Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Alpine ibex males grow large horns at no survival cost for most of their lifetime


Large horns or antlers require a high energy allocation to produce and carry both physiological and social reproductive costs. Following the principle of energy allocation that implies trade-offs among fitness components, growing large weapons early in life should thus reduce future growth and survival. Evidence for such costs is ambiguous, however, partly because individual heterogeneity can counterbalance trade-offs. Individuals with larger horns or antlers may be of better quality and thus have a greater capacity to survive. We investigated trade-offs between male early horn growth and future horn growth, baseline mortality, onset of actuarial senescence, and rate of ageing in an Alpine ibex (Capra ibex ibex) population. Horn growth of males in early life was positively correlated to their horn length throughout their entire life. Cohort variation and individual heterogeneity both accounted for among-individual variation in horn length, suggesting both long-lasting effects of early life conditions and individual-specific horn growth trajectories. Early horn growth did not influence annual survival until 12 years of age, indicating that males do not invest in horn growth at survival costs over most of their lifetime. However, males with fast-growing horns early in life tended to have lower survival at very old ages. Individual heterogeneity, along with the particular life-history tactic of male ibex (weak participation to the rut until an old age after which they burn out in high mating investment), are likely to explain why the expected trade-off between horn growth and survival does not show up, at least until very old ages.

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

Fig. 1
Fig. 2
Fig. 3


  1. Andersson MB (1994) Sexual selection. Princeton University Press, Princeton

  2. Aubry LM, Cam E, Koons DN, Monnat JY, Pavard S (2011) Drivers of age-specific survival in a long-lived seabird: contributions of observed and hidden sources of heterogeneity. J Anim Ecol 80:375–383

  3. Barbraud C, Weimerskirch H (2005) Environmental conditions and breeding experience affect costs of reproduction in blue petrels. Ecology 86:682–692

  4. Bergeron P, Festa-Bianchet M, von Hardenberg A, Bassano B (2008) Heterogeneity in male horn growth and longevity in a highly sexually dimorphic ungulate. Oikos 117:77–82

  5. Bergeron P, Grignolio S, 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

  6. Bonenfant C, Pelletier F, Garel M, Bergeron P (2008) Age-dependent relationship between horn growth and survival in wild sheep. J Anim Ecol 78:161–171

  7. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach, 2nd edn. Springer, New York

  8. Cam E, Link WA, Cooch EG, Monnat JY, Danchin E (2002) Individual covariation in life-history traits: seeing the trees despite the forest. Am Nat 159:96–105

  9. Choquet R, Reboulet A-M, Pradel R, Gimenez O, Lebreton J-D (2004) M-SURGE: new software specifically designed for multistate capture–recapture models. Anim Biodivers Conserv 27:207–215

  10. Choquet R, Lebreton J-D, Gimenez O, Reboulet A-M, Pradel R (2009a) U-CARE: utilities for performing goodness of fit tests and manipulating CApture–REcapture data. Ecography 32:1071–1074

  11. Choquet R, Rouan L, Pradel R (2009) Program E-SURGE: a software application for fitting multievent models. In: Thomson D, Cooch EG, Conroy MJ (eds) Modeling demographic processes in marked populations. Environmental and ecological statistics, vol 3. Springer, New York, pp 845–865

  12. Clutton-Brock TH (1987) Sexual selection in cervidae. In: Wemmer (ed) Research symposium of the National Zoological Park

  13. Clutton-Brock TH (ed) (1988) Reproductive success. University of Chicago Press, Chicago

  14. Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: behavior and ecology of two sexes. University of Chicago Press, Chicago

  15. Cody ML (1966) A general theory of clutch size. Evolution 20:174–184

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

  17. Darwin C (1871) The descent of man and selection in relation to sex. Murray, London

  18. Descamps S, Boutin S, Berteaux D, Gaillard JM (2006) Best squirrels trade a long life for an early reproduction. Proc R Soc Lond B 273:2369–2374

  19. Drent RH, Daan S (1980) The prudent parent—energetic adjustments in avian breeding. Ardea 68:225–252

  20. Festa-Bianchet M, Jorgenson JT, Réale D (2000) Early development, adult mass and reproductive success in bighorn sheep. Behav Ecol 15:305–312

  21. Festa-Bianchet M, Coltman DW, Turelli L, Jorgenson JT (2004) Relative allocation to horn and body growth in bighorn rams varies with resource availability. Behav Ecol 15:305–312

  22. Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622

  23. Garel M, Forsyth DM, Loison A, Dubray D, Jullien JM, Tustin KG, Maillard D, Gaillard JM (2011) Age-related male reproductive effort in two mountain ungulates of contrasting sexual size dimorphism. Can J Zool 89:929–937

  24. Geist V (1966) The evolutionary significance of mountain sheep horns. Evolution 20:558–566

  25. Geist V (1971) Mountain sheep: a study in behaviour and evolution. University of Chicago Press, Chicago

  26. Grosbois V, Harris MP, Anker-Nilssen T, McCleery RH, Shaw DN, Morgan BJT, Gimenez O (2009) Modeling survival at multi-population scales using mark–recapture data. Ecology 90:2922–2932

  27. Hamel S, Gaillard J-M, Yoccoz NG, Loison A, Bonenfant C, Descamps S (2010) Fitness costs of reproduction depend on life speed: empirical evidence from mammalian populations. Ecol Lett 13:915–935

  28. Hamel S, Cote SD, Festa-Bianchet M (2011) Tradeoff between offspring mass and subsequent reproduction in a highly iteroparous mammal. Oikos 120:690–695

  29. Hamilton WD (1966) The moulding of senescence by natural selection. J Theor Biol 12:12–45

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

  31. Jennings DJ, Carlin CM, Hayden TJ, Gammell MP (2010) Investment in fighting in relation to body condition, age and dominance rank in the male fallow deer, Dama dama. Anim Behav 79:1293–1300

  32. Kirkwood TBL (1977) Evolution of aging. Nature 270:301–304

  33. Kirkwood TBL, Holliday R (1979) Evolution of aging and longevity. Proc R Soc Lond B 205:531–546

  34. Kirkwood TBL, Rose MR (1991) Evolution of senescence—late survival sacrificed for reproduction. Philos Trans R Soc Lond B 332:15–24

  35. Knape J, Jonzen N, Skold M, Kikkawa J, McCallum H (2011) Individual heterogeneity and senescence in Silvereyes on Heron Island. Ecology 92:813–820

  36. Kodric-Brown A, Sibly RM, Brown JH (2006) The allometry of ornaments and weapons. Proc Natl Acad Sci USA 103:8733–8738

  37. Kruuk LEB, Clutton-Brock TH, Rose KE, Guinness FE (1999) Early determinants of lifetime reproductive success differ between the sexes in red deer. Proc R Soc Lond B 266:1655–1661

  38. Lebreton J-D, Burnham KP, Clobert J, Anderson DR (1992) Modeling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecol Monogr 62:67–118

  39. Lescroël A, Dugger KM, Ballard G, Ainley DG (2009) Effects of individual quality, reproductive success and environmental variability on survival of a long-lived seabird. J Anim Ecol 78:798–806

  40. Loehr J, Carey J, Hoefs M, Suhonen J, Ylonen H (2007) Horn growth rate and longevity: implications for natural and artificial selection in thinhorn sheep (Ovis dalli). J Evol Biol 20:818–828

  41. Lott DF (1991) Intraspecific variation in the social systems of wild vertebrates. Cambridge University Press, Cambridge

  42. Malo AF, Roldan ERS, Garde J, Soler AJ, Gomendio M (2005) Antlers honestly advertise sperm production and quality. Proc R Soc Lond B 272:149–157

  43. Maynard Smith J (1991) Theories of sexual selection. Tree 6:146–151

  44. Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260

  45. Michallet J, Grand B, Bonardi J (1988) La population de bouquetins des Alpes du massif de Belledonne-Sept Laux (département de l’Isère). Bull Mens ONC 125:19–24

  46. Miquelle DG (1990) Why don’t bull moose eat during the rut? Behav Ecol Sociobiol 27:145–151

  47. Mysterud A, Holand O, Roed KH, Gjostein H, Kumpula J, Nieminen M (2003) Effects of age, density and sex ratio on reproductive effort in male reindeer (Rangifer tarandus). J Zool 261:341–344

  48. Mysterud A, Heisingset E, Langvantn R, Yoccoz NG, Stenseth NC (2005) Climate-dependent allocation of resources to secondary sexual traits in red deer. Oikos 111:245–252

  49. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956

  50. Nussey DH, Kruuk LEB, Morris A, Clutton-Brock TH (2007) Environmental conditions in early life influence ageing rates in a wild population of red deer. Curr Biol 17:1000–1001

  51. Orell M, Belda EJ (2002) Delayed cost of reproduction and senescence in the willow tit Parus montanus. J Anim Ecol 71:55–64

  52. Pelletier F, Hogg JT, Festa-Bianchet M (2006) Male mating effort in a polygynous ungulate. Behav Ecol Sociobiol 60:645–654

  53. Pelletier F, Mainguy J, Côté SD (2009) Rut-induced hypophagia in male bighorn sheep and mountain goats: foraging under time budget constraints. Ethology 115:141–151

  54. Picard K, Thomas DW, Festa-Bianchet M, Lanthier C (1994) Bovid horns—an important site for heat-loss during winter. J Mamm 75:710–713

  55. Picard K, Festa-Bianchet M, Thomas D (1996) The cost of horniness: heat loss may counter sexual selection for large horns in temperate bovids. Ecoscience 3:280–284

  56. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New York

  57. Pradel R (1993) Flexibility in survival analysis from recapture data: handling trap-dependence. In: Lebreton J-D, North PM (eds) Marked individuals in the study of bird population. Birkhaüser, Basel, pp 29–37

  58. Preston BT, Stevenson IR, Pemberton JM, Coltman DW, Wilson K (2003) Overt and covert competition in a promiscuous mammal: the importance of weaponry and testes size to male reproductive success. Proc R Soc Lond B 270:633–640

  59. Reznick DR, Nunney L, Tessier A (2000) Big houses, big cars, superfleas and the costs of reproduction. Trends Evol Evol 15:421–425

  60. Robinson MR, Pilkington JG, Clutton-Brock TH, Pemberton JM, Kruuk LEB (2006) Live fast, die young: trade-offs between fitness components and sexually antagonistic selection on weaponry in Soay sheep. Evolution 60:2168–2181

  61. Singer FJ, Zeigenfuss LC (2002) Influence of trophy hunting and horn size on mating behavior and survivorship of mountain sheep. J Mamm 83:682–698

  62. Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

  63. Tavecchia G et al (2005) Predictors of reproductive cost in female Soay sheep. J Anim Ecol 74:201–213

  64. Toïgo C, Gaillard J-M (2003) Causes of sex-biased adult survival in ungulates: sexual size dimorphism, mating tactic or environmental harshness? Oikos 101:376–384

  65. Toïgo C, Gaillard J-M, Michallet J (1999) Cohort affects growth of males but not females in Alpine ibex (Capra ibex ibex). J Mamm 80:1021–1027

  66. Toïgo C, Gaillard J-M, 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 76:679–686

  67. Trivers RL (1972) Parental investment and sexual selection. Sexual selection and the descent of man. Aldline-Atherton, Chicago, pp 136–179

  68. van Noordwijk AJ, de Jong G (1986) Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 128:137–142

  69. Vanpé C et al (2007) Antler size provides an honest signal of male phenotypic quality in roe deer. Am Nat 169:481–493

  70. von Hardenberg A, Bassano B, del Pilar Zumel Arrance M, Bogliani G (2004) Horn growth but not asymmetry heralds the onset of senescence in male Alpine ibex (Capra ibex). J Zool 263:425–432

  71. von Hardenberg A, Bassano B, Festa-Bianchet M, Luikart G, Lanfranchi P, Coltman D (2007) Age-dependent genetic effects on a secondary sexual trait in male Alpine ibex, Capra ibex. Mol Ecol 16:1969–1980

  72. Williams GC (1966) Adaptation and natural selection. Princeton University Press, Princeton

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

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

  75. Willisch CS et al (2012) 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

  76. Wilson AJ, Nussey DH (2010) What is individual quality? An evolutionary perspective. Trends Evol Evol 25:207–214

  77. Yoccoz NG, Mysterud A, Langvatn R, Stenseth NC (2002) Age- and density-dependent reproductive effort in male red deer. Proc Nat Acad Sci USA 269:1523–1528

  78. Zahavi A (1975) Mate selection—a selection for handicap. J Theor Biol 53:205–214

  79. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

Download references


We are especially grateful to Jacques Michallet, who initiated the foundation of this ibex population and began the CMR monitoring. Many thanks are due to Daniel Blanc, Pascal Bégon, and all the national wardens who are strongly involved in ibex captures, as well as François Couilloud for his help in the ibex population monitoring. We also thank Marco Festa-Bianchet, Atle Mysterud and Marco Rughetti for insightful comments on previous drafts of this paper.

Author information

Correspondence to Carole Toïgo.

Additional information

Communicated by Gøran Ericsson.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Toïgo, C., Gaillard, J. & Loison, A. Alpine ibex males grow large horns at no survival cost for most of their lifetime. Oecologia 173, 1261–1269 (2013).

Download citation


  • Individual heterogeneity
  • Life-history tactic
  • Reproductive cost
  • Sexual selection
  • Trade-off