You mate, I mate: Macaque females synchronize sex not cycles

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Fürtbauer, Ines ^a,b,c   Mundry, Roger ^b   Heistermann, Michael ^c   Schülke, Oliver ^a,b   Ostner, Julia ^a,b  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b MAX PLANCK INSTITUTE FOR EVOLUTIONARY ANTHROPOLOGY   (Germany)

^c GERMAN PRIMATE CENTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; COPULATION; FEMALE; HORMONAL REGULATION; MACACA; MATING; MATING TYPE; MOUSE; NONHUMAN; OVARY CYCLE; OVARY FUNCTION; SEXUAL BEHAVIOR; SEXUAL FUNCTION; SOCIAL BEHAVIOR;

ANIMALS; COPULATION; FEMALE; MACACA; MALE; MENSTRUAL CYCLE; SEXUAL BEHAVIOR, ANIMAL;

MACACA; MACACA ASSAMENSIS; PRIMATES;

EID: 80053977907     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0026144     Document Type: Article

References (79)

1. Arnqvist G, Nilsson, T, (2000) The evolution of polyandry: multiple mating and female fitness in insects. Animal Behavior 60: 145-164.
2. Hrdy SB, (1979) Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethology and Sociobiology 1: 13-40.
3. Hrdy SB, (2000) The optimal number of fathers: evolution, demography, and history in the shaping of female mate preferences. Annals of the New York Academy of Sciences 907: 75-96.
4. Gangestad SW, Thornhill R, (2008) Human oestrus. Proceedings of the Royal Society B 275: 991-1000.
5. Rodriguez-Gironés MA, Enquist M, (2001) The evolution of female sexuality. Animal Behavior 61: 695-704.
6. Soltis J, (2002) Do primate females gain nonprocreative benefits by mating with multiple males? Theoretical and empirical considerations. Evolutionary Anthropology 11: 187-197.
7. Thornhill R, Gangestad SW, (2008) The Evolutionary Biology of Human Female Sexuality. New York, NY Oxford University Press.
8. Birkhead TR, Møller AP, (1992) Sperm competition in birds. London Academic press.
9. Borries C, Launhardt K, Epplen C, Epplen JT, Winkler P, (1999) Males as infant protectors in Hanuman langurs (Presbytis entellus) living in multimale groups: defence, paternity and sexual behaviour. Behavioral Ecology and Sociobiology 46: 350-356.
10. Heistermann M, Ziegler T, van Schaik CP, Launhardt K, Winkler P, et al. (2001) Loss of oestrus, concealed timing of ovulation and paternity confusion in free-ranging Hanuman langurs. Proceedings of the Royal Society B 268: 2445-2451.
11. Van Schaik CP, Hodges KJ, Nunn C, (2000) Paternity confusion and the ovarian cycles of female primates. In: van Schaik CP, Janson CH, editors. Infanticide by Males and its Consequences Cambridge Cambridge University Press pp. 361-387.
12. Van Schaik CP, Pradhan GR, van Noordwijk MA, (2004) Mating conflict in primates: infanticide, sexual harassment and female sexuality. In: Kappeler PM, van Schaik CP, editors. Sexual Selection in Primates Cambridge New and Comparative Perspectives. Cambridge University Press pp. 131-150.
13. Van Schaik CP, van Noordwijk MA, Nunn CL, (1999) Sex and social evolution in primates. In: Lee PC, editors. Comparative Primate Socioecology Cambridge Cambridge University Press pp. 204-231.
14. Altmann SA, (1962) A field study of the sociobiology of rhesus monkeys, Macaca mulatta. Annals of the New York Academy of Sciences 102: 338-435.
15. Cowlishaw G, Dunbar RIM, (1991) Dominance rank and mating success in male primates. Animal Behavior 41: 1045-1056.
16. Emlen ST, Oring LW, (1977) Ecology, sexual selection, and the evolution of mating systems. Science 197: 215-223.
17. Ims RA, (1988) The potential for sexual selection in males: effect of sex ratio and spatiotemporal distribution of receptive females. Evolutionary Ecology 2: 338-352.
18. Ims RA, (1990) The ecology and evolution of reproductive synchrony. Trends in Ecology and Evolution 5: 135-140.
19. Kutsukake N, Nunn CL, (2006) Comparative tests of reproductive skew in male primates: the roles of demographic factors and incomplete control. Behavioral Ecology and Sociobiology 60: 695-706.
20. Nunn CL, (1999) The number of males in primate social groups: a comparative test of the socioecological model. Behavioral Ecology and Sociobiology 46: 1-13.
21. Ostner J, Nunn C, Schülke O, (2008) Female reproductive synchrony predicts skewed paternity across primates. Behavioral Ecology 19: 1150-1158.
22. Ridley M, (1986) The number of males in a primate troop. Animal Behavior 34: 1848-1858.
23. Eberhard WG, (1996) Female Control: Sexual Selection by Cryptic Female Choice. Princeton, N Princeton University Press.
24. Knowlton N, (1979) Reproductive synchrony, parental investment, and the evolutionary dynamics of sexual selection. Animal Behavior 27: 1022-1033.
25. Brockman DK, van Schaik CP, (2005) Seasonality and reproductive function. In: Brockman DK, van Schaik CP, editors. Seasonality in Primates: Studies of Living and Extinct Human and Non-human Primates Cambridge Cambridge University Press pp. 269-305.
26. Knobil E, Neill JD, (2006) Physiology of Reproduction (3rd Edition). 2 volumes Academic Press.
27. Pereira ME, (1991) Asynchrony within estrous synchrony among ringtailed lemurs (primates, lemuridae). Physiology and Behavior 49: 47-52.
28. Gattermann R, Ulbrich K, Weinandy R, (2002) Asynchrony in the estrous cycles of golden hamsters (Mesocricetus auratus). Hormones and Behavior 42: 70-77.
29. French JA, Stribley JA, (1987) Synchronization of ovarian cycles within and between social groups in golden lion tamarins (Leontopithecus rosalia). American Journal of Primatology 12: 469-478.
30. Handelmann G, Ravizza R, Ray WJ, (1980) Social dominance determines estrous entrainment among female hamsters. Hormones and Behavior 14: 107-115.
31. Matsumoto-Oda A, Hamai M, Hayaki H, Hosaka K, Hunt KD, et al. (2007) Estrus cycle asynchrony in wild female chimpanzees, Pan troglodytes schweinfurthii. Behavioral Ecology and Sociobiology 61: 661-668.
32. McClintock MK, (1971) Menstrual synchrony and suppression. Nature 229: 244-245.
33. McClintock MK, (1978) Estrous synchrony and its mediation by airborne chemical communication (Rattus norvegicus). Hormones and Behavior 10: 264-276.
34. Monfort SL, Bush M, Wildt DE, (1996) Natural and induced ovarian synchrony in golden lion tamarins (Leontopithecus rosalia). Biology of Reproduction 55: 875-882.
35. Setchell JM, Kendal J, Tyniec P, (2010) Do non-human primates synchronise their menstrual cycles? A test in mandrills. Psychoneuroendocrinology 36: 51-59.
36. Tobler R, Pledger S, Linklater W, (2010) No evidence for ovarian synchrony or asynchrony in hamadryas baboons. Animal Behavior 80: 829-837.
37. Wallis J, (1985) Synchrony of estrous swelling in captive group-living chimpanzees (Pan troglodytes). International Journal of Primatology 6: 335-350.
38. Schank JC, (2001) Do Norway rats (Rattus norvegicus) synchronize their estrous cycles? Physiology and Behavior 72: 12-139.
39. Schank JC, (2001) Measurement and cycle variability: reexamining the case for ovarian-cycle synchrony in primates. Behavioural Processes 56: 131-146.
40. Schank JC, (2001) Menstrual-cycle synchrony: problems and new directions for research. Journal of Comparative Psychology 115: 3-15.
41. Strassmann BI, (1997) The biology of menstruation in Homo sapiens: total lifetime menses, fecundity, and nonsynchrony in a natural fertility population. Current Anthropology 38: 123-129.
42. Zinner D, Schwibbe MH, Kaumanns W, (1994) Cycle synchrony and probability of conception in female hamadryas baboons Papio hamadryas. Behavioral Ecology and Sociobiology 35: 175-183.
43. Dixson AF, (1998) Primate Sexuality: Comparative studies of the prosimians, monkeys, apes, and human beings. Oxford Oxford University Press.
44. Wallen K, (1990) Desire and ability: Hormones and the regulation of female sexual behaviour. Neuroscience and Biobehavioral Reviews 14: 233-241.
45. Van Noordwijk MA, van Schaik CP, (2000) Reproductive patterns in eutherian mammals: Adaptations against infanticide? In: van Schaik CP, Janson CH, editors. Infanticide by Males and its Consequences Cambridge Cambridge University Press pp. 322-360.
46. Clarke P, Pradhan G, van Schaik C, (2009) Intersexual Conflict in Primates: Infanticide, Paternity Allocation, and the Role of Coercion. In: Muller MN, Wrangham RW, editors. Sexual coercion in primates and humans: an evolutionary perspective on male aggression against females Harvard University Press pp. 42-80.
47. Deschner T, Heistermann M, Hodges K, Boesch C, (2004) Female sexual swelling size, timing of ovulation, and male behavior in wild West African chimpanzees. Hormones and Behavior 46: 204-215.
48. McClintock MK, (1984) Estrous synchrony: modulation of ovarian cycle length by females pheremone. Physiology and Behavior 32: 701-705.
49. Stern K, McClintock MK, (1998) Regulation of ovulation by human pheromones. Nature 392: 177-189.
50. Russell MJ, Switz GM, Thompson K, (1980) Olfactory influences on the human menstrual cycle. Pharmacology Biochemistry and Behavior 13: 737-738.
51. Coussi-Korbel S, Fragaszy D, (1995) On the relation between social dynamics and social learning. Animal Behavior 50: 1441-1453.
52. Fürtbauer I, Schülke O, Heistermann M, Ostner J, (2010) Reproductive and life history parameters of wild female Macaca assamensis. International Journal of Primatology 31: 501-517.
53. Fürtbauer I, Heistermann M, Schülke O, Ostner J, Concealed fertility and extended female sexuality in a non-human primate (Macaca assamensis). PLoS ONE 6 (8): e23105 (in press) doi:10.1371/journal.pone.0023105.
54. Ostner J, Heistermann M, Schülke O, (2011) Male competition and its hormonal correlates in Assamese macaques (Macaca assamensis). Hormones and Behavior 59: 105-113.
55. van Hooff J, (1967) The facial displays of the catarrhine monkeys and apes. In: Morris D, editors. Primate Ethology London Weidenfeld & Nieholson pp. 7-68.
56. Ostner J, Heistermann M, Schülke O, (2008) Dominance, aggression and physiological stress in wild male Assamese macaques (Macaca assamensis). Hormones and Behavior 54: 613-619.
57. Sokal RR, Rohlf FJ, (1995) Biometry- The Principles and Practice of Statistics in Biological Research, 3rd ed. New York Freeman & Co.
58. Baayen RH, (2008) Analyzing Linguistic Data. Cambridge Cambridge University Press.
59. Burnham KP, Anderson DR, (2002) Model Selection and Multimodel Inference. 2nd ed. Berlin Springer.
60. Dobson AJ, (2002) An Introduction to Generalized Linear Models. Chapman & Hall/CRC, Boca Raton.
61. R Development Core Team 2010 R: A language and environment for statistical computing. R Foundation for Statistical Computing Vienna, Austria.
62. Bates D, Maechler M, (2010) lme4: Linear mixed-effects models using S4 classes. R package version 0.999375-35.
63. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, et al. (2008) Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology and Evolution 24: 127-135.
64. Matsumoto-Oda A, Kasuya E, (2005) Proximity and Estrous Synchrony in Mahale Chimpanzees. American Journal of Primatology 66: 159-166.
65. Radespiel U, Zimmermann E, (2001) Dynamics of Estrous Synchrony in Captive Gray Mouse Lemurs (Microcebus murinus). International Journal of Primatology 22: 71-90.
66. Bercovitch FB, (1987) Female weight and reproductive condition in a population of olive baboons (Papio anubis). American Journal of Primatology 12: 189-195.
67. Maninger N, Sackett GP, Ruppenthal GC, (2000) Weaning, body weight, and postpartum amenorrhea duration in pigtailed macaques (Macaca nemestrina). American Journal of Primatology 52: 81-91.
68. Rowell TE, Hartwell KM, (1978) The interaction of behaviour and reproductive cycles in patas monkeys. Behavioral Biology 24: 141-167.
69. Vandenbergh JG, Drickamer LC, (1974) Reproductive coordination among free-ranging rhesus monkeys. Physiology and Behavior 13: 373-376.
70. Cords M, Mitchell BJ, Tsingalia HM, Rowell TE, (1986) Promiscuous mating among Blue monkeys in the Kakamega forest, Kenya. Ethology 72: 214-226.
71. Andelman SJ, Else JG, Hearn JP, Hodges JK, (1985) The non-invasive monitoring or reproductive events in wild vervet monkeys (Cercopithecus aethiops) using urinary pregnanediol-3á-glucuronide and its correlation with behavioural observations. Journal of Zoology (London) 205: 467-477.
72. Andelman SJ, (1987) Evolution of concealed ovulation in Vervet monkeys (Cercopithecus aethiops). American Naturalist 12: 785-799.
73. Li JH, Yin HB, Wang QS, (2005) Seasonality of reproduction and sexual activity in female Tibetan macaques (Macaca thibetana) at Mt. Huangshan, China. Acta Zoologica Sinica 51: 365-375.
74. Nunn CL, van Schaik CP, Zinner D, (2001) Do exaggerated sexual swellings function in female mating competition in primates? A comparative test of the reliable indicator hypothesis. Behavioral Ecology 12: 646-654.
75. Doran-Sheehy DM, Fernadez D, Borries C, (2009) The strategic use of sex in wild female western gorillas. American Journal of Primatology 71: 1011-120.
76. Stoinski TS, Perdue BM, Legg AM, (2009) Sexual behaviour in female western lowland gorillas (Gorilla gorilla gorilla): evidence for sexual competition. American Journal of Primatology 71: 587-593.
77. Pradhan GR, van Schaik CP, (2008) Infanticide-driven intersexual conflict over matings in primates and its effects on social organization. Behaviour 145: 251-275.
78. Schwensow N, Eberle M, Sommer S, (2008) Compatibility counts: MHC-associated mate choice in a wild promiscuous primate. Proceedings of the Royal Society B 275: 555-564.
79. Setchell JM, Charpentier MJE, Abbott KM, Wickings EJ, Knapp LA, (2010) Opposites attract: MHC-associated mate choice in a polygynous primate. Journal of Evolutionary Biology 23: 136-148.