24.
go back to reference Kroboth PD, Salek FS, Pittenger AL, Fabian TJ, Frye RF: DHEA and DHEA-S: a review. J Clin Pharmacol. 1999, 39: 327-348. 10.1177/00912709922007903.CrossRefPubMed Kroboth PD, Salek FS, Pittenger AL, Fabian TJ, Frye RF: DHEA and DHEA-S: a review. J Clin Pharmacol. 1999, 39: 327-348. 10.1177/00912709922007903.CrossRefPubMed
25.
go back to reference Chen CC, Parker CR: Adrenal androgens and the immune system. Semin Reprod Med. 2004, 22: 369-377. 10.1055/s-2004-861553.CrossRefPubMed Chen CC, Parker CR: Adrenal androgens and the immune system. Semin Reprod Med. 2004, 22: 369-377. 10.1055/s-2004-861553.CrossRefPubMed
26.
go back to reference Arquitt AB, Stoecker BJ, Hermann JS, Winterfeldt EA: Dehydroepiandrosterone sulfate, cholesterol, hemoglobin, and anthropometric measures related to growth in male adolescents. J Am Diet Assoc. 1991, 91: 575-579.PubMed Arquitt AB, Stoecker BJ, Hermann JS, Winterfeldt EA: Dehydroepiandrosterone sulfate, cholesterol, hemoglobin, and anthropometric measures related to growth in male adolescents. J Am Diet Assoc. 1991, 91: 575-579.PubMed
27.
go back to reference Hunt PJ, Gurnell EM, Huppert FA, Richards C, Prevost AT, Wass JA, Herbert J, Chatterjee VK: Improvement in mood and fatigue after dehydroepiandrosterone replacement in Addison's disease in a randomized, double blind trial. J Clin Endocrinol Metab. 2000, 85: 4650-4656. 10.1210/jc.85.12.4650.PubMed Hunt PJ, Gurnell EM, Huppert FA, Richards C, Prevost AT, Wass JA, Herbert J, Chatterjee VK: Improvement in mood and fatigue after dehydroepiandrosterone replacement in Addison's disease in a randomized, double blind trial. J Clin Endocrinol Metab. 2000, 85: 4650-4656. 10.1210/jc.85.12.4650.PubMed
28.
go back to reference Suzuki M, Wright LS, Marwah P, Lardy HA, Svendsen CN: Mitotic and neurogenic effects of dehydroepiandrosterone (DHEA) on human neural stem cell cultures derived from the fetal cortex. Proc Natl Acad Sci USA. 2004, 101: 3202-3207. 10.1073/pnas.0307325101.CrossRefPubMedPubMedCentral Suzuki M, Wright LS, Marwah P, Lardy HA, Svendsen CN: Mitotic and neurogenic effects of dehydroepiandrosterone (DHEA) on human neural stem cell cultures derived from the fetal cortex. Proc Natl Acad Sci USA. 2004, 101: 3202-3207. 10.1073/pnas.0307325101.CrossRefPubMedPubMedCentral
29.
go back to reference Hochberg Z: Evo-devo of child growth II: human life history and transition between its phases. Eur J Endocrinol. 2009, 160: 135-141.CrossRefPubMed Hochberg Z: Evo-devo of child growth II: human life history and transition between its phases. Eur J Endocrinol. 2009, 160: 135-141.CrossRefPubMed
30.
go back to reference Cutler GB, Glenn M, Bush M, Hodgen GD, Graham CE, Loriaux DL: Adrenarche: a survey of rodents, domestic animals, and primates. Endocrinology. 1978, 103: 2112-2118. 10.1210/endo-103-6-2112.CrossRefPubMed Cutler GB, Glenn M, Bush M, Hodgen GD, Graham CE, Loriaux DL: Adrenarche: a survey of rodents, domestic animals, and primates. Endocrinology. 1978, 103: 2112-2118. 10.1210/endo-103-6-2112.CrossRefPubMed
31.
go back to reference Stearns SC: Life history evolution: successes, limitations, and prospects. Naturwissenschaften. 2000, 87: 476-486. 10.1007/s001140050763.CrossRefPubMed Stearns SC: Life history evolution: successes, limitations, and prospects. Naturwissenschaften. 2000, 87: 476-486. 10.1007/s001140050763.CrossRefPubMed
32.
go back to reference Parent AS, Teilmann G, Juul A, Skakkebaek NE, Toppari J, Bourguignon JP: The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr Rev. 2003, 24: 668-693. 10.1210/er.2002-0019.CrossRefPubMed Parent AS, Teilmann G, Juul A, Skakkebaek NE, Toppari J, Bourguignon JP: The timing of normal puberty and the age limits of sexual precocity: variations around the world, secular trends, and changes after migration. Endocr Rev. 2003, 24: 668-693. 10.1210/er.2002-0019.CrossRefPubMed
33.
go back to reference Ellis BJ: Timing of pubertal maturation in girls: an integrated life history approach. Psychol Bull. 2004, 130 (6): 920-958.CrossRefPubMed Ellis BJ: Timing of pubertal maturation in girls: an integrated life history approach. Psychol Bull. 2004, 130 (6): 920-958.CrossRefPubMed
34.
go back to reference Ong KK, Elks CE, Li S, Zhao JH, Luan J, Andersen LB, Bingham SA, Brage S, Smith GD, Ekelund U, Gillson CJ, Glaser B, Golding J, Hardy R, Khaw KT, Kuh D, Luben R, Marcus M, McGeehin MA, Ness AR, Northstone K, Ring SM, Rubin C, Sims MA, Song K, Strachan DP, Vollenweider P, Waeber G, Waterworth DM, Wong A, et al: Genetic variation in LIN28B is associated with the timing of puberty. Nat Genet. 2009, 41: 729-733. 10.1038/ng.382.CrossRefPubMedPubMedCentral Ong KK, Elks CE, Li S, Zhao JH, Luan J, Andersen LB, Bingham SA, Brage S, Smith GD, Ekelund U, Gillson CJ, Glaser B, Golding J, Hardy R, Khaw KT, Kuh D, Luben R, Marcus M, McGeehin MA, Ness AR, Northstone K, Ring SM, Rubin C, Sims MA, Song K, Strachan DP, Vollenweider P, Waeber G, Waterworth DM, Wong A, et al: Genetic variation in LIN28B is associated with the timing of puberty. Nat Genet. 2009, 41: 729-733. 10.1038/ng.382.CrossRefPubMedPubMedCentral
35.
go back to reference Templeton A: Has human evolution stopped?. Rambam Maimonides Medical Journal. 2010, 1:e0006: 1-10. Templeton A: Has human evolution stopped?. Rambam Maimonides Medical Journal. 2010, 1:e0006: 1-10.
36.
go back to reference Gluckman PD, Hanson MA: Evolution, development and timing of puberty. Trends Endocrinol Metab. 2006, 17: 7-12. 10.1016/j.tem.2005.11.006.CrossRefPubMed Gluckman PD, Hanson MA: Evolution, development and timing of puberty. Trends Endocrinol Metab. 2006, 17: 7-12. 10.1016/j.tem.2005.11.006.CrossRefPubMed
37.
go back to reference Hochberg Z, Gawlik A, Walker RS: Evolutionary fitness as a function of pubertal age in 22 subsistence-based traditional societies. Int J Pediatr Endocrinol. 2011, 2011: 2-10.1186/1687-9856-2011-2.CrossRefPubMedPubMedCentral Hochberg Z, Gawlik A, Walker RS: Evolutionary fitness as a function of pubertal age in 22 subsistence-based traditional societies. Int J Pediatr Endocrinol. 2011, 2011: 2-10.1186/1687-9856-2011-2.CrossRefPubMedPubMedCentral
38.
go back to reference Migliano AB, Vinicius L, Lahr MM: Life history trade-offs explain the evolution of human pygmies. Proc Natl Acad Sci USA. 2007, 104: 20216-20219. 10.1073/pnas.0708024105.CrossRefPubMedPubMedCentral Migliano AB, Vinicius L, Lahr MM: Life history trade-offs explain the evolution of human pygmies. Proc Natl Acad Sci USA. 2007, 104: 20216-20219. 10.1073/pnas.0708024105.CrossRefPubMedPubMedCentral
39.
go back to reference Cooper C, Kuh D, Egger P, Wadsworth M, Barker D: Childhood growth and age at menarche. Br J Obstet Gynaecol. 1996, 103: 814-817. 10.1111/j.1471-0528.1996.tb09879.x.CrossRefPubMed Cooper C, Kuh D, Egger P, Wadsworth M, Barker D: Childhood growth and age at menarche. Br J Obstet Gynaecol. 1996, 103: 814-817. 10.1111/j.1471-0528.1996.tb09879.x.CrossRefPubMed
40.
go back to reference Ong KK, Potau N, Petry CJ, Jones R, Ness AR, Honour JW, de Zegher F, Ibanez L, Dunger DB: Opposing influences of prenatal and postnatal weight gain on adrenarche in normal boys and girls. J Clin Endocrinol Metab. 2004, 89: 2647-2651. 10.1210/jc.2003-031848.CrossRefPubMed Ong KK, Potau N, Petry CJ, Jones R, Ness AR, Honour JW, de Zegher F, Ibanez L, Dunger DB: Opposing influences of prenatal and postnatal weight gain on adrenarche in normal boys and girls. J Clin Endocrinol Metab. 2004, 89: 2647-2651. 10.1210/jc.2003-031848.CrossRefPubMed
41.
go back to reference Proos LA, Hofvander Y, Tuvemo T: Menarcheal age and growth pattern of Indian girls adopted in Sweden. I. Menarcheal age. Acta Paediatr Scand. 1991, 80: 852-858. 10.1111/j.1651-2227.1991.tb11960.x.CrossRefPubMed Proos LA, Hofvander Y, Tuvemo T: Menarcheal age and growth pattern of Indian girls adopted in Sweden. I. Menarcheal age. Acta Paediatr Scand. 1991, 80: 852-858. 10.1111/j.1651-2227.1991.tb11960.x.CrossRefPubMed
42.
go back to reference Krstevska-Konstantinova M, Charlier C, Craen M, Du Caju M, Heinrichs C, de Beaufort C, Plomteux G, Bourguignon JP: Sexual precocity after immigration from developing countries to Belgium: evidence of previous exposure to organochlorine pesticides. Hum Reprod. 2001, 16: 1020-1026. 10.1093/humrep/16.5.1020.CrossRefPubMed Krstevska-Konstantinova M, Charlier C, Craen M, Du Caju M, Heinrichs C, de Beaufort C, Plomteux G, Bourguignon JP: Sexual precocity after immigration from developing countries to Belgium: evidence of previous exposure to organochlorine pesticides. Hum Reprod. 2001, 16: 1020-1026. 10.1093/humrep/16.5.1020.CrossRefPubMed
43.
go back to reference Deng F, Tao FB, Liu DY, Xu YY, Hao JH, Sun Y, Su PY: Effects of growth environments and two environmental endocrine disruptors on children with idiopathic precocious puberty. Eur J Endocrinol. 2012, 166: 803-809. 10.1530/EJE-11-0876.CrossRefPubMed Deng F, Tao FB, Liu DY, Xu YY, Hao JH, Sun Y, Su PY: Effects of growth environments and two environmental endocrine disruptors on children with idiopathic precocious puberty. Eur J Endocrinol. 2012, 166: 803-809. 10.1530/EJE-11-0876.CrossRefPubMed
44.
go back to reference Simondon KB, Simondon F: Mothers prolong breastfeeding of undernourished children in rural Senegal. Int J Epidemiol. 1998, 27: 490-494. 10.1093/ije/27.3.490.CrossRefPubMed Simondon KB, Simondon F: Mothers prolong breastfeeding of undernourished children in rural Senegal. Int J Epidemiol. 1998, 27: 490-494. 10.1093/ije/27.3.490.CrossRefPubMed
45.
go back to reference Bowlby J: Attachment theory and its therapeutic implications. Adoles Psychiatry. 1978, 6: 5-33. Bowlby J: Attachment theory and its therapeutic implications. Adoles Psychiatry. 1978, 6: 5-33.
46.
go back to reference Bowlby J: The making and breaking of affectional bonds. I. Aetiology and psychopathology in the light of attachment theory. An expanded version of the Fiftieth Maudsley Lecture, delivered before the Royal College of Psychiatrists, 19 November 1976. Br J Psychiatry. 1977, 130: 201-210. 10.1192/bjp.130.3.201.CrossRefPubMed Bowlby J: The making and breaking of affectional bonds. I. Aetiology and psychopathology in the light of attachment theory. An expanded version of the Fiftieth Maudsley Lecture, delivered before the Royal College of Psychiatrists, 19 November 1976. Br J Psychiatry. 1977, 130: 201-210. 10.1192/bjp.130.3.201.CrossRefPubMed
47.
go back to reference James J, Ellis BJ, Schlomer GL, Garber J: Sex-specific pathways to early puberty, sexual debut, and sexual risk taking: tests of an integrated evolutionary-developmental model. Dev Psychol. 2012, 48: 687-702.CrossRefPubMed James J, Ellis BJ, Schlomer GL, Garber J: Sex-specific pathways to early puberty, sexual debut, and sexual risk taking: tests of an integrated evolutionary-developmental model. Dev Psychol. 2012, 48: 687-702.CrossRefPubMed
48.
go back to reference Belsky J, Fearon RM: Early attachment security, subsequent maternal sensitivity, and later child development: does continuity in development depend upon continuity of caregiving?. Attach Hum Dev. 2002, 4: 361-387. 10.1080/14616730210167267.CrossRefPubMed Belsky J, Fearon RM: Early attachment security, subsequent maternal sensitivity, and later child development: does continuity in development depend upon continuity of caregiving?. Attach Hum Dev. 2002, 4: 361-387. 10.1080/14616730210167267.CrossRefPubMed
49.
go back to reference Belsky J, Steinberg L, Houts RM, Halpern-Felsher BL: The development of reproductive strategy in females: early maternal harshness --> earlier menarche --> increased sexual risk taking. Dev Psychol. 2010, 46: 120-128.CrossRefPubMed Belsky J, Steinberg L, Houts RM, Halpern-Felsher BL: The development of reproductive strategy in females: early maternal harshness --> earlier menarche --> increased sexual risk taking. Dev Psychol. 2010, 46: 120-128.CrossRefPubMed
50.
go back to reference Belsky J, Steinberg LD, Houts RM, Friedman SL, DeHart G, Cauffman E, Roisman GI, Halpern-Felsher BL, Susman E: Family rearing antecedents of pubertal timing. Child Dev. 2007, 78: 1302-1321. 10.1111/j.1467-8624.2007.01067.x.CrossRefPubMed Belsky J, Steinberg LD, Houts RM, Friedman SL, DeHart G, Cauffman E, Roisman GI, Halpern-Felsher BL, Susman E: Family rearing antecedents of pubertal timing. Child Dev. 2007, 78: 1302-1321. 10.1111/j.1467-8624.2007.01067.x.CrossRefPubMed
51.
go back to reference Belsky J: The development of human reproductive strategies: progress and prospects. Curr Dir Psychol Sci. Belsky J: The development of human reproductive strategies: progress and prospects. Curr Dir Psychol Sci.
52.
go back to reference Ellis BJ, Essex MJ: Family environments, adrenarche, and sexual maturation: a longitudinal test of a life history model. Child Dev. 2007, 78: 1799-1817. 10.1111/j.1467-8624.2007.01092.x.CrossRefPubMed Ellis BJ, Essex MJ: Family environments, adrenarche, and sexual maturation: a longitudinal test of a life history model. Child Dev. 2007, 78: 1799-1817. 10.1111/j.1467-8624.2007.01092.x.CrossRefPubMed
53.
go back to reference Belsky J, Houts RM, Fearon RM: Infant attachment security and the timing of puberty: testing an evolutionary hypothesis. Psychol Sci. 2010, 21: 1195-1201. 10.1177/0956797610379867.CrossRefPubMed Belsky J, Houts RM, Fearon RM: Infant attachment security and the timing of puberty: testing an evolutionary hypothesis. Psychol Sci. 2010, 21: 1195-1201. 10.1177/0956797610379867.CrossRefPubMed
54.
go back to reference Tither JM, Ellis BJ: Impact of fathers on daughters' age at menarche: a genetically and environmentally controlled sibling study. Dev Psychol. 2008, 44: 1409-1420.CrossRefPubMed Tither JM, Ellis BJ: Impact of fathers on daughters' age at menarche: a genetically and environmentally controlled sibling study. Dev Psychol. 2008, 44: 1409-1420.CrossRefPubMed
55.
go back to reference Pesonen AK, Raikkonen K, Heinonen K, Kajantie E, Forsen T, Eriksson JG: Reproductive traits following a parent-child separation trauma during childhood: a natural experiment during World War II. Am J Hum Biol. 2008, 20: 345-351. 10.1002/ajhb.20735.CrossRefPubMed Pesonen AK, Raikkonen K, Heinonen K, Kajantie E, Forsen T, Eriksson JG: Reproductive traits following a parent-child separation trauma during childhood: a natural experiment during World War II. Am J Hum Biol. 2008, 20: 345-351. 10.1002/ajhb.20735.CrossRefPubMed
56.
go back to reference Cameron NM, Champagne FA, Parent C, Fish EW, Ozaki-Kuroda K, Meaney MJ: The programming of individual differences in defensive responses and reproductive strategies in the rat through variations in maternal care. Neurosci Biobehav Rev. 2005, 29: 843-865. 10.1016/j.neubiorev.2005.03.022.CrossRefPubMed Cameron NM, Champagne FA, Parent C, Fish EW, Ozaki-Kuroda K, Meaney MJ: The programming of individual differences in defensive responses and reproductive strategies in the rat through variations in maternal care. Neurosci Biobehav Rev. 2005, 29: 843-865. 10.1016/j.neubiorev.2005.03.022.CrossRefPubMed
57.
go back to reference Belsky J: Patterns of attachment mating and parenting: an evolutionary interpretation. Hum Nat. 1997, 8: 361-381. 10.1007/BF02913039.CrossRefPubMed Belsky J: Patterns of attachment mating and parenting: an evolutionary interpretation. Hum Nat. 1997, 8: 361-381. 10.1007/BF02913039.CrossRefPubMed
58.
go back to reference Belsky J: Conditional and alternative reproductive strategies: individual differences in susceptibility to rearing experience. Genetic Influences on Human Fertility and Sexuality: Theoretical and Empirical Contributions from the Biological and Behavioral Sciences. Edited by: Rodgers J, Rowe, D, Miller, W. 2000, Boston: Kluwer, 127-146.CrossRef Belsky J: Conditional and alternative reproductive strategies: individual differences in susceptibility to rearing experience. Genetic Influences on Human Fertility and Sexuality: Theoretical and Empirical Contributions from the Biological and Behavioral Sciences. Edited by: Rodgers J, Rowe, D, Miller, W. 2000, Boston: Kluwer, 127-146.CrossRef
59.
go back to reference Belsky J, Pluess M: Beyond diathesis stress: differential susceptibility to environmental influences. Psychol Bull. 2009, 135: 885-908.CrossRefPubMed Belsky J, Pluess M: Beyond diathesis stress: differential susceptibility to environmental influences. Psychol Bull. 2009, 135: 885-908.CrossRefPubMed
60.
go back to reference Belsky J, Jonassaint C, Pluess M, Stanton M, Brummett B, Williams R: Vulnerability genes or plasticity genes?. Mol Psychiatry. 2009, 14: 746-754. 10.1038/mp.2009.44.CrossRefPubMedPubMedCentral Belsky J, Jonassaint C, Pluess M, Stanton M, Brummett B, Williams R: Vulnerability genes or plasticity genes?. Mol Psychiatry. 2009, 14: 746-754. 10.1038/mp.2009.44.CrossRefPubMedPubMedCentral
61.
go back to reference Boyce WT, Ellis BJ: Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity. Dev Psychopathol. 2005, 17: 271-301.CrossRefPubMed Boyce WT, Ellis BJ: Biological sensitivity to context: I. An evolutionary-developmental theory of the origins and functions of stress reactivity. Dev Psychopathol. 2005, 17: 271-301.CrossRefPubMed
62.
go back to reference Ellis BJ, Boyce WT: Differential susceptibility to the environment: toward an understanding of sensitivity to developmental experiences and context. Dev Psychopathol. 2011, 23: 1-5. 10.1017/S095457941000060X.CrossRefPubMed Ellis BJ, Boyce WT: Differential susceptibility to the environment: toward an understanding of sensitivity to developmental experiences and context. Dev Psychopathol. 2011, 23: 1-5. 10.1017/S095457941000060X.CrossRefPubMed
63.
go back to reference Ellis BJ, Shirtcliff EA, Boyce WT, Deardorff J, Essex MJ: Quality of early family relationships and the timing and tempo of puberty: effects depend on biological sensitivity to context. Dev Psychopathol. 2011, 23: 85-99. 10.1017/S0954579410000660.CrossRefPubMedPubMedCentral Ellis BJ, Shirtcliff EA, Boyce WT, Deardorff J, Essex MJ: Quality of early family relationships and the timing and tempo of puberty: effects depend on biological sensitivity to context. Dev Psychopathol. 2011, 23: 85-99. 10.1017/S0954579410000660.CrossRefPubMedPubMedCentral
64.
go back to reference Manuck SB, Craig AE, Flory JD, Halder I, Ferrellc RE: Reported early family environment covaries with menarcheal age as a function of polymorphic variation in estrogen receptor-α (ESR). Dev Psychopathol. 2011, 23: 69-83. 10.1017/S0954579410000659.CrossRefPubMedPubMedCentral Manuck SB, Craig AE, Flory JD, Halder I, Ferrellc RE: Reported early family environment covaries with menarcheal age as a function of polymorphic variation in estrogen receptor-α (ESR). Dev Psychopathol. 2011, 23: 69-83. 10.1017/S0954579410000659.CrossRefPubMedPubMedCentral
65.
go back to reference Westendorp RG, Kirkwood TB: Human longevity at the cost of reproductive success. Nature. 1998, 396: 743-746. 10.1038/25519.CrossRefPubMed Westendorp RG, Kirkwood TB: Human longevity at the cost of reproductive success. Nature. 1998, 396: 743-746. 10.1038/25519.CrossRefPubMed
66.
go back to reference Pembrey ME, Bygren LO, Kaati G, Edvinsson S, Northstone K, Sjostrom M, Golding J: Sex-specific, male-line transgenerational responses in humans. Eur J Hum Genet. 2006, 14: 159-166. 10.1038/sj.ejhg.5201538.CrossRefPubMed Pembrey ME, Bygren LO, Kaati G, Edvinsson S, Northstone K, Sjostrom M, Golding J: Sex-specific, male-line transgenerational responses in humans. Eur J Hum Genet. 2006, 14: 159-166. 10.1038/sj.ejhg.5201538.CrossRefPubMed
67.
go back to reference Copeland W, Shanahan L, Miller S, Costello EJ, Angold A, Maughan B: Outcomes of early pubertal timing in young women: a prospective population-based study. Am J Psychiatry. 2010, 167: 1218-1225. 10.1176/appi.ajp.2010.09081190.CrossRefPubMedPubMedCentral Copeland W, Shanahan L, Miller S, Costello EJ, Angold A, Maughan B: Outcomes of early pubertal timing in young women: a prospective population-based study. Am J Psychiatry. 2010, 167: 1218-1225. 10.1176/appi.ajp.2010.09081190.CrossRefPubMedPubMedCentral
68.
go back to reference Celio M, Karnik NS, Steiner H: Early maturation as a risk factor for aggression and delinquency in adolescent girls: a review. Int J Clin Pract. 2006, 60: 1254-1262. 10.1111/j.1742-1241.2006.00972.x.CrossRefPubMed Celio M, Karnik NS, Steiner H: Early maturation as a risk factor for aggression and delinquency in adolescent girls: a review. Int J Clin Pract. 2006, 60: 1254-1262. 10.1111/j.1742-1241.2006.00972.x.CrossRefPubMed
69.
go back to reference Hochberg Z, Feil R, Constancia M, Fraga M, Junien C, Carel JC, Boileau P, Le Bouc Y, Deal CL, Lillycrop K, Scharfmann R, Sheppard A, Skinner M, Szyf M, Waterland RA, Waxman DJ, Whitelaw E, Ong K, Albertsson-Wikland K: Child health, developmental plasticity, and epigenetic programming. Endocr Rev. 2011, 32: 159-224. 10.1210/er.2009-0039.CrossRefPubMed Hochberg Z, Feil R, Constancia M, Fraga M, Junien C, Carel JC, Boileau P, Le Bouc Y, Deal CL, Lillycrop K, Scharfmann R, Sheppard A, Skinner M, Szyf M, Waterland RA, Waxman DJ, Whitelaw E, Ong K, Albertsson-Wikland K: Child health, developmental plasticity, and epigenetic programming. Endocr Rev. 2011, 32: 159-224. 10.1210/er.2009-0039.CrossRefPubMed
Metadata
Title
Evo-devo of human adolescence: beyond disease models of early puberty
Authors
Ze'ev Hochberg
Jay Belsky
Publication date
01-12-2013
Publisher
BioMed Central
Published in
BMC Medicine / Issue 1/2013
Electronic ISSN: 1741-7015
DOI
https://doi.org/10.1186/1741-7015-11-113

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