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Genetica

, Volume 135, Issue 1, pp 7–11 | Cite as

Variation in the peacock’s train shows a genetic component

  • Marion Petrie
  • Peter Cotgreave
  • Thomas W. Pike
Article

Abstract

Female peafowl (Pavo cristatus) show a strong mating preference for males with elaborate trains. This, however, poses something of a paradox because intense directional selection should erode genetic variation in the males’ trains, so that females will no longer benefit by discriminating among males on the basis of these traits. This situation is known as the ‘lek paradox’, and leads to the theoretical expectation of low heritability in the peacock’s train. We used two independent breeding experiments, involving a total of 42 sires and 86 of their male offspring, to estimate the narrow sense heritabilities of male ornaments and other morphometric traits. Contrary to expectation, we found significant levels of heritability in a trait known to be used by females during mate choice (train length), while no significant heritabilities were evident for other, non-fitness related morphological traits (tarsus length, body weight or spur length). This study adds to the building body of evidence that high levels of additive genetic variance can exist in secondary sexual traits under directional selection, but further emphasizes the main problem of what maintains this variation.

Keywords

Lek paradox Fitness-related traits Narrow sense heritability Additive genetic variation 

Notes

Acknowledgements

We are grateful to Anders Møller, Doug Maisie, James Futter, John Howe and Ellen Vale for help in measuring the peacocks, Michael Jennions and two anonymous referees for comments on earlier drafts of the manuscript, Loeske Kruuk for discussion on the statistical analyses and Quinton Spratt for allowing us to work at his farm. This work was funded by the Natural Environment Research Council (NERC) and the Association for the Study of Animal Behaviour (ASAB).

References

  1. Amos W, Balmford A (2001) When does conservation genetics matter? Heredity 87:257–265PubMedCrossRefGoogle Scholar
  2. Andersson MB (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  3. Bakker TCM (1993) Positive genetic correlation between female preference and preferred male ornament in sticklebacks. Nature 363:255–257CrossRefGoogle Scholar
  4. Birkhead TR, Petrie M (1995) Ejaculate features and sperm utilisation in the peafowl Pavo cristatus. Proc R Soc Lond B 261:153–158CrossRefGoogle Scholar
  5. Birkhead TR, Pellatt EJ, Matthews IM, Roddis NJ, Hunter FM, McPhie F, Castillo-Juarez H (2006) Genic capture and the genetic basis of sexually selected traits in the zebra finch. Evolution 60:2389–2398PubMedGoogle Scholar
  6. Borgia G (1979) Sexual selection and the evolution of mating systems. In: Blum MS, Blum NA (eds) Sexual selection and reproductive competition in insects. Academic Press, NY, pp 19–80Google Scholar
  7. Bulmer MG (1980) The mathematical theory of quantitative genetics. Clarenon Press, Oxford, UKGoogle Scholar
  8. Cotton S, Fowler K, Pomiankowski A (2004) Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap principle? Proc R Soc Lond B 271:771–783CrossRefGoogle Scholar
  9. Cunningham EJ, Russell AF (2000) Egg investment is influenced by male attractiveness in the mallard. Nature 404:74–77PubMedCrossRefGoogle Scholar
  10. David P, Bjorksten P, Fowler K, Pomiankowski A (2000) Condition-dependent signalling of genetic variation in stalk-eyed flies. Nature 406:186–188PubMedCrossRefGoogle Scholar
  11. Falconer DS (1981) Introduction to quantitative genetics. Longmans, London, UKGoogle Scholar
  12. Felsenstein J (1976) The theoretical population genetics of variable selection and migration. Ann Rev Genet 10:253–280PubMedCrossRefGoogle Scholar
  13. Fisher RA (1930) The genetical theory of natural selection. Clarendon Press, Oxford, UKGoogle Scholar
  14. Garant D, Sheldon BC, Gustafsson L (2004) Climatic and temporal effects on the expression of secondary sexual characters: genetic and environmental components. Evolution 58:634–644PubMedGoogle Scholar
  15. Gil D, Graves J, Hazon N, Wells A (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286:126–128PubMedCrossRefGoogle Scholar
  16. Gilmour AR, Gogel BJ, Cullis BR, Welham SJ, Thompson R (2002) ASReml user guide release 1.0. VSN International Ltd., Hemel Hempstead, UKGoogle Scholar
  17. Gustafsson L (1986) Lifetime reproductive success and heritability––empirical support for Fisher’s fundamental theorem. Am Nat 128:761–764CrossRefGoogle Scholar
  18. Hamilton W, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387PubMedCrossRefGoogle Scholar
  19. Hine E, Chenoweth SF, Blows MW (2004) Multivariate quantitative genetics and the lek paradox: genetic variance in male sexually selected traits of Drosophila serrata. Evolution 58:2754–2762PubMedGoogle Scholar
  20. Jia FY, Greenfield MD, Collins RD (2000) Genetic variance of sexually selected traits in waxmoths: maintenance by genotype × environment interaction. Evolution 54:953–967PubMedGoogle Scholar
  21. Johnsen A, Delhey K, Andersson S, Kempenaers B (2003) Plumage colour in nestling blue tits: sexual dichromatism, condition dependence and genetic effects. Proc R Soc Lond B 270:1263–1270CrossRefGoogle Scholar
  22. Johnson K, Thronhill R, Ligon JD, Zuk M (1993) The direction of mothers and daughters preferences and the heritability of male ornaments in red jungle fowl (Gallus gallus). Behav Ecol 4:254–259CrossRefGoogle Scholar
  23. Johnstone RA (1995) Sexual selection, honest advertisement and the handicap principle: reviewing the evidence. Biol Rev 70:1–65PubMedCrossRefGoogle Scholar
  24. Kirkpatrick M, Ryan MJ (1991) The evolution of mating preferences and the paradox of the lek. Nature 350:33–38CrossRefGoogle Scholar
  25. Kotiaho JS, Simmons LW, Tomkins JL (2001) Towards a resolution of the lek paradox. Nature 410:684–686PubMedCrossRefGoogle Scholar
  26. Knott SA, Sibly RM, Smith RH, Moller H (1995) Maximum-likelihood estimation of genetic parameters in life-history studies using the animal model. Funct Ecol 9:122–126CrossRefGoogle Scholar
  27. Kruuk LEB (2004) Estimating genetic parameters in wild populations using the ‘animal model’. Phil Trans R Soc Lond B 359:873–890CrossRefGoogle Scholar
  28. Kruuk LEB, Clutton-Brock TH, Slate J, Pemberton JM, Brotherstone S, Guinness FE (2000) Heritability of fitness in a wild mammal population. Proc Natl Acad Sci USA 97:698–703PubMedCrossRefGoogle Scholar
  29. 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
  30. Lanctot RB, Scribner KT, Kempenaers B, Weatherhead PJ (1997) Lekking without a paradox in the buff-breasted sandpiper. Am Nat 149:1051–1070PubMedCrossRefGoogle Scholar
  31. Lande R (1982) A quantitative genetic theory of life history evolution. Ecology 63:607–615CrossRefGoogle Scholar
  32. Loyau A, Saint Jalme M, Cagniant C, Sorci G (2005) Multiple sexual advertisements honestly reflect health status in peacocks (Pavo cristatus). Behav Ecol Sociobiol 58:552–557CrossRefGoogle Scholar
  33. Lynch M, Walsh B (1998) Genetic analysis of quantitative traits. Sinauer, Sunderland, MAGoogle Scholar
  34. Maynard Smith J (1978) The evolution of sex. Cambridge University Press, Cambridge, UKGoogle Scholar
  35. Maynard Smith J (1985) Sexual selection, handicaps and true fitness. J Theor Biol 115:1–8CrossRefGoogle Scholar
  36. Miller CW, Moore AJ (2007) A potential resolution to the lek paradox through indirect genetic effects. Proc R Soc Lond B 274:1279–1286CrossRefGoogle Scholar
  37. Moore AJ, Moore PJ (1999) Balancing sexual selection through opposing mate choice and male competition. Proc R Soc Lond B 266:711–716CrossRefGoogle Scholar
  38. Mousseau TA, Roff DA (1987) Natural selection and the heritability of fitness components. Heredity 59:181–197PubMedCrossRefGoogle Scholar
  39. Petrie M (1992) Peacocks with low mating success are more likely to suffer predation. Anim Behav 44:585–586CrossRefGoogle Scholar
  40. Petrie M (1994) Improved growth and survival of offspring of peacocks with more elaborate trains. Nature 371:598–599CrossRefGoogle Scholar
  41. Petrie M, Halliday T (1994) Experimental and natural changes in the peacocks (Pavo cristatus) train can affect mating success. Behav Ecol Sociobiol 35:213–217CrossRefGoogle Scholar
  42. Petrie M, Halliday T, Sanders C (1991) Peahens prefer peacocks with elaborate trains. Anim Behav 41:323–331CrossRefGoogle Scholar
  43. Petrie M, Roberts G (2006) Sexual selection and the evolution of evolvability. Heredity 98:198–205PubMedCrossRefGoogle Scholar
  44. Pomiankowski A, Møller AP (1995) A resolution to the lek paradox. Proc R Soc Lond B 260:21–29CrossRefGoogle Scholar
  45. Quinn JL, Charmantier A, Garant D, Sheldon BC (2006) Data depth, data completeness, and their influence on quantitative genetic estimation of two contrasting bird populations. J Evol Biol 19:994–1002PubMedCrossRefGoogle Scholar
  46. Qvarnström A (1999) Genotype-by-environment interactions in the determination of the size of a secondary sexual character in the collared flycatcher Ficedula albicollis. Evolution 53:1564–1572CrossRefGoogle Scholar
  47. Randerson JP, Jiggins FM, Hurst LD (2000) Male killing can select for male mate choice: a novel solution to the paradox of the lek. Proc R Soc Lond B 267:867–874CrossRefGoogle Scholar
  48. Reynolds JD, Gross MR (1990) Costs and benefits of female mate choice: is there a lek paradox? Am Nat 136:230–243CrossRefGoogle Scholar
  49. Roff DA, Mousseau TA (1987) Quantitative genetics and fitness––lessons from Drosophila. Heredity 58:103–118PubMedCrossRefGoogle Scholar
  50. Rowe L, Houle D (1996) The lek paradox and the capture of genetic variance by condition dependent traits. Proc R Soc Lond B 263:1415–1421CrossRefGoogle Scholar
  51. Simons AM, Roff DA (1994) The effect of environmental variability on the heritabilities of traits of a field cricket. Evolution 48:1637–1649CrossRefGoogle Scholar
  52. Taylor PD, Williams GC (1982) The lek paradox is not resolved. Theor Popul Biol 22:392–409CrossRefGoogle Scholar
  53. Tomkins JL, Radwan J, Kotiaho JS, Tregenza T (2004) Genic capture and resolving the lek paradox. Trends Ecol Evol 19:323–328PubMedCrossRefGoogle Scholar
  54. Weigensberg I, Roff DA (1996) Natural heritabilities: can they be reliably estimated in the laboratory? Evolution 50:2149–2157CrossRefGoogle Scholar
  55. Westneat D, Birkhead T (1998) Alternative hypotheses linking the immune system and mate choice for good genes. Proc R Soc Lond B 265:1065–1073CrossRefGoogle Scholar
  56. Whitlock MC, Fowler K (1999) The changes in genetic and environmental variance with inbreeding in Drosophila melanogaster. Genetics 152:345–353PubMedGoogle Scholar
  57. Wilson AJ, Coltman DW, Pemberton JM, Overall ADJ, Byrne KA, Kruuk LEB (2005) Maternal genetic effects set the potential for evolution in a free-living vertebrate population. J Evol Biol 18:405–414PubMedCrossRefGoogle Scholar
  58. Wilson AJ, Pemberton JM, Pilkington JG, Coltman DW, Mifsud DV, Clutton-Brock T, Kruuk LEB (2006) Environmental coupling of selection and heritability limits evolution. PLoS Biol 4:1270–1275CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Marion Petrie
    • 1
  • Peter Cotgreave
    • 2
    • 4
  • Thomas W. Pike
    • 3
    • 5
  1. 1.Evolutionary Biology Research Group, School of Clinical Medical SciencesUniversity of NewcastleNewcastle-upon-TyneUK
  2. 2.Department of ZoologyUniversity of OxfordOxfordUK
  3. 3.School of BiologyUniversity of NewcastleNewcastle-upon-TyneUK
  4. 4.Campaign for Science & EngineeringLondonUK
  5. 5.Division of Environmental and Evolutionary Ecology, Graham Kerr BuildingUniversity of GlasgowGlasgowUK

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