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Carotenoid-derived ornaments reflect parental quality in male and female yellow-eyed penguins (Megadyptes antipodes)

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Abstract

The handicap principle suggests that ornamental traits that function as honest signals in mate selection must be costly to be effective. We evaluated in the sexually monochromatic yellow-eyed penguin (Megadyptes antipodes) whether the carotenoid-derived plumage and eye coloration predicts parental quality and whether males and females within pairs mate assortatively in relation to these carotenoid-derived ornaments. In addition, we investigated whether age or body condition was related to the coloration of the ornamental traits. In yellow-eyed penguins, parental quality of males and females was predicted by eye and head plumage coloration. Even when we controlled for gender- and age-specific differences, eye and head plumage coloration reflected honestly parental quality. Males and females mated assortatively in relation to these ornamental traits. While age influenced coloration of both the eye and head plumage, body condition was related only to the saturation of plumage coloration. These results provide evidence that the carotenoid-derived ornaments in yellow-eyed penguins reflect the parental abilities of birds and, therefore, may be costly signals. Potentially, female and male yellow-eyed penguins could use eye and plumage coloration as an indirect cue in assessing age and quality of individual birds during mate choice. This is only the second study to examine plumage coloration in relation to sexual selection in penguins, while conspicuous ornamental traits in other species of penguin beg the question whether they also play a role in sexual selection.

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References

  • Adobe Systems (1994) Adobe Photoshop 3.0 user guide. Adobe, Mountain View, Calif.

  • Ainley DG, Emison WB (1972) Sexual size dimorphism in Adélie penguins. Ibis 114:267–271

    Google Scholar 

  • Alatalo RV, Höglund J, Lundberg A (1988) Patterns of variation in tail ornament size in birds. Biol J Linn Soc 34:363–374

    Google Scholar 

  • Amundsen T (2000) Why are female birds ornamented? Trends Ecol Evol 15:149–155

    PubMed  Google Scholar 

  • Amundsen T, Forsgren E, Hansen LTT (1997) On the function of female ornaments: male bluethroats prefer colourful females. Proc R Soc Lond B 264:1579–1586

    Article  Google Scholar 

  • Balmford A, Read AF (1991) Testing alternative models of sexual selection through female choice. Trends Ecol Evol 6:274–276

    Google Scholar 

  • Bendich A (1989) Carotenoids and the immune response. J Nutr 119:112–115

    CAS  PubMed  Google Scholar 

  • Bendich A (1993) Biological functions of dietary carotenoids. Ann NY Acad Sci 691:61–67

    CAS  PubMed  Google Scholar 

  • Bortolotti GR, Iko W (1992) Non-random pairing in American kestrels: mate choice versus intra-sexual competition. Anim Behav 44:811–821

    Google Scholar 

  • Bortolotti GR, Negro JJ, Tella JL, Marchant TA, Bird DM (1996) Sexual dichromatism in birds independent of diet, parasites and androgens. Proc R Soc Lond B 263:1171–1176

    CAS  Google Scholar 

  • Bortolotti GR, Tella JL, Forero MG, Dawson RD, Negro JJ (2000) Genetics, local environment and health as factors influencing plasma carotenoids in wild American kestrels (Falco sparverius). Proc R Soc Lond B 267:1433–1438

    Article  CAS  PubMed  Google Scholar 

  • Brush AH (1981) Carotenoids in wild and captive birds. In: Bauernfeind JC (ed) Carotenoids as colorants and vitamin A precursors. Academic Press, New York, pp 539–562

  • Brush AH (1990) Metabolism of carotenoid pigments in birds. J Fed Am Soc Exp Biol 4:2969–2977

    CAS  Google Scholar 

  • Camplani A, Saino N, Møller AP (1999) Carotenoids, sexual signals and immune function in barn swallows from Chernobyl. Proc R Soc Lond B 266:1111–1116

    Article  CAS  PubMed  Google Scholar 

  • Coulson JC, Duncan N, Thomas CS, Monaghan P (1981) An age-related difference in the bill depth of herring gulls Larus argentatus. Ibis 123:499–503

    Google Scholar 

  • Cronin H (1991) The ant and the peacock. Cambridge University Press, Cambridge

  • Cuervo JJ, de Lope F, Møller AP (1996) The function of long tails in female barn swallows (Hirundo rustica): an experimental study. Behav Ecol 7:132–136

    Google Scholar 

  • Darby JT, Seddon PJ (1990) Breeding biology of yellow-eyed penguins (Megadyptes antipodes). In: Davis LS, Darby JT (eds) Penguin biology. Academic Press, San Diego, Calif., pp 45–62

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

  • Davis LS (1991) Mate choice and sexual dimorphism in penguins. Proc Int Ornithol Congr 20:1352–1360

    Google Scholar 

  • Davis LS, Speirs EAH (1990) Mate choice in penguins. In: Davis LS, Darby JT (eds) Penguin biology. Academic Press, San Diego, Calif., pp 377–397

  • Fisher RA (1930) The genetical theory of natural selection. Clarendon Press, Oxford

  • Fitze PS, Richner H (2002) Differential effects of a parasite on ornamental structures based on melanins and carotenoids. Behav Ecol 13:401–407

    Article  Google Scholar 

  • Forero MG, Tella JL, Donázar JA, Blanco G, Bertellotti M, Ceballos O (2001) Phenotypic assortative mating and within-pair sexual dimorphism and its influence on breeding success and offspring quality in Magellanic penguins. Can J Zool 79:1414–1422

    Article  Google Scholar 

  • Fox DL (1979) Biochromy: natural coloration of living things. University of California Press, Berkeley, Calif.

  • Grafen A (1990) Biological signals as handicaps. J Theor Biol 144:517–546

    CAS  PubMed  Google Scholar 

  • Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites. Science 218:384–387

    CAS  PubMed  Google Scholar 

  • Hill GE (1990) Female house finches prefer colourful males: sexual selection for a condition-dependent trait. Anim Behav 40:563–572

    Google Scholar 

  • Hill GE (1991) Plumage coloration is a sexually selected indicator of male quality. Nature 350:337–339

    Article  Google Scholar 

  • Hill GE (1993) Male mate choice and the evolution of female plumage coloration in the house finch. Evolution 47:1515–1525

    Google Scholar 

  • Hill GE (1999) Is there an immunological cost of carotenoid-based ornamental coloration? Am Nat 154:589–595

    Article  PubMed  Google Scholar 

  • Hill GE, Brawner WR III (1998) Melanin-based plumage coloration in the house finch is unaffected by coccidial infection. Proc R Soc Lond B 265:1105–1109

    Article  Google Scholar 

  • Hoelzer GA (1989) The good parent process of sexual selection. Anim Behav 38:1067–1078

    Google Scholar 

  • Iwasa Y, Pomiankowski A, Nee S (1991) The evolution of costly mate preference II. The 'handicap principle'. Evolution 45:1431–1442

    Google Scholar 

  • Johnstone RA, Reynolds JD, Deutsch JC (1996) Mutual mate choice and sex differences in choosiness. Evolution 50:1382–1391

    Google Scholar 

  • Jones IL, Hunter FM (1993) Mutual sexual selection in a monogamous seabird. Nature 362:238–239

    Article  Google Scholar 

  • Jones IL, Hunter FM (1999) Experimental evidence for mutual inter- and intrasexual selection favouring a crested auklet ornament. Anim Behav 57:521–528

    PubMed  Google Scholar 

  • Jouventin P (1982) Visual and vocal signals in penguins, their evolution and adaptive characters. Adv Ethol 24:1–149

    Google Scholar 

  • Jouventin P, Lequette B, Dobson S (1999) Age-related mate choice in the wandering albatross. Anim Behav 57:1099–1106

    Google Scholar 

  • Kirkpatrick M, Ryan MJ (1991) The evolution of mating preferences and the paradox of the lek. Nature 350:33–38

    Article  Google Scholar 

  • Kodric-Brown A, Brown JH (1984) Truth in advertising: the kinds of traits favoured by sexual selection. Am Nat 124:309–323

    Article  Google Scholar 

  • Lande R (1980) Sexual dimorphism, sexual selection, and adaptation in polygenic characters. Evolution 34:292–305

    Google Scholar 

  • Lande R (1981) Models of speciation by sexual selection on polygenic traits. Proc Nat Acad Sci USA 78:3721–3725

    Google Scholar 

  • Ligon JD (1999) The evolution of avian breeding systems. Oxford University Press, Oxford

  • Lozano GA (1994) Carotenoids, parasites and sexual selection. Oikos 70:309–311

    Google Scholar 

  • Massaro M, Darby JT, Davis LS, Edge K-A, Hazel MJ (2002) Investigation of interacting effects of female age, laying dates and egg size in Yellow-eyed Penguins (Megadyptes antipodes). Auk 119:1137–1141

    Google Scholar 

  • Møller AP (1993) Sexual selection in the barn swallow Hirunda rustica III. Female tail ornaments. Evolution 47:417–431

    Google Scholar 

  • Negro JJ, Bortolotti GR, Tella JL, Fernie KJ, Bird DM (1998) Regulation of integumentary colour and plasma carotenoids in American Kestrels consistent with sexual selection theory. Funct Ecol 12:307–312

    Article  Google Scholar 

  • Olsen VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514

    Article  Google Scholar 

  • Owens IPF, Short RV (1995) Hormonal basis of sexual dimorphism in birds: implications for new theories of sexual selection. Trends Ecol Evol 10:44–47

    Article  Google Scholar 

  • Pomiankowski A, Iwasa Y, Nee S (1991) The evolution of costly mate preferences I. Fisher and biased mutation. Evolution 45:1422–1430

    Google Scholar 

  • Reid WV (1988) Age correlations within pairs of breeding birds. Auk 105:278–285

    Google Scholar 

  • Richdale LE (1957) A population study of penguins. Clarendon Press, Oxford

  • Rock CL, Jacob RA, Bowen PE (1996) Update on the biological characteristics of the antioxidant micronutrients: vitamin C, vitamin E, and the carotenoids. J Am Diet Assoc 96:693–702

    Article  CAS  PubMed  Google Scholar 

  • Roulin A (1999) Nonrandom pairing by male barn owls (Tyto alba) with respect to a female plumage trait. Behav Ecol 10:688–695

    Article  Google Scholar 

  • Saetre GP, Fossnes T, Slagsvold T (1995) Food provisioning in the pied flycatcher: do females gain direct benefits from choosing bright-colored males? J Anim Ecol 64:21–30

    Google Scholar 

  • Schantz T von, Bensch S, Grahn M, Hasselquist D, Wittzell H (1999) Good genes, oxidative stress and condition-dependent sexual signals. Proc R Soc Lond B 266:1–12

    PubMed  Google Scholar 

  • SPSS (2000) SPSS 10.0 for Macintosh, version 10.0.7a. SSPS, Chicago, Ill.

  • Tella JL, Forero MG, Donázar JA, Hiraldo F (1997) Is the expression of male traits in female lesser kestrels related to sexual selection? Ethology 103:72–81

    Google Scholar 

  • Warham J (1975) The crested penguins. In: Stonehouse B (ed) The biology of penguins. Macmillan, London, pp. 189–269

  • Weimerskirch H (1990) The influence of age and experience on breeding performance of the Antarctic Fulmar, Fulmarus glacialoides. J Anim Ecol 59:867–875

    Google Scholar 

  • Wiebe KL (2000) Assortative mating by color in a population of hybrid northern flickers. Auk 117:525–529

    Google Scholar 

  • Wolfenbarger LL (1999) Red coloration of male northern cardinals correlates with mate quality and territory quality. Behav Ecol 10:80–90

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Zahavi A, Zahavi A (1997) The handicap principle: a missing piece of Darwin's puzzle. Oxford University Press, Oxford

    Google Scholar 

  • Zuk M, Thornhill R, Ligon JD, Johnson K, Austad S, Ligon SH, Wilmsen Thornhill N, Costin C (1990) The role of male ornaments and courtship behavior in female mate choice of red jungle fowl. Am Nat 136:459–473

    Article  Google Scholar 

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Acknowledgements

We thank Alvin Setiawan, Mike Hazel, Sylviane Neumann, Danilo Hegg, Brad Robson and all the volunteers that helped during these years of data collection on yellow-eyed penguins breeding at Boulder Beach. We are grateful to Ken Miller for assistance with photography and graphics. We thank the Yellow-eyed Penguin Trust for financial, logistical and moral support. We are grateful to Ian Jamieson and two anonymous reviewers for making helpful comments to improve this manuscript. Flipper banding of penguins and all collecting of data, which were used in this manuscript, has been approved by the Department of Conservation and the University of Otago Animal Ethics Committee and comply with the current laws of New Zealand. In particular, we thank Dean Nelson, Bruce McKinlay and Dave Houston from the Department of Conservation for support and permits. The study was supported by grants from the Yellow-eyed Penguin Trust, the Department of Conservation, a University of Otago Postgraduate Scholarship to M.M. and an Otago Research Grant to L.S.D.

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Correspondence to Melanie Massaro.

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Communicated by C.R. Brown

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Massaro, M., Davis, L.S. & Darby, J.T. Carotenoid-derived ornaments reflect parental quality in male and female yellow-eyed penguins (Megadyptes antipodes). Behav Ecol Sociobiol 55, 169–175 (2003). https://doi.org/10.1007/s00265-003-0683-3

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