Abstract
Mating and consequently reproductive success in male vertebrates are predominantly determined by intermale competition and female mate choice. Their relative importance however, is still poorly understood. We investigated the interrelationship between male dominance rank — a formal indicator of male competitive ability — female mate choice, and male mating success in a multimale-multifemale group of captive chimpanzees. In addition, we examined the relationship between male dominance rank and reproductive success determined by genetic paternity analysis over a 13-yr period in the same captive population. We related the frequencies of sociosexual behaviors to the female anogenital swelling stage and female fertile phase as determined by urinary and fecal progestogen analysis. Rates of behaviors in both sexes increased with increasing intensity of female swelling, but they were not influenced by the timing of the fertile phase. Male mating success was clearly related to male dominance rank, with high-ranking males performing the overwhelming majority of copulations. This was mainly due to both rank-related rates of male soliciting behavior and intermale aggressiveness during the period of well-developed female anogenital swelling. Although females solicited copulations mainly from the high-ranking males and thus expressed a mate choice based on rank, their overall contribution in initiating copulations and thus influencing male mating success was low. The data on paternity from the population, which always contained 4 adult males, revealed that α-males sired the majority (65%) of offspring. We conclude, that male dominance rank is an important determinant of male mating and reproductive success in captive (and presumably wild) chimpanzees and that female mate choice is of minor importance in modulating male reproductive outcome.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allen, M. (1981). Indivudual copulatory preference and the “strange female effect” in a captive group-living male chimapanzee (Pan troglodyes). Primates 22: 221–236.
Altmann, J. (1974). Observational study of behavior: sampling methods. Behaviour 49: 227–267.
Altmann, J., Alberts, S. C., Haines, S. A., Dubach, J., Muruthi, P., Coote, T., Geffen, E., Cheesman, D. J., Mututua, R. S., Saiyalel, S. N., Wayne, R. K., Lacy, R. C., and Bruford, M. W. (1996). Behavior predicts genetic structure in a wild primate group. Proc. Natl. Acad. Sci. USA. 93: 5797–5801.
Andersson, M. (1994). Sexual Selection, Princeton University Press, Princeton, New Jersey.
Aujard, F., Heistermann, M., Thierry, B., and Hodges, J. K. (1998). Functional significance of behavioral, morphological, and endocrine corelates across the ovarian cycle in semifree ranging female tonkean macaques. Am. J. Primatol. 46: 285–309.
Bauers, K. A., and Hearn, J. P. (1994). Patterns of paternity in relation to male social rank in the stumptailed macaque, Macaca arctoides. Behav. 129: 149–176.
Berard, J. (1999). A four-year study of the association between male dominance rank, residency status, and reproductice activity in rhesus macaques (Macaca mulatta). Primates 40: 159–175.
Berard, J. D., Nuernberg, P., Epplen, J. T., and Schmidtke, J. (1994). Alternative reproductive tactics and reproductive success in male rhesus macaques. Behaviour 129: 177–201.
Bercovitch, F. B. (1986). Male rank and reproductive activity in savanna baboons. Int. J. Primatol. 7: 533–550.
Boesch, C., and Boesch-Achermann, H. (2000). The chimpanzees of the Taï forest, Oxford University Press, Oxford.
Carosi, M., Heistermann, M., and Visalberghi, E. (1999). Display of proceptive behaviors in relation to urinary and fecal progestin levels over the ovarian cycle in female tufted capuchin monkeys. Horm. Behav. 36: 252–265.
Collins, W. P. (1983). Biochemical approaches to ovulation prediction and detection and the location of the fertile period in women. In Jeffcoate (ed.), Ovulation: methods for its prediction and detection, John Wiley & Sons, Ltd, Chester, pp. 49–66.
Constable, J. L., Ashley, M. V., Goodall, J., and Pusey, A. E. (2001). Noninvasive paternity assignment in Gombe chimpanzees. Mol. Ecol. 10: 1279–1300.
Cowlishaw, G., and Dunbar, R. I. M. (1991). Dominance rank and mating success in male primates. Anim. Behav. 41: 1045–1056.
Dahl, J. F., Nadler, R. D., and Collins, D. C. (1991). Monitoring the ovarian cycles of Pan troglodytes and P. paniscus: a comparative approach. Am. J. Primatol. 24: 195–209.
de Ruiter, J. R., van Hooff, J. A. R. A. M., and Scheffrahn, W. (1994). Social and genetic aspects of paternity in wild long-tailed macaques (Macaca fascicularis). Behaviour 129: 203–224.
Deschner, T., Heistermann, M., Hodges, K., and Boesch, K. (2003). Timing and probability of ovulation in relation to sex skin swelling in wild West African chimpanzees, Pan troglodytes verus. Anim. Behav. 66: 551–560.
Deschner, T., Heistermann M., Hodges K., and Boesch, C. (2004). Female swelling, timing of ovulation and male behavior in wild West African chimpanzees. Horm. Behav. 46: 204–215.
de Waal, F. (1998). Chimpanzee Politics: Power and Sex among Apes, Johns Hopkins University Press, Baltimore.
Dewsbury, D. A. (1982). Dominance rank, copulatory behavior, and differential reproduction. The Q. Rev. Biol. 57: 135–159.
Dixson, A. F. (1998). Primate sexuality, Oxford University Press, Oxford, New York, Tokyo.
Dunbar, R. I. M. (1988). Primate Social Systems. Croom Helm, London.
Ellis, L. (1995). Dominance and reproductive success among nonhuman animals: a cross-species comparison. Ethol. Sociobiol. 16: 257–333.
Ely, J., Alford, P., and Ferrell, R. E. (1991). DNA “fingerprinting” and the genetic management of a captive chimpanzee population (Pan troglodytes). Am. J. Primatol. 24: 39–54.
Emery, M. A., and Whitten, P. L. (2003). Size of sexual swelling reflects ovarian function in chimpanzees (Pan troglodytes). Behav. Ecol. Sociobiol. 54: 340–351.
Engelhardt, A., Pfeifer, J.-B., Heistermann, M., Niemitz, C., van Hooff, J. A. R. A. M., and Hodges, J. K. (2004). Assessment of female reproductive status by male long-tailed macaques (Macaca fascicularis) under natural conditions. Anim. Behav. 67: 915–924.
Fedigan, L. M. (1983). Dominance and Reproductive Success in primates. Yearbook Phy. Anthropol. 26: 91–129.
Goebelsmann, U., Midgley, A. R., and Jaffe, R. B. (1969). Regulation of human gonadotropins: VII. Daily individual urinary estrogens, pregnanediol and serum luteinizing and follicle stimulating hormones during the menstrual cycle. J. Clin. Endocrinol. Metab. 29: 1222–1230.
Goodall, J. (1986). The Chimpanzees of Gombe: Patterns of Behavior, Harvard University Press, Cambridge.
Hasegawa, T., and Hiragawa-Hasegawa, M. (1983). Oportunistic and restrictive matings among wild chimpanees in the Mahale Mountains, Tanzania. J. Ethol. 1: 75–85.
Hasegawa, T., and Hiraiwa-Hasegawa, M. (1990). Sperm competition and mating behavior. In Nishida T. (ed.), The chimpanzees of the Mahale mountains. Sexual and life history strategies. University of Tokyo Press, Tokyo, pp. 116–187.
Heistermann, M., Finke, M., and Hodges, J. K. (1995). Assessment of female reproductive status in captive-housed hanuman langures (Presbytis entellus) by measurement of urinary and fecal steroid excretion patterns. Am. J. Primatol. 37: 275–284.
Heistermann, M., Möhle, U., Vervaecke, H., van Elsacker, L., and Hodges, J. K. (1996). Application of urinary and fecal steroid measurements for monitoring ovarian function and pregnancy in the bonobo (Pan paniscus) and evaluation of perineal swelling patterns in relation to endocrine events. Biol. Reprod. 55: 844–853.
Heistermann, M., Ziegler, T., van Schaik, C. P., Launhardt, K., Winkler, P., and Hodges, J. K. (2001). Loss of oestrus, concealed ovulation and paternity confusion in free-ranging Hanuman langurs. Proc. Roy. Soc. Lond. 268: 2445–2451.
Holm, S. (1979). A simple sequentially rejective multiple test procedure. Scand. J. Statist. 6: 65–70.
Janson, C. (1984). Female choice and the mating system of the brown capuchin monkey, Cebus apella (Primates: Cebidae). Z. Tierpsychol. 65: 177–200.
Keddy, A. C. (1986). Female mate choice in vervet monkeys (Cercopithecus aethiops). Am. J. Primatol. 10: 125–143.
Klinkova, E., Heistermann, M., and Hodges, J. K. (2004). Social parameters and urinary testosterone level in male chimpanzees (Pan troglodytes). Horm. Behav. 46: 474–481.
Launhardt, K., Borries, C., Hardt, C., Epplen, J. T., and Winkler, P. (2001). Paternity analysis of alternative male reproductive routes among the langurs (Semnopithecus entellus) of Ramnagar. Anim. Behav. 61: 53–64.
Manson, J. H. (1994). Male aggression: a cost of female mate choice in Cayo Santiago rhesus macaques. Anim. Behav. 48: 473–475.
Matsumoto-Oda, A. (1999). Female choice in the opportunistic mations of wild chimpanees (Pan troglodytes schweinfurthii) at Mahale. Behav. Ecol. Sociobiol. 46: 258–266.
Meier, C., Hemelrijk, C. K., and Martin, R. D. (2000). Parternity determination, genetic characterization, and social corelates in a captive group of chimpanzees. Primates 41: 175–183.
Morin, P. A. (1993). Reproductive strategies in chimpanzees. Yearbook Phys. Anthropol. 36: 179–212.
Muller, M. N., and Wrangham, R. W. (2004). Dominance, aggression and testosterone in wild chimpanzees: a test of the ‘challenge hypothesis.’ Anim. Behav. 67: 113–123.
Murno, C. J., Stabenfeldt, G. H., Cragun, J. R., Addiego, L. A., Overstreet, J. W., and Lasley, B. L. (1991). Relationship of serum estradiol and progesterone concentrations to the excretion profiles of their major urinary metabolites as measured by enzyme immunoassay. Clin. Chem. 37: 838–844.
Nadler, R. D., Graham, C. E., Gosselin, R. E., and Collins, D. C. (1985). Serum levels of gonadotropins and gonadal steroids, including testosterone, during the menstrual cycle of the chimpanzee (Pan troglodytes). Am. J. Primatol. 9: 273–284.
Nishida, T. (1983). Alpha status and agonistic alliance in wild chimpanzees (Pan troglodytes schweinfurthii). Primates 24: 318–336.
Noe, R., de Waal, F. B. M., and van Hooff, J. A. R. A. M. (1980). Types of dominance in a chimpanzee colony. Folia Primatol. 34: 90–110.
Pauerstein, C. J., Eddy, C. A., Croxatto, H. D., Hess, R., Siler-Khodr, T. M., and Croxatto, H. B. (1978). Temporal relationships of estrogen, progesterone, and luteinizing hormone levels to ovulation in women and infrahuman primates. Am. J. Obstet. Gynecol. 130: 876–886.
Paul, A. (1997). Breeding seasonality affects the association between dominance and reproductive success in non-human male primates. Folia primatol. 68: 344–349.
Reichert, K. E., Heistermann, M., Hodges, K., Boesch, C., and Hohmann, G. (2002). What females tell males about ther reproductive status: are morphological and behavioural cues reliable signals of ovulation in bonobos (Pan paniscus)? Ethology 108: 583–600.
Reinartz, G. E., Karron, J. D., Phillips, R. B., and Weber, J. L. (2000). Patterns of microsatellite polymorphism in the range-restricted bonobo (Pan paniscus): considerations for interspecific comparison with chimpanzee (P. troglodytes). Mol. Ecol. 9: 315–328.
Sambrook, J., Fritch, E. F., and Maniatis, T. (1989). Molecular cloning: a laboratory manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
Shefferly, N., and Fritz, P. (1992). Male chimpanzee behavior in relation to female ano-genital sweling. Am. J. Primatol. 26: 119–131.
Small, M. F. (1989). Female choice in nonhuman primates. Yearbook Phys. Anthropol. 32: 103–127.
Soltis, J., Mitsunaga, F., Shimizu, K., Yanagihara, Y., and Nozaki, M. (1997a). Sexual selection in Japanese macaques I: female mate choice or male sexual coercion? Anim. Behav. 54: 725–736.
Soltis, J., Mitsunaga, F., Shimizu, K., Nozaki, M., Yanagihara, Y., Dominigo-Roura, X., and Takenaka, O. (1997b). Sexual selecion in Japanese macaques II: female mate choice and male-male competition. Anim. Behav. 54: 737–746.
Steinetz, B. G., Ducrot, C., Randolph, C., and Mahoney, C. J. (1992b). Determination of the time of ovulation in chimpanzees by measurement of LH, estrone sulfate, and pregnanediol 3a-glucuronide in urine: Comparison with serum hormone patterns. J. Med. Primatol. 21: 239–243.
Strier, K. B., and Ziegler, T. E. (1997). Behavioral and endocrine characteristics of the reproductive cycle in wild muriqui monkeys, Brachyteles arachnoides. Am. J. Primatol. 42: 299–310.
Takahata, Y., Huffman, M. A., Suzuki, S., Koyama, N., and Yamagiwa, J. (1999). Why dominance do not consistently attain high mating and reproduction success: a review of longitudinal Japanese macaque studies. Primates 40: 143–158.
Takasaki, H. (1985). Female life history and mating patterns among the M Group chimpanees of the Mahale National Park, Tanzania. Primates 26: 121–129.
Takahata, Y. (1990). Social relationships among adult males. In Nishida, T. (ed.), The chimpanzees of the Mahale mountains, University of Tokyo Press, Tokyo, pp. 148–170.
Takenaka, O., Kawamoto, S., Udono, T., Arakawa, M., Takasaki, H., and Takenaka, A. (1993). Chimpanzee microsatellite PCR primers applied to paternity testing in a captive colony. Primates 34: 357–363.
Tutin, C. E. G. (1979). Mating patterns and reproductive strategies in a community of wild chimpanzees (Pan troglodytes schweinfurthii). Behav. Ecol. Sociobiol. 6: 29–39.
Tutin, C. E. G., and McGinnis, P. R. (1981). Chimpanzee reproduction in the wild. In Granham, C. E. (ed.), Reproductive biology of the great apes: comparative and biochemical perspectives, Academic Press, New York, London, Toronto, Sydney, San Francisco, pp. 239–264.
van Hooff, J. A. R. A. M. (1973). A structural analysis of the social behaviour of a semicaptive group of chimpanzees. In von Cranach M., and Vine, I. (eds.), Social Communication and Movement, Academic Press, London and New York, pp. 75–162.
van Lawick-Goodall, J. (1968). The behaviour of free-living chimpanzees in the Gombe Stream Reserve. Anim. Behav. Monog. 1: 161–311.
Vigilant, L., Hofreiter, M., Siedel, H., and Boesch, C. (2001). Paternity and relatedness in wild chimpanzee communities. Proc. Natl. Acad. Sci. 98: 12890–12895.
Wallis, J. (1992). Chimpanzee genital swelling and its role in the pattern of sociosexual behavior. Am. J. Primatol. 28: 101–113.
Wallis, J. (1982). Sexual Behavior of captive chimpanzees (Pan trodlodytes): pregnant versus cycling females. Am. J. Primatol. 3: 77–88.
Watts, D. P. (1998). Coalitionary mate quarding by male chimpanzees at Ngogo, Kibale National Park, Uganda. Behav. Ecol. Sociobiol. 44: 43–55.
Wickings, E. J., Bossi, T., and Dixson, A. F. (1993). Reproductive success in the mandrill, Mandrillus sphinx: correlations of male dominance and mating success with paternity, as determined by DNA fingerprinting. J. Zool. Lond. B 231: 563–574.
Wilcox, A. J., Weinberg, C. R., and Baird, D. D. (1995). Timing of sexual intercourse in relation to ovulation. The New Eng. J. Med. 333: 1517–1521.
Wrangham, R. W. (2000). Why are male chimpanzees more gregarious than mothers? A scramble competition hypothesis. In Kappeler, P. M. (ed.), Primate Males, Cambridge University Press, UK, pp. 248–258.
Wrangham, R. W. (2002). The cost of sexual atraction: is there a tradeoff in female Pan between sex appeal and received coercion? In Boesch, C., Hohmann, G., and Marchant, L. (eds.), Behavioural Diversity in Chimpanzees and Bonobos, Cambridge University Press, Cambridge, UK.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Klinkova, E., Hodges, J.K., Fuhrmann, K. et al. Male Dominance Rank, Female Mate Choice and Male Mating and Reproductive Success in Captive Chimpanzees. Int J Primatol 26, 357–484 (2005). https://doi.org/10.1007/s10764-005-2929-6
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s10764-005-2929-6