Heritability of the algal-foraging ability: an indirect benefit of female mate preference for males' carotenoid-based coloration in the guppy, Poecilia reticulata

  • Kenji KarinoEmail author
  • Taeko Utagawa
  • Shinya Shinjo
Original Article


Several sexual selection theories assume certain benefits of female mate preference. The direct benefit, i.e., the direct contribution from males to their offspring and females, has been well tested empirically. However, the indirect benefit, i.e., the male's genetic contribution to their offspring, has been poorly demonstrated. Female preference for males' carotenoid-based coloration is known in some animals. Since animals must acquire carotenoids through foods, it is often hypothesized that the brightness of the carotenoid-based coloration is a reliable indicator of the male's foraging ability. Hence, females' indirect benefits, such as greater foraging ability in their offspring, through mate preference for the carotenoid-based coloration are assumed. However, the heritability of the foraging ability for foods that serve as carotenoid resources has not been tested. In this study, a maze experiment was performed in guppies (Poecilia reticulata) to examine the heritability of the foraging ability for algae, carotenoid resources in nature. The latency for completing algal-foraging tasks in this experiment showed high individual variation. Heritable estimates of the foraging ability were substantial (h 2 = 0.57 – 0.66) and significant, suggesting a genetic contribution to the foraging ability from fathers to their offspring. This result may support the hypothesis that indirect benefits influence the evolution of female choice.


Coloration Foraging ability Heritability Indirect benefit Sexual selection 



We are grateful to Anne E. Houde, Robert Brooks and anonymous reviewers for critical reading and helpful comments on our manuscript. This work was supported by Grant-in-Aids (#13740436 and #16570012) to K.K. from the Japan Society for the Promotion of Science. This research was performed in compliance with the guideline of the Animal Care and Use Committee of Tokyo Gakugei University as well as that of the Japan Ethological Society.


  1. Andersson M (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  2. Brooks R, Endler JA (2001) Direct and indirect sexual selection and quantitative genetics of male traits in guppies (Poecilia reticulata). Evolution 55:1002–1015PubMedCrossRefGoogle Scholar
  3. Craig JK, Foote CJ (2001) Countergradient variation and secondary sexual color: phenotypic convergence promotes genetic divergence in carotenoid use between sympatric anadromous and nonanadromous morphs of sockeye salmon (Oncorhynchus nerka). Evolution 55:380–391PubMedCrossRefGoogle Scholar
  4. Endler JA (1980) Natural selection on color patterns in Poecilia reticulata. Evolution 34:76–91CrossRefGoogle Scholar
  5. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longman, LondonGoogle Scholar
  6. Grether GF (2000) Carotenoid limitation and mate preference evolution: a test of the indicator hypothesis in guppies (Poecilia reticulata). Evolution 54:1712–1724PubMedGoogle Scholar
  7. Grether GF, Hudon J, Millie DF (1999) Carotenoid limitation of sexual coloration along an environmental gradient in guppies. Proc R Soc Lond B 266:1317–1322CrossRefGoogle Scholar
  8. Gwynne DT (1984) Courtship feeding increases female reproductive success in bushcrickets. Nature 307:361–363CrossRefGoogle Scholar
  9. Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387PubMedCrossRefGoogle Scholar
  10. Hill GE (2002) A red bird in a brown bag: the function and evolution of colorful plumage in the house finch. Oxford University Press, New YorkGoogle Scholar
  11. Houde AE (1997) Sex, color, and mate choice in guppies. Princeton University Press, PrincetonGoogle Scholar
  12. Houde AE, Endler JA (1990) Correlated evolution of female mating preferences and male color patterns in the guppy Poecilia reticulata. Science 248:1405–1408PubMedCrossRefGoogle Scholar
  13. Houde AE, Torio AJ (1992) Effects of parasitic infection on male color pattern and female choice in guppies. Behav Ecol 3:346–351CrossRefGoogle Scholar
  14. Johnson K, Dalton R, Burley N (1993) Preferences of female American goldfinches (Carduelis tristis) for natural and artificial male traits. Behav Ecol 4:138–143CrossRefGoogle Scholar
  15. Karino K, Haijima Y (2001) Heritability of male secondary sexual traits in feral guppies in Japan. J Ethol 19:33–37CrossRefGoogle Scholar
  16. Karino K, Haijima Y (2004) Algal-diet enhances sexual ornament, growth and reproduction in the guppy. Behaviour 141:585–601CrossRefGoogle Scholar
  17. Karino K, Shinjo S (2004) Female mate preference based on male orange spot patterns in the feral guppy Poecilia reticulata in Japan. Ichthyol Res 51:316–320CrossRefGoogle Scholar
  18. Knapp RA, Kovach JT (1991) Courtship as an honest indicator of male parental quality in the bicolor damselfish, Stegastes partitus. Behav Ecol 2:295–300CrossRefGoogle Scholar
  19. Kodric-Brown A (1989) Dietary carotenoids and male mating success in the guppy: an environmental component to female choice. Behav Ecol Sociobiol 25:393–401CrossRefGoogle Scholar
  20. Kodric-Brown A, Brown JH (1984) Truth in advertising: the kinds of traits favored by sexual selection. Am Nat 124:309–323CrossRefGoogle Scholar
  21. Kokko H, Brooks R, Jennions MD, Morley J (2003) The evolution of mate choice and mating biases. Proc R Soc Lond B 270:653–664CrossRefGoogle Scholar
  22. Krinsky NI, Mathews-Roth MM, Taylor RF (1989) Carotenoids; chemistry and biology. Plenum Press, New YorkGoogle Scholar
  23. Lozano GA (1994) Carotenoids, parasites, and sexual selection. Oikos 70:309–311CrossRefGoogle Scholar
  24. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer, SunderlandGoogle Scholar
  25. Milinski M, Bakker TCM (1990) Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature 344:330–333CrossRefGoogle Scholar
  26. Møller AP (1994) Sexual selection and the barn swallow. Oxford University Press, OxfordGoogle Scholar
  27. Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514CrossRefGoogle Scholar
  28. Petrie M (1983) Female moorhens compete for small fat males. Science 220:413–415PubMedCrossRefGoogle Scholar
  29. Reader SM, Laland KN (2000) Diffusion of foraging innovations in the guppy. Anim Behav 60:175–180CrossRefPubMedGoogle Scholar
  30. Rutowski RL, Gilchrist GW, Terkanian B (1987) Female butterflies mated with recently mated males show reduced reproductive output. Behav Ecol Sociobiol 20:319–322CrossRefGoogle Scholar
  31. Wootton RJ (1998) Ecology of teleost fishes, 2nd edn. Kluwer Academic Publishers, DordrechtGoogle Scholar
  32. Zahavi A (1975) Mate selection – a selection for a handicap. J Theor Biol 53:205–214CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Department of BiologyTokyo Gakugei UniversityTokyoJapan

Personalised recommendations