Skip to main content Accessibility help
  • Get access
    Check if you have access via personal or institutional login
  • Cited by 5
  • Print publication year: 2004
  • Online publication date: August 2009

6 - Female multiple mating and genetic benefits in humans: investigations of design



William James, one of the founders of scientific psychology (see James, 1890), tells a personal story in which he awoke from a dream one night with a flash of insight. Wanting not to forget it, he scribbled down, in his half-wakened state, the insight and went back to bed. In the morning he recalled having this revelation but not its content, and excitedly went to read his recording. Disappointed, he found these words: Higamus, hogamus, women are monogamous; Hogamus, higamus, men are polygamous (Kitcher, 1987).

Almost certainly, James would not have been able to anticipate that, 100 years later, the whole question of female monogamy or its absence, polyandry, would become one of the most fascinating topics in behavioural biology.

A recent paper published in Animal Behaviour (Zeh & Zeh, 2001, p. 1051) claimed that behavioural ecology is in the process of undergoing a paradigm shift, with ‘the traditional concept of the choosy, monogamous female increasingly giving way to the realisation that polyandry is pervasive in natural populations’ even when males invest substantially in offspring. One form of polyandry that has received much attention is extra-pair copulation (EPC) – sex that a female with a social mate has with a male who is not the social mate. The data showing a mean extra-pair paternity rate of 10–15 per cent in socially monogamous birds (with some rates as high as 70 per cent) are highly familiar (Birkhead & Møller, 1995; Petrie & Kempenaers, 1998).

Aiello, L. C. & Key, C. 2002. Energetic consequences of being a Homo erectus female. American Journal of Human Biology, 14, 551–65
Alexander, R. D. & Noonan, K. 1979. Concealment of ovulation, parental care, and human social evolution. In Evolutionary Biology and Human Behavior: An Anthropological Perspective, ed. N. A. Chagnon & W. Irons. North Scituate, MA: Duxbury, pp. 402–35
Andersson, M. 1994. Sexual Selection. Princeton, NJ: Princeton University Press
Andrews, P. W., Gangestad, S. W. & Matthews, D. 2003. Adaptationism – how to carry out the exaptationist program. Behavioral and Brain Sciences, in press
Arnqvist, G. & Rowe, L. 2002. Antagonistic coevolution between the sexes in a group of insects. Nature, 415, 787–9
Arnqvist, G., Edvardsson, M., Friberg, U. & Nilsson, T. 2000. Sexual conflict promotes speciation in insects. Proceedings of the National Academy of Sciences, USA, 97, 10460–4
Baker, R. R. & Bellis, M. A. 1995. Human Sperm Competition: Copulation, Masturbation and Infidelity. London: Chapman and Hall
Beckerman, S., Lizarralde, R., Ballew, al. 1998. The Bari partible paternity project: preliminary results. Current Anthropology, 39, 164–7
Bellis, M. A. & Baker, R. R. 1990. Do females promote sperm competition? Data for humans. Animal Behaviour, 40, 997–9
Benshoof, L. & Thornhill, R. 1979. The evolution of monogamy and loss of estrus in humans. Journal of Social and Biological Structures, 2, 95–106
Berry, D. S. & Wero, J. L. 1993. Accuracy of face perception: a view from ecological psychology. Journal of Personality, 61, 497–503
Birkhead, T. R. & M⊘ller, A. P. 1995. Extra-pair copulation and extra-pair paternity in birds. Animal Behaviour, 49, 843–8
Birkhead, T. R. & Pizzari, T. 2002. Postcopulatory sexual selection. Nature Reviews Genetics, 3, 262–73
Bock, J. 2002. Learning, life history, and productivity: children's lives in the Okavango Delta, Botswana. Human Nature, 13, 161–97
Brooks, R. & Kemp, D. J. 2001. Can older males deliver the good genes?Trends in Ecology and Evolution, 16, 308–13
Buchanan, K. L. & Catchpole, C. K. 2000. Extrapair paternity in the sedge warbler Acrosephalus schoenobaenus as veiled by multilocus DNA fingerprinting. Ibis, 142, 12–20
Burley, N. 1986. Sexual selection for aesthetic traits in species with biparental care. American Naturalist, 127, 415–45
Burt, A. 1992. Concealed ovulation and sexual signals in primates. Folia Primatologica, 58, 1–6
Burt, A. 1995. Perspective: the evolution of fitness. Evolution, 49, 1–8
Buss, D. M. 1988. From vigilance to violence: mate retention tactics in American undergraduates. Ethology and Sociobiology, 9, 291–317
Buss, D. M. 2000. Dangerous Passions. New York, NY: Free
Buss, D. M. & Schmitt, D. P. 1993. Sexual strategies theory: a contextual evolutionary analysis of human mating. Psychological Review, 100, 204–32
Cerda-Flores, R. M., Barton, S. A., Marty-Gonzalez, L. F., Rivas, F. & Chakraborty, R. 1999. Estimation of nonpaternity in the Mexican population of Nueveo Leon: a validation study with blood group markers. American Journal of Physical Anthropology, 109, 281–93
Charlesworth, B. 1987. The heritability of fitness. In Sexual Selection: Testing the Alternatives, ed. J. W. Bradbury & M. B. Andersson. New York, NY: Wiley, pp. 22–40
Charlesworth, B. 1990. Mutation–selection balance and the evolutionary advantage of sex and recombination. Genetical Research, 55, 199–221
Charlesworth, B. & Hughes, K. A. 1998. The maintenance of genetic variation in life history traits. In Evolutionary Genetics from Molecules to Morphology, ed. R. S. Singh & C. B. Krimbas. Cambridge: Cambridge University Press, pp. 369–91
Ellegren, H., Gustafsson, L. & Sheldon, B. C. 1996. Sex ratio adjustment in relation to paternal attractiveness in a wild bird population. Proceedings of the National Academy of Sciences, USA, 93, 11723–8
Ellis, P., Cristello, M. & Whitmeyer, J. 2003. FA and sperm quality in a sample of Boston men. Evolution and Human Behavior, in press
Fisher, R. A. 1930. The Genetical Theory of Natural Selection. Oxford: Clarendon
Flinn, M. 1987. Mate guarding in a Caribbean village. Ethology and Sociobiology, 8, 1–28
Forstmeier, W., Kempenaers, B., Meyer, A. & Leisler, B. 2002. A novel song parameter correlates with extra-pair paternity and reflects male longevity. Proceedings of the Royal Society of London, Series B, 269, 1479–85
Fuller, R. C. & Houle, D. 2003. Inheritance of developmental instability. In Developmental Instability: Causes and Consequences, ed. M. Polak, in press. New York, NY: Oxford University Press
Furlow, B. F., Armijo-Prewitt, T., Gangestad, S. W. & Thornhill, R. 1997. Fluctuating asymmetry and psychometric intelligence. Proceedings of the Royal Society of London, Series B, 264, 823–9
Furlow, B. F., Gangestad, S. W. & Armijo-Prewitt, T. 1998. Developmental stability and human violence. Proceedings of the Royal Society of London, Series B, 266, 1–6
Gangestad, S. W. & Simpson, J. A. 1990. Toward an evolutionary history of female sociosexual variation. Journal of Personality, 58, 69–96
Gangestad, S. W. & Thornhill, R. 1997a. Human sexual selection and developmental stability. In Evolutionary Social Psychology, ed. J. A. Simpson & D. T. Kenrick. Mahwah, NJ: Lawrence Erlbaum Associates, pp. 169–95
Gangestad, S. W., Thornhill, R. 1997b. The evolutionary psychology of extrapair sex: the role of fluctuating asymmetry. Evolution and Human Behavior, 18, 69–88
Gangestad, S. W., Thornhill, R. 1998. Menstrual cycle variation in women's preferences for the scent of symmetrical men. Proceedings of the Royal Society of London, Series B, 265, 927–33
Gangestad, S. W., Thornhill, R. 1999. Individual differences in developmental precision and fluctuating asymmetry: a model and its implications. Journal of Evolutionary Biology, 12, 402–16
Gangestad, S. W., Thornhill, R. 2003a. Facial masculinity and fluctuating asymmetry. Evolution and Human Behavior, in press
Gangestad, S. W., Thornhill, R. 2003b. Fluctuating asymmetry, developmental stability, and fitness: toward model-based interpretation. In Developmental Instability: Causes and Consequences, ed. M. Polak, in press. New York, NY: Oxford University Press
Gangestad, S. W., Thornhill, R. & Yeo, R. A. 1994. Facial attractiveness, developmental stability, and fluctuating asymmetry. Ethology and Sociobiology, 15, 73–85
Gangestad, S. W., Bennett, K. L. & Thornhill, R. 2001. A latent variable model of developmental stability in relation to men's number of sex partners. Proceedings of the Royal Society of London, Series B, 268, 1677–84
Gangestad, S. W., Thornhill, R. & Garver, C. E. 2002. Changes in women's sexual interests and their partners' mate retention tactics across the menstrual cycle: evidence for shifting conflicts of interest. Proceedings of the Royal Society of London, Series B, 269, 975–82
Gangestad, S. W., Simpson, J. A., Cousins, A. J., Garver, C. E. & Christensen, P. N. 2003a. Women's preferences for male behavioural displays shift across the menstrual cycle. Manuscript under review
Gangestad, S. W., Thornhill, R., Quinlan, R. J. & Flinn, M. V. 2003b. Fluctuating asymmetry, attractiveness, and reproduction in a rural Caribbean village. Manuscript under review
Gavrilets, S., Arnqvist, G. & Friberg, U. 2001. The evolution of female mate choice by sexual conflict. Proceedings of the Royal Society of London, Series B, 268, 531–9
Geary, D. C. 1998. Male, Female: The Evolution of Human Sex Differences. Washington, DC: American Psychological Association
Geary, D. C. 2000. Evolution and proximate expression of human paternal investment. Psychological Bulletin, 126, 55–77
Geary, D. C. & Flinn, M. V. 2002. Sex differences in behavioural and hormonal response to social threat: commentary on Taylor et al. 2000. Psychological Review, 109, 745–50
Getty, T. 1999. Handicap signalling: when fecundity and mortality do not add up. Animal Behaviour, 56, 127–30
Gil, D., Graves, J., Hazon, N. & Wells, A. 1999. Male attractiveness and differential testosterone investment in zebra finch eggs. Science, 286, 126–8
Grafen, A. 1990. Biological signals as handicaps. Journal of Theoretical Biology, 144, 517–46
Gray, P. B., Kahlenberg, S. M., Barrett, E. S., Lipson, S. F. & Ellison, P. T. 2002. Marriage and fatherhood are associated with lower testosterone in males. Evolution and Human Behavior, 23, 193–201
Graziano, W. G., Jensen-Campbell, L. A., Todd, M. & Finch, J. F. 1997. Interpersonal attraction from an evolutionary perspective: women's reactions to dominant and prosocial men. In Evolutionary Social Psychology, ed. J. A. Simpson & D. T. Kenrick. Mahwah, NJ: Lawrence Erlbaum Associates, pp. 141–67
Greiling, H. & Buss, D. M. 2000. Women's sexual strategies: the hidden dimension of short-term extra-pair mating. Personality and Individual Differences, 28, 929–63
Griffith, S. C. & Sheldon, B. C. 2001. Phenotypic plasticity in the expression of sexually selected traits: neglected components of variation. Animal Behaviour, 61, 987–93
Gustafsson, L., Nordling, D., Andersson, M. S., Sheldon, B. C. & Qvarnström, A. 1994. Infectious diseases, reproductive effort and the cost of reproduction in birds. Philosophical Transactions of the Royal Society of London, Series B, 346, 323–31
Gustafsson, L., Qvarnström, A. & Sheldon, B. C. 1995. Trade-offs between life history traits and a secondary sexual character in male collared flycatchers. Nature, 375, 311–13
Hagen, E. H., Hames, R. B., Craig, N. M., Lauer, M. T. & Price, M. E. 2001. Parental investment and child health in a Yanomamo village suffering short-term food stress. Journal of Biosocial Science, 33, 503–28
Hamilton, W. D. 1982. Pathogens as causes of genetic diversity in their host populations. In Population Biology of Infectious Diseases, ed. R. M. Anderson & R. M. May. New York, NY: Springer-Verlag, pp. 269–96
Hamilton, W. D. & Zuk, M. 1982. Heritable true fitness and bright birds: a role for parasites. Science, 218, 384–7
Hasselquist, D. 1998. Polygyny in great reed warblers: a long-term study of factors contributing to male fitness. Ecology, 79, 2376–90
Hasselquist, D., Bensch, S. & Schantz, T. 1996. Correlation between male song repertoire, extrapair paternity and offspring survival in the great reed warbler. Nature, 381, 229–32
Hawkes, K. & Bird, R. B. 2002. Showing off, handicap signaling, and men's work. Evolutionary Anthropology, 11, 58–67
Hawkes, R., Connell, J. F. & Blurton Jones, N. G. 2001. Hunting and nuclear families: some lessons from the Hadza about men's work. Current Anthropology, 42, 681–709
Herz, R. S. & Cahill, E. D. 1997. Differential use of sensory information in sexual behavior as a function of gender. Human Nature, 8, 275–86
Hill, K. & Hurtado, A. M. 1996. Ache Life History. New York, NY: Aldine de Gruyter
Hoi, H. 1997. Assessment of the quality of copulation partners in the monogamous bearded tit. Animal Behaviour, 53, 277–86
Houle, D. 1992. Comparing evolvability and variability of traits. Genetics, 130, 195–204
Houle, D. 2000. A simple model of the relationship between asymmetry and developmental stability. Journal of Evolutionary Biology, 13, 720–30
Houle, D. & Kondrashov, A. S. 2002. Coevolution of costly mate choice and condition-dependent display of good genes. Proceedings of the Royal Society of London, Series B, 269, 97–104
Houtman, A. M. 1992. Female zebra finches choose extra-pair copulations with genetically attractive males. Proceedings of the Royal Society of London, Series B, 249, 3–6
Hrdy, S. B. 1979. Infanticide among animals: a review, classification, and examination of the implications for the reproductive strategies of females. Ethology and Sociobiology, 1, 13–40
Hrdy, S. B. 1999. Mother Nature: A History of Mothers, Infants and Natural Selection. New York, NY: Pantheon
Hughes, S. M., Harrison, M. A. & Gallup, G. G. 2002. The sound of symmetry: voice as a marker of developmental instability. Evolution and Human Behavior, 23, 173–80
Iwasa, Y. & Pomiankowski, A. 1994. The evolution of mate preferences for multiple sexual ornaments. Evolution, 48, 853–67
Iwasa, Y., Pomiankowski, A. & Nee, S. 1991. The evolution of costly mate preferences. II. The ‘handicap’ principle. Evolution, 45, 1431–42
Jacob, S., McClintock, M. K., Zelano, B. & Ober, C. 2002. Paternally inherited alleles are associated with women's choice of male odor. Nature Genetics, 30, 175–9
James, W. 1890. The Principles of Psychology. London: Macmillan
Jennions, M. D. & Petrie, M. 2000. Why do females mate multiply? A review of the genetic benefits. Biological Reviews, 75, 21–64
Jöchle, W. 1973. Coitus induced ovulation. Contraception, 7, 523–64
Johnsen, A., Andersen, V., Sunding, C. & Lifjeld, J. T. 2000. Female bluethroats enhance offspring immunocompetence through extra-pair copulations. Nature, 406, 296–9
Johnsen, A., Lifjeld, J. T., Andersson, S., Ornborg, J. & Amundsen, T. 2001. Male characteristics and fertilisation success in male bluethroats. Behavior, 138, 1371–90
Johnston, V. S., Hagel, R., Franklin, M., Fink, B. & Grammer, K. 2001. Male facial attractiveness: evidence for hormone mediated adaptive design. Evolution and Human Behavior, 23, 251–67
Kaplan, H. S., Hill, K., Lancaster, J. B. & Hurtado, A. M. 2000. A theory of human life history evolution: diet, intelligence, and longevity. Evolutionary Anthropology, 9, 156–85
Kinsey, A. C., Pomeroy, W. B., Martin, C. E. & Gebhard, P. H. 1953. Sexual Behavior in the Human Female. Philadelphia, PA: W. B. Saunders
Kirkpatrick, M. 1996. Good genes and direct selection in the evolution of mating preferences. Evolution, 50, 2125–40
Kirkpatrick, M. & Barton, N. H. 1997. The strength of indirect selection on female mating preferences. Proceedings of the National Academy of Sciences, USA, 94, 1282–6
Kitcher, P. 1987. Vaulting Ambition: Sociobiology and the Quest for Human Nature. Cambridge, MA: MIT Press
Kokko, H. 1998. Good genes, old age and life history trade-offs. Evolutionary Ecology, 12, 739–50
Laumann, E. O., Gagnon, J. H., Michael, R. T. & Michaels, S. 1994. The Social Organization of Sexuality. Chicago, IL: University of Chicago Press
Leigh, S. R. 2001. Evolution of human growth. Evolutionary Anthropology, 10, 223–36
Lens, L., Dongen, S., Kark, S. & Matthysen, E. 2002. Fluctuating asymmetry as an indicator of fitness: can we bridge the gap between studies?Biological Reviews, 77, 27–38
Leonard, W. R. & Robertson, M. L. 1997. Comparative primate energetics and hominid evolution. American Journal of Physical Anthropology, 102, 265–81
Lubjuhn, T., Strohbach, S., Brun, J., Gerken, T. & Epplen, J. T. 1999. Extra-pair paternity in great tits (Parus major): a long-term study. Behavior, 136, 1157–72
Luuthe, V., Sugimoto, Y., Puy, al. 1994. Characterization, expression, and immunohistochemical localization of 5-alpha-reductase activity in human skin. Journal of Investigative Dermatology, 102, 221–6
Lynch, M., Blanchard, J., Houle, al. 1999. Perspective: spontaneous deleterious mutation. Evolution, 53, 645–63
Manning, J. T. & Wood, D. 1998. Fluctuating asymmetry and aggression in boys. Human Nature, 9, 53–65
Manning, J. T., Koukourakis, K. & Brodie, D. A. 1997. Fluctuating asymmetry, metabolic rate and sexual selection in human males. Evolution and Human Behavior, 18, 15–21
Manning, J. T., Scutt, D. & Lewis-Jones, D. I. 1998. Developmental stability, ejaculate size and sperm quality in men. Evolution and Human Behavior, 19, 273–82
Marlowe, F. 2000. Paternal investment and the human mating system. Behavioural Processes, 51, 45–61
McIntyre, S. & Sooman, A. 1991. Non-paternity and prenatal genetic screening. Lancet, 338, 869
Michl, G., Torok, J., Griffith, S. C. & Sheldon, B. C. 2002. Experimental analysis of sperm competition mechanisms in a wild bird population. Proceedings of the National Academy of Sciences, USA, 99, 5466–70
M⊘ller, A. P. 1999. Asymmetry as a predictor of growth, fecundity and survival. Ecology Letters, 2, 149–56
M⊘ller, A. P. & Alatalo, R. V. 1999. Good-genes effects in sexual selection. Proceedings of the Royal Society of London, Series B, 266, 85–91
M⊘ller, A. P. & Swaddle, J. P. 1997. Asymmetry, Developmental Stability and Evolution. Oxford: Oxford University Press
M⊘ller, A. P. & Thornhill, R. 1998a. Bilateral symmetry and sexual selection: a meta-analysis. American Naturalist, 151, 174–92
M⊘ller, A. P. & Thornhill, R. 1998b. Male parental care, differential parental investment by females, and sexual selection. Animal Behaviour, 55, 1507–15
M⊘ller, A. P., Saino, N., Taramino, G., Galeotti, P. & Ferrario, S. 1998. Paternity and sexual signaling: effects of a secondary sexual character and song on paternity in the barn swallow. American Naturalist, 151, 236–42
M⊘ller, A. P., Gangestad, S. W. & Thornhill, R. 1999. Nonlinearity and the importance of fluctuating asymmetry as a predictor of fitness. Oikos, 86, 366–8
Montgomerie, R. & Bullock, H. 1999. Fluctuating asymmetry and the human female orgasm. Paper presented at the annual meeting of the Human Behavior and Evolution Society, Salt Lake City, UT, June
Oliver-Rodriguez, J. C., Guan, Z. & Johnston, V. S. 1999. Gender differences in late positive components evoked by human faces. Psychophysiology, 36, 176–85
Otter, K., Ratcliffe, L., Michaud, D. & Boag, P. T. 1998. Do female black-capped chickadees prefer high-ranking males as extra-pair partners?Behavioral Ecology and Sociobiology, 43, 25–36
Otter, K. A., Stewart, I. R. K., McGregor, P. al. 2001. Extra-pair paternity among great tits Parus major following manipulation of male signals. Journal of Avian Biology, 32, 338–42
Pärt, T. & Qvarnström, A. 1997. Badge size in collared flycatchers predicts outcome of male competition over territories. Animal Behaviour, 54, 893–9
Pawlowski, B. 1999. Loss of oestrus and concealed ovulation in human evolution: the case against the sexual-selection hypothesis. Current Anthropology, 40, 257–75
Penton-Voak, I. S. & Perrett, D. I. 2000. Female preference for male faces changes cyclically: further evidence. Evolution and Human Behavior, 21, 39–48
Penton-Voak, I. S., Perrett, D. I., Castles, al. 1999. Female preference for male faces changes cyclically. Nature, 399, 741–2
Perrett, D. I., Lee, K. J., Penton-Voak, al. 1998. Effects of sexual dimorphism on facial attractiveness. Nature, 394, 884–7
Petrie, M. & Kempenaers, B. 1998. Extra-pair paternity in birds: explaining variation between species and populations. Trends in Ecology and Evolution, 13, 52–8
Pizzari, T., Froman, D. P. & Birkhead, T. R. 2002. Pre- and post-insemination episodes of sexual selection in the fowl, Gallus g. domesticus. Heredity, 88, 112–16
Pomiankowski, A. N. 1988. The evolution of mate preferences for male genetic quality. Oxford Surveys in Evolutionary Biology, 5, 136–84
Pomiankowski, A. N. & M⊘ller, A. P. 1995. A resolution of the lek paradox. Proceedings of the Royal Society of London, Series B, 260, 21–9
Qvarnström, A. 1997. Experimentally increased badge size increases male competition and reduces male parental care in the collared flycatcher. Proceedings of the Royal Society of London, Series B, 264, 1225–31
Qvarnström, A. 1999a. Genotype-by-environment interactions in the determination of the size of a secondary sexual character in the collared flycatcher (Ficedula albicollis). Evolution, 53, 1564–72
Qvarnström, A. 1999b. Different reproductive tactics in male collared flycatchers signalled by size of secondary sexual character. Proceedings of the Royal Society of London, Series B, 266, 2089–93
Qvarnström, A., Part, T. & Sheldon, B. C. 2000. Adaptive plasticity in mate preference linked to differences in reproductive effort. Nature, 405, 344–7
Ratti, O., Hovi, M., Lundberg, A., Telegstrom, H. & Alatalo, R. V. 1995. Extra-pair paternity and male characteristics in the pied flycatcher. Behavioral Ecology and Sociobiology, 37, 419–25
Reeve, H. K. & Sherman, P. W. 1993. Adaptation and the goals of evolutionary research. Quarterly Review of Biology, 68, 1–32
Regan, P. C. & Berscheid, E. 1995. Gender differences in beliefs about the causes of male and female sexual desire. Personal Relationships, 2, 345–58
Rice, W. R. 1996. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature, 381, 232–4
Rice, W. R. & Holland, B. 1998. The enemies within: intragenomic conflict, interlocus contest evolution (ICE), and the intraspecific Red Queen. Behavioral Ecology and Sociobiology, 41, 1–10
Richardson, D. S. & Burke, T. 1999. Extra-pair paternity in relation to male age in Bullock's orioles. Molecular Ecology, 8, 2115–26
Rikowski, A. & Grammer, K. 1999. Human body odour, symmetry and attractiveness. Proceedings of the Royal Society of London, Series B, 266, 869–74
Rowe, L. & Houle, D. 1996. The lex paradox and the capture of genetic variance by condition-dependent traits. Proceedings of the Royal Society of London, Series B, 263, 1415–21
Sasse, G., Muller, H., Chakraborty, R. & Ott, J. 1994. Estimating the frequency of nonpaternity in Switzerland. Human Heredity, 44, 337–43
Scheib, J. E., Gangestad, S. W. & Thornhill, R. 1999. Facial attractiveness, symmetry, and cues of good genes. Proceedings of the Royal Society of London, Series B, 266, 1318–21
Shackelford, T. K., Weekes-Shackelford, V. A., LeBlanc, et al. 1999. Female coital orgasm and male attractiveness. Human Nature, 11, 299–306
Shackelford, T. K., LeBlanc, G. J., Weekes-Shakelford, et al. 2002. Psychological adaptation to human sperm competition. Evolution and Human Behavior, 23, 123–38
Sheldon, B. C. & Ellegren, H. 1999. Sexual selection resulting from extrapair paternity in collared flycatchers. Animal Behaviour, 57, 285–98
Sheldon, B. C., Merila, J., Qvarnström, A., Gustafsson, L. & Ellegren, H. 1997. Paternal genetic contribution to offspring condition predicted by size of male secondary sexual character. Proceedings of the Royal Society of London, Series B, 264, 297–302
Sheldon, B. C., Davidson, P. & Lindgren, G. 1999. Mate replacement in experimentally widowed collared flycatchers (Ficedula albicollis): determinants and outcomes. Behavioral Ecology and Sociobiology, 46, 141–8
Sillén-Tullberg, B. & M⊘ller, A. P. 1993. The relationship between concealed ovulation and mating systems in anthropoid primates: a phylogenetic analysis. American Naturalist, 141, 1–25
Simpson, J. A., Gangestad, S. W., Christensen, P. N. & Leck, K. 1999. Fluctuating asymmetry, sociosexuality and intrasexual competitive tactics. Journal of Personality and Social Psychology, 76, 159–72
Singh, D. & Bronstad, P. M. 2001. Female body odour is a potential cue to ovulation. Proceedings of the Royal Society of London, Series B, 268, 797–801
Smuts, B. B. & Smuts, R. W. 1993. Male aggression and sexual coercion of females in nonhuman primates and other mammals: evidence and theoretical implications. Advances in the Study of Behavior, 22, 1–63
Stanford, C. B. 1998. The social behavior of chimpanzees and bonobos. Current Anthropology, 39, 399–419
Stutchbury, B. J. M., Piper, W. H., Neudorf, D. al. 1997. Correlates of extra-pair fertilization success in hooded warblers. Behavioral Ecology and Sociobiology, 40, 119–26
Swaddle, J. P. & Reierson, G. W. 2002. Testosterone increases the perceived dominance but not attractiveness of human males. Proceedings of the Royal Society of London, Series B, 269, 2285–9
Symons, D. 1979. The Evolution of Human Sexuality. Oxford: Oxford University Press
Symons, D. 1992. On the use and misuse of Darwinism in the study of human behavior. In The Adapted Mind: Evolutionary Psychology and the Generation of Culture, ed. J. Barkow, L. Cosmides & J. Tooby. Oxford: Oxford University Press, pp. 137–59
Thoma, R. J., Yeo, R. A., Gangestad, S. W., Lewine, J. D. & Davis, J. T. 2002. Fluctuating asymmetry and the human brain. Laterality, 7, 45–58
Thompson, A. P. 1983. Extramarital sex: a review of the research literature. Journal of Sex Research, 19, 1–22
Thornhill, R. 1990. The study of adaptation. In Interpretation and Explanation in the Study of Behavior, ed. M. Bekoff & D. Jamieson. Boulder, CO: Westview, pp. 31–62
Thornhill, R. 1997. The concept of an evolved adaptation. In Characterizing Human Psychological Adaptations, ed. M. Daly. London: Wiley, pp. 4–13
Thornhill, R. & Gangestad, S. W. 1993. Human facial beauty: averageness, symmetry, and parasite resistance. Human Nature, 4, 237–70
Thornhill, R. & Gangestad, S. W. 1994. Fluctuating asymmetry and human sexual behavior. Psychological Science, 5, 297–302
Thornhill, R. & Gangestad, S. W. 1999a. The scent of symmetry: a human sex pheromone that signals fitness?Evolution and Human Behavior, 20, 175–201
Thornhill, R. & Gangestad, S. W. 1999b. Facial attractiveness. Trends in Cognitive Sciences, 3, 452–60
Thornhill, R. & Gangestad, S. W. 2003. Do women have evolved adaptation for extra-pair copulation? In Evolutionary Aesthetics, ed. E. Voland & K. Grammer. Hamburg: Springer-Verlag, pp. 341–68
Thornhill, R. & M⊘ller, A. P. 1997. Developmental stability, disease and medicine. Biological Reviews, 72, 497–548
Thornhill, R. & Palmer, C. T. 2000. A Natural History of Rape: Biological Bases of Sexual Coercion. Cambridge, MA: MIT Press
Thornhill, R., Gangestad, S. W. & Comer, R. 1995. Human female orgasm and mate fluctuating asymmetry. Animal Behaviour, 50, 1601–15
Thornhill, R., Gangestad, S. W., Miller, R. et al. 2003. MHC, symmetry and body scent attractiveness in men and women (Homo sapiens). Behavioral Ecology
Tooby, J. 1982. Pathogens, polymorphism, and the evolution of sex. Journal of Theoretical Biology, 97, 557–76
Trivers, R. L. 1972. Parental investment and sexual selection. In Sexual Selection and the Descent of Man, 1871–1971, ed. B. Campbell. Chicago, IL: Aldine, pp. 139–79
Troisi, A. & Carosi, M. 1998. Female orgasm rate increases with male dominance in Japanese macaques. Animal Behaviour, 56, 1261–6
Dongen, S. 2000. The heritability of fluctuating asymmetry: a Bayesian hierarchical model. Acta Zoologica Fennici, 37, 15–23
Wagner, G. P. & Altenberg, L. 1996. Perspective: complex adaptations and the evolution of evolvability. Evolution, 50, 967–76
Wagner, R. H. 1992. The pursuit of extra-pair copulations by female razorbills: how do females benefit?Behavioral Ecology and Sociobiology, 29, 455–64
Watson, P. J. 1998. Multi-male mating and female choice increase offspring growth in the spider Neriene litigiosa (Linyphiidae). Animal Behaviour, 55, 387–403
Wedekind, C. & Füri, S. 1997. Body odour preference in men and women: do they aim for specific MHC combinations or simply heterozygosity?Proceedings of the Royal Society of London, Series B, 264, 1471–9
Wedekind, C., Seebeck, T., Bettens, F. & Paepke, A. J. 1995. MHC-dependent mate preferences in humans. Proceedings of the Royal Society of London, Series B, 260, 245–9
Wilcox, A. J., Weinberg, C. R. & Baird, B. D. 1995. Timing of sexual intercourse in relation to ovulation. New England Journal of Medicine, 333, 1517–21
Williams, G. C. 1966. Adaptation and Natural Selection: A Critique of Some Current Evolutionary Thought. Princeton, NJ: Princeton University Press
Wilson, M. & Daly, M. 1992. The man who mistook his wife for a chattel. In The Adapted Mind: Evolutionary Psychology and the Generation of Culture, ed. J. Barkow, L. Cosmides & J. Tooby. Oxford: Oxford University Press, pp. 289–326
Yeo, R. A., Hill, D., Campbell, R., Vigil, J. & Brooks, W. M. 2000. Developmental instability and working memory ability in children: a magnetic resonance spectroscopy investigation. Developmental Neuropsychology, 17, 143–59
Zeh, J. A. & Zeh, D. W. 2001. Reproductive mode and the genetic benefits of polyandry. Animal Behaviour, 61, 1051–63