Testing the priority-of-access model in a seasonally breeding primate species

Behavioral Ecology and Sociobiology

Volumn 65, Issue 8, 2011, Pages 1615-1627

  Dubuc, Constance ^a,b,c,d   Muniz, Laura ^c   Heistermann, Michael ^a   Engelhardt, Antje ^a,d   Widdig, Anja ^c,e  

^a GERMAN PRIMATE CENTER   (Germany)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

^c MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^d UNIVERSITY OF GÖTTINGEN   (Germany)

^e UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Dominance; Genetic paternity analysis; Mating skew; Primates; Priority of access model; Reproductive skew; Rhesus macaques

Indexed keywords

BREEDING POPULATION; DOMINANCE; ECOLOGICAL MODELING; FIGHTING; GENETIC ANALYSIS; HORMONE; MALE BEHAVIOR; MATE LOCATION; MODEL TEST; PATERNITY; PRIMATE; RANKING; REPRODUCTIVE STRATEGY; REPRODUCTIVE SUCCESS; SOCIAL BEHAVIOR; SYNCHRONY;

CAYO SANTIAGO; PUERTO RICO;

MACACA; MACACA MULATTA; MAMMALIA; POA; PRIMATES;

EID: 79960186093     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-011-1172-8     Document Type: Article

References (97)

1. Alberts SC, Buchan JC, Altmann J (2006) Sexual selection in wild baboons: from mating opportunities to paternity success. Anim Behav 72: 1177-1196.
2. Alberts SC, Watts HE, Altmann J (2003) Queuing and queue-jumping: long-term patterns of reproductive skew in male savannah baboons, Papio cynocephalus. Anim Behav 65: 821-840.
3. Altmann J (1974) Observational study of behaviour: sampling methods. Behaviour 49: 227-267.
4. Altmann SA (1962) A field study of the sociobiology of rhesus monkeys, Macaca mulatta. Ann N Y Acad Sci 102: 338-435.
5. Andersson M (1994) Sexual selection. Princeton University Press, Princeton.
6. Bates D, Maechler M (2010) lme4: linear mixed-effects models using S4 classes. R package version 0. 999375-34 http://CRAN. R-project. org/package=lme4. Accessed 10 March 2011.
7. Baulu J (1976) Seasonal sex skin coloration and hormonal fluctuations in free-ranging and captive monkeys. Horm Behav 7: 481-494.
8. Behboodi E, Katz DF, Samuels SJ, Tell L, Hendrickx AG, Lasley BL (1991) The use of a urinary estrone conjugate assay for detection of optimal mating time in the cynomologus macaque (Macaca fascicularis). J Med Primatol 20: 229-234.
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. Berard JD, Nuernberg P, Epplen JT, Schmidtke J (1993) Male rank, reproductive behavior, and reproductive success in free-ranging rhesus macaques. Primates 34: 481-489.
11. Bercovitch F, Harvey NC (2004) Reproductive life history. In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: a model for the study of social organization. Cambridge University Press, Cambridge, pp 61-79.
12. Bercovitch FB (1992a) Re-examining the relationship between rank and reproduction in male primates. Anim Behav 44: 1168-1170.
13. Bercovitch FB (1992b) Sperm competition, reproductive tactics, and paternity in savanna baboons and rhesus macaques. In: Martin RD, Dixson AF, Wickings EJ (eds) Paternity in primates: genetic tests and theories. Karger, Basel, pp 225-237.
14. Bercovitch FB (1997) Reproductive strategies of rhesus macaques. Primates 38: 247-263.
15. Bercovitch FB, Nürnberg P (1996) Socioendocrine and morphological correlates of paternity in rhesus macaques (Macaca mulatta). J Reprod Fertil 107: 59-68.
16. Bercovitch FB, Nürnberg P (1997) Genetic determination of paternity and variation in male reproductive success in two populations of rhesus macaques. Electrophoresis 18: 1701-1705.
17. Bercovitch FB, Rodriguez JF (1993) Testis size, epididymis weight, and sperm competition in rhesus macaques. Am J Primatol 30: 163-168.
18. Bercovitch FB, Widdig A, Trefilov A, Kessler MJ, Berard JD, Schmidtke J, Nuernberg P, Krawczak M (2003) A longitudinal study of age-specific reproductive output and body condition among male rhesus macaques, Macaca mulatta. Naturwissenschaften 90: 309-312.
19. Birkhead T, Kappeler PM (2004) Post-copulatory sexual selection in birds and primates. In: Kappeler PM, van Schaik CP (eds) Sexual selection in primates: new and comparative perspectives. Cambridge University Press, New York, pp 151-171.
20. Bissonnette A, Bischofberger N, van Schaik C (2011) Mating skew in Barbary macaque males: the role of female mating synchrony, female behavior, and male-male coalitions. Behav Ecol Sociobiol 65: 167-182.
21. Boesch C, Kohou G, Nene H, Vigilant L (2006) Male competition and paternity in wild chimpanzees of the Tai forest. Am J Phys Anthropol 130: 103-115.
22. Brauch K, Pfefferle D, Hodges K, Möhle U, Fischer J, Heistermann M (2007) Female sexual behavior and sexual swelling size as potential cues for males to discern the female fertile phase in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar. Horm Behav 52: 375-383.
23. Brent LJN, Semple S, Dubuc C, Heistermann M, MacLarnon A (2011) Social capital and physiological stress levels in adult female rhesus macaques. Physiol Behav 102: 76-83.
24. Callen DF, Thompson AD, Shen Y, Phillips HA, Richards R, Mulley JC, Sutherland GR (1993) Incidence and origin of "null" alleles in the (AC)n microsatellite markers. Am J Hum Genet 52: 922-927.
25. Chapais B (1983) Reproductive activity in relation to male dominance and the likelihood of ovulation in rhesus monkeys. Behav Ecol Sociobiol 12: 215-228.
26. Clutton-Brock TH, Harvey PH (1976) Evolutionary rules and primate societies. In: Bateson PPG, Hinde RA (eds) Growing points in ethology. Cambridge University Press, Cambridge, pp 195-237.
27. Clutton-Brock TH, McAuliffe K (2009) Female mate choice in mammals. Q Rev Biol 84: 3-27.
28. Cowlishaw G, Dunbar RIM (1991) Dominance rank and mating success in male primates. Anim Behav 41: 1045-1056.
29. Darwin C (1871) The descent of man and selection in relation to sex. J. Murray, London.
30. de Vries H (1995) An improved test of linearity in dominance hierarchies containing unknown or tied relationships. Anim Behav 50: 1375-1389.
31. de Vries H (1998) Finding a dominance order most consistent with a linear hierarchy: a new procedure and review. Anim Behav 55: 827-843.
32. Dewsbury DA (1982) Dominance rank, copulatory behavior, and differential reproduction. Q Rev Biol 57: 135-159.
33. Dixson AF (1998) Primate sexuality: comparative studies of the prosimians, monkeys, apes, and human beings. Oxford University Press, Oxford.
34. Dubuc C, Brent LJN, Accamando AK, Gerald MS, MacLarnon A, Semple S, Heistermann M, Engelhardt A (2009) Sexual skin color contains information about the timing of the fertile phase in free-ranging Macaca mulatta. Int J Primatol 30: 777-789.
35. Ellis L (1995) Dominance and reproductive success among nonhuman animals: a cross-species comparison. Ethol Sociobiol 16: 257-333.
36. Emlen ST, Oring LW (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197: 215-223.
37. Engelhardt A, Heistermann M, Hodges JK, Nuernberg P, Niemitz C (2006) Determinants of male reproductive success in wild long-tailed macaques (Macaca fascicularis)-male monopolisation, female mate choice or post-copulatory mechanisms? Behav Ecol Sociobiol 59: 740-752.
38. Engh AL, Funk SM, van Horn RC, Scribner KT, Bruford MW, Libants S, Szykman M, Smale L, Holekampa KE (2002) Reproductive skew among males in a female-dominated mammalian society. Behav Ecol 13: 193-200.
39. Fooden J (2000) Systematic review of the rhesus macaque, Macaca mulatta (Zimmermann, 1780). Fieldiana: Zool 96: 1-180.
40. Harcourt AH, Purvis A, Liles L (1995) Sperm competition: mating system, not breeding system, affects testes size of primates. Funct Ecol 9: 468-476.
41. Hausfater G (1975) Dominance and reproduction in baboons (Papio cynocephalus): quantitative analysis. Contrib Primatol 7: 2-150.
42. Hayakawa S (2007) Female defensibility in small troops of Japanese macaques vis-a-vis nontroop males and copulation on the periphery of the troop. Int J Primatol 28: 73-96.
43. Heistermann M, Brauch K, Moehle U, Pfefferle D, Dittami J, Hodges K (2008) Female ovarian cycle phase affects the timing of male sexual activity in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar. Am J Primatol 70: 44-53.
44. Hirotani A (1994) Dominance rank, copulatory behaviour and estimated reproductive success in male reindeer. Anim Behav 48: 929-936.
45. Hoffman CL, Ruiz-Lambides AV, Davila E, Maldonado E, Gerald MS, Maestripieri D (2008) Sex differences in survival costs of reproduction in a promiscuous primate. Behav Ecol Sociobiol 62: 1711-1718.
46. Inoue M (1995) Application of paternity discrimination by DNA polymorphism to the analysis of the social behavior of primates. Hum Evol 10: 53-62.
47. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16: 1099-1106.
48. Kutsukake N, Nunn CL (2006) Comparative tests of reproductive skew in male primates: the roles of demographic factors and incomplete control. Behav Ecol Sociobiol 60: 695-706.
49. Lindburg DG (1983) Mating behavior and estrus in the Indian rhesus monkey. In: Seth PK (ed) Perspectives in primate ecology. Today & Tomorrow's Printers and Publishers, New Delhi, pp 45-61.
50. Manson JH (1992) Measuring female mate choice in Cayo Santiago rhesus macaques. Anim Behav 44: 405-416.
51. Manson JH (1995) Do female rhesus macaques choose novel males? Am J Primatol 37: 285-296.
52. Manson JH (1996) Male dominance and mount series duration in Cayo Santiago rhesus macaques. Anim Behav 51: 1219-1231.
53. Manson JH (1997) Primate consortships: a critical review. Curr Anthropol 38: 353-374.
54. Manson JH, Perry SE (1993) Inbreeding avoidance in rhesus macaques: whose choice? Am J Phys Anthropol 90: 285-288.
55. Martin P, Bateson P (1986) Measuring behaviour: an introductory guide. Cambridge University Press, Cambridge.
56. Matsubara M (2003) Costs of mate guarding and opportunistic mating among wild male Japanese macaques. Int J Primatol 24: 1057-1075.
57. McMillan CA (1989) Male age, dominance, and mating success among rhesus macaques. Am J Phys Anthropol 80: 83-89.
58. Ménard N (2004) Do ecological factors explain variation in social organization? In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: a model for the study of social organization. Cambridge University Press, New York, pp 237-262.
59. Møller AP, Mousseau TA, Rudolfsen G, Balbontín J, Marzal A, Hermosell I, De Lope F (2009) Senescent sperm performance in old male birds. J Evol Biol 22: 334-344.
60. Nonacs P (2000) Measuring and using skew in the study of social behavior and evolution. Am Nat 156: 577-589.
61. Nonacs P (2003) Measuring the reliability of skew indices: is there one best index? Anim Behav 65: 615-627.
62. Nürnberg P, Sauermann U, Kayser M, Lanfer C, Manns E, Widdig A, Berard J, Bercovitch FB, Kessler M, 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.
63. Ostner J, Nunn CL, Schuelke O (2008) Female reproductive synchrony predicts skewed paternity across primates. Behav Ecol Sociobiol 19: 1150-1158.
64. Paul A (1997) Breeding seasonality affects the association between dominance and reproductive success in non-human male primates. Folia Primatol (Basel) 68: 344-349.
65. Paul A (2004) Dominance and paternity. In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: a model for the study of social organization. Cambridge University Press, New York, pp 131-134.
66. Phoenix CH, Chambers KC (1988) Old age and sexual exhaustion in male rhesus macaques. Physiol Behav 44: 157-163.
67. Plavcan JM (2004) Sexual selection, measures of sexual selection, and sexual dimorphism in primates. In: Kappeler PM, van Schaik CP (eds) Sexual selection in primates: new and comparative perspectives. Cambridge University Press, New York, pp 230-252.
68. Plavcan JM, van Schaik CP (1992) Intrasexual competition and canine dimorphism in anthropoid primates. Am J Phys Anthropol 87: 461-477.
69. Port M, Kappeler PM (2010) The utility of reproductive skew models in the study of male primates, a critical evaluation. Evol Anthropol 19: 46-56.
70. R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.
71. Rawlins RG, Kessler MJ (1986) The history of the Cayo Santiago colony. In: Rawlins RG, Kessler MJ (eds) The Cayo Santiago macaques: history, behavior and biology. State University of New York Press, Albany, pp 13-45.
72. Reeder DM (2003) The potential for cryptic female choice in primates: behavioral, anatomical, and physiological considerations. In: Jones CB (ed) Sexual selection and reproductive competition in primates: new perspectives and directions. American Society of Primatologists, Norman, pp 255-303.
73. Rhodes L, Argersinger ME, Gantert LT, Friscino BH, Hom G, Pikounis B, Hess DL, Rhodes WL (1997) Effects of administration of testosterone, dihydrotestosterone, oestrogen and fadrozole, and aromatase inhibitor, on sex skin colour in intact male rhesus macaques. J Reprod Fertil 111: 51-57.
74. Rodriguez-Llanes JM, Verbeke G, Finlayson C (2009) Reproductive benefits of high social status in male macaques (Macaca). Anim Behav 78: 643-649.
75. 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 Primatol 89: 109-121.
76. Setchell JM, Charpentier M, Wickings J (2005) Mate guarding and paternity in mandrills: factors influencing alpha male monopoly. Anim Behav 70: 1105-1120.
77. Setchell JM, Wickings EJ (2006) Mate choice in male mandrills (Mandrillus sphinx). Ethol Sociobiol 112: 91-99.
78. Seth PK, Seth S (1986) Ecology and behavior of rhesus monkeys in India. In: Else JG, Lee PC (eds) Primate ecology and conservation, vol 2. Cambridge University Press, Cambridge, pp 192-305.
79. Silk J, Short J, Roberts J, Kusnitz J (1993) Gestation length in rhesus macaques (Macaca mulatta). Int J Primatol 14: 95-104.
80. Singh M, Sinha A (2004) Life-history traits: ecological adaptations or phylogenetic relics? In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: a model for the study of social organization. Cambridge University Press, New York, pp 80-83.
81. Sloter E, Schmid TE, Marchett F, Eskenazi B, Nath J, Wyrobek AJ (2006) Quantitative effects of male age on sperm motion. Hum Reprod 21: 2868-2875.
82. Smith DG (1994) Male dominance and reproductive success in a captive group of rhesus macaques (Macaca mulatta). Behaviour 129: 225-242.
83. Soltis J (2004) Mating systems. In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: a model for the study of social organization. Cambridge University Press, New York, pp 135-151.
84. Soltis J, Mitsunaga F, Shimizu K, Nozaki M, Yanagihara Y, Domingo-Roura X, Takenaka O (1997) Sexual selection in Japanese macaques II: female mate choice and male-male competition. Anim Behav 54: 737-746.
85. Soltis J, Mitsunaga F, Shizumi K, Yanagihara Y, Nozaki M (1999) Female mating strategy in an enclosed group of Japanese macaques. Am J Primatol 47: 263-278.
86. Southwick CH, Yongzu Z, Haisheng J, Zhenhe L, Wenyuan Q (1996) Population ecology of rhesus macaques in tropical and temperate habitats in China. In: Fa JE, Lindburg DG (eds) Evolution and ecology of macaque societies. Cambridge University Press, Cambridge, pp 95-105.
87. Takahata Y, Huffman MA, Suzuki S, Koyama N, Yamagiwa J (1999) Why dominants do not consistently attain high mating and reproductive success: a review of longitudinal Japanese macaque studies. Primates 40: 143-158.
88. van Noordwijk MA, van Schaik CP (2001) Career moves: transfer and rank challenge decisions by male long-tailed macaques. Behaviour 138: 359-395.
89. van Noordwijk MA, van Schaik CP (2004) Sexual selection and the careers of primate males: paternity concentration, dominance-acquisition tactics and transfer decisions. In: Kappeler PM, van Schaik CP (eds) Sexual selection in primates: new and comparative perspectives. Cambridge University Press, Cambridge, pp 208-229.
90. Waitt C, Little AC, Wolfensohn S, Honess P, Brown AP, Buchanan-Smith HM, Perrett DI (2003) Evidence from rhesus macaques suggests that male coloration plays a role in female primate mate choice. Proceedings of the Royal Society of London B270: S144-S146.
91. Weingrill T, Lycett JE, Barrett L, Hill RA, Henzi SP (2003) Male consortship behaviour in chacma baboons: the role of demographic factors and female conceptive probabilities. Behaviour 140: 405-427.
92. Whitehead H (2009a) Programs for analyzing social structure. SOCPROG Users' Manual.
93. Whitehead H (2009b) SOCPROG programs: analyzing animal social structures. Behav Ecol Sociobiol 63: 765-778.
94. Widdig A, Bercovitch FB, Streich WJ, Sauermann U, Nuernberg P, Krawczak M (2004) A longitudinal analysis of reproductive skew in male rhesus macaques. Proceedings of the Royal Society of London B271: 819-826.
95. Widdig A, Nuernberg P, Krawczak M, Streich WJ, Bercovitch F (2002) Affiliation and aggression among adult female rhesus macaques: a genetic analysis of paternal cohorts. Behaviour 139: 371-391.
96. Wilcox AJ, Weinberg CR, Baird DD (1995) Timing of sexual intercourse in relation to ovulation. N Engl J Med 333: 1517-1522.
97. Wroblewski EE, Murray CM, Keele BF, Schumacher-Stankey JC, Hahn BH, Pusey AE (2009) Male dominance rank and reproductive success in chimpanzees, Pan troglodytes schweinfurthii. Anim Behav 77: 873-885.