Preparation and activation: determinants of age at reproductive maturity in male baboons
Tóm tắt
Age at maturity is a particularly important life history trait, but maturational data are rare for males in natural populations of mammals. Here we provide information on three maturational milestones and their social and demographic correlates among 43 wild male baboons, Papio cynocephalus, in a natural population in Amboseli National Park, Kenya. We examined (1) age at testicular enlargement, which signals puberty and the onset of subadulthood, (2) age at attainment of adult dominance rank, which we consider to be the beginning of adulthood, and (3) age at first sexual consortship, which is the best measure available for age at first reproduction in male baboons. Testicular enlargement (median age = 5.69 years) occurred earlier among sons of high ranking mothers, and was not influenced by rainfall or seasonality. Attainment of adult dominance rank (median age = 7.41 years) was also accelerated among sons of high-ranking mothers, and among males whose mothers had died while the males were juveniles. First sexual consortship (median age = 7.92 years) was not influenced directly by maternal characteristics, but attainment of adult dominance rank always preceded first consortship. The lag time between attainment of adult rank and first consortship (median = 2.5 months; range = 5–526 days), was predicted by the number of sexually cycling females in the group when the male attained rank, and by how high ranking the male became in his first months as an adult. We suggest that the age at which a male baboon is ready to begin reproducing is influenced by a relatively stable maternal characteristic that exerts its influence early in development, but the timing with which this potential is realized depends on activation by more proximate, often stochastic triggers such as female availability. This two-level organization of influences is likely to contribute to the variance both in age at first reproduction and in lifetime fitness. Differences in the relative magnitude of the two levels will lead to both intra- and interspecific variability in the opportunity for maternal selection and sexual selection.
Tài liệu tham khảo
Abbott DH (1984) Behavioral and physiological suppression of fertility in subordinate marmoset monkeys. Am J Primatol 6:169–186
Abbott DH (1987) Behaviourally mediated suppression of reproduction in female primates. J Zool Lond 213:455–470
Alberts SC, Altmann J (1995) Balancing costs and opportunities: dispersal in male baboons. Am Nat 145:279–306
Altmann J, Alberts SC (1987) Body mass and growth rates among wild baboons. Oecologia 72:15–20
Altmann J, Altmann S, Hausfater G, McCuskey S (1977) Life histories of yellow baboons: physical development, reproductive parameters, and infant mortality. Primates 18:315–330
Altmann J, Altmann S, Hausfater G (1981) Physical maturation and age estimates of yellow baboons, Papio cynocephalus, in Amboseli National Park, Kenya. Am J Primatol 1:389–399
Altmann J, Hausfater G, Altmann S (1985) Demography of Amboseli baboons, 1963–1983. Am J Primatol 8:113–125
Altmann J, Altmann S, Hausfater G (1988) Determinants of reproductive success in savannah baboons (Papio cynocephalus). In: Clutton-Brock TH (ed) Reproductive success. University of Chicago Press, Chicago, pp 403–418
Altmann SA (1962) A field study of the sociobiology of the rhesus monkey, Macaca mulatta. Ann NY Acad Sci 102:338–435
Altmann SA, Altmann J (1979) Demographic constraints on behavior and social organization. In: Bernstein IS, Smith EO (eds) Primate ecology and human origins. Garland Press, New York, pp 47–63
Bell G (1980) The costs of reproduction and their consequences. Am Nat 116:45–76
Bercovitch FB (1987) Reproductive success in male savanna baboons. Behav Ecol Sociobiol 21:163–172
Bercovitch FB, Goy RW (1990) The socioendocrinology of reproductive development and reproductive success in macaques. In: Ziegler TE, Bercovitch FB (eds) Socioendocrinology of primate reproduction. Wiley-Liss, New York, pp 59–93
Bercovitch FB, Strum SC (1993) Dominance rank, resource availability, and reproductive maturation in female savanna baboons. Behav Ecol Sociobiol 33:313–318
Bronson FH (1989) Mammalian reproductive biology. University of Chicago Press, Chicago
Bulger, JB (1994) Dominance rank and access to estrous females in male savanna baboons. Behaviour 127:67–103
Castracane VD, Copeland KC, Reeves P, Kuehl T (1986) Pubertal endocrinology of yellow baboon (Papio cynocephalus): plasma testosterone, testis size, body weight and crown-rump length in males. Am J Primatol 11:263–270
Caswell H (1982) Life history theory and the equilibrium status of populations. Am Nat 120:317–339
Chapais B (1983) Matriline membership and male rhesus reaching high ranks in the natal troops. In: Hinde RA (ed) Primate social relationships. Sinauer, Sunderland, pp 171–175
Charnov EL, Berrigan D (1990) Dimensionless numbers and life history evolution: age of maturity versus the adult lifespan. Evol Ecol 4:273–275
Cheney DL (1977) The acquisition of rank and the development of reciprocal alliances among free-ranging immature baboons. Behav Ecol Sociobiol 2:303–318
Cheney DL (1983) Proximate and ultimate factors related to the distribution of male migration. In: Hinde RA (ed) Primate social relationships. Sinauer, Sunderland, pp 241–249
Coelho AM (1985) Baboon dimorphism: growth in weight, length and adiposity from birth to 8 years of age. In: Watts ES (ed) Nonhuman primate models for human growth and development. Liss, New York, pp 125–159
Cole LC (1954) The population consequences of life history phenomena. Q Rev Biol 29:103–137
Crockett CM, Pope TR (1993) Consequences of sex differences in dispersal for juvenile red howler monkeys. In: Pereira ME, Fairbanks LA (eds) Juvenile primates: Life history, development and behavior. Oxford Univeristy Press, New York, pp 104–118
Dittus WP (1977) The social regulation of population density and age-sex distribution in the toque monkey. Behaviour 63:281–322
Drickamer LC (1974) Social rank, observability and sexual behavior of rhesus monkeys. J Repro Fert 37:117–120
Drickamer LC, Vessey SH (1973) Group changing in free ranging male rhesus monkeys. Primates 14:359–368
Emlen ST (1991) Evolution of cooperative breeding in birds and mammals. In: Krebs JR, Davies NB (eds) Behavioural ecology: An evolutionary approach. Blackwell, London, pp 301–337
Epple G, Katz Y (1984) Social influences on estrogen excretion and ovarian cyclicity in saddle back tamarins (Saguinus fuscicollis). Am J Primatol 6:215–227
Erwin J, Mitchell G (1975) Initial heterosexual behavior of adolescent rhesus monkeys (Macaca mulatta). Arch Sex Behav 4:97–104
Foerg R (1982) Reproductive behavior in Varecia variegata. Folia Primatol 38:108
French JA, Abbott DH, Snowdon CT (1984) The effect of social environment on estrogen excretion, scent marking, and sociosexual behavior in tamarins (Saguinus oedipus). Am J Primatol 6:155–167
Frisch RE, MacArthur JW (1974) Menstrual cycles: fatness as a determinant of minimum weight for height necessary for their maintenance or onset. Science 185:949–951
Frisch RE, Revelle R (1970) Height and weight at menarche and a hypothesis of critical body weights and adolescent events. Science 169:397–399
Goldizen AW (1987) Tamarins and marmosets: communal care of offspring. In: Smuts BB, Cheney DL, Seyfarth R, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 34–43
Goldizen AW, Terborgh J (1989) Demography and dispersal patterns of a tamarin population: possible causes of delayed breeding. Am Nat 134:208–234
Goodall J (1986) The chimpanzees of gombe: patterns of behavior. Harvard University Press, Cambridge
Gouzoules H, Gouzoules S, Fedigan L (1982) Behavioural dominance and reproductive success in female Japanese monkeys (Macaca fuscata). Anim Behav 30:1138–1150
Hamilton WJ III, Bulger JB (1990) Natal male baboon rank rises and successful challenges to resident alpha males. Behav Ecol Sociobiol 26:357–362
Harvey PH, Zamrnuto RM (1985) Patterns of mortality and age at first reproduction in natural populations of mammals. Nature 315:319–320
Hausfater G (1975) Dominance and Reproduction in Baboons (Papio cynocephalus). Karger, Basel
Janson CH, Schaik CP van (1993) Ecological risk aversion in juvenile primates: slow and steady wins the race. In: Pereira ME, Fairbanks LA (eds) Juvenile Primates: life history, development and behavior. Oxford Univeristy Press, New York, pp 57–74
Johnson JA (1987) Dominance rank in juvenile olive baboons, Papio anubis: the influence of gender, size, maternal rank and orphaning. Anim Behav 35:1694–1708
Kalbfleisch JD, Prentice RL (1980) The statistical analysis of failure time data. Wiley, New York
Kirkpatrick M, Lande R (1989) The evolution of maternal characters. Evolution 43:485–503
Koford CB (1963) Ranks of mothers and sons in bands of rhesus monkeys. Science 146:356–357
Koyama N (1970) Changes in dominance rank and division of a wild Japanese monkey troop in Arashiyama. Primates 11:335–390
Lande R, Kirkpatrick M (1990) Selection response in traits with maternal inheritance. Genet Res 55:189–197
Lee ET (1992) Statistical methods for survival data analysis. Wiley, New York
Lee PC, Oliver JI (1979) Competition, dominance, and the acquisition of rank in juvenile yellow baboons (Papio cynocephalus). Anim Behav 27:576–585
Lessels CM (1991) The evolution of life histories. In: Krebs JR, Davies NB (eds) Behavioural Ecology: an evolutionary approach. Blackwell, London, pp 32–68
Lewontin RC (1965) Selection for colonizing ability. In: Baker HG, Stebbins GL (eds) The genetics of colonizing species. Academic Press, New York, pp 77–91
Loy J (1988) Effects of supplementary feeding on maturation and fertility in primate groups. In: Fa JE, Soputhwick CH (eds) Ecology and behavior of food-enhanced primate groups. Liss, New York, pp 153–166
Lyles AM, Dobson AP (1988) Dynamics of provisioned and unprovisioned primate populations. In: Fa JE, Southwick CH (eds) Ecology and behavior of food-enhanced primate groups. Liss, New York, pp 167–198
Mertz DB (1971) Life history phenomena in increasing and decreasing populations. In: Patil GP, Pielou EC, Waters WE (eds) Statistical ecology, vol II. Sampling and modeling biological populations and population dynamics. Pennsylvania State University Press, University Park, pp 361–392
Mori A (1979) Analysis of population changes by measurement of body weight in the Koshima troop of Japanese monkeys. Primates 20:371–398
Noë R, Sluijter AA (1990) Reproductive tactics of male savanna baboons. Behaviour 113:117–170
Packer C (1979) Male dominance and reproductive activity in Papio anubis. Anim Behav 27:37–45
Pagel MD, Harvey PH (1993) Evolution of the juvenile period in mammals. In: Pereira ME, Fairbanks LA (eds) Juvenile primates: life history, development and behavior. Oxford University Press, New York, pp 27–28
Pereira ME (1988) Agonistic interactions of juvenile savanna baboons I. Fundamental features. Ethology 79:195–217
Pereira ME (1989) Agonistic interactions of juvenile savanna baboons II. Agonistic support and rank acquisition. Ethology 80:152–171
Pereira ME (1992) Dominance relations before puberty in cercopithecines. In: Silverberg J, Gray JP (eds) Aggression and peacefulness in humans and other primates. Oxford University Press, New York, pp 117–149
Plant TM (1988) Puberty in primates. In: Krobil E, Neill J (eds) The physiology of reproduction. Raven Press, New York, pp 1763–1788
Pusey AE (1990) Behavioural changes at adolescence in chimpanzees. Behaviour 155:203–246
Roff DA (1992) The evolution of life histories. Chapman and Hall, New York
Rowell TE (1977) Variation in age at puberty in monkeys. Folia Primatol 27:284–296
Rubenstein DI (1993) On the evolution of juvenile life-styles in mammals. In: Pereira ME, Fairbanks LA (eds) Juvenile primates: life history, development and behavior. Oxford Univeristy Press, New York, pp 38–56
Sade DS, Cushing K, Cushing J, Dunaif J, Figueroa A, Kaplan JR, Lauer C, Rhodes D, Schneider J (1976) Population dynamics in relation to social structure on Cayo Santiago. Yrbk Phys Anthropol 20:253–262
SAS Institute (1988) SAS technical report P-179: additional SAS/STAT procedures, SAS 6.03. SAS Institute, Cary
Savage A, Ziegler TE, Snowdon CT (1988) Sociosexual development, pair bond formation, and mechanisms of fertility suppression in female cotton-top tamarins (Saguinus oedipus oedipus). Am J Primatol 14:345–359
Shea BT (1990) Dynamic morphology: growth, life history, and ecology in primate evolution. In: DeRousseau CJ (ed) Primate life history and evolution. Wiley-Liss, New York, pp 325–352
Silk JB (1987) Social behavior in evolutionary perspective. In: Smuts BB, Cheney DL, Seyfarth R, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 318–329
Smith DG, Smith S (1988) Parental rank and reproductive success of natal rhesus males. Anim Behav 36:554–562
Smuts BB (1985) Sex and friendship in baboons. Aldine, New York
Sokal RR, Rohlf FJ (1981) Biometry. WH Freeman, New York
Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford
Strum SC (1982) Agonistic dominance in male baboons: an alternative view. Int J Primatol 3:175–202
Strum SC (1991) Weight and age in wild olive baboons. Am J Primatol 25:219–237
Sugiyama Y (1976) Life history of male Japanese monkeys. In: Rosenblatt JS, Hinde RA, Shaw E, Beer C (eds) Advances in the study of behavior. Academic, New York, pp 255–284
Vandenbergh JG, Coppola DM (1986) The physiology and ecology of puberty modulation by primer pheromones. Adv Study Behav 16:71–107
Wagenen G van, Catchpole HR (1956) Physical growth of the rhesus monkey (Macaca mulatta). Am J Phys Anthropol 14:245–273
Wagenen G van, Simpson ME (1954) Testicular development in the rhesus monkey. Anat Rec 118:231–243
Walters JR, Seyrath RM (1987) Conflict and cooperation. In: Smuts BB, Cheney DL, Seyfarth R, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 306–317
Watts DP (1991) Mountain gorilla reproduction and sexual behavior. Am J Primatol 24:211–226
Watts DP, Pusey AE (1993) Behavior of juvenile and adolescent great apes. In: Pereira ME, Fairbanks LA (eds) Juvenile primates: life history, development and behavior. Oxford Univeristy Press, New York, pp 148–167
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
Wiley RH (1974) Effects of delayed reproduction on survival, fecundity, and the rate of population increase. Am Nat 108: 705–709
Wolfe LD (1979) Sexual maturation among members of a transported troop of Japanese macaques (Macaca fuscata). Primates 20:411–418
Ziegler TE, Snowdon CT, Uno H (1990) Social interactions and determinants of ovulation in tamarins (Saguinus). In: Ziegler TE, Bercovitch FB (eds) Socioendocrinology of primate reproduction. Wiley-Liss, New York, pp 113–133