Sexual selection, behaviour and sexually transmitted diseases

Charles L. Nunn; Sonia M. Altizer

doi:10.1017/CBO9780511542459.009

7 - Sexual selection, behaviour and sexually transmitted diseases

Published online by Cambridge University Press: 10 August 2009

Charles L. Nunn and

Sonia M. Altizer

Edited by

Peter M. Kappeler and

Carel P. van Schaik

Show author details

Charles L. Nunn: Affiliation:
Department of Biology, University of California, Davis, CA, USA
Sonia M. Altizer: Affiliation:
Department of Environmental Studies Emory, University Atlanta, GA, USA
Peter M. Kappeler: Affiliation:
Deutsches Primatenzentrum, Göttingen, Germany
Carel P. van Schaik: Affiliation:
Duke University, North Carolina

Book contents

Get access

Summary

INTRODUCTION

Factors that alter the contact structure of individuals within populations will influence the spread of parasites that are transmitted by direct contact (Anderson & May, 1991; Blower & McLean, 1991). Few cases illustrate this fundamental principle of epidemiology better than sexual selection and the spread of sexually transmitted diseases (STDs). Sexual selection involves variation in mating success mediated by male–male competition or female choice. By changing the structure of mating contacts within a population, sexual selection influences the spread of sexually transmitted infections. In particular, those individuals with the greatest mating success are at highest risk of contracting STDs, and will also contribute disproportionately to STD spread and persistence (Graves & Duvall, 1995; Thrall et al., 2000). Moreover, promiscuity associated with sperm competition is predicted to increase both the spread and virulence of STDs (Thrall et al., 1997). Therefore STDs may represent a substantial cost of sexual selection and non-monogamous mating behaviour (Thrall et al., 2000).

Sexually transmitted diseases have been virtually ignored in studies of animal mating systems (Smith & Dobson, 1992; Lockhart et al., 1996), but it is now possible to link epidemiological theory on STDs to patterns of infection in wild populations. In this chapter, we explore the consequences of sexual selection, for the spread of STDs in primates. We also examine behavioural defences to avoid infection, specifically addressing interactions between parasite fitness and host reproductive success.

Type: Chapter
Information: Sexual Selection in Primates
New and Comparative Perspectives
, pp. 117 - 130

DOI: https://doi.org/10.1017/CBO9780511542459.009 [Opens in a new window]

Publisher: Cambridge University Press

Print publication year: 2004

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abbot, P. & Dill, L. M. 2001. Sexually transmitted parasites and sexual selection in the milkweed leaf beetle, Labidomera clivicollis. Oikos, 92, 91–100CrossRef Google Scholar

Able, D. J. 1996. The contagion indicator hypothesis for parasite-mediated sexual selection. Proceedings of the National Academy of Sciences, USA, 93, 2229–33CrossRef Google Scholar PubMed

Alexander, N. J. 1990. Sexual transmission of human immunodeficiency virus: virus entry into the male and female genital tract. Fertility and Sterility, 54, 1–18Google Scholar PubMed

Anderson, C. M. 1986. Female age: male preference and reproductive success in primates. International Journal of Primatology, 7, 305–26CrossRef Google Scholar

Anderson, R. M. & May, R. M. 1991. Infectious Diseases of Humans: Dynamics and Control. Oxford: Oxford University Press

Baron, S., Singh, I., Chopra, A., Coppenhaver, D. & Pan, J. Z. 2000. Innate antiviral defenses in body fluids and tissues. Antiviral Research, 48, 71–89CrossRef Google Scholar PubMed

Barratt, C. L. R., Bolton, A. E. & Cooke, I. D. 1990. Functional significance of white blood cells in the male and female reproductive tract. Human Reproduction, 5, 639–48CrossRef Google Scholar PubMed

Bibollet-Ruch e, F., Galat-Luong, A., Cuny, G.et al. 1996. Simian immunodeficiency virus infection in a patas monkey (Erythrocebus patas): evidence for cross-species transmission from African green monkeys (Cercopithecus aethiops sabaeus) in the wild. Journal of General Virology, 77, 773–81CrossRef Google Scholar

Blower, S. M. & McLean, A. R. 1991. Mixing ecology and epidemiology. Proceedings of the Royal Society of London, Series B, 245, 187–92CrossRef Google Scholar PubMed

Boinski, S. 1992. Olfactory communication among Costa Rican squirrel monkeys: a field study. Folia Primatologica, 59, 127–36CrossRef Google Scholar PubMed

Botha, M. C., Jones, M., Deklerk, W. A. & Yamamoto, N. 1985. Spread and distribution of human T-cell leukemia-virus type-I-reactive antibody among baboons and monkeys in the northern and eastern Transvaal. South African Medical Journal, 67, 665–8Google Scholar

Bull, J. J. 1994. Virulence. Evolution, 48, 1423–37Google Scholar PubMed

Courgnaud, V., Pourrut, X., Bibollet-Ruche, F.et al. 2001. Characterization of a novel simian immunodeficiency virus from guereza colobus monkeys (Colobus guereza) in Cameroon: a new lineage in the nonhuman primate lentivirus family. Journal of Virology, 75, 857–66CrossRef Google Scholar PubMed

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

Dixson, A. F. 1998. Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes, and Humans. Oxford: Oxford University Press

Donovan, B. 2000a. The repertoire of human efforts to avoid sexually transmissible diseases: past and present. Part 1: strategies used before or instead of sex. Sexually Transmitted Infections, 76, 7–12CrossRef Google Scholar

Donovan, B. 2000b. The repertoire of human efforts to avoid sexually transmissible diseases: past and present. Part 2: strategies used during or after sex. Sexually Transmitted Infections, 76, 88–93CrossRef Google Scholar

Dracopoli, N. C., Turner, T. R., Else, J. G.et al. 1986. STLV-I antibodies in feral populations of east-african vervet monkeys (Cercopithecus aethiops). International Journal of Cancer, 38, 523–9CrossRef Google Scholar

Eberhard, W. G. 1985. Sexual Selection and Animal Genitalia. Cambridge, MA: Harvard University Press

Ebert, D. 1994. Virulence and local adaptation of a horizontally transmitted parasite. Science, 265, 1084–6CrossRef Google Scholar PubMed

Ewald, P. W. 1994. Evolution of Infectious Disease. Oxford: Oxford University Press

Galat-Luong, A., Bibollet-Ruche, F., Pourrut, X.et al. 1994a. Social organization and SIV seroepidemiology of a patas monkey population in Senegal. Folia Primatologica, 63, 226–8CrossRef Google Scholar

Galat-Luong, A., Galat, G., Bibollet-Ruche, F. et al. 1994b. Social structure and SIVagm prevalence in two groups of green monkeys, Cercopithecus aethiops sabaeus, in Senegal. In Current Primatology. Vol. 3: Behavioral Neuroscience, Physiology and Reproduction, ed. J. R. Anderson, J. J. Roeder, B. Thierry & N. Herrenschmidt. Strasbourg: Université Louis Pasteur, pp. 259–62

Garnett, G. P. & Anderson, R. M. 1993. No reason for complacency about the potential demographic impact of AIDS in Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene, 87, 19–22CrossRef Google Scholar PubMed

Georges-Courb ot, M. C., Moisson, P., Leroy, E.et al. 1996. Occurrence and frequency of transmission of naturally occurring simian retroviral infections (SIV, STLV, and SRV) at the CIRMF Primate Center, Gabon. Journal of Medical Primatology, 25, 313–26CrossRef Google Scholar

Getz, W. M. & Pickering, J. 1983. Epidemic models: thresholds and population regulation. American Naturalist, 121, 892–8CrossRef Google Scholar

Goldizen, A. W. 1988. Tamarin and marmoset mating systems: unusual flexibility. Trends in Ecology and Evolution, 3, 36–40CrossRef Google Scholar PubMed

Graves, B. M. & Duvall, D. 1995. Effects of sexually-transmitted diseases on heritable variation in sexually selected systems. Animal Behaviour, 50, 1129–31CrossRef Google Scholar

Hahn, B. H., Shaw, G. M., Cock, K. M. & Sharp, P. M. 2000. AIDS as a zoonosis: scientific and public health implications. Science, 287, 607–14CrossRef Google Scholar PubMed

Hamilton, W. D. & Zuk, M. 1982. Heritable true fitness and bright birds: a role for parasites?Science, 218, 384–7CrossRef Google Scholar

Hart, B. J., Korinek, E. & Brennan, P. 1987. Postcopulatory genital grooming in male rats: prevention of sexually transmitted infections. Physiology and Behavior, 41, 321–5CrossRef Google Scholar PubMed

Hausfater, G. & Hrdy, S. B. 1984. Infanticide: Comparative and Evolutionary Perspectives. New York, NY: Aldine de Gruyter

Hayami, M., Komuro, A., Nozawa, K.et al. 1984. Prevalence of antibody to adult T-cell leukemia virus-associated antigens (ATLA) in Japanese monkeys and other non-human primates. International Journal of Cancer, 33, 179–83CrossRef Google Scholar PubMed

Herre, E. A. 1995. Factors affecting the evolution of virulence: nematode parasites of fig wasps as a case study. Parasitology, 111, S179–91CrossRef Google Scholar

Hoeprich, P. D., Jordan, M. C. & Ronald, A. R. 1994. Infectious Diseases: A Treatise of Infectious Processes. Philadelphia, PA: J. B. Lippincott

Holmes, K. K., Sparling, P. F., Mardh, P.-A. et al. 1999. Sexually Transmitted Diseases. New York, NY: McGraw Hill

Hooper, R. R., Reynolds, G. H., Jones, O. G.et al. 1978. Cohort study of venereal disease. I: The risk of gonorrhea transmission from infected women to men. American Journal of Epidemiology, 108, 136–44CrossRef Google Scholar PubMed

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, 13–40CrossRef Google Scholar

Huffman, M. A., Gotoh, S., Turner, L. A., Hamai, M. & Yoshida, K. 1997. Seasonal trends in intestinal nematode infection and medicinal plant use among chimpanzees in the Mahale Mountains, Tanzania. Primates, 38, 111–25CrossRef Google Scholar

Immerman, R. S. 1986. Sexually transmitted disease and human evolution: survival of the ugliest?Human Ethology Newsletter, 4, 6–7Google Scholar

Ishida, T., Yamamoto, K., Kaneko, R., Tokita, E. & Hinuma, Y. 1983. Seroepidemiological study of antibodies to adult T-cell leukemia virus-associated antigen (ATLA) in free-ranging Japanese monkeys (Macaca fuscata). Microbiology and Immunology, 27, 297–301CrossRef Google Scholar

Ishikawa, K., Fukasawa, M., Tsujimoto, H.et al. 1987. Serological survey and virus isolation of simian T-cell leukemia/lymphotropic virus Type-I (STLV-I) in nonhuman primates in their native countries. International Journal of Cancer, 40, 233–9CrossRef Google Scholar

Jolly, A. 1966. Lemur Behavior. Chicago, IL: University of Chicago Press

Jolly, C. J., Phillips-Conroy, J. E., Turner, T. R., Broussard, S. & Allan, J. S. 1996. SIVagm incidence over two decades in a natural population of Ethiopian grivet monkeys (Cercopithecus aethiops aethiops). Journal of Medical Primatology, 25, 78–83CrossRef Google Scholar

Kappeler, P. M. 2000. Causes and consequences of unusual sex ratios among lemurs. In Primate Males: Causes and Consequences of Variation in Group Composition, ed. P. M. Kappeler. Cambridge: Cambridge University Press, pp. 55–63

Knell, R. J. 1999. Sexually transmitted disease and parasite-mediated sexual selection. Evolution, 53, 957–61CrossRef Google Scholar PubMed

Lockhart, A. B., Thrall, P. H. & Antonovics, J. 1996. Sexually transmitted diseases in animals: ecological and evolutionary implications. Biological Reviews, 71, 415–71CrossRef Google Scholar PubMed

Loehle, C. 1995. Social barriers to pathogen transmission in wild animal populations. Ecology, 76, 326–35CrossRef Google Scholar

Mason, W. A. 1966. Social organization of the South American monkey, Callicebus moloch: a preliminary report. Tulane Studies in Zoology, 13, 23–8Google Scholar

M⊘ller, A. P. 1993. A fungus infecting domestic flies manipulates sexual behavior of its host. Behavioral Ecology and Sociobiology, 33, 403–7Google Scholar

Nerrienet, E., Amouretti, X., Mullertrutwin, M. C.et al. 1998. Phylogenetic analysis of SIV and STLV Type I in mandrills (Mandrillus sphinx): indications that intracolony transmissions are predominantly the result of male-to-male aggressive contacts. AIDS Research and Human Retroviruses, 14, 785–96CrossRef Google Scholar PubMed

Norley, S., Beer, B., Holzammer, S., Zur Megede, J. & Kurth, R. 1999. Why are natural hosts of SIV resistant to AIDS?Immunology Letters, 66, 47–52CrossRef Google Scholar PubMed

Nunn, C. L. 2002. A comparative study of leukocyte counts and disease risk in primates. Evolution, 56, 177–90CrossRef Google Scholar PubMed

Nunn, C. L. 2003. Behavioural defences against sexually transmitted diseases in primates. Animal Behaviour, in press

Nunn, C. L., Gittleman, J. L. & Antonovics, J. 2000. Promiscuity and the primate immune system. Science, 290, 1168–70CrossRef Google Scholar PubMed

Nunn, C. L., Gittleman, J. L. & Antonovics, J. 2003. A comparative study of white blood cell counts and disease risk in carnivores. Proceedings of the Royal Society of London, Series B. Biological Sciences, 270, 347–56CrossRef Google Scholar PubMed

Padian, N. S., Shiboski, S. C., Glass, S. O. & Vittinghoff, E. 1997. Heterosexual transmission of human immunodeficiency virus (HIV) in Northern California: results from a ten-year study. American Journal of Epidemiology, 146, 350–7CrossRef Google Scholar PubMed

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

Pandya, I. J. & Cohen, J. 1985. The leukocytic reaction of the human uterine cervix to spermatozoa. Fertility and Sterility, 43, 417–21CrossRef Google Scholar PubMed

Phillips, D. M. & Mahler, S. 1977. Leukocyte emigration and migration in the vagina following mating in the rabbit. Anatomical Record, 189, 45–60CrossRef Google Scholar PubMed

Phillips-Conroy, J. E., Jolly, C. J., Petros, B., Allan, J. S. & Desrosiers, R. C. 1994. Sexual transmission of SIV(agm) in wild grivet monkeys. Journal of Medical Primatology, 23, 1–7CrossRef Google Scholar

Purvis, A. 1995. A composite estimate of primate phylogeny. Philosophical Transactions of the Royal Society of London, Series B, 348, 405–21CrossRef Google Scholar PubMed

Purvis, A. & Rambaut, A. 1995. Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. Computer Applications in the Biosciences, 11, 247–51Google Scholar PubMed

Radolf, J. D., Sanchez, P. J., Schulz, K. F. & Murphy, F. K. 1999. Congenital syphilis. In Sexually Transmitted Diseases, ed. K. K. Holmes, P. F. Sparling, P.-A. Mardh, S. M. Lemon, W. E. Stamm, P. Piot & J. N. Wasserheit. New York, NY: McGraw-Hill, pp. 1165–89

Read, A. F. 1994. The evolution of virulence. Trends in Microbiology, 2, 73–6CrossRef Google Scholar PubMed

Reichard, U. 1995. Extra-pair copulation in a monogamous gibbon (Hylobates lar). Ethology, 100, 99–112CrossRef Google Scholar

Richards, A. L., Giri, A., Iskandriati, D.et al. 1998. Simian T-lymphotrophic virus type-I infection among wild-caught Indonesian pig-tailed macaques (Macaca nemestrina). Journal of Acquired Immune Deficiency Syndromes and Human Retrovirology, 19, 542–5CrossRef Google Scholar

Roberts, L. 1979. Bovine venereal campylobacteriosis (vibriosis) in north east Scotland. Veterinary Record, 105, 295–6CrossRef Google Scholar

Robinson, J. G. 1979. Correlates of urine washing in the wedge-capped capuchin Cebus nigrivittatus. In Vertebrate Ecology in the Northern Neotropics, ed. J. F. Eisenberg. Washington, DC: Smithsonian Institution Press, pp. 137–43

Santiago, M. L., Rodenburg, C. M., Kamenya, S.et al. 2002. SIVcpz in wild chimpanzees. Science, 295, 465CrossRef Google Scholar PubMed

Schwartländer, B., Garnett, G., Walker, N. & Anderson, R. 2000. AIDS in a new millennium. Science, 289, 64–7CrossRef Google Scholar

Sheldon, B. C. 1993. Sexually-transmitted disease in birds: occurrence and evolutionary significance. Philosophical Transactions of the Royal Society of London, Series B, 339, 491–7CrossRef Google Scholar PubMed

Smith, G. & Dobson, A. P. 1992. Sexually transmitted diseases in animals. Parasitology Today, 8, 159–66CrossRef Google Scholar PubMed

Sorci, G., M⊘ller, A. P. & Boulinier, T. 1997. Genetics of host–parasite interactions. Trends in Ecology and Evolution, 12, 196–200CrossRef Google Scholar PubMed

Swanstrom, R. & Wehbie, R. 1999. The biology of HIV, SIV and other lentiviruses. In Sexually Transmitted Diseases, ed. K. K. Holmes, P. F. Sparling, P.-A. Mardh, S. M. Lemon, W. E. Stamm, P. Piot & J. N. Wasserheit. New York, NY: McGraw-Hill, pp. 215–29

Thrall, P. H., Antonovics, J. & Bever, J. D. 1997. Sexual transmission of disease and host mating systems: within-season reproductive success. American Naturalist, 149, 485–506CrossRef Google Scholar

Thrall, P. H., Antonovics, J. & Dobson, A. P. 2000. Sexually transmitted diseases in polygynous mating systems: prevalence and impact on reproductive success. Proceeding of the Royal Society of London Series B, 267, 1555–63CrossRef Google Scholar PubMed

Thrall, P. H., Antonovics, J. & Hall, D. W. 1993. Host and pathogen coexistence in vector-borne and venereal diseases characterized by frequency-dependent disease transmission. American Naturalist, 142, 543–52CrossRef Google Scholar

Thrall, P. H., Antonovics, J. & Wilson, W. G. 1998. Allocation to sexual vs. non-sexual disease transmission. American Naturalist, 151, 29–45CrossRef Google Scholar

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

Webberley, K. M., Hurst, G. D. D., Buszko, J. & Majerus, M. E. N. 2002. Lack of parasite-mediated sexual selection in a ladybird/sexually transmitted disease system. Animal Behaviour, 63, 131–41CrossRef Google Scholar

Book contents

7 - Sexual selection, behaviour and sexually transmitted diseases

Summary

Access options

References

Save book to Kindle

Save book to Dropbox

Save book to Google Drive