Skip to main content
Log in

Male reproductive pattern in a polygynous ungulate with a slow life-history: the role of age, social status and alternative mating tactics

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

According to life-history theory age-dependent investments into reproduction are thought to co-vary with survival and growth of animals. In polygynous species, in which size is an important determinant of reproductive success, male reproduction via alternative mating tactics at young age are consequently expected to be the less frequent in species with higher survival. We tested this hypothesis in male Alpine ibex (Capra ibex), a highly sexually dimorphic mountain ungulate whose males have been reported to exhibit extremely high adult survival rates. Using data from two offspring cohorts in a population in the Swiss Alps, the effects of age, dominance and mating tactic on the likelihood of paternity were inferred within a Bayesian framework. In accordance with our hypothesis, reproductive success in male Alpine ibex was heavily biased towards older, dominant males that monopolized access to receptive females by adopting the ‘tending’ tactic, while success among young, subordinate males via the sneaking tactic ‘coursing’ was in general low and rare. In addition, we detected a high reproductive skew in male Alpine ibex, suggesting a large opportunity for selection. Compared with other ungulates with higher mortality rates, reproduction among young male Alpine ibex was much lower and more sporadic. Consistent with that, further examinations on the species level indicated that in polygynous ungulates the significance of early reproduction appears to decrease with increasing survival. Overall, this study supports the theory that survival prospects of males modulate the investments into reproduction via alternative mating tactics early in life. In the case of male Alpine ibex, the results indicate that their life-history strategy targets for long life, slow and prolonged growth and late reproduction.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Appleby MC (1982) The consequences and causes of high social rank in red deer stags. Behaviour 80:259–273

    Article  Google Scholar 

  • Bell G (1980) The costs of reproduction and their consequences. Am Nat 116(1):45–76

    Article  Google Scholar 

  • Bergeron P, Grignolio S, Apollonio M, Shipley B, Festa-Bianchet M (2010) Secondary sexual characters signal fighting ability and determine social rank in Alpine ibex (Capra ibex). Behav Ecol Sociobiol 64:1299–1307

    Article  Google Scholar 

  • Biebach I, Keller LF (2009) A strong genetic footprint of the re-introduction history of Alpine ibex (Capra ibex ibex). Mol Ecol 18(24):5046–5058

    Article  PubMed  Google Scholar 

  • Bonenfant C, Pelletier F, Garel M, Bergeron P (2009) Age-dependent relationship between horn growth and survival in wild sheep. J Anim Ecol 78(1):161–171

    Article  PubMed  Google Scholar 

  • Clutton-Brock TH (1984) Reproductive effort and terminal investment in iteroparous animals. Am Nat 123(2):212–229

    Article  Google Scholar 

  • Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer. Behavior and ecology of two sexes. The University of Chicago Press, Chicago

    Google Scholar 

  • Clutton-Brock TH, Albon SD, Guinness FE (1988a) Reproductive success in male and female red deer. In: Clutton-Brock TH (ed) Reproductive success. Studies of individual variation in contrasting breeding systems. The University of Chicago Press, Chicago, pp 325–343

    Google Scholar 

  • Clutton-Brock TH, Green D, Hiraiwa-Hasegawa M, Albon SD (1988b) Passing the buck: resource defence, lek breeding and mate choice in fallow deer. Behav Ecol Sociobiol 23:281–296

    Article  Google Scholar 

  • Clutton-Brock TH, Price OF, Albon SD, Jewell PA (1992) Early development and population fluctuations in Soay sheep. J Anim Ecol 61(2):381–396

    Article  Google Scholar 

  • Coltman DW, Bancroft DR, Robertson A, Smith JA, Clutton-Brock TH, Pemberton JM (1999a) Male reproductive success in a promiscuous mammal: behavioural estimates compared with genetic paternity. Mol Ecol 8(7):1199–1209

    Article  PubMed  CAS  Google Scholar 

  • Coltman DW, Smith JA, Bancroft DR, Pilkington J, MacColl ADC, Clutton-Brock TH, Pemberton JM (1999b) Density-dependent variation in lifetime breeding success and natural and sexual selection in Soay rams. Am Nat 154(6):730–746

    Article  PubMed  CAS  Google Scholar 

  • Coltman DW, Festa-Bianchet M, Jorgenson JT, Strobeck C (2002) Age-dependent sexual selection in bighorn rams. Proc R Soc Lond Ser B Biol Sci 269(1487):165–172

    Article  CAS  Google Scholar 

  • Coltman DW, O’Donoghue P, Jorgenson JT, Hogg JT, Strobeck C, Festa-Bianchet M (2003) Undesirable evolutionary consequences of trophy hunting. Nature 426(6967):655–658

    Article  PubMed  CAS  Google Scholar 

  • Conover DO, Munch SB (2002) Sustaining fisheries yields over evolutionary time scales. Science 297(5578):94–96

    Article  PubMed  CAS  Google Scholar 

  • Coté SD (2000) Dominance hierarchies in female mountain goats: stability, aggressiveness and determinants of rank. Behaviour 137:1541–1566

    Article  Google Scholar 

  • De Vries H (1998) Finding a dominance order most consistent with a linear hierarchy: a new procedure and review. Anim Behav 55:827–843

    Article  PubMed  Google Scholar 

  • De Vries H, Netto WJ, Hanegraaf PLH (1993) Matman—a program for the analysis of sociometric matrices and behavioral transition matrices. Behaviour 125:157–175

    Article  Google Scholar 

  • Dobson FS, Oli MK (2007) Fast and slow life histories of mammals. Ecoscience 14(3):292–299

    Article  Google Scholar 

  • Grotan V, Saether BE, Filli F, Engen S (2008) Effects of climate on population fluctuations of ibex. Glob Change Biol 14(2):218–228

    Article  Google Scholar 

  • Hadfield JD, Richardson DS, Burke T (2006) Towards unbiased parentage assignment: combining genetic, behavioural and spatial data in a Bayesian framework. Mol Ecol 15(12):3715–3730

    Article  PubMed  CAS  Google Scholar 

  • Harris RB, Wall WA, Allendorf FW (2002) Genetic consequences of hunting: what do we know and what should we do? Wildl Soc Bull 30(2):634–643

    Google Scholar 

  • Harvey PH, Zammuto RM (1985) Patterns of mortality and age at 1st reproduction in natural-populations of mammals. Nature 315(6017):319–320

    Article  PubMed  CAS  Google Scholar 

  • Hogg JT, Forbes SH (1997) Mating in bighorn sheep: frequent male reproduction via a high-risk ‘‘unconventional’’ tactic. Behav Ecol Sociobiol 41(1):33–48

    Article  Google Scholar 

  • Isvaran K (2005) Variation in male mating behaviour within ungulate populations: patterns and processes. Curr Sci 89(7):1192–1199

    Google Scholar 

  • Johnson PCD, Haydon DT (2007) Maximum-likelihood estimation of allelic dropout and false allele error rates from Microsatellite genotypes in the absence of reference data. Genetics 175(2):827–842

    Article  PubMed  CAS  Google Scholar 

  • Jones ME, Cockburn A, Hamede R, Hawkins C, Hesterman H, Lachish S, Mann D, McCallum H, Pemberton D (2008) Life-history change in disease-ravaged Tasmanian devil populations. Proc Natl Acad Sci USA 105(29):10023–10027. doi:10.1073/pnas.0711236105

    Article  PubMed  CAS  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(5):1099–1106

    Article  PubMed  Google Scholar 

  • Kozlowski J (1992) Optimal allocation of resources to growth and reproduction—implications for age and size at maturity. Trends Ecol Evol 7(1):15–19

    Article  PubMed  CAS  Google Scholar 

  • Loison A, Gaillard JM, Pelabon C, Yoccoz NG (1999) What factors shape sexual size dimorphism in ungulates? Evol Ecol Res 1(5):611–633

    Google Scholar 

  • Lüps P, Blöchlinger B, Schmid P, Zuber M (2007) Ontogenese und Variabilität verschiedener Körpermerkmale des Steinwildes Capra i. ibex im Berner Oberland (Schweizer Alpen). Beiträge zur Jagd- und Wildforschung 32:495–510

    Google Scholar 

  • McElligott AG, Hayden TJ (2000) Lifetime mating success, sexual selection and life-history of fallow bucks (Dama dama). Behav Ecol Sociobiol 48(3):203–210

    Article  Google Scholar 

  • McElligott AG, Mattiangeli V, Mattiello S, Verga M, Reynolds CA, Hayden TJ (1998) Fighting tactics of fallow bucks (Dama dama, Cervidae): Reducing the risks of serious conflict. Ethology 104(9):789–803

    Article  Google Scholar 

  • McElligott AG, Altwegg R, Hayden TJ (2002) Age-specific survival and reproductive probabilities: evidence for senescence in male fallow deer (Dama dama). Proc R Soc Lond Ser B Biol Sci 269(1496):1129–1137

    Article  Google Scholar 

  • Nussey DH, Kruuk LEB, Morris A, Clements MN, Pemberton JM, Clutton-Brock TH (2009) Inter- and intrasexual variation in aging patterns across reproductive traits in a wild red deer population. Am Nat 174(3):342–357

    Article  PubMed  Google Scholar 

  • Oliveira RF, Taborsky M, Brockmann HJ (2008) Alternative reproductive tactics. An integrative approach. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Pelletier F (2005) Foraging time of rutting bighorn rams varies with individual behavior, not mating tactic. Behav Ecol 16(1):280–285

    Article  Google Scholar 

  • Pemberton JM, Albon SD, Guinness FE, Cluttonbrock TH, Dover GA (1992) Behavioral estimates of male mating success tested by DNA fingerprinting in a polygynous mammal. Behav Ecol 3(1):66–75

    Article  Google Scholar 

  • Pemberton JM, Coltman DW, Smith JA, Pilkington JG (1999) Molecular analysis of a promiscuous, fluctuating mating system. Biol J Linnean Soc 68(1–2):289–301

    Article  Google Scholar 

  • Pianka ER, Parker WS (1975) Age-specific reproductive tactics. Am Nat 109(968):453–464

    Article  Google Scholar 

  • Preston BT, Stevenson IR, Pemberton JM, Wilson K (2001) Dominant rams lose out by sperm depletion—a waning success in siring counters a ram’s high score in competition for ewes. Nature 409(6821):681–682

    Article  PubMed  CAS  Google Scholar 

  • Promislow DEL, Harvey PH (1990) Living fast and dying young—a comparative analysis of life-history variation among mammals. J Zool 220:417–437

    Article  Google Scholar 

  • Ratti P, Habermehl KH (1977) Investigations into age estimation and age determination of mountain ibex (Capra ibex ibex) in Kanton Graubunden. Z Jagdwiss 23(4):188–213

    Article  Google Scholar 

  • Ricca MA, Anthony RG, Jackson DH, Wolfe SA (2002) Survival of Columbian white-tailed deer in western Oregon. J Wildl Manag 66(4):1255–1266

    Article  Google Scholar 

  • Roed KH, Holand O, Smith ME, Gjostein H, Kumpula J, Nieminen M (2002) Reproductive success in reindeer males in a herd with varying sex ratio. Mol Ecol 11(7):1239–1243

    Article  PubMed  Google Scholar 

  • Roed KH, Holand O, Gjostein H, Hansen H (2005) Variation in male reproductive success in a wild population of reindeer. J Wildl Manag 69(3):1163–1170

    Article  Google Scholar 

  • Say L, Naulty F, Hayden TJ (2003) Genetic and behavioural estimates of reproductive skew in male fallow deer. Mol Ecol 12(10):2793–2800

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Sorin AB (2004) Paternity assignment for white-tailed deer (Odocoileus virginianus): mating across age classes and multiple paternity. J Mammal 85(2):356–362

    Article  Google Scholar 

  • Stearns SC (1976) Life-history tactics—review of ideas. Q Rev Biol 51(1):3–47

    Article  PubMed  CAS  Google Scholar 

  • Stearns SC (1983) The influence of size and phylogeny on patterns of covariation among life-history traits in the mammals. Oikos 41(2):173–187

    Article  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, New York

    Google Scholar 

  • Stevenson IR, Bancroft DR (1995) Fluctuating trade-offs favour precocial maturity in male Soay sheep. Proc R Soc Lond Ser B Biol Sci 262(1365):267–275

    Article  CAS  Google Scholar 

  • Stevenson IR, Marrow P, Preston BT, Pemberton JM, Wilson K (2004) Adaptive reproductive strategies. In: Clutton-Brock TH, Pemberton J (eds) Soay sheep. Dynamics and selection in a island population. Cambrigde University Press, Cambridge

    Google Scholar 

  • Taberlet P, Waits LP, Luikart G (1999) Noninvasive genetic sampling: look before you leap. Trends Ecol Evol 14(8):323–327

    Article  PubMed  Google Scholar 

  • Toigo C, Gaillard JM (2003) Causes of sex-biased adult survival in ungulates: sexual size dimorphism, mating tactic or environment harshness? Oikos 101(2):376–384

    Article  Google Scholar 

  • Toïgo C, Gaillard JM, Festa-Bianchet M, Largo E, Michallet J, Maillard D (2007) Sex- and age-specific survival of the highly dimorphic Alpine ibex: evidence for a conservative life-history tactic. J Anim Ecol 76(4):679–686

    Article  PubMed  Google Scholar 

  • Valiere N (2002) GIMLET: a computer program for analysing genetic individual identification data. Mol Ecol Notes 2(3):377–379

    CAS  Google Scholar 

  • Vanpe C, Kjellander P, Galan M, Cosson JF, Aulagnier S, Liberg O, Hewison AJM (2008) Mating system, sexual dimorphism, and the opportunity for sexual selection in a territorial ungulate. Behav Ecol 19(2):309–316

    Article  Google Scholar 

  • Vanpe C, Gaillard JM, Morellet N, Kjellander P, Liberg O, Delorme D, Hewison AJM (2009) Age-specific variation in male breeding success of a territorial ungulate species, the European roe deer. J Mammal 90(3):661–665

    Article  Google Scholar 

  • Wehausen JD, Ramey RR, Epps CW (2004) Experiments in DNA extraction and PCR amplification from bighorn sheep feces: the importance of DNA extraction method. J Hered 95(6):503–509

    Article  PubMed  CAS  Google Scholar 

  • Williams GC (1966) Natural selection costs of reproduction and a refinement of lacks principle. Am Nat 100(916):687–690

    Article  Google Scholar 

  • Willisch CS, Neuhaus P (2009) Alternative mating tactics and their impact on survival in adult male Alpine ibex (Capra ibex ibex). J Mammal 90(6):1421–1430

    Article  Google Scholar 

  • Willisch CS, Neuhaus P (2010) Social dominance and conflict reduction in rutting male Alpine ibex, Capra ibex. Behav Ecol 21:372–380

    Article  Google Scholar 

  • Wilson GA, Olson W, Strobeck C (2002) Reproductive success in wood bison (Bison bison athabascae) established using molecular techniques. Can J Zool Revue Canadienne de Zoologie 80(9):1537–1548

    Article  Google Scholar 

  • Wolff JO (1998) Breeding strategies, mate choice, and reproductive success in American bison. Oikos 83(3):529–544

    Article  Google Scholar 

Download references

Acknowledgments

We thank J-C Roch, as well as K. Bieri Willisch, P. Decristophoris, P. Deleury, I. Glanzmann, N. Grandjean, C. Hebeisen, B. Hofer, I. Leathwood, H. Nimmervoll, B. Nussberger, L. Senn, C. Wittker, and numerous volunteers for their help with the captures, data collection and laboratory work. We are grateful to J. Hadfield, E. Postma and P. Wandeler for their assistance with genetic and statistical analyses. We thank R. Bshary, A. McElligott and M. Taborsky for comments and discussions on earlier drafts of the manuscript. The paper benefited greatly from the comments by two anonymous referees and J.A. Endler. Many thanks go to the authorities of the Canton Vaud who made this study in the population ‘Cape au Moine’ (VD) possible. Financial support by the Federal Office of the Environment (FOEN) is gratefully acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christian S. Willisch.

Appendix

Appendix

See Table 5.

Table 5 Expected heterozygosity (H e ) and locus-specific error rates (per genotype) for faecal and blood/tissue samples

Rights and permissions

Reprints and permissions

About this article

Cite this article

Willisch, C.S., Biebach, I., Koller, U. et al. Male reproductive pattern in a polygynous ungulate with a slow life-history: the role of age, social status and alternative mating tactics. Evol Ecol 26, 187–206 (2012). https://doi.org/10.1007/s10682-011-9486-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-011-9486-6

Keywords

Navigation