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.
Similar content being viewed by others
References
Amos W, Balmford A (2001) When does conservation genetics matter? Heredity 87:257–265
Andersson MB (1994) Sexual selection. Princeton University Press, Princeton
Bakker TCM (1993) Positive genetic correlation between female preference and preferred male ornament in sticklebacks. Nature 363:255–257
Birkhead TR, Petrie M (1995) Ejaculate features and sperm utilisation in the peafowl Pavo cristatus. Proc R Soc Lond B 261:153–158
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 60:2389–2398
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 19–80
Bulmer MG (1980) The mathematical theory of quantitative genetics. Clarenon Press, Oxford, UK
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 271:771–783
Cunningham EJ, Russell AF (2000) Egg investment is influenced by male attractiveness in the mallard. Nature 404:74–77
David P, Bjorksten P, Fowler K, Pomiankowski A (2000) Condition-dependent signalling of genetic variation in stalk-eyed flies. Nature 406:186–188
Falconer DS (1981) Introduction to quantitative genetics. Longmans, London, UK
Felsenstein J (1976) The theoretical population genetics of variable selection and migration. Ann Rev Genet 10:253–280
Fisher RA (1930) The genetical theory of natural selection. Clarendon Press, Oxford, UK
Garant D, Sheldon BC, Gustafsson L (2004) Climatic and temporal effects on the expression of secondary sexual characters: genetic and environmental components. Evolution 58:634–644
Gil D, Graves J, Hazon N, Wells A (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286:126–128
Gilmour AR, Gogel BJ, Cullis BR, Welham SJ, Thompson R (2002) ASReml user guide release 1.0. VSN International Ltd., Hemel Hempstead, UK
Gustafsson L (1986) Lifetime reproductive success and heritability––empirical support for Fisher’s fundamental theorem. Am Nat 128:761–764
Hamilton W, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387
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 58:2754–2762
Jia FY, Greenfield MD, Collins RD (2000) Genetic variance of sexually selected traits in waxmoths: maintenance by genotype × environment interaction. Evolution 54:953–967
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 270:1263–1270
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 4:254–259
Johnstone RA (1995) Sexual selection, honest advertisement and the handicap principle: reviewing the evidence. Biol Rev 70:1–65
Kirkpatrick M, Ryan MJ (1991) The evolution of mating preferences and the paradox of the lek. Nature 350:33–38
Kotiaho JS, Simmons LW, Tomkins JL (2001) Towards a resolution of the lek paradox. Nature 410:684–686
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 9:122–126
Kruuk LEB (2004) Estimating genetic parameters in wild populations using the ‘animal model’. Phil Trans R Soc Lond B 359:873–890
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 97:698–703
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 56:1683–1695
Lanctot RB, Scribner KT, Kempenaers B, Weatherhead PJ (1997) Lekking without a paradox in the buff-breasted sandpiper. Am Nat 149:1051–1070
Lande R (1982) A quantitative genetic theory of life history evolution. Ecology 63:607–615
Loyau A, Saint Jalme M, Cagniant C, Sorci G (2005) Multiple sexual advertisements honestly reflect health status in peacocks (Pavo cristatus). Behav Ecol Sociobiol 58:552–557
Lynch M, Walsh B (1998) Genetic analysis of quantitative traits. Sinauer, Sunderland, MA
Maynard Smith J (1978) The evolution of sex. Cambridge University Press, Cambridge, UK
Maynard Smith J (1985) Sexual selection, handicaps and true fitness. J Theor Biol 115:1–8
Miller CW, Moore AJ (2007) A potential resolution to the lek paradox through indirect genetic effects. Proc R Soc Lond B 274:1279–1286
Moore AJ, Moore PJ (1999) Balancing sexual selection through opposing mate choice and male competition. Proc R Soc Lond B 266:711–716
Mousseau TA, Roff DA (1987) Natural selection and the heritability of fitness components. Heredity 59:181–197
Petrie M (1992) Peacocks with low mating success are more likely to suffer predation. Anim Behav 44:585–586
Petrie M (1994) Improved growth and survival of offspring of peacocks with more elaborate trains. Nature 371:598–599
Petrie M, Halliday T (1994) Experimental and natural changes in the peacocks (Pavo cristatus) train can affect mating success. Behav Ecol Sociobiol 35:213–217
Petrie M, Halliday T, Sanders C (1991) Peahens prefer peacocks with elaborate trains. Anim Behav 41:323–331
Petrie M, Roberts G (2006) Sexual selection and the evolution of evolvability. Heredity 98:198–205
Pomiankowski A, Møller AP (1995) A resolution to the lek paradox. Proc R Soc Lond B 260:21–29
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 19:994–1002
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 53:1564–1572
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 267:867–874
Reynolds JD, Gross MR (1990) Costs and benefits of female mate choice: is there a lek paradox? Am Nat 136:230–243
Roff DA, Mousseau TA (1987) Quantitative genetics and fitness––lessons from Drosophila. Heredity 58:103–118
Rowe L, Houle D (1996) The lek paradox and the capture of genetic variance by condition dependent traits. Proc R Soc Lond B 263:1415–1421
Simons AM, Roff DA (1994) The effect of environmental variability on the heritabilities of traits of a field cricket. Evolution 48:1637–1649
Taylor PD, Williams GC (1982) The lek paradox is not resolved. Theor Popul Biol 22:392–409
Tomkins JL, Radwan J, Kotiaho JS, Tregenza T (2004) Genic capture and resolving the lek paradox. Trends Ecol Evol 19:323–328
Weigensberg I, Roff DA (1996) Natural heritabilities: can they be reliably estimated in the laboratory? Evolution 50:2149–2157
Westneat D, Birkhead T (1998) Alternative hypotheses linking the immune system and mate choice for good genes. Proc R Soc Lond B 265:1065–1073
Whitlock MC, Fowler K (1999) The changes in genetic and environmental variance with inbreeding in Drosophila melanogaster. Genetics 152:345–353
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 18:405–414
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 4:1270–1275
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).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Petrie, M., Cotgreave, P. & Pike, T.W. Variation in the peacock’s train shows a genetic component. Genetica 135, 7–11 (2009). https://doi.org/10.1007/s10709-007-9211-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10709-007-9211-0