, Volume 164, Issue 2, pp 357–368 | Cite as

Getting the timing right: antler growth phenology and sexual selection in a wild red deer population

  • Michelle N. Clements
  • Tim H. Clutton-Brock
  • Steve D. Albon
  • Josephine M. Pemberton
  • Loeske E. B. Kruuk
Population ecology - Original Paper


There has been growing interest in the determinants of the annual timing of biological phenomena, or phenology, in wild populations, but research on vertebrate taxa has primarily focused on the phenology of reproduction. We present here analyses of the phenology of the annual growth of a secondary sexual characteristic, antlers in red deer (Cervus elaphus) males. The long-term individual-based data from a wild population of red deer on the Isle of Rum, Scotland allow us to consider ecological factors influencing variation in the phenology of growth of antlers, and the implications of variation in antler growth phenology with respect to the phenotype of antler grown (antler mass) and annual breeding success. The phenology of antler growth was influenced by local environmental conditions: higher population density delayed both the start date (during spring) and the relative end date (in late summer) of antler growth, and warmer temperatures in the September and April prior to growth advanced start and end dates, respectively. Furthermore, there was variation between individuals in this phenotypic plasticity of start date, although not in that of end date of growth. The phenology of antler growth impacted on the morphology of antlers grown, with individuals who started and ended growth earliest having the heaviest antlers. The timing of antler growth phenology was associated with breeding success in the following mating season, independently of the mass of antlers grown: an earlier start of antler growth was associated with siring a higher number of the calves born the following spring. Our results suggest that the phenology of traits that are not directly correlated with offspring survival may also regularly show correlations with fitness.


Phenology Sexual selection Mixed models Ungulate Phenotypic plasticity 


  1. Albon SD, Clutton-Brock TH, Langvatn R (1992) Cohort variation in reproduction and survival: implications for population demography. In: Brown RD (ed) The biology of deer. Springer, New York, pp 15–21Google Scholar
  2. Albon SD, Coulson TN, Brown D, Guinness FE, Pemberton JM, Clutton-Brock TH (2000) Temporal changes in key factors and key age groups influencing the population dynamics of female red deer. J Anim Ecol 69:1099–1110CrossRefGoogle Scholar
  3. Bartos L (1980) The date of antler casting, age and social hierarchy relationships in the red deer stag. Behav Process 5:293–301CrossRefGoogle Scholar
  4. Bartos L, Bahbouh R (2006) Antler size and fluctuating asymmetry in red deer (Cervus elaphus) stags and probability of becoming a harem holder in rut. Biol J Linn Soc 87:59–68CrossRefGoogle Scholar
  5. Bates D (2007) lme4: Linear mixed-effects models using S4 classes. R package version 0.99875-9Google Scholar
  6. Bety J, Gauthier G, Giroux JF (2003) Body condition, migration, and timing of reproduction in snow geese: a test of the condition-dependent model of optimal clutch size. Am Nat 162:110–121CrossRefPubMedGoogle Scholar
  7. Breslow N (2003) Whither PQL? UW biostatistics working paper series, University of WashingtonGoogle Scholar
  8. Breslow NE, Clayton DG (1993) Approximate inference in generalized linear mixed models. J Am Stat Assoc 88:9–25CrossRefGoogle Scholar
  9. Breslow N, Lin X (1995) Bias correction in generalised linear mixed models with a single component of dispersion. Biometrika 82:81–91CrossRefGoogle Scholar
  10. Bubenik GA, Schams D, White RJ, Rowell J, Blake J, Bartos L (1997) Seasonal levels of reproductive hormones and their relationship to the antler cycle of male and female reindeer (Rangifer tarandus). Comp Biochem Physiol B Biochem Mol Biol 116:269–277CrossRefPubMedGoogle Scholar
  11. Cargnelli LM, Neff BD (2006) Condition-dependent nesting in bluegill sunfish Lepomis macrochirus. J Anim Ecol 75:627–633. doi:10.1111/j.1365-2656.2006.01083.x CrossRefPubMedGoogle Scholar
  12. Charmantier A, McCleery RH, Cole LR, Perrins C, Kruuk LEB, Sheldon BC (2008) Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320:800–803. doi:10.1126/science.1157174 CrossRefPubMedGoogle Scholar
  13. Clutton-Brock TH (1982) The functions of antlers. Behaviour 79:108–124CrossRefGoogle Scholar
  14. Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: behaviour and ecology of two sexes. University of Chicago Press, ChicagoGoogle Scholar
  15. Cockburn A, Osmond HL, Double MC (2008) Swingin’ in the rain: condition dependence and sexual selection in a capricious world. Proc R Soc B Biol Sci 275:605–612. doi:10.1098/rspb.2007.0916 CrossRefGoogle Scholar
  16. 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 269:165–172. doi:10.1098/rspb.2001.1851 CrossRefGoogle Scholar
  17. Coulson T, Kruuk LEB, Tavecchia G, Pemberton JM, Clutton-Brock TH (2003) Estimating selection on neonatal traits in red deer using elasticity path analysis. Evolution 57:2879–2892PubMedGoogle Scholar
  18. Garcia-Cortes LA, Sorensen D (2001) Alternative implementations of Monte Carlo EM algorithms for likelihood inferences. Genet Sel Evol 33:443–452CrossRefPubMedGoogle Scholar
  19. Goss RJ (1968) Inhibition of growth and shedding of antlers by sex hormones. Nature 220:83–85CrossRefPubMedGoogle Scholar
  20. Goss R (1983) Deer antlers, regeneration, evolution and function. Academic Press, New YorkGoogle Scholar
  21. Green WCH, Rothstein A (1993) Persistent influences of birth date on dominance, growth and reproductive success in bison. J Zool 230:177–186CrossRefGoogle Scholar
  22. Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22Google Scholar
  23. 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. doi:10.1111/j.1365-294X.2007.03089.x CrossRefPubMedGoogle Scholar
  24. Kerkhoff AJ, Enquist BJ (2009) Multiplicative by nature: why logarithmic transformation is necessary in allometry. J Theor Biol 257:519–521. doi:10.1016/j.jtbi.2008.12.026 CrossRefGoogle Scholar
  25. Kruuk LEB, Slate J, Pemberton JM, Brotherstone S, Guinness F, Clutton-Brock T (2002) Antler size in red deer: heritability and selection but no evolution. Evolution 56:1683–1695PubMedGoogle Scholar
  26. Langvatn R, Albon SD, Burkey T, CluttonBrock TH (1996) Climate, plant phenology and variation in age of first reproduction in a temperate herbivore. J Anim Ecol 65:653–670CrossRefGoogle Scholar
  27. Li CY, Suttie JM, Clark DE (2004) Morphological observation of antler regeneration in red deer (Cervus elaphus). J Morphol 262:731–740. doi:10.1002/jmor.10273 CrossRefPubMedGoogle Scholar
  28. Lincoln GA (1992) Biology of antlers. J Zool 226:517–528CrossRefGoogle Scholar
  29. Mysterud A, Meisingset E, Langvatn R, Yoccoz NG, Stenseth NC (2005) Climate-dependent allocation of resources to secondary sexual traits in red deer. Oikos 111:245–252CrossRefGoogle Scholar
  30. Nussey DH, Wilson AJ, Brommer JE (2007) The evolutionary ecology of individual phenotypic plasticity in wild populations. J Evol Biol 20:831–844. doi:10.1111/j.1420-91001.2007.01300.x CrossRefPubMedGoogle Scholar
  31. 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 3:66–75CrossRefGoogle Scholar
  32. Perrins CM (1970) Timing of birds breeding seasons. Ibis 112:242CrossRefGoogle Scholar
  33. Pigliucci M (2001) Phenotypic plasticity. Johns Hopkins University Press, BaltimoreGoogle Scholar
  34. Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-Plus. Springer, New YorkCrossRefGoogle Scholar
  35. Post ES, Pedersen C, Wilmers CC, Forchhammer MC (2008) Phenological sequences reveal aggregate life history response to climatic warming. Ecology 89:363–370CrossRefPubMedGoogle Scholar
  36. Price T, Kirkpatrick M, Arnold SJ (1988) Directional selection and the evolution of breeding date in birds. Science 240:798–799CrossRefPubMedGoogle Scholar
  37. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  38. Rausher MD (1992) The measurement of selection on quantitative traits—biases due to environmental covariances between traits and fitness. Evolution 46:616–626CrossRefGoogle Scholar
  39. Schmidt KT, Stien A, Albon SD, Guinness FE (2001) Antler length of yearling red deer is determined by population density, weather and early life-history. Oecologia 127:191–197. doi:10.1007/s004420000583 CrossRefGoogle Scholar
  40. Sorensen D, Gianola D (2002) Likelihood, Bayseian and MCMC methods in quantitative genetics. Springer, New YorkGoogle Scholar
  41. Torbjorn von S, Grahn M, Goransson G (1994) Intersexual selection and reproductive success in the Pheasant Phasianus colchicus. Am Nat 144:510–527CrossRefGoogle Scholar
  42. Verhulst S, van Balen JH, Tinbergen JM (1995) Seasonal decline in reproductive success of the great tie—variation in time or quality? Ecology 76:2392–2403CrossRefGoogle Scholar
  43. Watson A (1971) Climate and the antler-shedding and performance of red deer in North-East Scotland. J Appl Ecol 8:53–67CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Michelle N. Clements
    • 1
    • 3
  • Tim H. Clutton-Brock
    • 2
  • Steve D. Albon
    • 3
  • Josephine M. Pemberton
    • 1
  • Loeske E. B. Kruuk
    • 1
  1. 1.Institute of Evolutionary BiologyUniversity of EdinburghEdinburghUK
  2. 2.Department of ZoologyUniversity of CambridgeCambridgeUK
  3. 3.Macaulay Land Use Research InstituteAberdeenUK

Personalised recommendations