Sex ratios in primate groups

doi:10.1017/CBO9780511542459.016

14 - Sex ratios in primate groups

Published online by Cambridge University Press: 10 August 2009

Joan B. Silk and

Gillian R. Brown

Edited by

Peter M. Kappeler and

Carel P. van Schaik

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Joan B. Silk: Affiliation:
Department of Anthropology, University of California, Los Angeles, CA, USA
Gillian R. Brown: Affiliation:
Department of Zoology, University of Cambridge, Cambridge, UK
Peter M. Kappeler: Affiliation:
Deutsches Primatenzentrum, Göttingen, Germany
Carel P. van Schaik: Affiliation:
Duke University, North Carolina

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Summary

I formerly thought that when a tendency to produce the two sexes in equal numbers was advantageous to the species, it would follow from natural selection, but I now see the whole problem is so intricate that it is safer to leave its solution for the future.

Charles Darwin, 1871

Introduction

Sexual selection is an important evolutionary force in mammalian species because of one simple fact – males are a glut on the market. From the females' point of view, there are more males than needed to meet their reproductive requirements. And from the males' point of view, there are not nearly enough females to go around to satisfy their reproductive potential. The relative abundance of males generates strong intrasexual competition among them.

The goals of this chapter are to explore the selective factors that influence the evolution of birth sex ratios, and to weigh the empirical evidence that primate females facultatively manipulate birth sex ratios to enhance their own fitness. We will begin by briefly enumerating some of the ways in which adult sex ratios influence the evolution of male and female life histories, morphology and reproductive strategies in primate groups. Then, we will explain how natural selection shapes the evolution of birth sex ratios, and consider the empirical evidence for adaptive manipulation of birth sex ratios in primate groups.

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Type: Chapter
Information: Sexual Selection in Primates
New and Comparative Perspectives
, pp. 253 - 265

DOI: https://doi.org/10.1017/CBO9780511542459.016 [Opens in a new window]

Publisher: Cambridge University Press

Print publication year: 2004

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References

Alberts, S. A. & Altmann, J. 1995. Preparation and activation: determinants of age at reproductive maturity in male baboons. Behavioral Ecology and Sociobiology, 36, 397–406CrossRef Google Scholar

Altmann, J., Hausfater, G. & Altmann, S. A. 1988. Determinants of reproductive success in savannah baboons. In Reproductive Success, ed. T. H. Clutton-Brock. Cambridge: Cambridge University Press, pp. 403–18

Altmann, J., Alberts, S. C., Haines, S. A.et al. 1996. Behavior predicts genetic structure in a wild primate group. Proceedings of the National Academy of Sciences, USA, 93, 5797–801CrossRef Google Scholar

Bercovitch, F. B. 1993. Dominance rank and reproductive maturation in male rhesus macaques (Macaca mulatta). Journal of Reproduction and Fertility, 99, 113–20CrossRef Google Scholar

Bercovitch, F. B. 2002. Sex-biased parental investment in primates. International Journal of Primatology, 23, 905–21CrossRef Google Scholar

Bercovitch, F. B., Widdig, A. & Nürnberg, P. 2000. Maternal investment in rhesus macaques (Macaca mulatta): reproductive costs and consequences of raising sons. Behavioral Ecology and Sociobiology, 48, 1–11CrossRef Google Scholar

Berman, C. M. 1988. Maternal condition and offspring sex ratio in a group of free-ranging rhesus monkeys: an 11-year study. American Naturalist, 131, 307–28CrossRef Google Scholar

Bramblett, C. A., Bramblett, S. S., Bishop, D. & Coelho, A. M. Jr. 1982. Longitudinal stability in adult hierarchies among vervet monkeys (Cercopithecus aethiops). American Journal of Primatology, 2, 10–19CrossRef Google Scholar

Brown, G. R. 2001. Sex-biased investment in nonhuman primates: can Trivers and Willard's theory be tested?Animal Behaviour, 61, 683–94CrossRef Google Scholar

Brown, G. R. & Silk, J. B. 2002. Reconsidering the null hypothesis: is maternal rank associated with birth sex ratios in primate groups?Proceedings of the National Academy of Sciences, USA, 99, 11252–5CrossRef Google Scholar PubMed

Bulmer, M. G. & Taylor, P. D. 1980. Sex ratio under the haystack model. Journal of Theoretical Biology, 86, 83–9CrossRef Google Scholar PubMed

Chapais, B. 1992. The role of alliances in social inheritance of rank among female primates. In Coalitions and Alliances in Humans and Other Animals, ed. A. H. Harcourt & F. B. M. de Waal. Oxford: Oxford Science Publications, pp. 29–59

Charnov, E. L. 1979. Simultaneous hermaphroditism and sexual selection. Proceedings of the National Academy of Sciences, USA, 76, 2480–4CrossRef Google Scholar PubMed

Clark, A. B. 1978. Sex ratio and local resource competition in a prosimian primate. Science, 201, 163–5CrossRef Google Scholar

Clutton-Brock, T. H. 1986. Sex ratio variation in birds. Ibis, 128, 317–29CrossRef Google Scholar

Clutton-Brock, T. H. 1991. The Evolution of Parental Care. Princeton, NJ: Princeton University Press

Clutton-Brock, T. H. & Albon, S. D. 1982. Parental investment in male and female offspring in mammals. In Current Problems in Sociobiology, ed. King's College Sociobiology Group. Cambridge: Cambridge University Press, pp. 223–47

Clutton-Brock, T. H., Harvey, P. H. & Rudder, B. 1977. Sexual dimorphism, socionomic sex ratio, and body weight in primates. Nature, 269, 797–800CrossRef Google Scholar PubMed

Clutton-Brock, T. H., Albon, S. D. & Guinness, F. E. 1984. Maternal dominance, breeding success, and birth sex ratios in red deer. Nature, 308, 358–60CrossRef Google Scholar

Clutton-Brock, T. H., Albon, S. D. & Guinness, F. E. 1986. Great expectations: maternal dominance, sex ratios, and offspring reproductive success in red deer. Animal Behaviour, 34, 460–71CrossRef Google Scholar

Cowlishaw, G. & Dunbar, R. I. M. 1991. Dominance rank and mating success in male primates. Animal Behaviour, 41, 1045–56CrossRef Google Scholar

Darwin, C. 1871. The Descent of Man and Selection in Relation to Sex. London: John Murray

Debyser, I. W. J. 1995a. Prosimian juvenile mortality in zoos and primate centers. International Journal of Primatology, 16, 889–907CrossRef Google Scholar

Debyser, I. W. J. 1995b. Platyrrhine juvenile mortality in captivity and in the wild. International Journal of Primatology, 16, 909–33CrossRef Google Scholar

Debyser, I. W. J. 1995c. Catarrhine juvenile mortality in captivity, under seminatural conditions, and in the wild. International Journal of Primatology, 16, 935–69CrossRef Google Scholar

de Ruiter, J. R., Scheffrahn, W., Trommelen, G. J. J. M. et al. 1992. Male social rank and reproductive success in wild long-tailed macaques. In Paternity in Primates: Genetic Tests and Theories, ed. R. D. Martin, A. F. Dixson & E. J. Wickings. Basel: Karger, pp. 175–91

Dittus, W. P. J. 1998. Birth sex ratios in toque macaques and other mammals: integrating the effects of maternal condition and competition. Behavioral Ecology and Sociobiology, 44, 149–60CrossRef Google Scholar

Dixson, A. F. & Nevison, C. M. 1997. The socioendocrinology of adolescent development in male rhesus monkeys (Macaca mulatta). Hormones and Behavior, 31, 126–35CrossRef Google Scholar

Drews, C. 1996. Contexts and patterns of injuries in free-ranging male baboons (Papio cynocephalus). Behaviour, 133, 443–74CrossRef Google Scholar

Emlen, S. T. & Oring, L. W. 1977. Ecology, sexual selection, and the evolution of mating systems. Science, 197, 215–23CrossRef Google Scholar PubMed

Fedigan, L. M. & Zohar, S. 1997. Sex differences in mortality of Japanese macaques: twenty-one years of data from the Arashiyama West population. American Journal of Physical Anthropology, 102, 161–753.0.CO;2-1>CrossRef Google Scholar PubMed

Fisher, R. A. 1930. The Genetical Theory of Natural Selection. Oxford: Oxford University Press

Greenwood, P. J. 1980. Mating systems, philopatry, and dispersal in birds and mammals. Animal Behaviour, 28, 1140–62CrossRef Google Scholar

Hamilton, W. D. 1967. Extraordinary sex ratios. Science, 156, 477–88CrossRef Google Scholar PubMed

Hamilton, W. D. 1975. Innate social aptitudes of man: an approach from evolutionary genetics. In Biosocial Anthropology, ed. R. Fox. New York, NY: John Wiley, pp. 133–55

Hamilton, W. D. 1979. Wingless and fighting males in fig wasps and other insects. In Sexual Selection and Reproductive Competition in Insects, ed. M. S. Blum & N. A. Blum. New York, NY: Academic Press, pp. 167–220

Harcourt, A. H. 1987. Dominance and fertility among female primates. Journal of Zoology, London, 213, 471–87CrossRef Google Scholar

Harcourt, A. H., Harvey, P. H., Larson, S. G. & Short, R. V. 1981. Testis weight, body weight and breeding system in primates. Nature, 293, 55–7CrossRef Google Scholar PubMed

Harvey, P. H. & Harcourt, A. H. 1984. Sperm competition, testis size and breeding systems in primates. In Sperm Competition and the Evolution of Animal Mating Systems, ed. R. L. Smith. New York, NY: Academic Press, pp. 589–600

Hausfater, G., Altmann, J. & Altmann, S. A. 1982. Long-term consistency of dominance relations among female baboons (Papio cynocephalus). Science, 217, 752–5CrossRef Google Scholar

Hrdy, S. B. & Whitten, P. L. 1987. Patterning of sexual activity. In Primate Societies, ed. B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham & T. T. Struhsaker. Chicago, IL: University of Chicago Press, pp. 370–84

Johnson, C. N. 1988. Dispersal and the sex ratio at birth in primates. Nature, 332, 726–8CrossRef Google Scholar PubMed

Launhardt, K., Borries, C., Hardt, C., Epplen, J. T. & Winkler, P. 2001. Paternity analysis of alternative male reproductive routes among the langurs (Semnopithecus entellus) of Ramnagar. Animal Behaviour, 61, 53–64CrossRef Google Scholar PubMed

Leimar, O. 1996. Life history analysis of the Trivers and Willard sex-ratio problem. Behavioral Ecology, 7, 316–25CrossRef Google Scholar

Maynard Smith, J. 1978. The Evolution of Sex. Cambridge: Cambridge University Press

Meikle, D. B., Tilford, B. L. & Vessey, S. H. 1984. Dominance rank, secondary sex ratio, and reproduction of offspring in polygynous primates. American Naturalist, 124, 173–88CrossRef Google Scholar

Mitani, J. C., Gros-Louis, J. & Richards, A. 1996b. Sexual dimorphism, the operational sex ratio, and the intensity of male competition in polygynous primates. American Naturalist, 147, 966–80CrossRef Google Scholar

Nunn, C. L. & Pereira, M. E. 2000. Group histories and offspring sex ratios in ringtailed lemurs (Lemur catta). Behavioral Ecology and Sociobiology, 48, 18–28CrossRef Google Scholar

Packer, C., Collins, D. A. & Eberly, L. E. 2000. Problems with primate sex ratios. Proceedings of the Royal Society of London, Series B, 355, 1627–35CrossRef Google Scholar PubMed

Palmer, A. R. 2000. Quasireplication and the contract of error: lessons from sex ratios, heritabilities and fluctuating asymmetry. Annual Review of Ecology and Systematics, 31, 441–80CrossRef Google Scholar

Palombit, R. A. 1994. Extra-pair copulations in a monogamous ape. Animal Behaviour, 47, 721–3CrossRef Google Scholar

Palombit, R. A. 2000. Infanticide and the evolution of male–female bonds in animals. In Infanticide by Males and Its Implications, ed. C. P. van Schaik & C. H. Janson. Cambridge: Cambridge University Press, pp. 239–68

Palombit, R. A., Seyfarth, R. M. & Cheney, D. L. 1997. The adaptive value of ‘friendships’ to female baboons: experimental and observational evidence. Animal Behaviour, 54, 599–614CrossRef Google Scholar PubMed

Paul, A. & Kuester, J. 1990. Adaptive significance of sex ratio adjustment in semifree-ranging Barbary macaques (Macaca sylvanus) at Salem. Behavioral Ecology and Sociobiology, 27, 287–93CrossRef Google Scholar

Paul, A., Kuester, J. & Arnemann, J. 1992. Maternal rank affects reproductive success of male barbary macaques (Macaca sylvanus) – evidence from DNA fingerprinting. Behavioral Ecology and Sociobiology, 30, 337–41Google Scholar

Pusey, A. E. & Packer, C. 1987. Dispersal and philopatry. In Primate Societies, ed. B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham & T. T. Struhsaker. Chicago, IL: University of Chicago Press, pp. 250–66

Rawlins, R. G. & Kessler, M. J. 1986. Secondary sex ratio variation in the Cayo Santiago macaque population. American Journal of Primatology, 10, 9–23CrossRef Google Scholar

Rhine, R. J. 1994. A twenty-one-year study of maternal dominance and secondary sex ratio in a colony group of stumptail macaques (Macaca arctoides). American Journal of Primatology, 32, 145–8CrossRef Google Scholar

Rhine, R. J., Norton, G. W., Rogers, J. & Wasser, S. K. 1992. Secondary sex ratio and maternal dominance rank among wild yellow baboons (Papio cynocephalus) of Mikumi National Park, Tanzania. American Journal of Primatology, 27, 261–73CrossRef Google Scholar

Rorie, R. W. 1999. Effect of timing on artificial insemination on sex ratio. Theriogenology, 52, 1273–80CrossRef Google Scholar PubMed

Samuels, A., Silk, J. B. & Altmann, J. 1987. Continuity and change in dominance relations among female baboons. Animal Behaviour, 35, 785–93CrossRef Google Scholar

Silk, J. B. 1983. Local resource competition and facultative adjustment of sex ratio in relation to competitive abilities. American Naturalist, 121, 56–66CrossRef Google Scholar

Silk, J. B. 1984. Local resource competition and the evolution of male-biased sex ratios. Journal of Theoretical Biology, 108, 203–13CrossRef Google Scholar PubMed

Silk, J. B. 1987. Social behavior in evolutionary perspective. In Primate Societies, ed. B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham & T. T. Struhsaker. Chicago, IL: University of Chicago Press, pp. 318–29

Silk, J. B. 1988. Maternal investment in captive bonnet macaques (Macaca radiata). American Naturalist, 132, 1–19CrossRef Google Scholar

Silk, J. B., Clark-Wheatley, C. B., Rodman, P. S. & Samuels, A. 1981. Differential reproductive success and facultative adjustment of sex ratios among captive female bonnet macaques (Macaca radiata). Animal Behaviour, 29, 1106–20CrossRef Google Scholar

Silk, J. B., Short, J ., Roberts, J. & Kemnitz, J. 1993. Gestation length in rhesus macaques (Macaca mulatta). International Journal of Primatology, 14, 95–104CrossRef Google Scholar

Simpson, M. J. A. & Simpson, A. E. 1982. Birth sex ratios and social rank in rhesus monkey mothers. Nature, 300, 440–1CrossRef Google Scholar PubMed

Small, M. F. & Hrdy, S. B. 1986. Secondary sex ratios by maternal rank, parity, and age in captive rhesus macaques (Macaca mulatta). International Journal of Primatology, 7, 289–304CrossRef Google Scholar

Smuts, B. B. 1987. Gender, aggression, and influence. In Primate Societies, ed. B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham & T. T. Struhsaker. Chicago, IL: University of Chicago Press, pp. 400–12

Soltis, J. & McElreath, R. 2001. Can females gain extra paternal investment by mating with multiple males? A game theoretic approach. American Naturalist, 58, 519–29CrossRef Google Scholar

Sommer, V. 2000. The holy wars about infanticide: which side are you on? And why? In Infanticide by Males and Its Implications, ed. C. P. van Schaik & C. H. Janson. Cambridge: Cambridge University Press, pp. 9–26

Sommer, V. & Reichard, U. 2000. Rethinking monogamy: the gibbon case. In Primate Males: Causes and Consequences of Variation in Group Composition, ed. P. M. Kappeler. Cambridge: Cambridge University Press, pp. 159–68

Trivers, R. L. 1972. Parental investment and sexual selection. In Sexual Selection and the Descent of Man, ed. B. Campbell. Chicago, IL: Aldine, pp. 136–79

Trivers, R. L. 1985. Social Evolution. Menlo Park, CA: Benjamin Cummings

Trivers, R. L. & Willard, D. 1973. Natural selection of parental ability to vary the sex ratio of offspring. Science, 179, 90–2CrossRef Google Scholar PubMed

Uyenoyama, M. & Feldman, M. 1980. Theories of kin and group selection: a population genetics perspective. Theoretical Population Biology, 17, 380–414CrossRef Google Scholar PubMed

Noordwijik, M. A. & Schaik, C. P. 1999. The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques, Macaca fasicularis. Primates, 40, 105–30CrossRef Google Scholar

Noordwijik, M. A. & Schaik, C. P. 2001. Career moves: transfer and rank challenge decision by male long-tailed macaques. Behaviour, 138, 359–95CrossRef Google Scholar

Schaik, C. P. & Visser, J. A. G. M. 1990. Fragile sons or harassed daughters? Sex differences in mortality among juvenile primates. Folia Primatologica, 55, 10–23CrossRef Google Scholar PubMed

Schaik, C. P. & Hrdy, S. B. 1991. Intensity of local resource competition shapes the relationship between maternal rank and sex ratios at birth in cercopithecine primates. American Naturalist, 138, 1555–62CrossRef Google Scholar

van Schaik, C. P. & Janson, C. H. (eds.) 2000. Infanticide by Males and Its Implications. Cambridge: Cambridge University Press

Wade, M. J. 1978. A critical review of the models of group selection. Quarterly Review of Biology, 53, 101–14CrossRef Google Scholar

Wasser, S. K. & Norton, G. 1993. Baboons adjust secondary sex ratio in response to predictors of sex-specific offspring survival. Behavioral Ecology and Sociobiology, 32, 273–81CrossRef Google Scholar

Watanabe, K., Mori, A. & Kawai, M. 1992. Characteristic features of the reproduction of Koshima monkeys, Macaca fuscata fuscata: a summary of thirty-four years of observation. Primates, 33, 1–32CrossRef Google Scholar

West, S. A. & Sheldon, B. C. 2002. Constraints in the evolution of sex ratio adjustment. Science, 295, 1685–8CrossRef Google Scholar PubMed

West, S. A., Herre, E. A. & Sheldon, B. C. 2000. The benefits of allocating sex. Science, 290, 288–90CrossRef Google Scholar PubMed

Williams, G. C. 1979. On the question of adaptive sex ratio in outcrossed vertebrates. Proceedings of the Royal Society of London, Series B, 205, 567–80CrossRef Google Scholar PubMed

Wilson, D. S. 1977. Structured demes and the evolution of group advantageous traits. American Naturalist, 111, 157–85CrossRef Google Scholar

Wilson, D. S. 1980. The Natural Selection of Populations and Communities. Menlo Park, CA: Benjamin Cummings

Wilson, D. S. & Colwell, R. K. 1981. Evolution of sex ratio in structured demes. Evolution, 35, 882–97CrossRef Google Scholar PubMed

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