Summary
In the new colony of rhesus macaques at Madingley, no overall difference was found in the length of the inter-birth intervals following the birth of male and female infants. The lack of overall differences in the reproductive costs of raising sons and daughters, was associated with an absence of differences in suckling patterns between male and female infants. It is argued that similar pre-weaning investment in sons and daughters may be related to the presence of similar growth rates for male and female infants during the first year of life. Most high ranking mothers reproduced in consecutive years, while low ranking mothers were more likely to experience two year long inter-birth intervals. Further analyses revealed that this difference was mainly due to the fact that low ranking mothers always failed to reproduce the year after raising a daughter. Thus, no difference was found in the length of inter-birth intervals between high ranking mothers with infants of either sex and low ranking mothers with sons. The daughters of low ranking females suckled more frequently and making more nipple contacts per bout, and such high nipple stimulation was responsible for the reproductive inhibition experienced by their mothers. It is suggested that the high degrees of nipple stimulation may have been a consequence of the high levels of aggression that low ranking females with daughters have been shown to receive, since their mothers could have allowed frequent ventro-ventral contact in order to protect them. Given that low ranking mothers find daughters reproductively costly to raise, it is possible that such high reproductive costs have played a significant role in the evolution of sex ratio biases at birth. As in other primate populations, in this colony low ranking females produced a greater proportion of sons than daughters, and high ranking mothers showed the opposite trend.
Similar content being viewed by others
References
Abbott DH (1984) Behavioural 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 (London) 213:455–470
Abbott DH, McNeilly AS, Lunn SF, Hulme MJ, Burden FJ (1981) Inhibition of ovarian function in subordinate female marmoset monkeys (Callithrix jacehus jaechus). J Reprod Fertil 63:335–345
Abbott DH, Keverne EB, Moore F, Yodyingyuad U (1986) Social suppression of reproduction in subordinate talapoin monkeys, Miopithecus talapoin. In: Else JG, Lee PC (eds) Primate ontogeny, cognition and social behaviour. Cambridge University Press, Cambridge, pp 329–341
Altmann J (1980) Baboon mothers and infants. Harvard University Press, Cambridge, MA
Altmann J, Alberts S (1987) Body mass and growth rates in a wild primate population. Oecologia 72:15–20
Altmann J, Hausfater G, Altmann SA (1988) Determinants of reproductive success in savannah baboons, Papio eynocephalus. In: Clutton-Brock TH (ed) Reproductive success. The University of Chicago Press, Chicago, pp 403–418
Anderson SS, Fedak MA (1987) Grey seal, Halichoerus grypus, energetics: females invest more in male offspring. J Zool (London) 211:667–679
Austad SN, Sunquist ME (1986) Sex-ratio manipulation in the common opossum. Nature 324:58–60
Berman CM (1988) Maternal condition and offspring sex ratio in a group of free-ranging rhesus monkeys: an eleven-year study. Am Nat 131:307–328
Bernstein IS (1981) Dominance: the baby and the bathwater. Behav Brain Sci 4:419–458
Boyd IL, McCann TS (1989) Pre-natal investment in reproduction by female Antarctic fur seals. Behav Ecol Sociobiol 24:377–385
Cheney L, Seyfarth RM, Andelman SJ, Lee PC (1988) Reproductive success in vervet monkeys. In: Clutton-Brock TH (ed) Reproductive success. The University of Chicago Press, Chicago, pp 384–402
Clark AB (1978) Sex ratio and local resource competition in a prosimian primate. Science 201:163–165
Clutton-Brock TH (1982) Sons and daughters. Nature 298:11–13
Clutton-Brock TH (1985) Birth sex ratios and the reproductive success of sons and daugthers. In: Greenwood PJ, Harvey PH, Slatkin M (eds) Evolution. Essays in honour of John Maynard Smith. Cambridge University Press, Cambridge, pp 221–235
Clutton-Brock TH (1988) Reproductive success. In: Clutton-Brock TH (ed) Reproductive success. The University of Chicago Press, Chicago, pp 472–485
Clutton-Brock TH, Albon SD (1982) Parental investment in male and female offspring in mammals. In: King's College Sociobiology Group (eds) Current problems in sociobiology. Cambridge University Press, Cambridge, pp 223–247
Clutton-Brock TH, Iason GR (1986) Sex ratio variation in mammals. Q Rev Biol 61:339–374
Clutton-Brock TH, Albon SD, Guinness FE (1981) Parental investment in male and female offspring in polygynous mammals. Nature 289:487–489
Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer. Behaviour and ecology of the two sexes. Edinburgh University Press, Edinburgh
Clutton-Brock TH, Albon SD, Guinness FE (1984) Maternal dominance, breeding success and birth sex ratios in red deer. Nature 308:358–360
Clutton-Brock TH, Albon SD, Guinness FE (1986) Great expectations: dominance, breeding success and offspring sex ratios in red deer. Anim Behav 34:460–471
Clutton-Brock TH, Albon SD, Guinness FE (1988) Reproductive success in male and female red deer. In: Clutton-Brock TH (ed) Reproductive success. The University of Chicago Press, Chicago, pp 325–343
Coehlo AM (1985) Baboon dimorphism: growth in weight, length and adiposity from birth to 8 years of age. In: Watts ES (ed) Non-human primate models for human growth and development. Alan R Liss, New York, pp 125–159
Costa DP, Gentry RL (1986) Free ranging and reproductive energetics of the northern fur seal. In: Gentry RL, Kooyman GL (eds) Fur seals: maternal strategies on land and at sea. Princeton University Press, Princeton, pp 79–101
Czaja JA, Eisele SG, Goy RW (1975) Cyclical changes in the sexual skin of female rhesus: relationship to mating behaviour and successful artifical insemination. Proc Fedn Ann Soc Exp Biol 34:1680–1684
Datta SB (1981) Dynamics of dominance among rhesus females. Unpublished Ph.D. Thesis, University of Cambridge
Dittus WPJ (1979) The evolution of behaviours regulating density and age-specific sex ratios in a primate population. Behaviour 69:265–302
Dittus WPJ (1980) The social regulation of primate populations: a synthesis. In: Lindburg DG (ed) The Macaques. Van Nostrand, New York, pp 263–286
Dittus WPJ (1988) Group fission among wild toque macaques as a consequence of female resource competition and environmental stress. Anim Behav 36:1626–1645
Drickamer LC (1974) A ten-year summary of reproductive data for free-ranging Macaca mulatta. Folia Primatol 21:61–80
Dunbar RIM (1980) Determinants and evolutionary consequences of dominance among female gelada baboons. Behav Ecol Socio biol 7:253–265
Dunbar RIM (1984) Reproductive decisions: an economic analysis of gelada baboon social strategies. Princeton University Press, Princeton
Dunbar RIM (1987) Habitat quality, population dynamics and group composition in colobus monkeys (Colobus guereza). Int J Primatol 8:299–329
Dunbar RIM (1988) Primate social systems. Croom Helm, London
Dunbar RIM, Dunbar P (1977) Dominance and reproductive success among female gelada baboons. Nature 266:351–352
Dunbar RIM, Sharman M (1983) Female competition for access to males affects birth rate in baboons. Behav Ecol Sociobiol 13:157–159
Fa JE (1986) Use of time and resources by provisioned troops of monkeys. Karger, Basel
Fairbanks LA, McGuire MT (1984) Determinants of fecundity and reproductive success in captive vervet monkeys. Am J Primatol 7:27–38
Fairbanks LA, McGuire MT (1986) Age, reproductive value and dominance related behaviour in vervet monkey females: cross-generational influences on social relationships and reproduction. Anim Behav 34:1710–1721
Glassman DM, Coelho AM, Carey KD, Bramblett CA (1984) Weight growth in savannah baboons: a longitudinal study from birth to adulthood. Growth 48:425–433
Gomendio M (1988) Mother-offspring relationships and consequences for fertility in rhesus macaques. Ph.D. Thesis, University of Cambridge
Gomendio M (1989) Suckling behaviour and fertility in rhesus macaques. J Zool (London) 217:449–467
Gomendio M, Clutton-Brock TH, Albon SD, Guinness FE, Simpson MJA (1990) Mammalian sex ratios and variation in the costs of rearing sons and daughters. Nature 343:261–263
Gordon TP (1981) Reproductive behaviour in the rhesus monkey: social and endocrine variables. Am Zool 21:185–195
Gosling LM (1986) Selective abortion of entire litters in the coypu: adaptive control of offspring production in relation to quality and sex. Am Nat 127:772–795
Guinness FE, Albon SD, Clutton-Brock TH (1978) Factors affecting reproduction in red deer (Cervus elaphus). J Reprod Fertil 54:325–334
Gray JP (1985) Primate sociobiology. HRAF Press, New Haven
Harcourt AH (1987) Dominance and fertility among female primates. J Zool (London) 213:471–487
Hinde RA (1978) Dominance and role — two concepts with dual meanings. J Social Biol Struct 1:27–38
Horrocks J (1986) Life-history characteristics of a wild population of vervets (Cercopithecus aethiops sabaeus) in Barbados, West Indies. Int J Primatol 7:31–47
Hrdy SB (1987) Sex-biased parental investment among primates and other mammals: a critical evaluation of the Trivers-Willard hypothesis. In: Gelles R, Lancaster J (eds) Child abuse and neglect: biosocial dimensions. Aldine, Hawthorne NY, pp 97–147
Hrdy SB, Whitten PL (1987) Patterning of sexual activity. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. The University of Chicago Press, Chicago, pp 370–384
Johnson CN (1988) Dispersal and the sex ratio at birth in primates. Nature 332:726–728
Le Boeuf B, Reiter J (1988) Lifetime reproductive success in northern elephant seals. In: Clutton-Brock TH (ed) Reproductive success. Chicago University Press, Chicago, pp 344–362
Le Boeuf B, Condit R, Reiter J (1989) Parental investment and the secondary sex ratio in northern elephant seals. Behav Ecol Sociobiol 25:109–117
Lee PC (1987) Nutrition, fertility and maternal investment in primates. J Zool (London) 213:409–422
Lee PC, Moss CJ (1986) Early maternal investment in male and female African elephant calves. Behav Ecol Sociobiol 18:353–362
Lloyd PH, Rasa OAE (1989) Status, reproductive success and fitness in Cape mountain zebra (Equus zebra zebra). Behav Ecol Sociobiol 25:411–420
Loudon ASI, McNeilly AS, Milne JA (1983) Nutrition and lactational control of fertility in red deer. Nature 302:145–147
Lunn PG (1988) Malnutrition and fertility. In: Diggory P, Potts M, Teper S (eds) Natural human fertility. The MacMillan Press, London, pp 135–152
Martin P, Bateson P (1986) Measuring behaviour. Cambridge University Press, Cambridge
Melnick DJ, Pearl MC (1987) Cercopithecines in multimale groups: Genetic diversity and population structure. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. The University of Chicago Press, Chicago, pp 121–134
Nicolson NA (1982) Weaning and the development of independence in olive baboons. Unpublished Ph.D. Thesis, Harvard University
Noordwijk MA, Schaik CP van (1987) Competition among female long-tailed macaques, Macaca fascicularis. Anim Behav 35:577–589
Pope NS, Gordon TP, Wilson ME (1986) Age, social rank and lactational status influence ovulatory patterns in seasonally breeding rhesus monkeys. Biol Reprod 35:353–359
Pusey AE, Packer C (1987) Dispersal and philopatry. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. The University of Chicago Press, Chicago, pp 250–266
Reiter J, Stinson NL, Le Boeuf BJ (1978) Northern elephant seal development: the transition from weaning to nutritional independence. Behav Ecol Sociobiol 3:337–367
Robinson JG (1988) Group size in wedge-capped capuchin monkeys Cebus olivaceus and the reproductive success of males and females. Behav Ecol Sociobiol 23:187–197
Rowell TE (1966) Hierarchy in the organisation of a captive baboon group. Anim Behav 14:430–443
Rowell TE, Chism J (1986) The ontogeny of sex differences in the behavior of patas monkeys. Int J Primatol 7:83–106
Sade DS, Cushing K, Cushing P, Dunaif J, Figueroa A, Kaplan JR, Laurer C, Rhodes D, Schneider J (1976) Population dynamics in relation to social structure on Cayo Santiago. Yrbk Phys Anthropol 20:253–262
Schaik CP van (1983) Why are diurnal primates living in groups? Behaviour 87:120–144
Sharma DN, Lal KC (1986) Age-related growth patterns of colony-born rhesus monkeys. In: Else JG, Lee PC (eds) Primate ontogeny, cognition and social behaviour. Cambridge University Press, Cambridge, pp 141–146
Sigg H, Stolba A, Abegglen J-J, Dasser V (1982) Life history of hamadryas baboons: physical development, infant mortality, reproductive parameters and family relationships. Primates 23:473–487
Silk JB (1983) Local resource competition and facultative adjustment of sex ratios in relation to competitive abilities. Am Nat 121:56–66
Silk JB (1987) Social behaviour in evolutionary perspective. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 318–329
Silk JB (1988) Maternal investment in captive bonnet macaques (Macaca radiata). Am Nat 132:1–19
Silk JB, Clark-Wheatley CB, Rodman PS, Samuels A (1981a) Differential reproductive success and facultative adjustment of sex ratios among captive female bonnet macaques (Macaca radiata). Anim Behav 29:1106–1120
Silk JB, Samuels A, Rodman PS (1981b) The influence of kinship, rank, and sex on affiliation and aggression between adult female and immature bonnet macaques (Macaca radiata). Behaviour 78:111–137
Simpson MIA (1983) Effect of the sex of an infant on the mother-infant relationship and the mother's subsequent reproduction. In: Hinde RA (ed) Primate social relationships. Blackwell, Oxford, pp 53–57
Simpson MJA, Simpson AE (1982) Birth sex ratios and social rank in rhesus monkey mothers. Nature 300:440–441
Simpson AE, Simpson MJA (1985) Short-term consequencs of different breeding histories for captive rhesus macaque mothers and young. Behav Ecol Sociobiol 18:83–89
Simpson MJA, Simpson AE, Hooley J, Zunz M (1981) Infant-related influences on birth intervals in rhesus monkeys. Nature 290:49–51
Small ME, Smith DG (1984) Sex differences in maternal investment by Macaca mulatta. Behav Ecol Sociobiol 14:313–314
Snow CC (1967) The physical growth and development of the open-land Baboon, Papio doguera. Unpublished PhD Thesis, University of Arizona
Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. Freeman, San Francisco
Stewart K (1988) Suckling and lactational anoestrus in wild gorillas. J Reprod Fertil 83:627–634
Sugiyama Y, Ohsawa H (1982) Population dynamics of Japanese monkeys with special reference to the effect of artifical feeding. Folia Primatol 39:238–263
Takahata Y (1980) The reproductive biology of a free-ranging troop of Japanese monkeys. Primates 21:303–329
Trillmich F (1986) Maternal investment and sex-allocation in the Galapagos fur seal, Arctocephalus galapagoensis. Behav Ecol Sociobiol 19:157–164
Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136–179
Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex ratio. Science 179:90–92
Vandenbergh JG, Vessey SH (1968) Seasonal breeding of free-ranging rhesus monkeys and related ecological factors. J Reprod Fertil 15:71–79
Wagenen G van (1972) Vital statistics from a breeding colony: reproductive and pregnancy outcome in Macaca mulatta. J Med Primatol 1: 3–28
Wagenen G van, Catchpole HR (1956) Physical growth of the rhesus monkey (Macaca mulatta). Am J Phys Anthropol 14:245–273
Walker ML, Gordon TP, Wilson ME (1983) Menstrual cycle characteristics of seasonally breeding rhesus monkeys. Biol Reprod 29:841–848
Wasser SK (1983) Reproductive competition and cooperation among female yellow baboons. In: Wasser SK (ed) Social behaviour of female vertebrates. Academic Press, New York, pp 349–390
Wasser SK, Barash DP (1983) Reproductive suppression among female mammals: implications for biomedicine and sexual selection theory. Q Rev Biol 58:513–538
Whitten PL (1982) Female reproductive strategies among vervet monkeys. PhD diss, Harvard University
Whitten PL (1983) Diet and dominance among female vervet monkeys (Cercopithecus aethiops). Am J Primatol 5:139–159
Wilson ME, Gordon TP, Bernstein IS (1978) Timing of births and reproductive success in rhesus monkey social groups. J Med Primatol 7:202–212
Wilson ME, Walker ML, Pope NS, Gordon TP (1988) Prolonged lactational infertility in adolescent rhesus monkeys. Biol Reprod 38:163–174
Wolff JO (1988) Maternal investment and sex ratio adjustment in American Bison calves. Behav Ecol Sociobiol 23:127–133
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Gomendio, M. The influence of maternal rank and infant sex on maternal investment trends in rhesus macaques: birth sex ratios, inter-birth intervals and suckling patterns. Behav Ecol Sociobiol 27, 365–375 (1990). https://doi.org/10.1007/BF00164008
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00164008