Adrenarche in bonobos (Pan paniscus): Evidence from ontogenetic changes in urinary dehydroepiandrosterone-sulfate levels

Journal of Endocrinology

Volumn 214, Issue 1, 2012, Pages 55-65

  Behringer, Verena ^a   Hohmann, Gottfried ^a   Stevens, Jeroen M G ^b   Weltring, Anja ^a   Deschner, Tobias ^a  

^a MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^b CENTRE FOR RESEARCH AND CONSERVATION   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

PRASTERONE SULFATE;

ADRENARCHE; ANIMAL EXPERIMENT; ARTICLE; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HORMONE DETERMINATION; MALE; NONHUMAN; ONTOGENE; ONTOGENY; PAN PANISCUS; PRIORITY JOURNAL; URINALYSIS;

ADRENARCHE; AGE FACTORS; ANIMALS; BIOLOGICAL EVOLUTION; DEHYDROEPIANDROSTERONE SULFATE; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; MALE; PAN PANISCUS; PAN TROGLODYTES; SPECIES SPECIFICITY;

EID: 84864323574     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-12-0103     Document Type: Article

References (65)

1. Anestis SF, Blanco M & Bribiescas RG 2009 Changes in urinary dehydroepiandrosterone sulfate (DHEA-S) levels with age in juvenile captive chimpanzees (Pan troglodytes) (abstract). American Journal of Physical Anthropology, 138, 78.
2. Bahr NI, Palme R, Möhle U, Hodges JK & Heistermann M 2000 Comparative aspects of the metabolism and excretion of cortisol in three individual non-human primates. General and Comparative Endocrinology 117 427-438
3. Barrett-Connor E, Khaw KT & Yen SSC 1986 A prospective study of dehydroepiandrosterone sulfate, mortality, and cardiovascular disease. New England Journal of Medicine 315 1519-1524
4. Bech K, Tygstrup I & Nerup I 1969 The involution of the fetal adrenal cortex. A light microscopic study. Acta Pathologica et Microbiologica Scandinavica 76 391-400
5. Bernstein RM, Sterner KN & Wildman DE 2012 Adrenal androgen production in catarrhine primates and the evolution of adrenarche. American Journal of Physical Anthropology 147 389-400
6. Campbell B 2006 Adrenarche and the evolution of human life history. American Journal of Human Biology 18 569-589
7. Castracane VD, Cutler GB Jr & Loriaux DL 1981 Pubertal endocrinology of the baboon: adrenarche. American Journal of Physiology 241 E305-E309.
8. Collins DC, Nadler RD & Preedy JRK 1981 Adrenarche in the great apes (abstract). American Journal of Primatology 1 344.
9. Conley AJ, Pattison JC & Bird IM 2004 Variations in adrenal androgen production among (nonhuman) primates. Seminars in Reproductive Medicine 22 311-326
10. Conley AJ, Plant TM, Abbott DH, Moeller BC & Stanley SD 2011 Adrenal androgen concentrations increase during infancy in male rhesus macaques (Macaca mulatta). American Journal of Physiology. Endocrinology and Metabolism 301 E1229-E1235
11. Conley AJ, Bernstein RM & Nguyen AD 2012 Adrenarche in non-human primates: the evidence for it and the need to re-define it. Journal of Endocrinology. In press
12. Copeland KC, Eichberg JW, Parker CR Jr & Bartke A 1985 Puberty in the chimpanzee: somatomedin-C and its relationship to somatic growth and steroid hormone concentrations. Journal of Clinical Endocrinology and Metabolism 60 1154-1160
13. Crawford BA, Harewood WJ & Handelsman DJ 1997 Growth and hormone characteristics of pubertal developmental in the hamadryas baboon. Journal of Medical Primatology 26 153-163
14. Cutler GB Jr, Glenn M, Bush M, Hodgen GD, Graham CE & Loriaux DL 1978 Adrenarche: a survey of rodents, domestic animals, and primates. Endocrinology 103 2112-2118
15. Dhom G 1973 The prepuberal and puberal growth of the adrenal (adrenarche). Beitraege zur Pathologie 150 357-377
16. Ducharme J-R, Forest MG, de Peretti E, Sempé M, Collu R & Bertrand J 1976 Plasma adrenal and gonadal sex steroids in human pubertal development. Journal of Clinical Endocrinology and Metabolism 42 468-476
17. Fontenote MB, Stavisky RC, Seraphin SB & Whitten PL 2001 Aging primates: patterns of dehydroepiandrosterone sulfate excretion in chimpanzees (Pan troglodytes). (abstract). In Association of the American Society of Primatologists Twenty-fourth Meeting. Savannah, Georgia.
18. Furuichi T 2011 Female contributions to the peaceful nature of bonobo society. Evolutionary Anthropology: Issues, News, and Reviews 20 131-142
19. Furuichi T, Idani G, Ihobe H, Hashimoto C, Tashiro Y, Sakamaki T, Mulavwa MN, Yangozene K & Kuroda S 2012 Long-term studies on wild bonobos at Wamba, Luo Scientific Reserve, D. R. Congo: towards the understanding of female life history in a male-philopatric species. In Long-Term Field Studies of Primates, pp 413-433. Eds PM Kappeler & DPWatts. Berlin Heidelberg: Springer-Verlag (doi: 10.1007/978-3-642-22514-7_18).
20. Gupta D 1970 A longitudinal study of steroid excretion patterns in children during adolescent growth. Steroidologia 1 267-294.
21. Haning RV, Chabotc JM, Flood CA, Hackett R & Longcope C 1989 Metabolic clearance rate (MCR) of dehydroepiandrosterone sulfate (DS), its metabolism to dehydroepiandrosterone, androstenedione, testosterone, and dihydrotestosterone, and the effect of increased plasma DS concentration on DS MCR in normal women. Journal of Clinical Endocrinology and Metabolism 69 1047-1052
22. Hare B, Wobber V & Wrangham R 2012 The self-domestication hypothesis: evolution of bonobo psychology is due to selction against aggression. Animal Behaviour 83 573-585
23. Hauser B, Deschner T & Boesch C 2008 Development of a liquid chromatography-tandem mass spectrometry method for the determination of 23 endogenous steroids in small quantities of primate urine. Journal of Chromatography B 862 100-112
24. Havelock JC, Auchus RJ & Rainey WE 2004 The rise in adrenal androgen biosynthesis: adrenarche. Seminars in Reproductive Medicine 22 337-347
25. Ibáñez L, Dimartino-Nadir J, Potau N & Saenger P 2000 Premature adrenarche - normal variant or forerunner of adult disease? Endocrine Reviews 21 671-696
26. Ilondo MM, Vanderschueren-Lodeweyckx M, Vlietinck R, Pizarro M, Malvaux P, Eggermont E & Eeckels R 1982 Androgens in children and adolescents. Hormone Research 16 78-95
27. Kelnar CJH & Brook CGD 1983 A mixed longitudinal study of adrenal steroid excretion in childhood and the mechanism of adrenarche. Clinical Endocrinology 19 117-129
28. Kemnitz JW, Roecker EB, Haffa ALM, Pinheiro J, Kurzmann I, Ramsey JJ & MacEwn EG 2000 Serum dehydroepiandrosterone sulfate concentrations across the life span of laboratory-housed rhesus monkeys. Journal of Medical Primatology 29 330-337
29. Korth-Schutz S, Levine LS & New MI 1976 Serum androgens in normal prepubertal and pubertal children and in children with precocious adrenarche. Journal of Clinical Endocrinology and Metabolism 42 117-124
30. Lane MA, Ingram DK, Ball SS & Roth GS 1997 Dehydroepiandrosterone sulfate: a biomarker of primate aging slowed by calorie restriction. Journal of Clinical Endocrinology and Metabolism 82 2093-2096
31. Lasley BL & Kirkpatrick JF 1991 Monitoring ovarian function in captive and free-ranging wildlife by means of urinary and fecal steroids. Journal of Zoo and Wildlife Medicine 22 23-31.
32. Lieberman DE, Carlo J, Ponce de León M & Zollikofer CPE 2007 A geometric morphometric analysis of heterochrony n the cranium of chimpanzees and bonobos. Journal of Human Evolution 52 647-662
33. Martin DD, Schweizer R, Schwarze CP, Elmlinger MW, Ranke MB &Binder G 2004 The early dehydroepiandrosterone sulfate rise of adrenarche and the delay of pubarche indicate primary ovarian failure in Turner syndrome. Journal of Clinical Endocrinology and Metabolism 89 1164-1168
34. Meusy-Dessolle N & Dang DC 1985 Plasma concentrations of testosterone, dihydrotestosterone, D4-androstenedione, dehydroepiandrosterone and oestradiol-17b in the crabeating monkey (Macaca fascicularis) from birth to adulthood. Journal of Reproduction and Fertility 74 347-359
35. Nadler RD, Wallis J, Roth-Meyer C, Cooper RW & Baulieu E-E 1987 Hormones and behavior of prepubertal and peripubertal chimpanzees. Hormones & Behavior 21 118-131
36. Nguyen AD & Conley AJ 2008 Adrenal androgens in humans and nonhuman primates: production, zonation and regulation. In Disorders of the Human Adrenal Cortex, pp 33-54. Eds CE Flück & WL Miller. Basel: Karger
37. Oberfield SE &White PC 2009 Adrenarche. Reviews in Endocrine and Metabolic Disorders 10 1-2
38. Orentreich N, Brind JL, Rizer RL & Vogelman JH 1984 Age changes and sex differences in serum dehydroepiandrosterone sulfate concentrations throughout adulthood. Journal of Clinical Endocrinology and Metabolism 59 551-555
39. Palmert MR, Hayden DL, Mansfield MJ, Crigler JF Jr, Crowley WF Jr, Chandler DW & Boeppel PA 2001 The longitudinal study of adrenal maturation during gonadal suppression: evidence that adrenarche is a gradual process. Journal of Clinical Endocrinology and Metabolism 86 4536-4542
40. Parker CR Jr 1999 Dehydroepiandrosterone and dehydroepiandrosterone sulfate production in the human adrenal during development and aging. Steroids 64 640-647
41. Pattison JC, Abbott DH, Saltzmann W, Nguyen AD, Henderson G, Jing H, Pryce CR, Allen AJ, Conley AJ & Bird IM 2005 Male marmoset monkeys express an adrenal fetal zone at birth, but not a zona reticularis in adulthood. Endocrinology 146 365-374
42. Pattison JC, Abbott DH, Saltzmann W, Conley AJ & Bird IM 2009 Plasticity of the zona reticularis in the adult marmoset adrenal cortex: voyages of discovery in the New World. Journal of Endocrinology 203 313-326
43. de Peretti E & Forest MG 1978 Pattern of plasma dehydroepiandrosterone sulfate levels in humans from birth to adulthood: evidence for testicular production. Journal of Clinical Endocrinology and Metabolism 47 572-577
44. Pintor C, Loche S, Faedda A, Fanni V, Nurchi AM & Corda R 1984 Adrenal androgens in obese boys before and after weight loss. Hormone and Metabolic Research 16 544-548
45. Reinehr T, de Sousa G, Roth CL & Andler W 2005 Androgens before and after weight loss in obese children. Journal of Clinical Endocrinology and Metabolism 90 5588-5595
46. Remer T & Manz F 1999 Role of nutritional status in the regulation of adrenarche. Journal of Clinical Endocrinology and Metabolism 84 3936-3944
47. Remer T, Pietrzik K & Manz F 1994 Measurement of urinary androgen sulfates without previous hydrolysis: a tool to investigate adrenarche. Validation of a commercial radioimmunoassay for dehydroepiandrosterone sulfate. Steroids 59 10-15
48. Remer T, Boye KR, Hartmann MF & Wudy SA 2005 Urinary markers of adrenarche: reference values in healthy subjects, aged 3-18 years. Journal of Clinical Endocrinology and Metabolism 90 2015-2021
49. Rosenfeld R, Hellman L, Roffwarg H, Weitzman ED, Fukushima DK & Gallagher T 1971 Dehydroisoandrosterone is secreted episodically and synchronously with cortisol by normal man. Journal of Clinical Endocrinology and Metabolism 33 87-92
50. Rosenfield RL & Eberlein WR 1969 Plasma 17-ketosteroid levels during adolescence. Journal of Pediatrics 74 932-936
51. Salvini S, Stampfer MJ, Barbieri RL & Hennekens CH 1992 Effects of age, smoking and vitamins on plasma DHEA-S levels: a cross sectional study in men. Journal of Clinical Endocrinology and Metabolism 74 139-143
52. Seraphin SB, Whitten PL & Reynolds V 2008 The influence of age on fecal steroid hormone levels in male Budongo Forest chimpanzees (Pan troglodytes schweinfurthii). American Journal of Primatology 70 661-669
53. Shea BT 1983 Paedomorphosis and neoteny in the pygmy chimpanzee. Science 22 521-522
54. Sheriff MJ, Dantzer B, Delehanty B, Palme R & Boonstra R 2011 Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 166 869-887
55. Sizonenko PC, Paunier L & Carmignac D 1976 Hormonal changes during puberty. Hormone Research 7 228-302
56. 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. Journal of Clinical Endocrinology and Metabolism 51 548-556
57. Smail PJ, Faiman C, Hobson WC, Fuller GB & Winter JSD 1982 Further studies of adrenarche in nonhuman primates. Endocrinology 111 844-848
58. Šulcová J, Hill M, Hampl R & Stárka L 1997 Age and sex related differences in serum levels of unconjugated dehydroepiandrosterone and its sulphate in normal subjects. Journal of Endocrinology 154 57-62
59. Tanner JM & Gupta D 1968 A longitudinal study of the urinary excretion of individual steroids in children from 8 to 12 years old. Journal of Endocrinology 41 139-156
60. Weltring A, Schaebs FS, Perry SE & Deschner T 2012 Simultaneous measurement of endogenous steroid hormones and their metabolites with LC-MS/MS in faeces of a New World primate species, Cebus capucinus. Physiology & Behavior 105 510-521
61. Wiermann ME, Beardsworth DE, Crawford JD, Crigler JF Jr, Mansfield MJ, Bode HH, Boepple PA, Kushner DC & Crowley WF Jr 1986 Adrenarche and skeletal maturation during luteinizing hormone releasing hormone analogue suppression of gonadarche. Journal of Clinical Investigation 77 121-126
62. Winter JSD, Faiman C, Hobson WC & Reyes FI 1980 The endocrine basis of sexual development in the chimpanzee. Journal of Reproduction and Fertility. Supplement 28 131-138.
63. Wobber V, Wrangham R & Hare B 2010 Application of the heterochrony framework to the study of behavior and cognition. Communicative & Integrative Biology 3 337-339
64. Zhao Z-Y, Xie Y, Fu Y-R, Li Y-Y, Bogdan A & Touitou Y 2003 Circadian rhythm characteristics of serum cortisol and dehydroepiandrosterone sulfate in healthy Chinese men aged 30 to 60 years. A cross-sectional study. Steroids 68 133-138
65. Zihlman A 1996 Reconstructions reconsidered: chimpanzee models and human evolution. In Great Ape Societies, pp 293-304. Eds WC McGrew, LF Marchant & T Nishida. Cambridge: Cambridge University Press.