Behavioral Ecology and Sociobiology

, Volume 69, Issue 5, pp 715–722 | Cite as

Female house mice initially shun infected males, but do not avoid mating with them

  • Sarah M. Zala
  • Amber Bilak
  • Michael Perkins
  • Wayne K. Potts
  • Dustin J. Penn
Original Paper

Abstract

Female house mice (Mus musculus) show preferences for the scent of healthy versus infected males, which may function to reduce risks of disease transmission or to obtain healthy, disease-resistant mates. It is not known whether such odor preferences result in differential male reproductive success (sexual selection), and therefore, we performed mate choice experiments with wild-derived mice. Females were allowed to freely choose to mate between two males, one infected (Salmonella enterica) versus a sham control, and we conducted genetic paternity analyses on the offspring to assess male reproductive success. The males were restricted to their own cages to prevent male-male interactions and sexual coercion, and we performed the experiment in two different settings: in large-connected cages and in large enclosures. In the enclosures, we found that 86 % of females were initially more attracted to the control males (initial social preference); however, our paternity analyses detected no difference in male reproductive success in either setting. Females often mated with both males (connected cages 32 %, enclosures 44 %), which shows that females frequently mate multiply—despite differences in male health—when they can choose their mates. These results raise caveats about mate choice studies that rely on proxy measures, such as odor preferences or time spent with potential mates. On the other hand, if females are less likely to locate infected than healthy males in the wild, then such a bias could still result in nonrandom mating. We suggest several additional issues that also need to be considered before ruling out parasite-mediated mate choice.

Keywords

Mus Mate choice Sexual selection Hamilton-Zuk hypothesis Infection Parasite-mediated sexual selection 

References

  1. Able DJ (1996) The contagion indicator hypothesis for parasite-mediated sexual selection. Proc Natl Acad Sci U S A 93:2229–2233CrossRefPubMedCentralPubMedGoogle Scholar
  2. Adamo SA (2004) How should behavioural ecologists interpret measurements of immunity? Anim Behav 68:1443–1449CrossRefGoogle Scholar
  3. Avitsur R, Cohen E, Yirmiya R (1997) Effects of interleukin-1 on sexual attractivity in a model of sickness behavior. Physiol Behav 63:25–30CrossRefPubMedGoogle Scholar
  4. Barske J, Schlinger BA, Wikelski M, Fusani L (2011) Female choice for male motor skills. Proc R Soc Lond B 278:3523–3528CrossRefGoogle Scholar
  5. Beltran-Bech S, Richard FJ (2014) Impact of infection on mate choice. Anim Behav 90:159–170CrossRefGoogle Scholar
  6. Byers J, Hebets E, Podos J (2010) Female mate choice based upon male motor performance. Anim Behav 79:771–778CrossRefGoogle Scholar
  7. Candolin U (1999) Male-male competition facilitates females choice in sticklebacks. Proc R Soc Lond B 266:785–789CrossRefGoogle Scholar
  8. Candolin U, Voigt HR (2001) No effect of a parasite on reproduction in stickleback males: a laboratory artefact? Parasitology 122:457–464CrossRefPubMedGoogle Scholar
  9. Dean M, Ardlie G, Nachman M (2006) The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus). Mol Ecol 15:4141–4151CrossRefPubMedCentralPubMedGoogle Scholar
  10. Desjardins C, Maruniak JA, Bronson FH (1973) Social rank in house mice: differentiation revealed by ultraviolet visualization of urinary marking patterns. Science 182:939–941CrossRefPubMedGoogle Scholar
  11. Dewsbury DA (1988) Copulatory behavior as courtship communication. Ethology 79:218–234CrossRefGoogle Scholar
  12. Edward DA (2014) The description of mate choice. Behav Ecol (published online, doi:10.1093/beheco/aru142)
  13. Ehman KD, Scott ME (2001) Urinary odour preferences of MHC congenic female mice, Mus domesticus: implications for kin recognition and detection of parasitized males. Anim Behav 62:781–789CrossRefGoogle Scholar
  14. Ehman KD, Scott M (2002) Female mice mate preferentially with non-parasitized males. Parasitology 125:461–466CrossRefPubMedGoogle Scholar
  15. Ehman KD, Scott ME (2004) Microsatellite analysis reveals that female mice are indiscriminate when choosing infected or dominant males in an arena setting. Parasitology 129:723–731CrossRefPubMedGoogle Scholar
  16. Firman RC, Simmons LW (2008) The frequency of multiple paternity predicts variation in testes size among island populations of house mice. J Evol Biol 21:1524–1533CrossRefPubMedGoogle Scholar
  17. Freeland W (1981) Parasitism and behavioral dominance among male mice. Science 213:461–462CrossRefPubMedGoogle Scholar
  18. García-Pérez I, Whitfield P, Bartlett A, Angulo S, Legido-Quigley C, Hanna-Brown M, Barbas C (2008) Metabolic fingerprinting of Schistosoma mansoni infection in mice urine with capillary electrophoresis. Electrophoresis 29:3201–3206CrossRefPubMedGoogle Scholar
  19. Gerlinskaya LA, Shnayder EP, Dotsenko AS, Maslennikova SO, Zavjalov EL, Moshkin MP (2012) Antigen-induced changes in odor attractiveness and reproductive output in male mice. Brain Behav Immun 26:451–458CrossRefPubMedGoogle Scholar
  20. Getty T (2002) Signaling Health versus Parasites. Am Nat 159:363–371CrossRefPubMedGoogle Scholar
  21. Gourbal B, Lacroix A, Gabrion C (2002) Behavioural dominance and Taenia crassiceps parasitism in BALB/c male mice. Parasitol Res 88:912–917CrossRefPubMedGoogle Scholar
  22. Hamilton W, Poulin R (1997) The Hamilton and Zuk hypothesis revisited: A meta-analytical approach. Behaviour 134:299–320CrossRefGoogle Scholar
  23. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: arole for parasites? Science 218:384–387CrossRefPubMedGoogle Scholar
  24. Kavaliers M, Colwell DD (1995a) Discrimination by female mice between the odours of parasitized and non-parasitized males. Proc R Soc Lond B 261:31–35CrossRefGoogle Scholar
  25. Kavaliers M, Colwell DD (1995b) Odours of parasitized males induce aversive response in female mice. Anim Behav 50:1161–1169CrossRefGoogle Scholar
  26. Kavaliers M, Fudge MA, Colwell DD, Choleris E (2003) Aversive and avoidance responses of female mice to the odors of males infected with an ectoparasite and the effects of prior familiarity. Behav Ecol Sociobiol 54:423–430CrossRefGoogle Scholar
  27. Kimball BA, Opiekun M, Yamazaki K, Beauchamp GK (2014) Immunization alters body odor. Physiol Behav 128:80–85CrossRefPubMedGoogle Scholar
  28. Klein S, Gamble H, Neslon R (1999) Trichinella spiralis infection in voles alters female odor preference but not partner preference. Behav Ecol Sociobiol 45:323–329CrossRefGoogle Scholar
  29. Li JV, Wang Y, Saric J, Nicholson JK, Dirnhofer S, Singer BH, Tanner M, Wittlin S, Holmes E, Utzinger J (2008) Global metabolic responses of NMRI mice to an experimental Plasmodium bergheiinfection. J Proteome Res 7:3948–3956CrossRefPubMedGoogle Scholar
  30. Litvinova EA, Kudaeva OT, Mershieva LV, Moshkin MP (2005) High level of circulating testosterone abolishes decline in scent attractiveness in antigen-treated male mice. Anim Behav 69:511–517CrossRefGoogle Scholar
  31. Manivannan B, Rawson P, Jordan TW, Secor WE, La Flamme AC (2010) Differential patterns of liver proteins in experimental murine hepatosplenic schistosomiasis. Infect Immun 78:618–628CrossRefPubMedCentralPubMedGoogle Scholar
  32. Meagher S, Penn DJ, Potts WK (2000) Male-male competition magnifies inbreeding depression in wild house mice. Proc Natl Acad Sci U S A 97:3324–3329CrossRefPubMedCentralPubMedGoogle Scholar
  33. Møller AP, Christe P, Lux E (1999) Parasitism, host immune function, and sexual selection. Q Rev Biol 74:3–20CrossRefPubMedGoogle Scholar
  34. Morales J, Larralde C, Arteaga M, Govezensky T, Romano MC, Morali G (1996) Inhibition of sexual behavior in male mice infected with Taenia crassiceps cysticerci. J Parasitol 82:689–693CrossRefPubMedGoogle Scholar
  35. Moshkin M, Gerlinskaya L, Morozova O, Bakhvalova V, Evsikov V (2002) Behaviour, chemosignals and endocrine functions in male mice infected with tick-borne encephalitis virus. Psychoneuroendocrino 27:603–608CrossRefGoogle Scholar
  36. Oakeshott JG (1974) Social dominance, aggressiveness and ating success among male house mice (Mus musculus). Oecologia 15:143–158CrossRefGoogle Scholar
  37. Penn D, Potts WK (1998) Chemical signals and parasite-mediated sexual selection. Trends Ecol Evol 13:391–396CrossRefPubMedGoogle Scholar
  38. Penn D, Schneider G, White K, Slev P, Potts W (1998) Influenza infection neutralizes the attractiveness of male odour to female mice (Mus musculus). Ethology 104:685–694CrossRefGoogle Scholar
  39. Potts WK, Manning J, Wakeland EK (1991) Mating patterns in seminatural populations of mice influenced by MHC genotype. Nature 352:619–621CrossRefPubMedGoogle Scholar
  40. Rau ME (1983) The open-field behavior of mice infected with Trichinella spiralis. Parasitology 86:311–318CrossRefPubMedGoogle Scholar
  41. Rau ME (1984) Loss of behavioral dominance in male mice infected with Trichinella spiralis. Parasitology 88:371–373CrossRefPubMedGoogle Scholar
  42. Raveh S, Sutalo S, Thonhauser KE, Thoß M, Hettyey A, Winkelser F, Penn DJ (2014) Female partner preferences enhance offspring ability to survive an infection. BMC Evol Biol 14:14CrossRefPubMedCentralPubMedGoogle Scholar
  43. Rolland C, MacDonald DW, de Fraipont M, Berdoy M (2003) Free female choice in house mice: Leaving best for last. Behaviour 140:1371–1388CrossRefGoogle Scholar
  44. Sadd BM, Holman L, Armitage H, Lock F, Marland R, Siva-Jothy MT (2006) Modulation of sexual signalling by immune challenged male mealworm beetles (Tenebrio molitor, L.): evidence for terminal investment and dishonesty. J Evol Biol 19:321–325CrossRefPubMedGoogle Scholar
  45. Simmons LW (2005) The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Annu Rev Ecol Evol Syst 36:125–146CrossRefGoogle Scholar
  46. Soh LJT, Vasudevan A, Vyas A (2013) Infection with Toxoplasma gondii does not elicit predator aversion in male mice nor increase their attractiveness in terms of mate choice. Parasitol Res 112:3373–3378CrossRefPubMedGoogle Scholar
  47. Thonhauser KE, Raveh S, Hettyey A, Beissmann H, Penn DJ (2013a) Scent marking enhances male reproductive success in wild house mice. Anim Behav 86:1013–1021CrossRefPubMedCentralPubMedGoogle Scholar
  48. Thonhauser KE, Raveh S, Hettyey A, Beissmann H, Penn DJ (2013b) Why do female mice mate with multiple males? Behav Ecol Sociobiol 67:1961–1970CrossRefPubMedCentralPubMedGoogle Scholar
  49. Van Etten WJ, Steen RG, Nguyen H, Castle AB, Slonim DK, Ge B, Nusbaum C, Schuler GD, Lander ES, Hudson TJ (1999) Radiation hybrid map of the mouse genome. Nat Genet 22:384–387CrossRefPubMedGoogle Scholar
  50. Wagner WE Jr (1998) Measuring female mating preferences. Anim Behav 55:1029–1042CrossRefPubMedGoogle Scholar
  51. Wang YL, Utzinger J, Saric J, Li JV, Burckhardt J, Dirnhofer S, Nicholson JK, Singer BH, Brun R, Holmes E (2008) Global metabolic responses of mice to Trypanosoma bruceibrucei infection. Proc Natl Acad Sci U S A 105:6127–6132CrossRefPubMedCentralPubMedGoogle Scholar
  52. Wolff RJ (1985) Mating behaviour and female choice: their relation to social structure in wild caught House mice (Mus musculus) housed in a semi-natural environment. J Zool 207:43–51CrossRefGoogle Scholar
  53. Zala SM, Potts WK, Penn DJ (2004) Scent-marking displays provide honest signals of health and infection. Behav Ecol 15:338–344CrossRefGoogle Scholar
  54. Zala SM, Chan B, Bilbo SD, Potts WK, Nelson RJ, Penn DJ (2008a) Genetic resistance to infection influences a male’s sexual attractiveness and modulation of testosterone. Brain Behav Immun 22:381–387CrossRefPubMedGoogle Scholar
  55. Zala SM, Potts WK, Penn DJ (2008b) Exposing males to female scent increases the cost of controlling Salmonella infection in wild house mice. Behav Ecol Sociobiol 62:895–900CrossRefGoogle Scholar
  56. Zhang J-X, Sun L, Zhang Y-H (2010) Foxn1 gene knockout suppresses sexual attractiveness and pheromonal components of male urine in inbred mice. Chem Senses 35:47–56CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Sarah M. Zala
    • 1
    • 2
  • Amber Bilak
    • 2
  • Michael Perkins
    • 2
  • Wayne K. Potts
    • 2
  • Dustin J. Penn
    • 1
    • 2
  1. 1.Konrad Lorenz Institute of Ethology, Department of Integrative Biology and EvolutionUniversity of Veterinary MedicineVienna, Savoyenstraße 1aAustria
  2. 2.Department of BiologyUniversity of UtahSalt Lake CityUSA

Personalised recommendations