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

BMC Medicine

Jay Belsky¹  Ze'ev Hochberg² 

[1]Department of Psychological Science, Birkbeck University of London, Malet Street, London WC1B 3HE, UK

[2]Rappaport Family Faculty of Medicine, Technion - Israel Institute of Technology, Efron Street, Haifa 31096, Israel

关键词: youth;    puberty;    juvenility;    evolution;    adolescence;   

Others  :  857081
DOI  :  10.1186/1741-7015-11-113

 received in 2012-08-31, accepted in 2012-11-30,  发布年份 2013

【 摘 要 】

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.

【 授权许可】

   
2013 Hochberg and Belsky; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Muller GB: Evo-devo: extending the evolutionary synthesis. Nat Rev Genet 2007, 8:943-949.
• [2]Hochberg Z: Evo Devo of Child Growth: Treatize on Child Growth and Human Evolution. New York: Wiley; 2012.
• [3]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.
• [4]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.
• [5]Smith BH, Tompkins RL: Toward a life history of the hominidae. Annu Rev Anthropol 1995, 24:257-279.
• [6]Sisk CL, Foster DL: The neural basis of puberty and adolescence. Nat Neurosci 2004, 7:1040-1047.
• [7]Bogin B: Evolutionary perspective on human growth. Annu Rev Anthropol 1999, 28:109-153.
• [8]Tardieu C: Short adolescence in early hominids: infantile and adolescent growth of the human femur. Am J Phys Anthropol 1998, 107:163-178.
• [9]Howell N: Life Histories of the Dobe !Kung. Berkley: University of California Press; 2010.
• [10]Klein KO, Baron J, Colli MJ, McDonnell DP, Cutler GB Jr: Estrogen levels in childhood determined by an ultrasensitive recombinant cell bioassay. J Clin Invest 1994, 94:2475-2480.
• [11]Ankarberg Lindgren C: Testosterone and 17beta-oestradiol secretion in children and adolescents. Assay development, levels for comparison and clinical applications. In PhD Thesis. Goteborg University; 2005.
• [12]Mead M: Coming of Age in Samoa. New York: Perrenial Classics; 2001. Originally published in 1928 by Williams Morrow and Company
• [13]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 280-325
• [14]Wingfield JC, Jacobs J, Hillgarth N: Ecological constraints and the evolution of hormone-behavior interrelationships. Ann N Y Acad Sci 1997, 807:22-41.
• [15]Campbell B: Adrenarche and the evolution of human life history. Am J Hum Biol 2006, 18(5):569-589.
• [16]Hochberg Z: Juvenility in the context of life history theory. Arch Dis Child 2008, 93:534-539.
• [17]Del Giudice M: Sex, attachment, and the development of reproductive strategies. Behav Brain Sci 2009, 32:1-21. discussion 21-67
• [18]White S: The child's entry into the age of reason. In The five to seven year shift: the age of reason and responsibility. Edited by Sameroff A, Haith, MM. Chicago: University of Chicago Press; 1996:17-32.
• [19]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.
• [20]Belsky J, Steinberg L, Draper P: Childhood experience, interpersonal development, and reproductive strategy: and evolutionary theory of socialization. Child Dev 1991, 62:647-670.
• [21]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.
• [22]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.
• [23]Palmert MR, Hayden DL, Mansfield MJ, Crigler JF Jr, Crowley WF Jr, 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.
• [24]Kroboth PD, Salek FS, Pittenger AL, Fabian TJ, Frye RF: DHEA and DHEA-S: a review. J Clin Pharmacol 1999, 39:327-348.
• [25]Chen CC, Parker CR Jr: Adrenal androgens and the immune system. Semin Reprod Med 2004, 22:369-377.
• [26]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.
• [27]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.
• [28]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.
• [29]Hochberg Z: Evo-devo of child growth II: human life history and transition between its phases. Eur J Endocrinol 2009, 160:135-141.
• [30]Cutler GB Jr, Glenn M, Bush M, Hodgen GD, Graham CE, Loriaux DL: Adrenarche: a survey of rodents, domestic animals, and primates. Endocrinology 1978, 103:2112-2118.
• [31]Stearns SC: Life history evolution: successes, limitations, and prospects. Naturwissenschaften 2000, 87:476-486.
• [32]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.
• [33]Ellis BJ: Timing of pubertal maturation in girls: an integrated life history approach. Psychol Bull 2004, 130(6):920-958.
• [34]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.
• [35]Templeton A: Has human evolution stopped? Rambam Maimonides Medical Journal 2010, 1:e0006:1-10.
• [36]Gluckman PD, Hanson MA: Evolution, development and timing of puberty. Trends Endocrinol Metab 2006, 17:7-12.
• [37]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. BioMed Central Full Text
• [38]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.
• [39]Cooper C, Kuh D, Egger P, Wadsworth M, Barker D: Childhood growth and age at menarche. Br J Obstet Gynaecol 1996, 103:814-817.
• [40]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.
• [41]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.
• [42]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.
• [43]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.
• [44]Simondon KB, Simondon F: Mothers prolong breastfeeding of undernourished children in rural Senegal. Int J Epidemiol 1998, 27:490-494.
• [45]Bowlby J: Attachment theory and its therapeutic implications. Adoles Psychiatry 1978, 6:5-33.
• [46]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.
• [47]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.
• [48]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.
• [49]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.
• [50]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.
• [51]Belsky J: The development of human reproductive strategies: progress and prospects. Curr Dir Psychol Sci, in press.
• [52]Ellis BJ, Essex MJ: Family environments, adrenarche, and sexual maturation: a longitudinal test of a life history model. Child Dev 2007, 78:1799-1817.
• [53]Belsky J, Houts RM, Fearon RM: Infant attachment security and the timing of puberty: testing an evolutionary hypothesis. Psychol Sci 2010, 21:1195-1201.
• [54]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.
• [55]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.
• [56]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.
• [57]Belsky J: Patterns of attachment mating and parenting: an evolutionary interpretation. Hum Nat 1997, 8:361-381.
• [58]Belsky J: Conditional and alternative reproductive strategies: individual differences in susceptibility to rearing experience. In 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. Boston: Kluwer; 2000:127-146.
• [59]Belsky J, Pluess M: Beyond diathesis stress: differential susceptibility to environmental influences. Psychol Bull 2009, 135:885-908.
• [60]Belsky J, Jonassaint C, Pluess M, Stanton M, Brummett B, Williams R: Vulnerability genes or plasticity genes? Mol Psychiatry 2009, 14:746-754.
• [61]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.
• [62]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.
• [63]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.
• [64]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.
• [65]Westendorp RG, Kirkwood TB: Human longevity at the cost of reproductive success. Nature 1998, 396:743-746.
• [66]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.
• [67]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.
• [68]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.
• [69]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.