Abstract
We examined growth changes in concentrations of plasma insulin-like growth factor-1 (IGF-1) and testosterone, and somatometric parameters in two captive male agile gibbons from birth to about 4 years of age, to examine the evolution of growth patterns in primates. Plasma IGF-1 concentrations in agile gibbons generally increased with age with values ranging from 200 to 1,100 ng/ml. The growth profiles in plasma IGF-1 in the gibbons were similar to those reported for chimpanzees. The highest concentrations of plasma testosterone (230 and 296 ng/dl) were observed within the first 0.3 years from birth, then the concentrations rapidly decreased and fluctuated below 100 ng/dl. Continuously higher IGF-1 concentrations were observed after 2.6 and 3.5 years of age. The profiles of plasma testosterone in these gibbons also resembled those of other primates including humans. However, their plasma testosterone levels in both neonate and adult stages (60 ng/dl) were lower than those reported for macaques and chimpanzees of respective stages. The obtained growth profiles of plasma IGF-1 and testosterone suggest that the adolescent phase starts around 2.6 or 3.5 years of age in male agile gibbons. The growth trend in many morphological parameters including body weight showed a linear increase without a significant growth spurt at approximately the onset of puberty. Head length and first digit length had reached a plateau during the study period. Brachial index, which indicates the relative length of forearm to upper arm, significantly increased gradually through the growth period. This result indicates that forearm becomes relatively longer than the upper arm with growth, which may be an evolutionary adaptation for brachiation.
Similar content being viewed by others
References
Araki K, Samekawa T, Furukawa N, Mochizuki Y, Nishi H (1989) Breeding and hand-rearing the white-handed gibbon, Hylobates lar, and the concolor gibbon, hylobates concolor at Takarazuka Zool and Bot Gardens. (in Japanese) J Jpn Assoc Zool Gardens Aquariums 31:41–46
Ashley-Montagu MF (1960) A handbook of anthropometry. Thomas, Springfied
Bogin B (1999) Evolutionary perspective on human growth. Annu Rev Anthropol 28:109–153
Coelho J, A.M. (1985) Baboon dimorphism: growth in weight, length and adiposity from birth to 8 years of age. In: Nonhuman primate models for human growth and development. Liss, New York, pp 125–159
Copeland KC, Kuehl TJ, Castracane VD (1982) Pubertal endocrinology of the baboon: elevated somatomedin-C/insulin-like growth factor I at puberty. J Clin Endocrinol Metab 55:1198–1201
Copeland KC, Johnson DM, Kuehl TJ, Castracane VD (1984) Estrogen stimulates growth hormone and somatomedin-C in castrate and intact female baboons. J Clin Endocrinol Metab 58:698–703
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. J Clin Endocrinol Metab 60:1154–1985
Forest MG, Sizonenko PC, Cathiard AM, Bertrand J (1974) Hypophyso-gonadal function in humans during the first year of life. 1. Evidence for testicular activity in early infancy. J Clin Endocrinol Metab 53:819–828
Geissmann T (1991) Reassessment of age of sexual maturity in gibbons (Hylobates spp.). Am J Primatol 23:11–22
Hamada Y (1994) Standard growth patterns and variations in growth patterns of the Japanese monkeys (Macaca fuscata) based on an analysis by the spline function method. Anthropol Sci 102 [Suppl]: 57–76
Humbel RE (1984) Insulin-like growth factors, somatomedins, and multiplication stimulation activity: chemistry. In: Li Ch (ed.) Hormonal proteins and peptides. Academic Press, Orlando, pp 57–79
Iwamoto M (1971) Morphological studies of Macaca fuscata (VI): somatometry. Primates 12:151–174
Jungers WL (1984) Scaling of the hominoid locomotor skeleton with special reference to lesser apes. In: Preuschoft H, Chivers DJ, Brockelman WY, Creel N (eds) The lesser apes. Edinburgh University Press, Edinburgh, pp 146–169
Katharina MM, Ida MM, Niels ES (2000) A possible role for reproductive hormones in newborn boys: progressive hypogonadism without the postnatal testosterone peak. J Clin Endocrinol Metab 85:4905–4907
Kimura K (1979) Growth. (in Japanese) Yuzankaku Shuppan, Tokyo
Leigh SR, Shea BT (1995) Ontogeny and the evolution of adult body size dimorphism in apes. Am J Primatol 36:37–60
Linke K (1988) Beobachtungen zur Entwicklung von 3 Gibbons bei einer Handaufzucht und 2 kombinierten Aufzuchten. Zool Garten N F Jena 58:229–250
Marson J, Meuris S, Cooper RW, Jouannet P (1991) Puberty in the male chimpanzee: time-related variations in luteinizing hormone, follicle-stimulating hormone, and testosterone. Biol Reprod 44:456–460
Martin CR (1985) Endocrine Physiology. Oxford University Press, New York
Martin R, Saller K (1957) Lehrbuch der Anthropologie. Fischer, Stuttgart
Matsubayashi K, Mochizuki K (1982) Growth of male reproductive organs with observation of their seasonal morphologic changes in the Japanese monkey (Macaca fuscata). Jpn J Vet Sci 44:891–902
Meusy-Dessolle N, Dang DC (1985) Plasma concentrations of testosterone, dihydrotestosterone, Δ4−androstenedione, dehydroepiandrosterone and oestradiol-17 β in the crab-eating monkey (Macaca fascicularis) from birth to adulthood. J Reprod Fertil 74:347–359
Napier JR, Napier PH (1967) A handbook of living primates. Academic Press, London
Nigi H, Tiba T, Yamamoto S, Floescheim Y, Ohsawa N (1980) Sexual maturation and seasonal changes in reproductive phenomena of male Japanese monkeys (Macaca fuscata) at Takasakiyama. Primates 21:230–240
Plant TM (1985) A study of the role of the postnatal testes in determining the ontogeny of gonadotropin secretion in the male rhesus monkey (Macaca mulatta). Endocrinology 116:1341–1350
Plant TM, Zorub DS (1982) The role of nongonadal restraint of gonadotropin secretion in the delay of the onset of puberty in the rhesus monkey (Macaca mulatta). J Anim Sci 55:43–55
Roonwall ML, Mohnot SM (1977) Primates of South Asia: ecology, sociobiology and behavior. Harvard University Press, Cambridge, Mass.
Sanayama K, Cho M, Ushihisa H, Sato K, Nishioka T, Sasaki N, Niimi H, Nakashima H (1984) Measurement of somatomedin-C in plasma by radioimmunoassay; basic evaluation and clinical applications (in Japanese). Clin Endocrinol 32:567–571
Sawina NW, Orpachowa WR (1981) Haltung und Zucht von Weisshandgibbons (Hylobates lar L., 1771) im Leningrader Zoo. Zool Garten N F Jena 51:343–352
Shohoji T, Sasaki H (1985) An aspect of growth analysis of weight in Savannah baboon. Growth 49:500–509
Smith BH (1992) Life history and the evolution of human maturation. Evol Anthropol 1:134–142
Smith BH, Crummett TL, Brandt KL (1994) Ages of eruption of Primate teeth: a compendium for aging individuals and comparing life histories. Yearb Phys Anthropol 37:177–231
Suzuki J, Ohkura S, Hayakawa S, Hamada Y (2000) Time series analysis of plasma insulin-like growth factor-I and gonadal steroids in adolescent Japanese macaques (Macaca fuscata). J Reprod Dev 46:157–166
Suzuki J, Ishida T, Ohkura S, Udono T, Hayasaka I, Arsaithamkul V (2001) Plasma IGF-1 levels in the great and lesser apes. In: The 18th Congress of the International Primatological Society, pp 485
Tachibana K, Suwa K, Yokoya S, Hizuka N, Tanaka T, Hibi I, Fujieda K, Miyachi Y, Irie M (1993) Clinical evaluation of the total IGF-I assay kit (Sm-C [Scitech Research]) (in Japanese). Clin Endocrinol 41:915–923
Tachibana K, Suwa K, Yokoya S, Hizuka N, Tanaka T, Hibi I, Fujieda K, Miyachi Y, Irie M (1994) Clinical evaluation of the total somatomedin-C (total IGF-I) assay kit (in Japanese). Clin Endocrinol 42:73–79
Watts ES (1985) Adolescent growth and development of monkeys, apes and humans. In: Watts ES (ed) Nonhuman primate models for human growth and development. Liss, New York, pp 41–65
Watts ES, Gavan JA (1982) Postnatal growth of nonhuman primates: the problem of the adolescent spurt. Hum Biol 54:53–70
Wilson ME (1986) Gonadal steroids influence serum somatomedin-C concentrations in prepubertal female rhesus monkeys. Endocrinology 119:666–671
Wilson ME, Schwartz SM, Walker ML, Gordon TP (1984) Oestradiol and somatomedin-C influence body weight patterns in premenarchial rhesus monkeys housed outdoors. J Endocrinol 102:311–317
Winter JS, Faiman C, Hobson WC, Prasad AV, Reyes FI (1975) Pituitary-gonadal relations in infancy. I. Patterns of serum gonadotropin concentrations from birth to four years of age in man and chimpanzee. J Clin Endocrinol Metab 40:545–551
Yoshida T (1994) Comparison between non-human primates and humans. II. Characterization of growth patterns (in Japanese). Hum Sci 7:52-77
Acknowledgements
We would like to thank the staff of the Center for Human Evolution Modeling Research, Primate Research Institute of Kyoto University, for their assistance throughout the study. We are also grateful to Prof. S. Sri Kantha, of the Center, for his valuable criticism, and to Ms. Y. Suzuki for her technical assistance.
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
Suzuki, J., Kato, A., Maeda, N. et al. Plasma insulin-like growth factor-I, testosterone and morphological changes in the growth of captive agile gibbons (Hylobates agilis) from birth to adolescence. Primates 44, 273–280 (2003). https://doi.org/10.1007/s10329-003-0044-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10329-003-0044-x