Behavioral Ecology and Sociobiology

, Volume 58, Issue 2, pp 175–180 | Cite as

Male coloration and chick condition in blue-footed booby: a cross-fostering experiment

Original Article

Abstract

Sexual selection models suggest that female choice is based on male traits that indicate their genetic or environmental condition, consequently enhancing her reproductive success by direct or indirect benefits. We investigated the relationship between male foot colour and offspring condition in the blue-footed booby, a socially monogamous seabird, with conspicuous and variably condition-dependent coloured feet that are selected by females. In a cross-fostering experiment, we found that chick condition was related to the foot colour of the foster father and, to some extent, to the foot colour of the genetic father; thus overall, the father’s sexual ornamentation (genetic and foster) explained 32% of variance of chick condition. These data suggest that foot colour, a dynamic sexually selected trait, is mostly a signal of parental contribution. In species in which males provide parental care, females may choose mates with higher parental ability. Overall, our data suggest that colourful integuments are honest signals of parental ability.

Keywords

Dynamic trait Condition-dependence Skin colour Sexual selection Sula nebouxii 

References

  1. Anderson D, Ricklefs RE (1992) Brood size and provisioning in masked and blue-footed boobies (Sula spp). Ecology 73:1363–1374Google Scholar
  2. Andersson M (1994) Sexual selection. Princeton University Press, New JerseyGoogle Scholar
  3. Andersson S (1999) Morphology of UV reflectance in a whistling-thrush: implications for the study of structural colour signalling in birds. J Avian Biol 30:193–204Google Scholar
  4. Apanius V (1998) The immune system. In: Starck JM, Ricklefs RE (eds) Avian growth and development: evolution within the altricial-precocial spectrum. Oxford University Press, Oxford, pp 130–145Google Scholar
  5. Bennett ATD, Cuthill I, Patridge J, Maier EJ (1996) Ultraviolet vision and mate choice in zebra finches. Nature 380:433–435CrossRefGoogle Scholar
  6. Burley N (1986) Sexual selection for aesthetic traits in species with biparental care. Am Nat 127:415–445CrossRefGoogle Scholar
  7. Chase ID (1980) Cooperative and noncooperative behaviour in animals. Am Nat 115:827–857CrossRefGoogle Scholar
  8. Christe P, Moller AP, Saino N, Lope F de (2000) Genetic and environmental components of phenotypic variation in immune response and body size of a colonial bird, Delichon urbica (the house martin). Heredity 85:75–83CrossRefPubMedGoogle Scholar
  9. Cunningham EJA, Russell A (2000) Egg investment is influenced by male attractiveness in the mallard. Nature 404:74–77CrossRefPubMedGoogle Scholar
  10. Drummond H, García Chavelas C (1989) Food shortage influences sibling aggression in the blue-footed booby. Anim Behav 37:806–819Google Scholar
  11. Drummond H, Torres R, Krishnan VV (2003) Buffered development: resiliance after aggressive subordination in infancy. Am Nat 161:794–807Google Scholar
  12. Faivre B, Grégoire A, Préault M, Cézilly F, Sorci G (2003) Immune activation rapidly mirrored in a secondary sexual trait. Science 300:103Google Scholar
  13. Gil D, Graves J, Hazon N, Wells A (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286:126–128CrossRefPubMedGoogle Scholar
  14. Grafen A (1990) Sexual selection unhandicapped by the Fisher process. J Theor Biol 144:473–516Google Scholar
  15. Grant BR, Grant PR (1987) Mate choice in Darwin’s finches. Biol J Linn Soc 32:247–270Google Scholar
  16. Griffith SC, Owens IPF, Burke T (1999) Environmental determination of a sexually selected trait. Nature 400:358–359CrossRefGoogle Scholar
  17. Guerra M, Drummond H (1995) Reversed sexual size dimorphism and parental care: minimal division of labour in the blue-footed booby. Behaviour 132:479–496Google Scholar
  18. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387PubMedGoogle Scholar
  19. Heywood JS (1989) Sexual selection by the handicap mechanism. Evolution 43:1387–1397Google Scholar
  20. Hill GE (1991) Plumage coloration is a sexually selected indicator of male quality. Nature 350:337–339CrossRefGoogle Scholar
  21. Hill GE (1999) Mate choice, male quality, and carotenoid based plumage coloration. In: Adams N, Slotow R (eds) Proceedings of 22nd International Ornithological Congress. BirdLife, Johannesburg, pp 1654–1668Google Scholar
  22. Hill GE, Montgomerie R (1994) Plumage colour signals nutritional condition in the house finch. Proc R Soc Lond B 258:47–52Google Scholar
  23. Hoelzer GA (1989) The good parent process of sexual selection. Anim Behav 38:1067–1078Google Scholar
  24. Houston AI, Davies NB (1985) The evolution of cooperation and life history in the dunnock, Prunella modularis. In: Sibly R, Smith R (eds) Behavioural ecology: the ecological consequences of adaptive behaviour. Blackwell, Oxford, pp 471–487Google Scholar
  25. Hoyt DG (1979) Practical methods of estimating volume and fresh weight of bird eggs. Auk 96:73–77Google Scholar
  26. Johnsen A, Andersson S, Ornborg J, Lifjeld JT (1998) Ultraviolet plumage ornamentation affects social mate choice and sperm competition in bluethroats (Aves: Luscinia s. svecica): a field experiment. Proc R Soc London B 265:1313–1318Google Scholar
  27. Kennamer RA, Alsum SK, Colwell SV (1997) Composition of wood duck eggs in relation to egg size, laying sequence, and skipped days of laying. Auk 114:479–487Google Scholar
  28. Kirkpatrick M (1985) Evolution of female choice and male parental investment in polygynous species: the demise of the ‘sexy son’. Am Nat 125:788–810Google Scholar
  29. Kirkpatrick M, Barton NH (1997) The strength of indirect selection on female mating preferences. Proc Natl Acad Sci USA 94:1282–1286Google Scholar
  30. Kirkpatrick M, Ryan MJ (1991) The evolution of mating preferences and the paradox of the lek. Nature 350:33–38CrossRefGoogle Scholar
  31. Kodric-Brown A, Brown JH (1984) Truth in advertising: the kinds of traits favoured by sexual selection. Am Nat 124:309–323Google Scholar
  32. Kokko H (1998) Should advertising parental care be honest? Proc R Soc Lond B 265:1871–1878Google Scholar
  33. Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348CrossRefPubMedGoogle Scholar
  34. Linville SU, Breitwisch R, Schilling AJ (1998) Plumage brightness as an indicator of parental care in northern cardinals. Anim Behav 55:119–127Google Scholar
  35. Lozano GA (1994) Carotenoids, parasites, and sexual selection. Oikos 70:309–311Google Scholar
  36. Lung NP, Thompson JP, Kollias GV, Olsen JH, Zdziarski JM, Klein PA (1996) Maternal immunoglobulin G antibody transfer and development of immunoglobulin G antibody responses in blue and gold macaw (Ara ararauna) chicks. Am J Vet Res 57:1162–1167Google Scholar
  37. Massaro M, Davis LS, Darby JT (2003) Carotenoid-derived ornaments reflect parental quality in male and female yellow-eyed penguind (Megadyptes antipodes). Behav Ecol Sociobiol 55:169–175CrossRefGoogle Scholar
  38. Mateos C, Carranza J (1995) Female choice for morphological features of male ring-necked pheasant. Anim Behav 49:737–748Google Scholar
  39. Mazuc J, Chastel O, Sorci G (2003) No evidence for differential maternal allocation to offspring in the house sparrow (Passer domesticus). Behav Ecol 14:340–346Google Scholar
  40. Merilä J (1996) Genetic variation in offspring condition: an experiment. Funct Ecol 10:465–474Google Scholar
  41. Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260CrossRefPubMedGoogle Scholar
  42. Møller AP, Birkhead TM (1994) The evolution of plumage brightness in birds is related to extra-pair paternity. Evolution 48:1089–1100Google Scholar
  43. Møller AP, Jennions MD (2001) How important are direct fitness benefits of sexual selection? Naturwissenschaften 88:401–415CrossRefGoogle Scholar
  44. Møller AP, Thornhill R (1998) Male parental care, differential parental investment by females and sexual selection. Anim Behav 55:1507–1515Google Scholar
  45. Mousseau TA, Fox CW (1998) Maternal effects as adaptations. Oxford University Press, New YorkGoogle Scholar
  46. Negro JJ, Bortolotti GR, Tella JL, Fernier KJ, Bird DM (1998) Regulation of intergumentary colour and plasma carotenoids in American kestrels consistent with sexual selection theory. Funct Ecol 12:307–312Google Scholar
  47. Nelson B (1978) The Sulidae: gannets and boobies. Oxford University Press, OxfordGoogle Scholar
  48. Norris KJ (1990) Female choice and quality of parental care in the great tit Parus major. Behav Ecol Sociobiol 27:275–281Google Scholar
  49. Osorio-Beristain M, Drummond H (1998) Non-aggressive mate guarding by the blue-footed booby: a balance of female and male control. Behav Ecol Sociobiol 43:307–315Google Scholar
  50. Palokangas P, Korpimäki E, Hakkarainen H, Huhta E, Tolonen P, Alatalo RV (1994) Female kestrels gain reproductive success by choosing brightly ornamented males. Anim Behav 47:443–448Google Scholar
  51. Price TD, Schluter D, Heckman NE (1993) Sexual selection when the female directly benfits. Biol J Linn Soc 48:187–211Google Scholar
  52. Prumm RO, Torres R (2003) Structural coloration of avian skin: convergent evolution or coherently scattering dermal colagen arrays. J Exp Biol 206:2409–2429Google Scholar
  53. Saetre GP, Fossnes T, Slagsvold T (1995) Food provisioning in the piedflycatcher: do females gain direct benefits from choosing bright-coloured males? J Anim Ecol 64:21–30Google Scholar
  54. Saino N, Bolzern AM, Møller AP (1997) Immunocompetence, ornamentation and viability of male barn swallows (Hirundo rustica). Proc Natl Acad Sci USA 97:579–585Google Scholar
  55. Saino N, Ferrari RP, Martinelli R, Romano M, Rubolini D, Møller AP (2002) Early maternal effects mediated by immunity depend on sexual ornamentation of the male partner. Proc R Soc Lond B 269:1005–1009CrossRefGoogle Scholar
  56. Schwabl H (1997) A hormonal mechanism for parental favoritism. Nature 386:231CrossRefGoogle Scholar
  57. Senar JC, Figuerola J, Pascual J (2002) Brighter yellow blue tits make better parents. Proc R Soc Lond B 269:257–261PubMedGoogle Scholar
  58. Sheldon B (2000) Diferential allocation: tests, mechanisms and implications. Trends Ecol Evol 15:397–402CrossRefPubMedGoogle Scholar
  59. Siitari H, Honkavaraa J, Huhta E, Viitala J (2002) Ultraviolet reflection and female mate choice in the pied flycatcher, Ficedula hypoleuca. Anim Behav 63:97–102Google Scholar
  60. Smiseth PT, Ornborg J, Andersson S, Amundsen T (2001) Is male plumage reflectance correlated with paternal care in bluethroats? Behav Ecol 12:164–170Google Scholar
  61. Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohemagglutinin skin testing technique in studies of avian immunocompetence. Funct Ecol 13:567–577CrossRefGoogle Scholar
  62. Sorci G, Moller AP, Boulinier T (1997) Genetics of host-parasite interactions. Trends Ecol Evol 12:196–200Google Scholar
  63. Sundberg J, Larsson C (1994) Male coloration as an indicator of parental quality in the yellowhammer Emberiza citrinella. Anim Behav 48:885–892CrossRefGoogle Scholar
  64. Tella JL, Bortolotti GR, Forero MG (2000) Environmental and genetic variation in T-cell-mediated immune response of fledgling American kestrels. Oecologia 123:453–459CrossRefGoogle Scholar
  65. Torres R, Drummond H (1997) Sex-biased mortality in nestlings of a bird with reversed sexual size dimorphism. J Anim Ecol 66:859–865Google Scholar
  66. Torres R, Drummond H (1999) Variably male-biased sex ratio in a marine bird with females larger than males. Oecologia 118:16–22CrossRefGoogle Scholar
  67. Torres R, Velando A (2003) A dynamic trait affects continuous pair assessment in the blue-footed booby (Sula nebouxii). Behav Ecol Sociobiol 55:65–72Google Scholar
  68. Velando A (2002) Experimental manipulation of maternal effort produces differential effects in sons and daughters: implications for adaptive sex ratios in the blue-footed booby. Behav Ecol 13:443–449Google Scholar
  69. Velando A, Alonso-Alvarez C (2003) Differential body condition regulation by males and females in response to experimental manipulations of brood size and parental effort in the blue-footed booby. J Anim Ecol 72:846–856CrossRefGoogle Scholar
  70. Voltura KM, Schwagmeyer PL, Mock DW (2002) Parental feeding rates in the house sparrow, Passer domesticus: are larger-badged males better fathers? Ethology 108:1011–1022Google Scholar
  71. Wiehn J (1997) Plumage characteristics as an indicator of male parental quality in the American kestrel. J Avian Biol 28:47–55Google Scholar
  72. Williams TD (1994) Intra-specific variation in egg size and egg composition in birds: effects on offspring fitness. Biol Rev 68:35–59Google Scholar
  73. Winkler DW (1987) A general model for parental care. Am Nat 130:526–543CrossRefGoogle Scholar
  74. Zahavi A (1975) Mate selection. A selection for a handicap. J Theor Biol 53:205–214PubMedGoogle Scholar
  75. Zuk M, Decruyenaere JG (1994) Measuring individual variation in colour—a comparison of two techniques. Biol J Linn Soc 53:165–173Google Scholar
  76. Zuk M, Thornhill R, Ligon JD, Johnson K, Austad S, Ligon SH, Thornhill NW, Costin C (1990) The role of male ornaments and courtship behavior in female mate choice of red jungle fowl. Am Nat 136:459–473Google Scholar
  77. Zuk M, Ligon JD, Thornhill R (1992) Effects of experimental manipulation of male secondary sex characters on female mate preference in red jungle fowl. Anim Behav 44:999–1006Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • Alberto Velando
    • 1
  • Roxana Torres
    • 2
  • Irene Espinosa
    • 2
  1. 1.Departamento de Ecoloxía e Bioloxía Animal, Facultade de CienciasUniversidade de VigoVigoSpain
  2. 2.Departamento de Ecología Evolutiva, Instituto de EcologíaUniversidad Nacional Autónoma de MéxicoMéxico

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