Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

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 via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

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

    Article  Google Scholar 

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

    Google Scholar 

  • 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 

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

    Google Scholar 

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

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

  • 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 

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

    Article  Google Scholar 

  • 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 

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

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • 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 

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

    Article  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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 

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

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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 

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

    Google Scholar 

  • 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 

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

    Article  PubMed  CAS  Google Scholar 

  • 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 

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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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

    Book  Google Scholar 

  • 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 

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

    Article  Google Scholar 

  • 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 

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

    Article  Google Scholar 

  • 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 

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

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

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

    Article  PubMed  Google Scholar 

  • 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 

  • 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 

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

    Article  Google Scholar 

  • 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 

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

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

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

    Article  Google Scholar 

  • 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 

  • 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 

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

    Article  Google Scholar 

  • 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 

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

    Article  Google Scholar 

  • 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 

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

    Google Scholar 

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

    Book  Google Scholar 

  • 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 

  • 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 

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

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

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

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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 

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

    Google Scholar 

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

    Article  Google Scholar 

  • 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

Author notes

  1. Shirley Raveh

    Present address: Konrad Lorenz Institute for Ethology, Austrian Academy of Sciences, Savoyenstr. 1a, 1160, Vienna, Austria

Authors and Affiliations

  1. Department of Eco-Ethology, Institute of Biology, University of Neuchâtel, Rue Emile-Argand 11, Case postale 158, 2009, Neuchâtel, Switzerland

    Shirley Raveh & Peter Neuhaus

  2. Department of Behavioural Ecology, University of Bern, 3032, Hinterkappelen, Switzerland

    Dik Heg

  3. Départment Ecologie, Physiologie et Ethologie, IPHC, UMR 7178, CNRS-UdS, 67087, Strasbourg Cedex 02, France

    Vincent A. Viblanc

  4. Department of Biological Sciences, University of Alberta, Edmonton, Alberta, T6G 2E9, Canada

    David W. Coltman & Jamieson C. Gorrell

  5. Centre d’Ecologie Fonctionnelle et Evolutive, Centre National de la Recherche Scientifique—UMR 5175, 1919, Route de Mende, 34293, Montpellier Cedex 5, France

    F. Stephen Dobson

  6. Department of Biological Sciences, Auburn University, 331 Funchess Hall, Auburn, AL, 36849, USA

    F. Stephen Dobson & Adele Balmer

  7. Department of Biological Sciences, University of Calgary, 2500 University Drive, NW, Calgary, Alberta, T2N 1N4, Canada

    Peter Neuhaus

Authors
  1. Shirley Raveh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dik Heg
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vincent A. Viblanc
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David W. Coltman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jamieson C. Gorrell
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. F. Stephen Dobson
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Adele Balmer
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Peter Neuhaus
    View author publications

    You can also search for this author in PubMed Google Scholar

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

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-010-1071-4

Keywords

Search

Navigation