Abstract
The detection and avoidance of parasitized males is a component of female mate choice. Here we show that female mice can distinguish between the odors of individual males infected with an ectoparasite, the murine louse, Polyplax serrata, and uninfected males. Female mice displayed aversive responses to, and avoided the odors of, parasitized males. A 15 min exposure to the urinary odors of infected males induced an endogenous opioid-peptide-mediated reduction in pain sensitivity or analgesia, while a brief 1 min exposure to the odors elicited a non-opioid-mediated analgesic response. These neuromodulatory mechanisms facilitate the expression of a variety of anxiety and stress associated responses of which pain inhibition is one component. Females further distinguished between novel and familiar infected males. Prior exposure to the odors of an infected males reduced the degree of analgesia expressed and the associated levels of anxiety and stress and their concomitant costs. In a Y-maze odor preference test females also displayed a marked overall preference for, and initial choice of, the odors of clean, uninfected males and an active discrimination against, and avoidance of, the odors of both familiar and novel infected males. These findings indicate that female mice can distinguish between males infected with an ectoparasite and clean uninfected males and display aversive and avoidance responses to infected males. They also show that females can discriminate between individual infected males and modulate their aversive responses to the odors of infected males on the basis of prior familiarity. This is likely part of the mechanisms whereby females can both reduce the transmission of ectoparasites, such as lice, to themselves and select for parasite-free males.
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References
Able DJ (1996) The contagion indicator hypothesis for parasite-mediated sexual selection. Proc Natl Acad Sci USA 93:2229–2233
Borgia G, Collis K (1989) Female choice for parasite-free male satin bower-birds and the evolution of bright male plumage. Behav Ecol Sociobiol 25:445–454
Brown RE (1995) What is the role of the immune system in determining individually distinct body odours ? Int J Immunopharmacol 17:651–661
Clayton DH (1990) Mate choice in experimentally parasitized rock doves: lousy males lose. Am Zool 30:251–262
Clayton DH (1991) The influence of parasites on host sexual selection. Parasitol Today 7:329–334
Clayton DH, Moore J (eds) (1997) Host-parasite evolution: general principles and avian models. Oxford University Press, Oxford
Coopersmith CB, Lenington S (1992) Female preference based on male quality in house mice: interactions between dominance rank and t-complex genotype. Ethology 90:1–6
Dhabhar FS (2002) Stress-induced augmentation of immune function—the role of stress hormones, leucocyte trafficking and cytokines. Brain Behav Immun 16:785–798
Drickamer LC, Gowaty PA, Holmes CM (2000) Free female mate choice in house mice affects reproductive success and offspring viability and performance. Anim Behav 59:371–378
Egid K, Brown JL (1989) The major histocompatibility complex and female mating preferences in mice. Anim Behav 38:448–450
Ehman KD, Scott ME (2001) Urinary odour preferences of MHC congeric female mice, Mus domesticus: implications for kin recognition and detection of parasitized males. Anim Behav 62:781–789
Eklund A, Egid K, Brown JL (1991) The major histocompatibility complex and mating preferences of male mice. Anim Behav 42:69-74.
Folstad I, Karter AJ (1992) Parasite, bright males and the immunocompetence handicap. Am Nat 139:603–622
Gheusi G, Blunthe R-M, Goodell G, Dantzer R (1994) Social and individual recognition in rodents: methodological aspects and neurobiological bases. Behav Process 33:59–88
Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites. Science 218:384–387
Hart BL (1992) Behavioral adaptations to parasites: an ethological approach. J Parasitol 78:256–265
Hunskaar S, Berge OG, Hole K (1986) A modified hot-plate test sensitive to mild analgesics. Behav Brain Res 21:1010–108
Hurst JL (1987) The functions of urine marking in a free-living population of house mice, Mus domesticus Rutty. Anim Behav 35:1433–1442
Hurst JL (1990) Urine marking in populations of wild house mice Mus domesticus Rutty. III. Communication between the sexes. Anim Behav 40:233–243
Hurst JL, Payne CE, Nevison CM, Maries AD, Humphries RE, Robertson DHL, Cavaggioni A, Beynon RJ (2001) Individual recognition in mice mediated by major urinary proteins. Nature 414:631–634
Jennions MD, Petrie M (1997) Variations in mate choice and mating preferences: a review of causes and consequences. Biol Rev 72:283–327
Kavaliers M, Colwell DD (1993) Aversive responses of female mice to the odors of parasitized males: neuromodulatory mechanisms and implications for mate choice. Ethology 95:206–212
Kavaliers M, Colwell DD (1995a) Discrimination by female mice between the odours of parasitized and non-parasitized males. Proc R Soc Lond B 261:31–35
Kavaliers M, Colwell DD (1995b) Odours of parasitized males induce aversive response in female mice. Anim Behav 50:1161–1169
Kavaliers M, Galea LAM (1995) Sex differences in the expression and antagonism of swim stress-induced analgesia in deer mice vary with the breeding season. Pain 63:327–334
Kavaliers M, Colwell DD, Ossenkopp K-P, Perrot-Sinal TS (1997) Altered responses to female odors in parasitized male mice: neuromodulatory mechanisms and relations to female choice. Behav Ecol Sociobiol 40:373–384
Kavaliers M, Colwell DD, Choleris E (2000) Parasites and behaviour: an ethopharmacological perspective. Parasitol Today 16:464–468
Kavaliers M, Colwell DD, Braun WJ, Choleris E (2003) Brief exposure to the odour of a parasitized male alters the subsequent mate odour response of female mice. Anim Behav 65:59–68
Kennedy CE J, Endler JA, Poynton SL, McMinn H (1987) Parasite load predicts mate choice in guppies. Behav Ecol Sociobiol 21:291–295
Klein SL, Gamble HR, Nelson RJ (1999) Trichinella spiralis alters female odor preferences, but not mate preferences, in voles. Behav Ecol Sociobiol 45:323–329
Kose M, Mand R, Møller AP (1999) Sexual selection for white tail spots in the barn swallow in relation to habitat choice by feather lice. Anim Behav 58:1201–1205
Krackow S, Matuschak M (1991) Mate choice for non-siblings in wild house mice: evidence from a choice test and reproductive test. Ethology 88:99–108
Lehmann T (1992) Ectoparasite impacts on Gerbillus andersoni allenbyi under natural conditions. Parasitology 104:479–488
Lehmann T (1993) Ectoparasites: direct impact on host fitness. Parasitol Today 9:9–13
Lenington A (1983) Social preferences for partners carrying 'good genes' in wild mice. Anim Behav 31:325–333
Lodmell DL, Bell JF, Clifford CM (1970) Effects of limb disability on lousiness of mice V: hierarchy disturbance on mutual grooming and reproductive capacities. Exp Parasitol 27:184–192
Milinski M, Bakker TC (1990) Female sticklebacks use male colouration in mate choice and hence avoid parasitized males. Nature 344:330–333
Murray MD (1960) The ecology of the louse Polyplax serrata (Burm.) on the mouse Mus musculus. Aust J Zool 9:1–13
Murray MD (1990) Influence of host behaviour on some ectoparasites of birds and mammals. In: Barnard CJ, Behnke JM (eds) Parasitism and host behaviour. Taylor & Francis, London, pp 290–315
Nelson WA, Bell JF, Stewart SJ (1979) Polyplax serrata: cutaneous cytologic reactions in mice that do (CFW strain) and do not (C57BL) develop resistance. Exp Parasitol 48:259–264
Nelson WA, Bell JF, Stewart SJ, Kozub GC (1983) Polyplax serrata (Phthiraptera: Hopolopleuridae): effects of corticosterone and cyclophosphamide on the acquired resistance response of mice to lice. J Med Entomol 20:551–557
Nevison CM, Barnard CJ, Beyon RJ, Hurst JL (2000) The consequences of inbreeding for recognizing competitors. Proc R Soc B 267:687–694
Penn D, Potts WK (1998) Chemical signals and parasite-mediated sexual selection. Trends Ecol Evol 13:391–396
Penn D, Schneider G, White K, Slev P, Potts W, (1998) Influenza infection neutralizes the attractiveness of male odours to female mice (Mus musculus). Ethology 104:685–694
Potts WK, Manning CJ, Wakeland EK (1994) The role of infectious disease, inbreeding and mating preferences in maintaining MHC genetic diversity: an experimental test. Philos Trans R Soc Lond B 346:369–378
Price MA, Graham OH (1997) Chewing and sucking lice as parasites of mammals and birds. United States Dept Agric Tech Bull 1849
Ratzllaff RE, Wikel SK (1990) Murine immune responses and immunization against Polyplax serrata (Anoplura: Polyplacidae). J Med Entomol 27:1002–1007
Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321
Singh PB (2001) Chemosensation and genetic individuality. Reproduction 21:529–539
Wagner WE Jr (1998) Measuring female mating preferences. Anim Behav 55:1029–1042
Wedekind C (1992) Detailed information about parasites revealed by sexual ornamentation. Proc R Soc Lond B 247:169–174
Willis C, Poulin R (2000) Preference of female rats for the odours of non-parasitized males: the smell of good genes. Folia Parasitol 47:6–10
Yamazaki K, Boyse EA, Mike V, Thaler HT, Mathieson BJ, Abbott J, Zoyas ZA, Thomas L (1976) Control of mating preferences in mice by genes in the major histocompatibility complex. J Exp Med 144:1324–1335
Zuk M (1992) The role of parasites in sexual selection: current evidence and future directions. Adv Stud Behav 21:39–68
Acknowledgements
We thank Terry Seely, Joan Ingoldsby and Dawn Gray for their assistance. This study was supported by Agriculture and Agri-Food Canada and the Natural Sciences and Engineering Research Council of Canada.
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Kavaliers, M., Fudge, M.A., Colwell, D.D. et al. 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, 423–430 (2003). https://doi.org/10.1007/s00265-003-0631-2
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DOI: https://doi.org/10.1007/s00265-003-0631-2