Maternal investment in rhesus macaques (Macaca mulatta): Reproductive costs and consequences of raising sons

Behavioral Ecology and Sociobiology

Volumn 48, Issue 1, 2000, Pages 1-11

  Bercovitch, Fred B ^a   Widdig, Anja ^b   Nürnberg, Peter ^b  

^a UNIVERSITY OF PUERTO RICO   (Puerto Rico)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Macaca mulatta; Maternal investment; Paternity; Sex ratio

Indexed keywords

BIRTH WEIGHT; DIMORPHISM; DNA FINGERPRINTING; GENETIC MARKER; LIVEWEIGHT GAIN; MOLECULAR TYPING; PROGENY; REPETITIVE DNA; SEX DIFFERENCE; SIZE;

MATERNAL CARE; PARENTAL INVESTMENT; PRIMATE; REPRODUCTIVE COST; REPRODUCTIVE SUCCESS; SEX ALLOCATION;

MACACA MULATTA;

EID: 0034047223     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s002650000204     Document Type: Article

References (131)

1. Alberts SC, Altmann J (1995a) Balancing costs and opportunities: dispersal in male baboons. Am Nat 145:279-306
2. Alberts SC, Altmann J (1995b) Preparation and activation: determinants of age at reproductive maturity in male baboons. Behav Ecol Sociobiol 36:397-406
3. Altmann J (1974) Observational study of behaviour: sampling methods. Behaviour 49:227-267
4. Altmann J (1980) Baboon mothers and infants. Harvard University Press, Cambridge, Mass
5. Altmann J, Hausfater G, Altmann S A (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
6. Altmann J, Alberts SC, Haines SA, Dubach J, Muruthi P, Coote T, Geffen E, Cheesman DJ, Mututua RS, Saiyael SN. Wayne RK, Lacy RC, Bruford MW (1996) Behavior predicts geneticstructure in a wild primate group. Proc Natl Acad Sci USA 93:5797-5801
7. Armitage KB (1987) Do female yellow-bellied marmots adjust the sex ratio of their offspring? Am Nat 125:501-519
8. Arnemann J, Schmidtke J, Epplen JT, Kuhn H-J, Kaumanns W (1989) DMA fingerprinting for paternity and maternity in group O Cayo Santiago-derived rhesus monkeys at the German Primate Center: results of a pilot study. P R Health Sci. J 8: 181-184
9. Berard JD (1999) A four-year study of the association between male dominance rank, residency status, and reproductive activity in rhesus macaques (Macaca mulatta). Primates 40:159-175
10. Bercovitch FB (1989) Body size, sperm competition, and determinants of male reproductive success in savanna baboons. Evolution 43:1507-1521
11. Bercovitch FB (1991) Social stratification, social strategies, and reproductive success in primates. Ethol Sociobiol 12:315-333
12. Bercovitch FB (1992) Estradiol concentrations, fat deposits, and reproductive strategies in male rhesus macaques. Horm Behav 26:272-282
13. Bercovitch FB (1993) Dominance rank and reproductive maturation in male rhesus macaques (Macaca mulatta). J Reprod Fertil 99:113-120
14. Bercovitch FB (1997) Reproductive strategies of rhesus macaques. Primates 38:247-263
15. Bercovitch FB, Berard JD (1993) Life history costs and consequences of rapid reproductive maturation in female rhesus macaques. Behav Ecol Sociobiol 32:103-109
16. 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
17. Bercovitch FB, Huffman MA (1999) The macaques. In: Dolhinow P, Fuentes A (eds) The nonhuman primates. Mayfield, Mountain View, Calif, pp 77-85
18. Bercovitch FB, Lebron MR (1991) Impact of artificial fissioning and social networks on levels of aggression and affiliation in primates. Aggr Behav 17:17-25
19. Bercovitch FB, Nürnberg P (1996) Socioendocrine and morphological correlates of paternity in rhesus macaques. J Reprod Fertil 107:59-68
20. Bercovitch FB, Strum SC (1993) Dominance rank, resource availability, and reproductive maturation in female savanna baboons. Behav Ecol Sociobiol 33:313-318
21. Berman CM (1980) Mother-infant relationships among free-ranging rhesus monkeys on Cayo Santiago: a comparison with captive pairs. Anim Behav 28:860-873
22. Berman CM (1984) Variation in mother-infant relationships: traditional and nontraditional factors. In: Small MF (ed). Female primates: studies by women primatologists. Liss, New York, pp 17-36
23. Berman CM (1986) Maternal lineages as tools for understanding infant social development and social structure. In: Rawlins RG, Kessler MJ (eds) The Cayo Santiago macaques. SUNY, Albany, pp 73-92
24. 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
25. Berman CM (1992) Immature siblings and mother-infant relationships among free-ranging rhesus monkeys on Cayo Santiago. Anim Behav 44:247-258
26. Berman CM, Rasmussen KLR, Suomi SJ (1993) Reproductive consequences of maternal care patterns during estrus among free-ranging rhesus monkeys. Behav Ecol Sociobiol 32:391-399
27. Bernstein IS, Ehardt CL (1986) Selective interference in rhesus monkey (Macaca mulatta) intragroup agonistic episodes by age-sex class. J Comp Psychol 100:380-384
28. Bernstein IS, Williams LE (1983) Ontogenetic changes and the stability of rhesus monkey dominance relationships. Behav Proc 8:379-392
29. Birgersson B, Tillbom M, Ekvall K (1998) Male-biased investment in fallow deer: an experimental study. Anim Behav 56:301-307
30. Bowman JE, Lee PC (1995) Growth and threshold weaning weights among captive rhesus macaques. Am J Phys Anthropol 96:159-175
31. Broadhurst PL, Jinks JL (1965) Parity as a determinant of birth weight in the rhesus monkey. Folia Primatol 3:201-210
32. Bulger J, Hamilton WJ III (1988) Inbreeding and reproductive success in a natural chacma baboon, Papio cynocephalus ursinus, population. Anim Behav 36:574-578
33. Cameron EZ (1998) Is suckling behaviour a useful predictor of milk intake? Anim Behav 56:521-532
34. Clark AB (1978) Sex ratio and local resource competition in a prosimian primate. Science 201:163-165
35. Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton
36. Clutton-Brock TH (1994) The costs of sex. In: Short RV, Balaban E (eds) The differences between the sexes. Cambridge University Press, Cambridge, UK, pp 347-362
37. Clutton-Brock TH, Iason GR (1986) Sex ratio variation in mammals. Q Rev Biol 61:339-374
38. Colvin JD (1986) Proximate causes of male emigration at puberty in rhesus monkeys. In: Rawlins RG, Kessler MJ (eds), The Cayo Santiago macaques. SUNY, Albany, NY, pp 131-157
39. Darwin CR (1871) The descent of man and selection in relation to sex. Murray, London
40. De Ruiter JR, Scheffrahn W, Trommelen GJJM, Uitterlinden AG, Martin RD, Hooff JARAM van (1992) Male social rank and reproductive success in wild long-tailed macaques: paternity exclusions by blood protein analysis and DNA fingerprinting. In: Martin RD, Dixson AF, Wickings EJ (eds) Paternity in primates: genetic tests and theories. Karger, Basel, pp 175-191
41. DiGiacomo RF, Shaughnessy PW (1972) Estimation of gestational age and birth weight in the rhesus monkey (Macaca mulatta). Am J Obstet Gynecol 112:519-628
42. DiGiacomo RF, Shaughnessy PW, Tomlin SL (1978) Fetal-placental weight relationships in the rhesus (Macaca mulatta). Biol Reprod 17:749-753
43. Dittus WPJ (1998) Birth sex ratios in toque macaques and other mammals: integrating the effects of maternal condition and competition. Behav Ecol Sociobiol 44:149-160
44. Dixson AF, Nevison CM (1997) The socioendocrinology of adolescent development in male rhesus monkeys (Macaca mulatta). Horm Behav 31:126-135
45. Dunbar RIM (1988) Primate social systems. Comstock, Ithaca
46. Dunbar RIM (1990) Environmental determinants of intraspecific variation in body weight in baboons (Papio spp.). J Zool (Lond) 220:157-169
47. Fairbanks LA, McGuire MT (1995) Maternal condition and the quality of maternal care in vervet monkeys. Behaviour 132: 733-754
48. Fisher RA (1930) The genetical theory of natural selection. Clarendon, Oxford
49. Frank SA (1990) Sex allocation theory for birds and mammals. Annu Rev Ecol Syst 21:13-55
50. Gomendio M (1990) 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
51. Gomendio M (1995) Maternal styles in Old World primates: their adaptive significance. In: Pryce CR, Martin RD, Skuse D (eds) Motherhood in human and nonhuman primates. Karger, Basel, pp 59-68
52. Goy RW, Bercovitch FB, McBrair MC (1988) Behavioral masculinization is independent of genital masculinization in prenatally androgenized female rhesus macaques. Horm Behav 22:552-571
53. Hamilton WD (1967) Extraordinary sex ratios. Science 156: 477-488
54. Hamilton WJ III, McNutt JW (1997) Determinants of conflict outcomes. In: Owings DH, Beecher MD, Thompson NS (eds) Perspectives in ethology. Plenum, New York, pp 179-224
55. Hardy ICW (1997) Possible factors influencing vertebrate sex ratios: an introductory overview. Appl Anim Behav Sci 51:217-241
56. Hauser MD (1988) Variation in maternal responsiveness in free-ranging vervet monkeys: a response to infant mortality risk? Am Nat 131:573-587
57. Hauser MD, Fairbanks LA (1988) Mother-offspring conflict in vervet monkeys: variation in response to ecological conditions. Anim Behav 36:802-813
58. Hewison AJM, Gaillard J-M (1999) Successful sons or advantaged daughters? The Trivers-Willard model and sex-biased maternal investment in ungulates. Trends Ecol Evol 14: 229-234
59. Hiraiwa-Hasegawa M (1993) Skewed birth sex ratios in primates: should high-ranking mothers have daughters or sons? Trends Ecol Evol 8:395-400
60. Hoogland JE (1995) The black-tailed prairie dog. University of Chicago Press, Chicago
61. Hrdy SB (1987) Sex-biased parental investment among primates and other mammals: a critical evaluation of the Trivers-Willard hypothesis. In: Gelles R, Lancaster JB (eds) Child abuse and neglect: biosocial dimensions. Aldine, New York, pp 97-147
62. Johnson CN (1988) Dispersal and the sex ratio at birth in primates. Nature 332:726-728
63. Johnson RL, Southwick CH (1987) Ecological constraints on the development of infant independence in rhesus. Am J Primatol 13:103-118
64. Kaplan JR (1977) Patterns of fight interference in free-ranging rhesus monkeys. Am J Phys Anthropol 47:279-288
65. Kayser M, Nürnberg P, Bercovitch F, Nagy J, Roewer L (1995) Increased microsatellite variability in Macaca mulatta compared to humans due to a large scale deletion/insertion event during primate evolution. Electrophoresis 16:1607-1611
66. Kayser M, Ritter H, Bercovitch F, Mrug M, Roewer L, Nürnberg P (1996) Identification of highly polymorphic microsatellites in the rhesus macaque Macaca mulatta by cross-species amplification. Mol Ecol 5:157-159
67. Keane B, Waser PH, Creel SR, Creel NM, Elliott LF, Minchella DJ (1994) Subordinate reproduction in dwarf mongooses. Anim Behav 47:65-75
68. Knapton RW (1984) Parental investment: the problem of currency. Can J Zool 62:2673-2674
69. Koenig WD, Pitelka FA, Carmen WJ, Mumme RL, Stanback MT (1992) The evolution of delayed dispersal in cooperative breeders. Q Rev Biol 67:111-150
70. Koford CB (1963) Rank of mothers and sons in bands of rhesus monkeys. Science 141:356-357
71. Krackow S (1995) Potential mechanisms for sex ratio adjustment in mammals and birds. Biol Rev 70:225-241
72. Krackow S (1997) Maternal investment, sex-differential prospects, and the sex ratio in wild house mice. Behav Ecol Sociobiol 41:435-443
73. Künkele J, Kenagy GJ (1997) Inefficiency of lactation in primiparous rats: the costs of first reproduction. Physiol Zool 70: 571-577
74. Lee PC (1984) Ecological constraints on the social development of vervet monkeys. Behaviour 91:245-262
75. Lee PC (1987) Nutrition, fertility and maternal investment in primates. J Zool (Lond) 213:409-422
76. Malik I, Johnson RL, Berman CM (1992) Control of postpartum mating behaviour in free-ranging rhesus monkeys. Am J Primatol 26:89-95
77. Marriott BM (1988) Time budgets of rhesus monkeys (Macaca mulatta) in a forest habitat in Nepal and on Cayo Santiago. In: Fa J, Southwick CH (eds) Ecology and behaviour of food-enhanced primate groups. Liss, New York, pp 125-149
78. Martin DP (1984) The effects of extended time in the laboratory on selected aspects of reproduction in the female rhesus monkey (Macaca mulatta). Am J Primatol 7:39-55
79. Maynard Smith J (1980) A new theory of sexual investment. Behav Ecol Sociobiol 7:247-251
80. Meikle DB, Vessey SH (1988) Maternal dominance rank and lifetime survivorship of male and female rhesus monkeys. Behav Ecol Sociobiol 22:379-383
81. Meikle DB, Tilford BL, Vessey SH (1984) Dominance rank, secondary sex ratio, and reproduction of offspring in polygynous primates. Am Nat 124:173-188
82. 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. University of Chicago Press, Chicago, pp 121-134
83. Mori A (1979) Analysis of population changes by measurement of body weight in the Koshima troop of Japanese monkeys. Primates 20:371-398
84. Moses RA, Boutin S, Teferi T (1998) Sex-biased mortality in woodrats occurs in the absence of parental intervention. Anim Behav 55:563-571
85. Myers JH (1978) Sex ratio adjustment under food stress: maximization of quality or numbers of offspring. Am Nat 112:381-388
86. Nevison CM, Rayment FDG, Simpson MJA (1996) Birth sex ratios and maternal social rank in a captive colony of rhesus macaques (Macaca mulatta). Am J Primatol 39:123-138
87. Noordwijk MA van, Schaik CP van (1999) The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques, Macaca fascicularis. Primates 40:105-130
88. Norman A, Litwack J (1997) Hormones. Academic Press, San Diego
89. Nürnberg P, Berard JD, Bercovitch F, Epplen JT, Schmidtke J, Krawczak M (1993) Oligonucleotide fingerprinting of free-ranging and captive rhesus macaques from Cayo Santiago: paternity assignment and comparison of heterozygosity. In: Pena SDJ, Chakraborty R, Epplen JT, Jeffreys AJ (eds) DNA fingerprinting: state of the science. Birkhauser, Basel, pp 445-451
90. Nürnberg P, Sauermann U, Kayser M, Lanfer C, Manz E, Widdig A, Berard J, Bercovitch FB, Kessler MJ, Schmidtke J, Krawczak M (1998) Paternity assessment in rhesus macaques (Macaca mulatta): multilocus DNA fingerprinting and PCR marker typing. Am J Primatol 44:1-18
91. Ono KA, Boness DJ (1996) Sexual dimorphism in sea lion pups: differential maternal investment, or sex-specific differences in energy allocation? Behav Ecol Sociobiol 38:31-41
92. Packer C (1979) Inter-troop transfer and inbreeding avoidance in Papio anubis. Anim Behav 27:1-36
93. Paul A, Kuester J (1990) Adaptive significance of sex ratio adjustment in semifree-ranging Barbary macaques (Macaca sylvanus) at Salem. Behav Ecol Sociobiol 27:287-293
94. Paul A, Kuester J (1996) Differential reproduction in Barbary macaques. In: Fa JE, Lindburg DG (eds) Evolution and ecology of macaque societies. Cambridge University Press, Cambridge, UK, pp 293-317
95. Paul A, Kuester J, Arnemann J (1992) Maternal rank affects reproductive success of male Barbary macaques (Macaca sylvanus): evidence from DNA fingerprinting. Behav Ecol Sociobiol 30:337-341
96. Pianka ER, Parker WS (1975) Age-specific reproductive tactics. Am Nat 109:453-464
97. Pope TR (1992) The influence of dispersal patterns and mating system on genetic differentiation within and between populations of the red howler monkey (Alouatta seniculus). Evolution 46:1112-1128
98. Ralls K (1977) Sexual dimorphism in mammals: avian models and unanswered questions. Am Nat 111:917-938
99. Rawlins RG, Kessler MJ (1986a) The history of the Cayo Santiago colony. In: Rawlins RG, Kessler MJ (eds) The Cayo Santiago macaques. SUNY Press, Albany, NY, pp 13-45
100. Rawlins RG, Kessler MJ (1986b) Demography of the free-ranging Cayo Santiago macaques. In: Rawlins RG, Kessler MJ (eds) The Cayo Santiago macaques. SUNY Press, Albany, NY, pp 47-72
101. Rawlins RG, Kessler MJ (1986c) Secondary sex ratio variation in the Cayo Santiago macaque population. Am J Primatol 10:9-23
102. Rawlins RG, Kessler MJ, Turnquist JT (1984) Reproductive performance, population dynamics and anthropometries of the free-ranging Cayo Santiago rhesus macaques. J Med Primatol 13:247-259
103. Resko JA, Ellinwood WE (1981) Testicular hormone production in fetal rhesus macaques. In: Novy MJ, Resko JA (eds) Fetal endocrinology. Academic Press, New York, pp 253-269
104. Reznick D (1985) Costs of reproduction: an evaluation of the empirical evidence. Oikos 44:257-267
105. Reznick D (1992) Measuring the costs of reproduction. Trends Ecol Evol 7:42-45
106. Roonwal ML, Mohnot SM (1977) Primates of South Asia. Harvard University Press, Cambridge, Mass
107. Sade DS (1967) Determinants of dominance in a group of free-ranging rhesus monkeys. In: Altmann SA (ed) Social communication among primates. University of Chicago Press, Chicago, pp 99-114
108. Sade DS, Chepko-Sade BD, Schneider JM, Roberts SS, Richtsmeier JT (1985) Basic demographic observations on free-ranging rhesus monkeys. Human Relations Area Files, New Haven
109. Schaik CP van, Hrdy SB (1991) Intenstity of local resource competition shapes the relationship between maternal rank and sex ratios at birth in cercopithecine primates. Am Nat 138:1555-1562
110. Schulman SR, Chapais B (1980) Reproductive value and rank relations among macaque sisters. Am Nat 115:580-593
111. Schwartz SM, Kemnitz JW (1992) Age- and gender-related changes in body size, adiposity, and endocrine and metabolic parameters in free-ranging rhesus macaques. Am J Phys Anthropol 89:109-121
112. Silk JB (1983) Local resource competition and facultative adjustment of sex ratios in relation to competitive abilities. Am Nat 121:56-66
113. Silk JB (1988) Maternal investment in captive bonnet macaques, Macaca radiata. Am Nat 132:1-19
114. Silk JB, Short J, Roberts J, Kusnitz J (1993) Gestation length in rhesus macaques (Macaca mulatta). Int J Primatol 14:95-104
115. Simpson MJA, Simpson AE (1982) Birth sex ratios and social rank in rhesus monkey mothers. Nature 300:440-441
116. Simpson MJA, Simpson AE, Hooley J, Zunz M (1981) Infant related influences on birth intervals in rhesus monkeys. Nature 290:49-51
117. Small MF, Hrdy SB (1986) Secondary sex ratios by maternal rank, parity, and age in captive rhesus macaques (Macaca mulatta). Am J Primatol 11:359-365
118. Small MF, Smith DG (1986) The influence of birth timing upon infant growth and survival in captive rhesus macaques (Macaca mulatta). Int J Primatol 7:289-304
119. Smith DG, Smith S (1988) Parental rank and reproductive success of natal rhesus males. Anim Behav 36:554-562
120. Smuts BB (1985) Sex and friendship in baboons. Aldine, Hawthorne, NY
121. Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. Freeman. New York
122. Solomon NG, French JA (eds) (1997) Cooperative breeding in mammals. Cambridge University Press, Cambridge, UK
123. Stockley P, Searle JB, MacDonald DW, Jones CS (1993) Female multiple mating behaviour in the common shrew as a strategy to reduce inbreeding. Proc R Soc Lond B, 254:173-179
124. Strum SC (1994) Reconciling aggression and social manipulation as means of competition. I. Life-history perspective. Int J Primatol 15:739-765
125. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136-179
126. Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90-92
127. Wagenen G van, Catchpole HR (1956) Physical growth of the rhesus monkey (Macaca mulatta). Am J Phys Anthropol 14: 245-273
128. Walters JR, Seyfarth RM (1987) Conflict and cooperation. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago, pp 306-317
129. Wasser SK, Norton GW (1993) Baboons adjust secondary sex ratio in response to predictors of sex-specific offspring survival. Behav Ecol Sociobiol 32:273-281
130. Williams GC (1979) The question of adaptive sex ratio in out-crossed vertebrates. Proc R Soc Lond B 205:567-580
131. Wilson ME, Walker ML, Gordon TP (1983) Consequences of first pregnancy in rhesus monkeys. Am J Phys Anthropol 61: 103-110