Male reproductive tactics to increase paternity in the polygynandrous Columbian ground squirrel (Urocitellus columbianus)

Abstract

In polyandrous and polygynandrous species where females mate with multiple partners, males are expected to maximize their fitness by exhibiting an array of reproductive behaviors to ensure fertilization success, such as competing for the best mating order within a mating sequence, optimizing their investment in copulation, and mate guarding. Though there is genetic evidence of a first-male precedence in siring success for many mammalian species, the causes of this effect are poorly understood. We studied influences on first-male precedence in Columbian ground squirrels (Urocitellus columbianus). We found that the time a male spent consorting and mate guarding declined with his mating order (both the highest for the first male to mate). Mate guarding by the first male significantly reduced, but did not exclude, the number of additional males a female accepted. Later mating males reduced the time spent consorting, suggesting a perceived decreased chance of fertilization success. Consortship and mate guarding durations were positively related to the male’s siring success and to each other, suggesting that males adjusted these behaviors strategically to increase their chances of fertilization success. Our results suggest that besides being the first male to consort, first-male sperm precedence is further enhanced through longer mating bouts and by suppressing the chances and/or efforts of later mating males.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Alcock J (1994) Postinsemination associations between males and females in insects: the mate guarding hypothesis. Annu Rev Entomol 39:1–21

    Article  Google Scholar 

  2. Andersson M (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  3. Baumgardner DJ, Hartung TG, Sawrey DK, Webster DG, Dewsbury DA (1982) Muroid copulatory plugs and female reproductive tracts: a comparative investigation. J Mammal 63:110–117

    Article  Google Scholar 

  4. Birkhead TR, Møller AP (1992) Sperm competition in birds: evolutionary causes and consequences. Academic, London

    Google Scholar 

  5. Birkhead TR, Møller AP (1998) Sperm competition and sexual selection. Academic, London

    Google Scholar 

  6. Birkhead TR, Pizzari T (2002) Postcopulatory sexual selection. Nat Rev Genet 3:262–273

    PubMed  Article  CAS  Google Scholar 

  7. Boellstorff DE, Owings DH, Penedo MCT, Hersek MJ (1994) Reproductive behaviour and multiple paternity of California ground squirrels. Anim Behav 47:1057–1064

    Article  Google Scholar 

  8. Bouchie L, Bennett NC, Jackson T, Waterman JM (2006) Are Cape ground squirrels (Xerus inauris) induced or spontaneous ovulators? J Mammal 87:60–66

    Article  Google Scholar 

  9. Clutton-Brock TH (1989) Mammalian mating systems. Proc R Soc Lond B 236:339–372

    PubMed  Article  CAS  Google Scholar 

  10. Clutton-Brock TH, Parker GA (1992) Potential reproductive rates and the operation of sexual selection. Q Rev Biol 67:437–456

    Article  Google Scholar 

  11. Cothran RD (2004) Precopulatory mate guarding affects predation risk in two freshwater amphipod species. Anim Behav 68:1133–1138

    Article  Google Scholar 

  12. Danchin E, Giraldeau LA, Cezilly FC (2008) Behavioural ecology: an evolutionary perspective on behaviour. Oxford University Press, Oxford

    Google Scholar 

  13. Dewsbury DA, Sawrey DK (1984) Male capacity as related to sperm production, pregnancy initiation, and sperm competition in deer mice (Peromyscus maniculatus). Behav Ecol Sociobiol 16:37–47

    Article  Google Scholar 

  14. Dobson FS (1983) Agonism and territoriality in the California ground squirrel. J Mammal 64:218–225

    Article  Google Scholar 

  15. Dobson FS, Murie JO (1987) Interpretation of intraspecific life history patterns: evidence from Columbian ground squirrels. Am Nat 129(3):382–397

    Article  Google Scholar 

  16. Dobson FS, Badry MJ, Geddes C (1992) Seasonal activity in the Columbian ground squirrel. Can J Zool 70:1364–1368

    Article  Google Scholar 

  17. Emlen ST, Oring LW (1977) Ecology, sexual selection, and evolution of mating systems. Science 197:215–223

    PubMed  Article  CAS  Google Scholar 

  18. Festa-Bianchet M, King WJ (1984) Behavior and dispersal of yearling Columbian ground squirrels. Can J Zool 62:161–167

    Article  Google Scholar 

  19. Foltz DW, Schwagmeyer PL (1989) Sperm competition in the thirteen-lined ground squirrel: differential fertilization success under field conditions. Am Nat 133:257–265

    Article  Google Scholar 

  20. Foster MA (1934) The reproductive cycle in the female ground squirrel, Citellus tridecemlineatus (Mitchill). Am J Anat 54:487–511

    Article  Google Scholar 

  21. Gomendio M, Harcourt AH, Roldàn ERS (1998) Sperm competition in mammals. In: Birkhead T, Møller AP (eds) Sperm competition and sexual selection. Academic, London, pp 667–755

    Google Scholar 

  22. Goossens B, Graziani L, Waits LP, Farand E, Magnolon S, Coulon J, Bel MC, Taberlet P, Allaine D (1998) Extra-pair paternity in the monogamous Alpine marmot revealed by nuclear DNA microsatellite analysis. Behav Ecol Sociobiol 43:281–288

    Article  Google Scholar 

  23. Hammerstein P, Parker GA (1982) The asymmetric war of attrition. J Theor Biol 96:647–682

    Article  Google Scholar 

  24. Hanken J, Sherman PW (1981) Multiple paternity in Belding’s ground squirrel litters. Science 212:351–353

    PubMed  Article  CAS  Google Scholar 

  25. Hanslik S, Kruckenhauser L (2000) Microsatellite loci for two European sciurid species (Marmota marmota, Spermophilus citellus). Mol Ecol 9:2163–2165

    PubMed  Article  CAS  Google Scholar 

  26. Hatchwell BJ, Davies NB (1992) An experimental study of mating competition in monogamous and polyandrous dunnocks, Prunella modularis: I. Mate guarding and copulations. Anim Behav 43:595–609

    Article  Google Scholar 

  27. Hoogland JL (1995) The black-tailed prairie dog: social life of a burrowing mammal. The University of Chicago Press, Chicago

    Google Scholar 

  28. Hoogland JL, Foltz DW (1982) Variation in male and female reproductive success in a harempolygynous mammal, the black-tailed prairie dog (Sciuridae: Cynomys ludovicianus). Behav Ecol Sociobiol 11:155–163

    Article  Google Scholar 

  29. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev Camb Philos Soc 75:21–64

    PubMed  Article  CAS  Google Scholar 

  30. Johnsen A, Lifjeld JT, Rohde PA, Primmer CR, Ellegren H (1998) Sexual conflict over fertilizations: female bluethroats escape male paternity guards. Behav Ecol Sociobiol 43:401–408

    Article  Google Scholar 

  31. Jormalainen V (1998) Precopulatory mate guarding in crustaceans: male competitive strategy and intersexual conflict. Q Rev Biol 73:275–304

    Article  Google Scholar 

  32. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    PubMed  Article  Google Scholar 

  33. Koenig WD, Dickinson JL (2004) Ecology and evolution of cooperative breeding in birds. Cambridge University Press, Cambridge

    Google Scholar 

  34. Kohda M, Heg D, Makino Y, Takeyama T, Shibata J, Watanabe K, Munehara H, Hori M, Awata S (2009) Living on the wedge: female control of paternity in a cooperatively polyandrous cichlid. Proc R Soc Lond B 276:4207–4214

    Article  Google Scholar 

  35. Kokko H, Morrell LJ (2005) Mate guarding, male attractiveness and paternity under social monogamy. Behav Ecol 16:724–731

    Article  Google Scholar 

  36. Komdeur J (2001) Mate guarding in the Seychelles warbler is energetically costly and adjusted to paternity risk. Proc R Soc Lond B 268:2103–2111

    Article  CAS  Google Scholar 

  37. Koprowski JL (1992) Removal of copulatory plugs by female tree squirrels. J Mammal 73:572–576

    Article  Google Scholar 

  38. Kraaijeveld-Smit FJL, Ward SJ, Temple-Smith PD, Paetkau D (2002) Factors influencing paternity success in Antechinus agilis: last-male sperm precedence, timing of mating and genetic compatibility. J Evol Biol 15:100–107

    Article  Google Scholar 

  39. Kvarnemo C, Ahnesjo I (1996) The dynamics of operational sex ratios and competition for mates. Trends Ecol Evol 11:404–408

    PubMed  Article  CAS  Google Scholar 

  40. Kyle CJ, Karels TJ, Clark B, Strobeck C, Hik DS, Davis CS (2004) Isolation and characterization of microsatellite markers in hoary marmots (Marmota caligata). Mol Ecol Notes 4:749–751

    Article  CAS  Google Scholar 

  41. Lacey EA, Wieczorek JR, Tucker PK (1997) Male mating behaviour and patterns of sperm precedence in Arctic ground squirrels. Anim Behav 53:767–779

    Article  Google Scholar 

  42. Lindén M, Moller AP (1989) Cost of reproduction and covariation of life history traits in birds. Trends Ecol Evol 4(12):367–371

    PubMed  Article  Google Scholar 

  43. Linn CD, Molina Y, Difatta J, Christenson TE (2007) The adaptive advantage of prolonged mating: a test of alternative hypotheses. Anim Behav 74:481–485

    Article  Google Scholar 

  44. Lisk RD, Huck UW, Gore AC, Armstrong MX (1989) Mate choice, mate guarding and other mating tactics in golden hamsters maintained under semi-natural conditions. Behaviour 348:58–75

    Article  Google Scholar 

  45. Manno TG, Dobson FS (2008) Why are male Columbian ground squirrels territorial? Ethology 114:1049–1060

    Article  Google Scholar 

  46. Manno TG, Nesterova AP, Debarbieri LM, Kennedy SE, Wright KS, Dobson FS (2007) Why do male Columbian ground squirrels give a mating call? Anim Behav 74:1319–1327

    Article  Google Scholar 

  47. Manno TG, DeBarbieri LM, Davidson J (2008) Why do Columbian ground squirrels copulate underground? J Mammal 89:882–888

    Article  Google Scholar 

  48. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7:639–655

    PubMed  Article  CAS  Google Scholar 

  49. Martin K (1984) Reproductive defence priorities of male willow ptarmigan (Lagopus lagopus): enhancing mate survival or extending paternity options? Behav Ecol Sociobiol 16:57–63

    Article  Google Scholar 

  50. Martín J, López P (1999) Nuptial coloration and mate guarding affect escape decisions of male lizards Psammodromus algirus. Ethology 105:439–447

    Article  Google Scholar 

  51. Møller AP (1987) Mate guarding in the swallow Hirundo rustica. An experimental study. Behav Ecol Sociobiol 21:119–123

    Article  Google Scholar 

  52. Murie JO (1995) Mating behavior of Columbian ground squirrels. 1. Multiple mating by females and multiple paternity. Can J Zool 73:1819–1926

    Article  Google Scholar 

  53. Murie JO, Harris MA (1982) Annual variation of offspring emergence and breeding in Columbian ground squirrels (Spermophilus columbianus). J Mammal 63(3):431–439

    Article  Google Scholar 

  54. Murie JO, McLean IG (1980) Copulatory plugs in ground squirrels. J Mammal 61:355–356

    Article  Google Scholar 

  55. Murie JO, Stevens SD, Leoppky B (1998) Survival of captive-born cross-fostered juvenile Columbian ground squirrels in the field. J Mammal 79:1152–1160

    Article  Google Scholar 

  56. Neuhaus P (2000) Timing of hibernation and molt in female Columbian ground squirrels. J Mammal 81:571–577

    Article  Google Scholar 

  57. Neuhaus P, Pelletier N (2001) Mortality in relation to season, age, sex, and reproduction in Columbian ground squirrels (Spermophilus columbianus). Can J Zool 79:465–470

    Article  Google Scholar 

  58. Norusis MJ (1994) SPSS graduate student statistical package (6.10). SPSS, Chicago

    Google Scholar 

  59. Oliveira R, Taborsky M, Brockmann HJ (2008) Alternative reproductive tactics: an integrative approach. Cambridge University Press, Cambridge

    Google Scholar 

  60. Parker GA (1970) Sperm competition and its evolutionary effect on copula duration in fly Scatophaga stercoraria. J Insect Physiol 16:1301–1328

    Article  Google Scholar 

  61. Parker GA (1979) Sexual selection and sexual conflict. In: Blum MS, Blum NA (eds) Sexual selection and reproductive competition in insects. Academic, London, pp 123–166

    Google Scholar 

  62. Parker GA (1982) Why are there so many tiny sperm–sperm competition and the maintenance of 2 sexes. J Theor Biol 96:281–294

    PubMed  Article  CAS  Google Scholar 

  63. Parker GA (1984) Sperm competition and the evolution of animal mating systems. Academic, Orlando, pp 1–61

    Google Scholar 

  64. Pinxten R, Eens M (1997) Copulation and mate-guarding patterns in polygynous European starlings. Anim Behav 54:45–58

    PubMed  Article  Google Scholar 

  65. Pizzari T, Snook RR (2003) Perspective: sexual conflict and sexual selection: chasing away paradigm shifts. Evolution 57:1223–1236

    PubMed  Google Scholar 

  66. Plaistow SJ, Bollache L, Cezilly F (2003) Energetically costly precopulatory mate guarding in the amphipod Gammarus pulex: causes and consequences. Anim Behav 65:683–691

    Article  Google Scholar 

  67. Raveh S, Heg D, Dobson FS, Coltman DW, Gorrell JC, Balmer A, Neuhaus P (2010) Mating order and reproductive success in male Columbian ground squirrels (Urocitellus columbianus). Behav Ecol 21(3):537–547

    Article  Google Scholar 

  68. Saeki Y, Kruse KC, Switzer PV (2005) Physiological costs of mate guarding in the Japanese beetle (Popillia japonica Newman). Ethology 111:863–877

    Article  Google Scholar 

  69. Schwagmeyer PL, Foltz DW (1990) Factors affecting the outcome of sperm competition in thirteen-lined ground squirrels. Anim Behav 39:156–162

    Article  Google Scholar 

  70. Schwagmeyer PL, Parker GA (1987) Queuing for mates in thirteen-lined ground squirrels. Anim Behav 35:1015–1025

    Article  Google Scholar 

  71. Sherman PW (1989) Mate guarding as paternity insurance in Idaho ground squirrels. Nature 338:418–420

    PubMed  Article  CAS  Google Scholar 

  72. Shuster SM, Wade MJ (2003) Mating systems and strategies. Princeton University Press, Princeton

    Google Scholar 

  73. Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton

    Google Scholar 

  74. Soulsbury CD (2010) Ovulation mode modifies paternity monopolization in mammals. Biol Lett 6:39–41

    PubMed  Article  Google Scholar 

  75. Stevens S, Coffin J, Strobeck C (1997) Microsatellite loci in Columbian ground squirrels Spermophilus columbianus. Mol Ecol 6:493–495

    PubMed  Article  CAS  Google Scholar 

  76. Waterman JM (2007) Male mating strategies in rodents. In: Wolff JO, Sherman PW (eds) Rodent societies, an ecological and evolutionary perspective. University of Chicago Press, Chicago

    Google Scholar 

  77. Wolff JO, Sherman PW (2007) Rodent societies, an ecological and evolutionary perspective. University of Chicago Press, Chicago

    Google Scholar 

  78. Yamamura N (1986) An evolutionarily stable strategy (ESS) model of postcopulatory guarding in insects. Theor Popul Biol 29:438–455

    Article  Google Scholar 

  79. Zaldivar Rae J, Drummond H (2007) Female accompaniment by male whiptail lizards: is it mate guarding? Behav 14:1383–1402

    Article  Google Scholar 

Download references

Acknowledgments

We thank for help in the field E. Emery, C. Grossen, D. Karlen, C. Heiniger, N. Tonetti, K. Bieri, M. Berger, C. Deleglise, N. Brunner, M. Binggeli, and the M.Sc. students S. Röösli, B. M. Fairbanks, and A. Skiebiel. Thanks to E. Kubanek who assisted with genotyping. C. Saraux and R. Bergmüller helped with statistical analyses. R. Bshary, B. König, F. Trillmich, S. G. Kenyon, and J. E. Lane provided insightful comments on earlier drafts of this manuscript. The study was funded by a Swiss National Science Foundation grant to P. Neuhaus (SNF 3100AO-109816). D. Heg was supported by SNF grant 3100A0-108473, J.C. Gorrell by an Alberta Conservation Association Biodiversity grant, and F. S. Dobson by a US National Science Foundation research grant (DEB-0089473). The research was conducted under animal use protocols from the Biosciences Animal Care Committee, University of Alberta; the Life and Environmental Sciences Animal Resource Center, University of Calgary; and the Institutional Animal Care and Use Committee at Auburn University. The Institute of Biogeosciences (University of Calgary) provided housing and laboratory facilities at the R. B. Miller Field Station during the field season; we thank Station Manager J. Buchanan-Mappin, Institute Director E. Johnson, and camp responsible K. Ruckstuhl for their support.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Shirley Raveh.

Additional information

Communicated by A. Schulte-Hostedde

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Raveh, S., Heg, D., Viblanc, V.A. et al. Male reproductive tactics to increase paternity in the polygynandrous Columbian ground squirrel (Urocitellus columbianus). Behav Ecol Sociobiol 65, 695–706 (2011). https://doi.org/10.1007/s00265-010-1071-4

Download citation

Keywords

  • Mating order
  • Multiple mating
  • Mate guarding
  • Paternity
  • Male reproductive success
  • Columbian ground squirrels