Why do female mice mate with multiple males?

Behavioral Ecology and Sociobiology

Volumn 67, Issue 12, 2013, Pages 1961-1970

  Thonhauser, Kerstin E ^a   Raveh, Shirley ^a,b   Hettyey, Attila ^a,c   Beissmann, Helmut ^a   Penn, Dustin J ^a  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^b UNIVERSITY OF BASEL   (Switzerland)

^c INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Infanticide avoidance; Male quality; Multiple mating; Polyandry; Scent marking; Sexual conflict

Indexed keywords

FEMALE; INFANTICIDE; LITTER SIZE; MALE; MATE CHOICE; MULTIPLE MATING; PATERNITY; POLYANDRY; RODENT; SCENT MARKING; SEXUAL CONFLICT;

MUS; MUS MUSCULUS; MUS MUSCULUS MUSCULUS;

EID: 84887621901     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-013-1604-8     Document Type: Article

References (84)

1. Agrell J, Wolff JO, Ylönen H (1998) Counter-strategies to infanticide in mammals: costs and consequences. Oikos 83: 507-517.
2. Anderson PK (1961) Density, social structure, and nonsocial environment in house-mouse populations and the implications for regulation of numbers. Trans NY Acad Sci 23: 447-451.
3. Arnqvist G, Nilsson T (2000) The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav 60: 145-164.
4. Arnqvist G, Rowe L (2005) Sexual conflict in nature. In: Arnqvist G, Rowe L (eds) Sexual conflict. Princeton University Press, pp 1-14.
5. Baker JD, Fowler CW (1992) Pup weight and survival of northern fur seals Callorhinus ursinus. J Zool 227: 231-238.
6. Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2: 349-368.
7. Bronson FH (1979) The reproductive ecology of the house mouse. Q Rev Biol 54: 265-299.
8. Calhoun JB (1962) Population density and social pathology. Sci Am 206: 139-148.
9. Clutton-Brock T, McAuliffe K (2009) Female mate choice in mammals. Q Rev Biol 84: 3-27.
10. Clutton-Brock TH, Parker GA (1995) Sexual coercion in animal societies. Anim Behav 49: 1345-1365.
11. Daly M (1978) Cost of mating. Am Nat 112: 771-774.
12. 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: 4141-4151.
13. Dietrich V, Schmoll T, Winkel W, Epplen JT, Lubjuhn T (2004) Pair identity-an important factor concerning variation in extra-pair paternity in the coal tit (Parus ater). Behaviour 141: 817-835.
14. Drake A, Fraser D, Weary D (2008) Parent-offspring resource allocation in domestic pigs. Behav Ecol Sociobiol 62: 309-319.
15. Drickamer LC (1992) Oestrous female house mice discriminate dominant from subordinate males and sons of dominant from sons of subordinate males by odour cues. Anim Behav 43: 868-870.
16. 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.
17. Ebensperger LA (1998) Strategies and counterstrategies to infanticide in mammals. Biol Rev 73: 321-346.
18. Elwood RW (1985) Inhibition of infanticide and onset of paternal care in male mice (Mus musculus). J Comp Psychol 99: 457-468.
19. Elwood RW, Ostermeyer MC (1984) Does copulation inhibit infanticide in male rodents? Anim Behav 32: 293-294.
20. Engqvist L (2005) The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Anim Behav 70: 967-971.
21. Firman RC (2011) Polyandrous females benefit by producing sons that achieve high reproductive success in a competitive environment. Proc R Soc Lond B 278: 2823-2831.
22. Firman RC, Simmons LW (2008a) The frequency of multiple paternity predicts variation in testes size among island populations of house mice. J Evol Biol 21: 1524-1533.
23. Firman RC, Simmons LW (2008b) Polyandry facilitates postcopulatory inbreeding avoidance in house mice. Evolution 62: 603-611.
24. Firman RC, Simmons LW (2008c) Polyandry, sperm competition, and reproductive success in mice. Behav Ecol 19: 695-702.
25. García-González F, Simmons LW (2005) The evolution of polyandry: intrinsic sire effects contribute to embryo viability. J Evol Biol 18: 1097-1103.
26. Gosling LM (1982) A reassessment of the function of scent marking in territories. Z Tierpsychol 60: 89-118.
27. Gowaty PA (2012) The evolution of multiple mating costs and benefits of polyandry to females and of polygyny to males. Fly 6: 3-11.
28. Grafen A, Hails R (2002) Modern statistics for the life sciences. Oxford University Press, Oxford.
29. Hager R, Johnstone RA (2003) The genetic basis of family conflict resolution in mice. Nature 421: 533-535.
30. Hoogland JL (1998) Why do Gunnison's prairie dogs copulate with more than one male? Anim Behav 55: 351-359.
31. Hosken DJ, Stockley P (2003) Benefits of polyandry: a life history perspective. Evol Biol 33: 173-194.
32. Hrdy SB (1979) Infanticide among animals. Ethol Sociobiol 1: 13-40.
33. Huck UW, Soltis RL, Coopersmith CB (1982) Infanticide in male laboratory mice: effects of social status, prior sexual experience, and basis for social discrimination between related and unrelated young. Anim Behav 30: 1158-1165.
34. Hurst JL (1990) Urine marking in populations of wild house mice, Mus domesticus Rutty. I. Communication between males. Anim Behav 40: 209-222.
35. Ilmonen P, Stundner G, Thoß M, Penn D (2009) Females prefer the scent of outbred males: good-genes-as-heterozygosity? BMC Evol Biol 9: 104.
36. Jennions MD, Petrie M (2000) Why do females mate multiply? a review of the genetic benefits. Biol Rev 75: 21-64.
37. Kalinowski ST, Taper ML, Marschall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16: 1099-1106.
38. Kempenaers B, Verheyen GR, van den Broeck M, Burke T, van Broeckhoven C, Dhondt AA (1992) Extra-pair paternity results from female preference for high-quality males in the blue tit. Nature 357: 494-496.
39. Klemme I, Ylönen H (2010) Polyandry enhances offspring survival in an infanticidal species. Biol Lett 6: 24-26.
40. Labov JB (1980) Factors influencing infanticidal behavior in wild male house mice (Mus musculus). Behav Ecol Sociobiol 6: 297-303.
41. Magnhagen C (1991) Predation risk as a cost of reproduction. Trends Ecol Evol 6: 183-186.
42. Manning CJ, Dewsbury DA, Wakeland EK, Potts WK (1995) Communal nesting and communal nursing in house mice, Mus musculus domesticus. Anim Behav 50: 741-751.
43. McFarlane SE, Lane JE, Taylor RW, Gorrell JC, Coltman DW, Humphries MM, Boutin S, McAdam AG (2011) The heritability of multiple male mating in a promiscuous mammal. Biol Lett 7: 368-371.
44. Montero I, Teschke M, Tautz D (2013) Paternal imprinting of mating preferences between natural populations of house mice (Mus musculus domesticus). Mol Ecol 22: 2549-2562.
45. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85: 935-956.
46. Oakeshott JG (1974) Social dominance, aggressiveness and mating success among male house mice (Mus musculus). Oecologia 15: 143-158.
47. Parker GA (1990) Sperm competition games: sneaks and extra-pair copulations. Proc R Soc Lond B 242: 127-133.
48. Parker GA (1998) Sperm competition and the evolution of ejaculates: towards a theory base. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic, London, United Kingdom, pp 3-54.
49. Penn DJ, Smith KR (2007) Differential fitness costs of reproduction between the sexes. Proc Natl Acad Sci U S A 104: 553-558.
50. Potts WK, Manning CJ, Wakeland EK (1991) Mating patterns in seminatural populations of mice influenced by MHC genotype. Nature 352: 619-621.
51. R Development Core Team (2011) R: A Language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria http://www. R-project. org.
52. Ramm SA, Stockley P (2007) Ejaculate allocation under varying sperm competition risk in the house mouse, Mus musculus domesticus. Behav Ecol 18: 491-495.
53. Ramm SA, Stockley P (2009a) Adaptive plasticity of mammalian sperm production in response to social experience. Proc R Soc Lond B 276: 745-751.
54. Ramm SA, Stockley P (2009b) Male house mice do not adjust sperm allocation in response to odours from related or unrelated rivals. Anim Behav 78: 685-690.
55. Reznick D (1985) Costs of reproduction: an evaluation of the empirical evidence. Oikos 44: 257-267.
56. Rich TJ, Hurst JL (1998) Scent marks as reliable signals of the competitive ability of mates. Anim Behav 56: 727-735.
57. Rich TJ, Hurst JL (1999) The competing countermarks hypothesis: reliable assessment of competitive ability by potential mates. Anim Behav 58: 1027-1037.
58. Rolland C, MacDonald DW, de Fraipont M, Berdoy M (2003) Free female choice in house mice: Leaving best for last. Behaviour 140: 1371-1388.
59. Rowe L (1994) The costs of mating and mate choice in water striders. Anim Behav 48: 1049-1056.
60. Royle NJ, Hartley IR, Parker GA (2004) Parental investment and family dynamics: interactions between theory and empirical tests. Popul Ecol 46: 231-241.
61. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. A laboratory manual, vol 1-3, 2nd edn. Cold Spring Harbor Lab, Plainview.
62. Simmons LW (2005) The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Annu Rev Ecol Evol Syst 36: 125-146.
63. Siva-Jothy MT (2006) Trauma, disease and collateral damage: conflict in cimicids. Philos Trans R 361: 269-275.
64. Smith CC, Fretwell SD (1974) The optimal balance between size and number of offspring. Am Nat 108: 499-506.
65. Smuts BB, Smuts RW (1993) Male aggression and sexual coercion of females in nonhuman primates and other mammals: evidence and theoretical implications. Adv Stud Behav 22: 1-63.
66. Soroker V, Terkel J (1988) Changes in incidence of infanticidal and parental responses during the reproductive cycle in male and female wild mice Mus musculus. Anim Behav 36: 1275-1281.
67. Speakman JR (2008) The physiological costs of reproduction in small mammals. Philos Trans R 363: 375-398.
68. Taborsky M, Oliveira RF, Brockmann HJ (2008) The evolution of alternative reproductive tactics: concepts and questions. In: Oliveira RF, Taborsky M, Brockmann HJ (eds) Alternative reproductive tactics. An Integrative Approach. Cambridge University Press, pp 1-21.
69. Thornhill R, Alcock J (1983) The evolution of insect mating systems. Harvard Univ. Press, Cambridge.
70. Tregenza T, Wedell N (2002) Polyandrous females avoid costs of inbreeding. Nature 415: 71-73.
71. Trivers R (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136-179.
72. vom Saal FS, Howard LS (1982) The regulation of infanticide and parental behavior: implications for reproductive success in male mice. Science 215: 1270-1272.
73. Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17: 313-320.
74. Whittingham LA, Dunn PO, Stapleton MK (2006) Repeatability of extra-pair mating in tree swallows. Mol Ecol 15: 841-849.
75. 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: 43-51.
76. Wolff JO, Macdonald DW (2004) Promiscuous females protect their offspring. Trends Ecol Evol 19: 127-134.
77. Wong BBM, Candolin U (2005) How is female mate choice affected by male competition? Biol Rev 80: 559-571.
78. Yasui Y (1997) A "good-sperm" model can explain the evolution of costly multiple mating by females. Am Nat 149: 573-584.
79. Yasui Y (1998) The 'genetic benefits' of female multiple mating reconsidered. Trends Ecol Evol 13: 246-250.
80. Yasui Y (2001) Female multiple mating as a genetic bet-hedging strategy when mate choice criteria are unreliable. Ecol Res 16: 605-616.
81. Zala SM, Potts WK, Penn DJ (2004) Scent-marking displays provide honest signals of health and infection. Behav Ecol 15: 338-344.
82. 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: 381-387.
83. 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: 895-900.
84. Zeh JA, Zeh DW (1997) The evolution of polyandry II: post-copulatory defences against genetic incompatibility. Proc R Soc Lond B 264: 69-75.