Behavioral Ecology and Sociobiology

, Volume 68, Issue 2, pp 283–290 | Cite as

Female fitness, sperm traits and patterns of paternity in an Australian polyandrous mouse

  • Renée C. Firman
Original Paper


Multiple mating is a common reproductive strategy among mammals, and rodents living in communal, mixed sex social groups are predisposed to a polygamous existence. The sandy inland mouse is a naturally polyandrous species that occurs across most of Australia’s arid region. Females typically have greater reproductive restrictions compared with males and are therefore expected to acquire substantial fitness benefits from copulating with more than one male. Here, I show that the reproductive output of female sandy inland mice did not differ between females mated monandrously (single male) or polyandrously (two males). Paternity data obtained from the polyandrous litters revealed that in most cases, there was a first male-to-mate advantage. I discuss this result in relation to the chastity enforcement hypothesis for the evolution of the copulatory plug. Finally, I compared ejaculate traits of competing males and found that the paternity loss of males that mated first was attributable to their own sperm density and sperm quality, and not to that of their rivals. The sperm data also revealed that second males gained greater paternity representation when sperm velocities and motilities were higher in first-mated males. This investigation indicates that mating position is a critical determinant of male fitness in mammalian sperm competition.


Sperm competition Multiple paternity Mammals Copulatory plug Genetic benefits Ejaculate quality 



I thank Shresta Lobind for assistance with animal husbandry. This research was funded by the Fortescue Metals Group Ltd. and the Australian Research Council (Australian Postdoctoral Fellowship).

Ethical standards

The author declares that this research complies with the current laws of the country in which it was performed (Australia). The research was approved by the University of Western Australia animal ethics committee (approval number: 07/100/607).

Supplementary material

265_2013_1643_MOESM1_ESM.doc (37 kb)
ESM 1 (DOC 37 kb)


  1. Baker RJ, Makova KD, Chesser RK (1999) Microsatellites indicate a high frequency of multiple paternity in Apodemus (Rodentia). Mol Ecol 8:107–111PubMedCrossRefGoogle Scholar
  2. Barker DM (1994) Copulatory plugs and paternity assurance in the nematode Caenorhabditis elegans. Anim Behav 48:147–156CrossRefGoogle Scholar
  3. Bateman AJ (1948) Intra-sexual selection in Drosophila. Heredity 2:349–368PubMedCrossRefGoogle Scholar
  4. Birkhead TR, Martinez JG, Burke T, Froman DP (1999) Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc R Soc Lond B 266:1759–1764CrossRefGoogle Scholar
  5. Breed WG (1990) Comparative studies on the timing of reporduction and foetal number in six species of Australian conilurine rodents (Muridae: Hydromyinae). J Zool 221:1–10CrossRefGoogle Scholar
  6. Breed WG, Adams M (1992) Breeding systems of spinifix hopping mice (Notomys alexis) and plains rats (Pseudomys australis): a test for multiple paternity in the laboratory. Aust J Zool 40:13–20CrossRefGoogle Scholar
  7. Breed B, Ford F (2007) Native mice and rats. CSIRO Publishing, Collingwood, VictoriaGoogle Scholar
  8. Bretman A, Tregenza T (2005) Measuring polyandry in wild populations: a case study using promiscuous crickets. Mol Ecol 14:2169–2179PubMedCrossRefGoogle Scholar
  9. Bretman A, Wedell N, Tregenza T (2004) Molecular evidence of post-copulatory inbreeding avoidance in the field cricket Gryllus bimaculatus. Proc R Soc Lond B 271:159–164CrossRefGoogle Scholar
  10. Byers SL, Wiles MV, Dunn SL, Taft RA (2012) Mouse estrous cycle identification tool and images. PLoS ONE 7:e35538PubMedCentralPubMedCrossRefGoogle Scholar
  11. Clutton-Brock TH (1989) Mammalian mating systems. Proc R Soc Lond B 236:339–372PubMedCrossRefGoogle Scholar
  12. Daly M (1978) The cost of mating. Am Nat 112:771–774CrossRefGoogle Scholar
  13. Dean MD (2013) Genetic disruption of the copulatory plug in mice leads to severely reduced fertility. PLoS Genet 9:e1003185PubMedCentralPubMedCrossRefGoogle Scholar
  14. Dean MD, Ardlie KG, Nachman MW (2006) The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus). Mol Ecol 15:4141–4151PubMedCentralPubMedCrossRefGoogle Scholar
  15. delBarco-Trillo J, Ferkin MH (2006) Male meadow voles respond differently to risk and intensity of sperm competition. Behav Ecol 17:581–585CrossRefGoogle Scholar
  16. Devine MC (1975) Copulatory plugs in snakes: enforced chastity. Science 187:844–845PubMedCrossRefGoogle Scholar
  17. Dewsbury DA (1982) Ejaculate cost and male choice. Am Nat 119:601–610CrossRefGoogle Scholar
  18. Dixson AF, Anderson MJ (2002) Sexual selection, seminal coagulation and copulatory plug formation in primates. Folia Primatol 73:63–69PubMedCrossRefGoogle Scholar
  19. Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, PrincetonGoogle Scholar
  20. Firman RC (2011) Polyandrous females benefit by producing sons that achieve high reproductive success in a competitive environment. Proc R Soc Lond B 278:2823–2831CrossRefGoogle Scholar
  21. Firman RC, Simmons LW (2008a) Polyandry facilitates postcopulatory inbreeding avoidance in house mice. Evolution 62:601–611CrossRefGoogle Scholar
  22. Firman RC, Simmons LW (2008b) Polyandry, sperm competition, and reproductive success in mice. Behav Ecol 19:695–702CrossRefGoogle Scholar
  23. Firman RC, Simmons LW (2008c) The frequency of multiple paternity predicts variation in testes size among island populations of house mice. J Evol Biol 21:1524–1533PubMedCrossRefGoogle Scholar
  24. Firman RC, Simmons LW (2010) Sperm midpiece length predicts sperm swimming velocity in house mice. Biol Lett 6:513–516PubMedCentralPubMedCrossRefGoogle Scholar
  25. Firman RC, Simmons LW (2011) Experimental evolution of sperm competitiveness in a mammal. BMC Evol Biol 11:19PubMedCentralPubMedCrossRefGoogle Scholar
  26. Firman RC, Simmons LW (2012) Male house mice evolving with post-copulatory sexual selection sire embryos with increased viability. Ecol Lett 15:42–46PubMedCrossRefGoogle Scholar
  27. Firman RC, Bentley B, Bowman F, Garcia-Solis Marchant F, Parthenay J, Sawyer J, Stewart T, O’Shea JE (2013a) No evidence of sperm conjugate formation in sn Australian mouse bearing sperm with three hooks. Ecol Evol 3:1856–1863PubMedCentralPubMedCrossRefGoogle Scholar
  28. Firman RC, Klemme I, Simmons LW (2013b) Strategic adjustments in sperm production within and between two island populations of house mice. Evolution 67:3061–3070PubMedGoogle Scholar
  29. Fisher DO, Double MC, Blomberg SP, Jennions MD, Cockburn A (2006) Post-mating sexual selection increase lifetime fitness of polyandrous females in the wild. Nature 444:89–92PubMedCrossRefGoogle Scholar
  30. Gage MJG (1991) Risk of sperm competition directly affects ejaculate size in the Mediterranean fruit-fly. Anim Behav 42:1036–1037CrossRefGoogle Scholar
  31. García-González F (2008) The relative nature of fertilization success: Implications for the study of post-copulatory sexual selection. BMC Evol Biol 8:140PubMedCentralPubMedCrossRefGoogle Scholar
  32. García-González F, Simmons LW (2007) Shorter sperm confer higher competitive fertilization success. Evolution 61:816–824PubMedCrossRefGoogle Scholar
  33. Gasparini C, Simmons LW, Beveridge M, Evans JP (2010) Sperm swimming velocity predicts competitive fertilization success in the green swordtail Xiphophorus helleri. PLoS ONE 5:1–5CrossRefGoogle Scholar
  34. Gomendio M, Harcourt AH, Roldan ERS (1998) Sperm competition in mammals. In: Sperm competition and sexual selection. Academic Press, London, pp 667–781CrossRefGoogle Scholar
  35. Hosken DJ, Garner TWJ, Tregenza T, Wedell N, Ward PI (2003) Superior sperm competitors sire higher-quality young. Proc R Soc Lond B 270:1933–1938CrossRefGoogle Scholar
  36. Huck UW, Banks EM, Coopersmith CB (1984) Social olfaction in male brown lemmings (Lemmus sibiricus = trimucronatus) and collared lemmings (Dicrostonyx groenlandicus): II. Discrimination of mated and unmated females. J Comp Psychol 98:60–65PubMedCrossRefGoogle Scholar
  37. Huck UW, Quinn RP, Lisk RD (1985) Determinants of mating success in the golden hamster (Mesocricetus auratus) iv. Sperm competition. Behav Ecol Sociobiol 17:239–252CrossRefGoogle Scholar
  38. Jones R (1999) To store or mature sperm? The primary role of the epididymis. Int J Androl 22:57–67PubMedCrossRefGoogle Scholar
  39. Klemme I, Firman RC (2013) Male house mice that have evolved with sperm competition have increased mating duration and paternity success. Anim Behav 85:751–758CrossRefGoogle Scholar
  40. Klemme I, Ylonen H, Eccard JA (2008) Long-term fitness benefits of polyandry in a small mammal, the bank vole Clethrionomys glareolus. Proc R Soc Lond B 275:1095–1100CrossRefGoogle Scholar
  41. Kraaijeveld-Smit FJL, Ward SJ, Temple-Smith PD (2002) Multiple paternity in a field population of a small carnivorous marsupial, the agile antechinus, Antechinus agilis. Behav Ecol Sociobiol 52:84–91CrossRefGoogle Scholar
  42. Mardia KV, Kent JT, Bibby JM (1979) Multivariate analysis. Academic Press, LondonGoogle Scholar
  43. Moro D, Spencer PBS (2003) Microsatellite primers for the Western Pebble-mound Mouse (Pseudomys chapmani) that show cross amplification for other species of Australian rodent. Mol Ecol Notes 3:259–261CrossRefGoogle Scholar
  44. Nakagawa S (2004) A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav Ecol 15:1044–1045CrossRefGoogle Scholar
  45. Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–567CrossRefGoogle Scholar
  46. Parker GA (1990) Sperm competition games: raffles and roles. Proc R Soc Lond B 242:120–126CrossRefGoogle Scholar
  47. Pizzari T, Cornwallis CK, Løvlie H, Jakobsson S, Birkhead TR (2003) Sophisticated sperm allocation in male fowl. Nature 426:70–74PubMedCrossRefGoogle Scholar
  48. Ramm SA, Stockley P (2007) Ejaculate allocation under varying sperm competition risk in the house mouse, Mus musculus domesticus. Behav Ecol 18:491–495CrossRefGoogle Scholar
  49. Ramm SA, Stockley P (2009) Adaptive plasticity of mammalian sperm production in response to social experience. Proc R Soc Lond B 276:745–751CrossRefGoogle Scholar
  50. Ramm SA, Parker GA, Stockley P (2005) Sperm competition and the evolution of male reproductive anatomy in rodents. Proc R Soc Lond B 272:949–955CrossRefGoogle Scholar
  51. Rugh R (1968) The mouse: its reproduction and development. Burgess Publishing Company, MinneapolisGoogle Scholar
  52. Simmons LW (2005) The evolution of polyandry: sperm competition, sperm selection, and offspring viability. Annu Rev Ecol Evol Syst 36:125–146CrossRefGoogle Scholar
  53. Simmons LW, Beveridge M, Wedell N, Tregenza T (2006) Postcopulatory inbreeding avoidance by female crickets only revealed by molecular markers. Mol Ecol 15:3817–3824PubMedCrossRefGoogle Scholar
  54. Simmons LW, Beveridge M, Kennington J (2007) Polyandry in the wild: temporal changes in female mating frequency and sperm competition intensity in natural populations of the tettigoniid Requena verticalis. Mol Ecol 16:4613–4623PubMedCrossRefGoogle Scholar
  55. Thornhill R, Alcock J (1983) The evolution of insect mating systems. Harvard University Press, CambridgeGoogle Scholar
  56. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual Selection and the Descent of Man. Aldine-Atherton, Chicago, pp 136–179Google Scholar
  57. Voss R (1979) Male accessory glands and the evolution of copulatory plugs in rodents. Occ Pap Mus Zool Univ Mich 689:1–17Google Scholar
  58. Williams-Ashman HG (1984) Transglutaminases and the clotting of mammalian seminal fluids. Mol Cell Biochem 58:51–61PubMedCrossRefGoogle Scholar
  59. Yasui Y (1997) A ‘good sperm’ model can explain the evolution of costly multiple mating by females. Am Nat 149:573–584CrossRefGoogle Scholar
  60. Zeh JA, Zeh DW (1997) The evolution of polyandry II: post-copulatory defences against genetic incompatibility. Proc R Soc Lond B 264:69–75CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Centre for Evolutionary Biology, School of Animal Biology (M092)University of Western AustraliaCrawleyAustralia

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