Elsevier

Animal Behaviour

Volume 90, April 2014, Pages 159-170
Animal Behaviour

Essay
Impact of infection on mate choice

https://doi.org/10.1016/j.anbehav.2014.01.026Get rights and content

Highlights

  • Infection by parasites can reduce individual fitness.

  • Host responses to infection during mate choice are intended to avoid infection.

  • We highlight the main limitations in current knowledge on infection avoidance.

  • We summarize key factors that should affect infection avoidance in mate choice.

  • The molecular mechanisms at the basis of infection avoidance need to be examined.

Sexual selection predicts that mate choice increases individual fitness. Infection by parasites (from eukaryotes to bacteria or viruses) can reduce this individual fitness, altering the infected individuals' sexual traits and molecular cues. In this case, one would expect to observe mechanisms for avoiding infection during mate choice. The vast majority of host responses to infection in terms of mate choice are intended to avoid infection, but the costs of mate choice can also hinder infection avoidance. This paper highlights the main limitations in current knowledge and empirical experiments, and summarizes the key factors that should be taken into account to test the hypothesis of infection avoidance in mate choice: the time of host–parasite coevolution in the biological interaction implied, the choosy sex tested (male, female or both) and the genetic background of the individuals tested.

Section snippets

Effect of Infection on Sexual Traits

Some traits (e.g. ornaments, coloration, calling song, odours) are altered by simple or multiple infections and correlate with these (Biard et al., 2010, Hamilton and Poulin, 1999, Hamilton and Zuk, 1982, Horak et al., 2004, Potti and Merino, 1996, Ryder and Siva-Jothy, 2000). For example, bill colour, plasma carotenoid levels and body mass are strongly related to the relative abundance of parasite species in blackbirds, Turdus merula (Biard et al., 2010).

Infection can have a negative impact on

General Context and Expected Host Responses

Mate choice for mate quality, linked to a criterion such as social status, individual size, ornamental traits or infection status, is widely accepted as a mechanism by which individuals can maximize their fitness and/or offspring quality (Dillen et al., 2010, Moreau et al., 2001, Peretti and Cordobon-Aguilar, 2007).

In this context, the expected host responses to infection in terms of mate choice are as follows.

(1) Infection avoidance and choice of parasite-free mates are expected even if the

Conclusion

Host responses to infection tend towards infection avoidance and choice of parasite-free mates. There are, however, some notable exceptions, such as when the costs of mate choice hinder the development of infection avoidance.

Infection can significantly modify an individual's phenotypic characteristics (from molecules to sexual traits), inducing a potential reduction in the individual's fitness. However, few biological models have been studied to identify the molecules involved in mate choice

Acknowledgments

We thank Mathieu Sicard, Nicolas Bech, David Puga, Alexander Hurley and the referees for their constructive comments and their help in improving our manuscript. We also thank Version Originale for checking the English in the paper.

References (84)

  • M. Kavaliers et al.

    Brief exposure to the odour of a parasitized male alters the subsequent mate odour responses of female mice

    Animal Behaviour

    (2003)
  • A.V. Markov et al.

    Symbiotic bacteria affect mating choice in Drosophila melanogaster

    Animal Behaviour

    (2009)
  • H.L. Mays et al.

    Choosing mates: good genes versus genes that are a good fit

    Trends in Ecology & Evolution

    (2004)
  • D. Penn et al.

    Chemical signals and parasite-mediated sexual selection

    Trends in Ecology & Evolution

    (1998)
  • D. Penn et al.

    How do major histocompatibility complex genes influence odor and mating preferences?

    Advances in Immunology

    (1998)
  • A. Pomiankowski

    The costs of choice in sexual selection

    Journal of Theoretical Biology

    (1987)
  • M.J. Poulton et al.

    The effects of the acanthocephalan parasite Pomphorhynchus laevis on mate choice in Gammarus pulex

    Animal Behaviour

    (1987)
  • F. Prugnolle et al.

    Infection and body odours: evolutionary and medical perspectives

    Infection, Genetics and Evolution

    (2009)
  • B.D. Worden et al.

    Parasites reduce attractiveness and reproductive success in male grain beetles

    Animal Behaviour

    (2000)
  • A. Zahavi

    The cost of honesty: further remarks on the handicap principle

    Journal of Theoretical Biology

    (1977)
  • D.J. Able

    The contagion indicator hypothesis for parasite-mediated sexual selection

    Proceedings of the National Academy of Sciences USA

    (1996)
  • T.M. Aguilar et al.

    Parasite levels in blue-black grassquits correlate with male displays but not female mate preference

    Behavioral Ecology

    (2008)
  • J.J. Ahtiainen et al.

    Sexual advertisement and immune function in an arachnid species (Lycosidae)

    Behavioral Ecology

    (2004)
  • M. Andersson

    Sexual selection

    (1994)
  • S. Beltran et al.

    Genetic dissimilarity between mates, but not male heterozygosity, influences divorce in schistosomes

    PLoS One

    (2008)
  • C. Biard et al.

    Carotenoid-based bill colour is an integrative signal of multiple parasite infection in blackbird

    Naturwissenschaften

    (2010)
  • R. Bonduriansky

    The evolution of male mate choice in insects: a synthesis of ideas and evidence

    Biological Reviews

    (2001)
  • J.L. Brown

    A theory of mate choice based on heterozygosity

    Behavioral Ecology

    (1997)
  • R. Buchholz

    Effects of parasitic infection on mate sampling by female wild turkeys (Meleagris gallopavo): should infected females be more or less choosy?

    Behavioral Ecology

    (2004)
  • J.P. Burand et al.

    Mate preference and mating behavior of male Helicoverpa zea (Lepidoptera: Noctuidae) infected with the sexually transmitted insect virus Hz-2V

    Annals of the Entomological Society of America

    (2006)
  • U. Candolin

    The use of multiple cues in mate choice

    Biological Reviews

    (2003)
  • F.E.C. Champion de Crespigny et al.

    Can cytoplasmic incompatibility inducing Wolbachia promote the evolution of mate preferences?

    Journal of Evolutionary Biology

    (2005)
  • S.W. Coleman

    Taxonomic and sensory biases in the mate-choice literature: there are far too few studies of chemical and multimodal communication

    Acta Ethologica

    (2009)
  • C. Combes

    Parasitism: The ecology and evolution of intimate interactions

    (2001)
  • R. Cothran et al.

    ‘Cryptic’ direct benefits of mate choice: choosy females experience reduced predation risk while in precopula

    Behavioral Ecology and Sociobiology

    (2012)
  • S.A.H. Dass et al.

    Protozoan parasite Toxoplasma gondii manipulates mate choice in rats by enhancing attractiveness of males

    PLoS One

    (2011)
  • K.D. Dunlap et al.

    Hormonal alterations and reproductive inhibition in male fence lizards (Sceloporus occidentalis) infected with the malarial parasite Plasmodium mexicanum

    Physiological Zoology

    (1995)
  • K.D. Ehman et al.

    Female mice mate preferentially with non-parasitized males

    Parasitology

    (2002)
  • N. González Quiñónez et al.

    Female mice preference: does Trypanosoma cruzi affect males' scent?

    Interciencia

    (2011)
  • W.J. Hamilton et al.

    Female preference and male nuptial colouration in the freshwater fish Gobiomorphus breviceps: geographic variation among populations

    Canadian Journal of Zoology

    (1999)
  • W.D. Hamilton et al.

    Heritable true fitness and bright birds: a role for parasites?

    Science

    (1982)
  • D. Henderson et al.

    Mate choice in captive American kestrels, Falco sparverius, parasitized by a nematode, Trichinella pseudospiralis

    Ethology

    (1995)
  • Cited by (79)

    • Does female shell disease status influence mating success in American lobsters?

      2022, Journal of Experimental Marine Biology and Ecology
    • The evolution and ecology of benign tumors

      2022, Biochimica et Biophysica Acta - Reviews on Cancer
    View all citing articles on Scopus
    View full text