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The Role of Females in Extrapair Copulations in Socially Monogamous Territorial Animals

  • Judy Stamps

Abstract

This chapter considers the role of females in the sexual and agonistic life of socially monogamous territorial species. Because of the obvious superficial similarities between such species and humans, this is a topic that has always attracted attention from evolutionary and behavioral biologists. However, despite longstanding interest in animal monogamy, most empirical and theoretical studies have relied on a relatively small set of seminal ideas and hypotheses, some of which are summarized here.

Keywords

Sperm Competition Territory Size Tree Swallow Prairie Vole Male Intruder 
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References

  1. Ahnesjo, I., A. Vincent, R. Alatalo, T. Halliday, W. Sutherland. 1993. The role of females in influencing mating patterns. Behavioral Ecology 4:187–189.CrossRefGoogle Scholar
  2. Alexander, R. D. and K. M. Noonan. 1979. Concealment of ovulation, parental care, and human social evolution. In N.A. Chagnon and W. Irons (Eds.), Evolutionary Biology and Human Social Behavior, pp. 436–453. North Scituate, MA: Duxbury Press.Google Scholar
  3. Anderson, M. 1994. Sexual Selection. Princeton, NJ: Princeton University Press.Google Scholar
  4. Bateman, A. J. 1948. Intra-sexual selection in Drosophila. Heredity 2:349–368.CrossRefPubMedGoogle Scholar
  5. Beecher, M. D. and I. M. Beecher. 1979. Sociobiology of bank swallows: Reproductive strategy of the male. Science 205:1282–1285.CrossRefPubMedGoogle Scholar
  6. Berglund, A., C. Magnhagen, A. Bisazza, B. König, F. Huntingford. 1993. Female-female competition over reproduction. Behavioral Ecology 4:184–187.CrossRefGoogle Scholar
  7. Birkhead, T. M. 1991. The Magpies: The Ecology and Behaviour of Black-Billed and Yellow-Billed Magpies. London: Poyser.Google Scholar
  8. Birkhead, T. M. and A. P. Møller. 1992. Sperm competition in birds: evolutionary causes and consequences. Academic Press, London.Google Scholar
  9. Birkhead, T. M. and A. P. Møller. 1993. Female control of paternity. Trends in Ecology and Evolution 8:100–104.CrossRefPubMedGoogle Scholar
  10. Birkhead, T. M., L. Atkin, and A. P. Møller. 1987. Copulation behaviour in birds. Behaviour 101:101–133.CrossRefGoogle Scholar
  11. Bradbury, J. W. and M. B. Andersson, eds. 1987. Sexual Selection: Testing the Alternatives. New York: Wiley.Google Scholar
  12. Bray, O. E., J. J. Kennelly, and J. L. Guarino. 1975. Fertility of eggs produced on territories of vasectomized red-winged blackbirds. Wilson Bulletin 87:187–195.Google Scholar
  13. Brown, J. L. 1964. The evolution of diversity in avian territorial systems. Wilson Bulletin 76:160–169.Google Scholar
  14. Brown, J. L. and G. H. Orians. 1970. Spacing patterns in mobile animals. Annual Review of Ecology and Systematics 1:239–269.CrossRefGoogle Scholar
  15. Bull, C. M. 1994. Population dynamics and pair fidelity in sleepy lizards. In L. J. Vitt and E. R. Pianka (Eds.), Lizard Ecology: Historical and Experimental Perspectives, pp. 159–174. Princeton, NJ: Princeton University Press.Google Scholar
  16. Burley, N. 1988. The differential-allocation hypothesis: An experimental test. American Naturalist 132:611–628.CrossRefGoogle Scholar
  17. Carter, C. S., A. C. DeVries, and L. L. Getz. 1995. Physiological substrates of mammalian monogamy: The prairie vole model. Neuroscience and Biobehavioral Reviews. 19:303–314.CrossRefPubMedGoogle Scholar
  18. Carter, C. S. and L. L. Getz. 1993. Monogamy and the prairie vole. Scientific American 1993 (June): 100-106.Google Scholar
  19. Carter, C. S., J. R. Williams, and D. M. Witt. 1990. The biology of social bonding in a monogamous mammal. In J. Balthazart (Ed.), Hormones, Brain and Behavior in Vertebrates, 2nd ed., pp. 154–164. New York: Karger.Google Scholar
  20. Carter, C. S., D. M. Witt, S. R. Manock, K. A. Adams, J. M. Bahr, and K. Carlstead. 1989. Hormonal correlates of sexual behavior and ovulation in prairie voles. Physiology and Behavior 46:941–948.CrossRefPubMedGoogle Scholar
  21. Clutton-Brock, T. H. 1989. Mammalian mating systems. Proceedings of the Royal Society of London B Biological Sciences 236:339–372.CrossRefGoogle Scholar
  22. Colwell, M. A. and L. W. Oring. 1989. Extra-pair mating in the spotted sandpiper: A female mate acquisition tactic. Animal Behaviour 38:675–684.CrossRefGoogle Scholar
  23. Darwin, C. 1871. The Descent of Man, and Selection in Relation to Sex. London: John Murray.CrossRefGoogle Scholar
  24. Darwin, C. 1877. The Descent of Man and Selection in Relation to Sex. 2nd ed., rev. London: John Murray.Google Scholar
  25. Davies, N. B. 1985. Cooperation and conflict among dunnocks, Prunella modularis, in a variable mating system. Animal Behaviour 33:628–648.CrossRefGoogle Scholar
  26. Davies, N. B. 1991. Mating systems. In J. R. Krebs and N. B. Davies (Eds.), Behavioral Ecology: An Evolutionary Approach, 3rd ed., pp. 263–299. Oxford: Blackwell Scientific Publications.Google Scholar
  27. Davies, N. B. 1992. Dunnock Behavior and Social Evolution. Oxford: Oxford University Press.Google Scholar
  28. Dunn, P. O. 1992. Do male birds adjust territory size to the risk of cuckoldry? Animal Behaviour 43:857–859.CrossRefGoogle Scholar
  29. Dunn, P. O. and J. T. Lifjeld. 1994. Can extra-pair copulations be used to predict extra-pair paternity in birds? Animal Behaviour 47:983–985.CrossRefGoogle Scholar
  30. Dunn, P. O. and R. J. Robertson. 1993. Extra-pair paternity in polygynous tree swallows. Animal Behaviour 45:231–239.CrossRefGoogle Scholar
  31. Dunn, P. O., L. A. Whittingham, J. T. Lifjeld, R. J. Robertson, and P. T. Boag. 1994. Effects of breeding density, synchrony, and experience on extra-pair paternity in tree swallows. Behavioral Ecology 5:123–129.CrossRefGoogle Scholar
  32. Eens, M. and R. Pinxten. 1990. Extra-pair courtship in the Starling, Sturnus vulgaris. Ibis 132:618–619.CrossRefGoogle Scholar
  33. Emlen, S. T. and L. W. Oring. 1977. Ecology, sexual selection and the evolution of mating systems. Science 197:215–223.CrossRefPubMedGoogle Scholar
  34. Ens, B. J. 1992. The social prisoner: Causes of natural variation in reproductive success in the oystercatcher. Ph.D. dissertation, University of Groningen, Groningen, Netherlands.Google Scholar
  35. Ens, B. J., U. N. Safriel, and M. P. Harris. 1993. Divorce in the long-lived and monogamous oystercatcher, Haematopus ostralegus: Incompatibility or choosing the better option? Animal Behaviour 45:1199–1217.CrossRefGoogle Scholar
  36. Fitch, M. A. and G. W. Shugart. 1984. Requirements for a mixed reproductive strategy in avian species. American Naturalist 124:116–126.CrossRefGoogle Scholar
  37. Frederick, P. C. 1987. Extra-pair copulations in the mating system of white ibis (Eudocimus albus). Behaviour 100:170–201.CrossRefGoogle Scholar
  38. Gowaty, P. A. 1985. Multiple paternity and apparent monogamy in birds. In P. A. Gowaty and D. W. Mock (Eds.), Avian Monogamy, pp. 11–21. Ornithological Monographs 37. Washington, DC: American Ornithologists’ Union.Google Scholar
  39. Gowaty, P. A. 1994. Architects of sperm competition. Trends in Ecology and Evolution 9:160–161.CrossRefPubMedGoogle Scholar
  40. Gowaty, P. A. 1996. Battles of the sexes and the origins of monogamy. In J. Black (Ed.), Partnerships in Birds, Oxford: Oxford University Press.Google Scholar
  41. Gowaty, P. A. and W. C. Bridges. 1991. Behavioral, demographic and environmental correlates of extra-pair fertilizations in eastern bluebirds, Sialia sialis. Behavioral Ecology 2:339–350.CrossRefGoogle Scholar
  42. Gowaty, P. A. and A. A. Karlin. 1984. Multiple maternity and paternity in single broods of apparently monogamous eastern bluebirds (Sialia sialis). Behavioral Ecology and Sociobiology 15:91–95.CrossRefGoogle Scholar
  43. Gowaty, P. A., J. H. Plissner, and T. G. Williams. 1989. Behavioral correlates of uncertain parentage: Mate guarding and nest guarding by eastern bluebirds, Sialia sialis. Animal Behaviour 38:272–284.CrossRefGoogle Scholar
  44. Gowaty, P. A. and S. J. Wagner. 1988. Breeding season aggression of female and male eastern bluebirds (Sialia sialis) to models of potential conspecific and interspecific egg dumping. Ethology 78:238–250.CrossRefGoogle Scholar
  45. Greenwood, P. J. 1980. Mating systems, philopatry and dispersal in birds and mammals. Animal Behaviour 28:1140–1162.CrossRefGoogle Scholar
  46. Gubernick, D. J. and R. L. Addington. 1994. The stability of female social and mating preferences in the monogamous California mouse, Peromyscus californicus. Animal Behaviour 47:559–567.CrossRefGoogle Scholar
  47. Gubernick, D. J. and J. C. Nordby. 1993. Mechanisms of sexual fidelity in the monogamous California mouse, Peromyscus californicus. Behavioral Ecology and Sociobiology 32:211–219.CrossRefGoogle Scholar
  48. Halliday, T. and S. J. Arnold. 1988. Multiple mating by females: A perspective from quantitative genetics. Animal Behaviour 35:939–941.CrossRefGoogle Scholar
  49. Hanski, I. and A. Laurila. 1993. Male chaffinches do not enlarge their territories to prevent cuckoldry. Animal Behaviour 46:1036–1038.CrossRefGoogle Scholar
  50. Haraway, D. 1986. Primatology is politics by other means. In R. Bleier (Ed.), Feminist Approaches to Science, pp. 77–118. New York: Pergamon Press.Google Scholar
  51. Hatch, S. A. 1987. Copulation and mate-guarding in the northern fulmar. Auk 104:450–461.CrossRefGoogle Scholar
  52. Heg, D., B. J. Ens, T. Burke, L. Jenkins, and J. P. Kruijt. 1993. Why does the typically monogamous oystercatcher, Haematopus ostralegus, engage in extra-pair copulations? Behaviour 126:247–289.CrossRefGoogle Scholar
  53. Hinde, R. A. 1956. The biological significance of the territories of birds. Ibis 98:340–369.CrossRefGoogle Scholar
  54. Horrigan, T. F. 1987. The behavioral ecology of three species of butterflyflshes (family Chaetodontidae). Ph.D. dissertation, University of Hawaii.Google Scholar
  55. Howard, E. 1920. Territory in Bird Life. London: Collins Sons.Google Scholar
  56. Hrdy, S. B. 1981. The Woman That Never Evolved. Cambridge, MA: Harvard University Press.Google Scholar
  57. Hrdy, S. B. 1986. Empathy, polyandry and the myth of the coy female. In R. Bleier (Ed.), Feminist Approaches to Science, pp. 119–145. New York: Pergamon Press.Google Scholar
  58. Hunter, F., M. Petrie, M. Otronen, T. Birkhead, and A. P. Møller. 1993. Why do females copulate repeatedly with one male? Trends in Ecology and Evolution 8:21–26.CrossRefPubMedGoogle Scholar
  59. Kempenaers, B. 1994. Polygyny in the blue tit: Unbalanced sex ratio and female aggression restrict mate choice. Animal Behaviour 47:943–957.CrossRefGoogle Scholar
  60. Kempenaers, B. and A. A. Dhondt. 1993. Why do females engage in extra-pair copulations: A review of hypotheses and their predictions. Belgian Journal of Zoology 123:93–103.Google Scholar
  61. Kempenaers, B., G. R. Verheyen, M. Van den Broeck, T. Burke, C. Van Broeckhoven, and A. A. Dhondt. 1992. Extra-pair paternity results from female preference for high-quality males in the blue tit. Nature 357:494–496.CrossRefGoogle Scholar
  62. Leighton, D. R. 1986. Gibbons: territoriality and monogamy. In B. Smuts, D. Cheney, R. M. Seyfarth, R. W. Wrangham, and T T. Shruhsaker (Eds.), Primate Societies, pp. 135–145. Chicago: University of Chicago Press.Google Scholar
  63. Lifjeld, J. T., P. O. Dunn, and D. F. Westneat. 1994. Sexual selection by sperm competition in birds: Male-male competition or female choice? Journal of Avian Biology 25:244–250.CrossRefGoogle Scholar
  64. Lifjeld, J. T. and R. J. Robertson. 1992. Female control of extra-pair fertilization in tree swallows. Behavioral Ecology and Sociobiology 31:86–96.CrossRefGoogle Scholar
  65. Lumpkin, S. 1983. Female manipulation of male avoidance of cuckoldry behavior in the ring dove. In S. K. Waser (Ed.), Social Behavior of Female Vertebrates, pp. 91–112. New York: Academic Press.Google Scholar
  66. McKinney, F., K. M. Cheng, and D. J. Bruggers. 1984. Sperm competition in apparently monogamous birds. In R. L. Smith (Ed.), Sperm Competition and the Evolution of Animal Mating Systems, pp. 523–545. New York: Academic Press.Google Scholar
  67. Meek, S. B. and R. J. Robertson. 1994. Interspecific competition for nestboxes affects mate guarding in eastern bluebirds, Sialia sialis. Animal Behaviour 47:295–302.CrossRefGoogle Scholar
  68. Møller, A. P. 1990. Changes in the size of avian territories in relation to the nesting cycle. Animal Behaviour 43:860–861.CrossRefGoogle Scholar
  69. Morton, E. S., L. Forman, and M. Braun. 1990. Extra-pair fertilizations and the evolution of colonial breeding in purple martins. Auk 107:275–283.CrossRefGoogle Scholar
  70. Mulder, R. A. 1992. Evolutionary ecology of the mating system of superb fairy-wrens. Ph.D. dissertation, Australian National University, Canberra.Google Scholar
  71. Orians, G. H. 1969. On the evolution of mating systems in birds and mammals. American Naturalist 103:589–603.CrossRefGoogle Scholar
  72. Petrie, M. 1992. Copulation frequency in birds: Why do females copulate more than once with the same male? Animal Behaviour 44:790–792.CrossRefGoogle Scholar
  73. Petrie, M. and F. M. Hunter. 1993. Intraspecific variation in courtship and copulation frequency: An effect of mismatch in partner attractiveness? Behaviour 127:265–277.CrossRefGoogle Scholar
  74. Petrie, M. and A. Williams. 1993. Peahens lay more eggs for peacocks with larger trains. Proceedings of the Royal Society of London B Biological Sciences 251:127–131.CrossRefGoogle Scholar
  75. Pinxten, R., L. van Elsacker, and R. F. Verheyen. 1987. Duration and temporal pattern of mate guarding in the starling. Ardea 75:263–269.Google Scholar
  76. Promislow, D. E., R. Montgomerie, and T. E. Martin. 1992. Mortality costs of sexual dimorphism in birds. Proceedings of the Royal Society of London B Biological Sciences 250:143–150.CrossRefGoogle Scholar
  77. Reese, E. S. 1991. How behavior influences community structure of butterflyfishes (family Chaetodontidae) on Pacific coral reefs. Ecology International Bulletin 19:29–41.Google Scholar
  78. Roskaft, T. 1983. Male promiscuity and female adultery in the rook, Corvus fuglegus. Ornis Scandinavica 14:175–179.CrossRefGoogle Scholar
  79. Rowley, I. 1983. Remating in birds. In P. Bateson (Ed.), Mate Choice, pp. 331–360. Cambridge, UK: Cambridge University Press.Google Scholar
  80. Russett, C. E. 1989. Sexual Science: The Victorian Construction of Womanhood. Cambridge, MA: Harvard University Press.Google Scholar
  81. Sheldon, B. C. 1994. Sperm competition in the chaffinch: The role of the female. Animal Behaviour 47:163–173.CrossRefGoogle Scholar
  82. Sheldon, B. C. and T. Burke. 1994. Copulation behavior and paternity in the chaffinch. Behavioral Ecology and Sociobiology 34:149–156.CrossRefGoogle Scholar
  83. Slagsvold, T. and J. T. Lifjeld. 1994. Polygyny in birds: The role of competition between females for male parental care. American Naturalist 143:59–94.CrossRefGoogle Scholar
  84. Smith, S. M. 1988. Extra-pair copulations in black-capped chickadees: The role of the female. Behaviour 107:15–23.CrossRefGoogle Scholar
  85. Smuts, B. B. 1985. Sex and Friendship in Baboons. New York: Aldine.Google Scholar
  86. Stamps, J. A. 1994. Territorial behavior: Testing the assumptions. Advances in the Study of Behavior 23:173–232.CrossRefGoogle Scholar
  87. Thornhill, R. 1984. Alternative hypotheses for traits believed to have evolved by sperm competition. In R. L. Smith (Ed.), Sperm Competition and the Evolution of Animal Mating Systems, pp. 151–178. New York: Academic Press.Google Scholar
  88. Tinbergen, N. 1939. The behavior of the snow bunting in spring. Transactions of the Linnaean Society of New York 5:1–93.Google Scholar
  89. Tinbergen, N. 1959. Comparative studies of the behaviour of gulls (Laridae): A progress report. Behaviour 15:1–70.CrossRefGoogle Scholar
  90. Trivers, R. L. 1972. Parental investment and sexual selection. In B. Campbell (Ed.), Sexual Selection and the Descent of Man: 1871–1971, pp. 136–179. London: Heinemann.Google Scholar
  91. Wagner, R. H. 1991a. The use of extra-pair copulations for mate appraisal by razorbills, Alca torda. Behavioral Ecology 2:198–203.CrossRefGoogle Scholar
  92. Wagner, R. H. 1991b. Pair bond formation in the razorbill. Wilson Bulletin 103:682–685.Google Scholar
  93. Wagner, R. H. 1992. The pursuit of extra-pair copulations by monogamous female razorbills: How do females benefit? Behavioral Ecology and Sociobiology 29:455–464.CrossRefGoogle Scholar
  94. West-Eberhardt, M. J., J. W. Bradbury, N. B. Davies, P. H. Gouyon, P. Hammerstein, B. König, G. A. Parker, N. Sachser, T. Slagsvold, F. Trillmich, C. Vogel. 1987. Conflicts between and within the sexes in sexual selection. In J. W. Bradbury and M. B. Andersson (Eds.), Sexual Selection: Testing the Alternatives, pp. 180–195. Chichester, UK: Wiley.Google Scholar
  95. Westneat, D. F. 1987a. Extra-pair copulations in a predominantly monogamous bird: Observations of behaviour. Animal Behaviour 35:865–876.CrossRefGoogle Scholar
  96. Westneat, D. F. 1987b. Extra-pair fertilizations in a predominantly monogamous bird: Genetic evidence. Animal Behaviour 35:877–886.CrossRefGoogle Scholar
  97. Westneat, D. F., P. W. Sherman, and M. L. Morton. 1990. The ecology and evolution of extra-pair copulations in birds. Current Ornithology 7:331–369.Google Scholar
  98. Whittingham, L. A., P. O. Dunn, and R. J. Robertson. 1994. Do female tree swallows guard their mates by copulating frequently? Animal Behaviour 47:994–997.CrossRefGoogle Scholar
  99. Williams, J. R., K. C. Catania, and S. C. Carter. 1992. Development of partner preferences in female prairie voles (Microtus ochrogaster): The role of social and sexual experience. Hormones and Behavior 26:339–349.CrossRefPubMedGoogle Scholar
  100. Williams, J. R., T. R. Insel, C. R. Harbaugh, and S. C. Carter. 1994. Oxytocin administered centrally facilitates formation of a partner preference in female prairie voles (Microtus ochrogaster). Journal of Neurobiology 6:247–250.Google Scholar
  101. Winslow, J. T., N. Hastings, C. S. Carter, C. R. Harbaugh, and T. R. Insel. 1993. A role for central vasopressin in pair bonding in monogamous prairie voles. Nature 356:545–548.CrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 1997

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  • Judy Stamps

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