Male Colors and Female Mate Preference in Korean Rosy Bitterling, Rhodeus uyekii (Cyprinidae: Acheilognathinae)

한국산 각시붕어 수컷의 혼인색과 암컷의 배우자 선택

  • Received : 2012.10.12
  • Accepted : 2012.12.13
  • Published : 2012.12.31

Abstract

A female preference is a potentially complex function relating variation in multiple male traits with her probability of accepting the most optimal individuals as a mate. If mate preference is dominantly driven by additive fitness benefits, different females tend to be congruent in the decision of choice, whereas females will not necessarily share their mate preferences if non-additive benefits more strongly operate. Here, a sequential blocked design ($4{\times}4$) was applied to experimentally assess the relative contribution of additive and non-additive components to the female mate preference with Korean rosy bitterling, Rhodeus uyekii. In a total of 48 single stimulus presentations, behavioral elements of courtship activities were analyzed to derive the 'index of female preference'. Females showed a clear preference for males with more elaborate carotenoid colors, but mated randomly with respect to male body size and other color patterns. However, they were not individually consistent in their choice of mates, suggesting that non-additive components probably contribute to the evolution of female preference.

암컷의 배우자 선택은 여러 수컷들이 가지고 있는 다양한 특성에서 각기 다른 종류의 정보를 수집, 종합하여 가장 최적의 개체를 배우자로 결정하는 매우 복잡한 행동이다. 본 연구에서는 순차적인 교배 시스템($4{\times}4$ block breeding)을 이용하여 각시붕어(Rhodeus uyekii) 암컷의 배우자 선택방식을 조사하였고, 가중과 비가중 유전적 이득의 상대적 기여도를 추정해 보고자 하였다. 실험장치 내에서 총 48회의 암, 수간 배우자 상호작용이 관찰되었고, 암컷은 일반적으로 카로티노이드 혼인색 발현이 강한 수컷들을 배우자로 선호하는 것으로 나타났다. 하지만, 배우자 선호 정도가 개체에 따라 차이가 나타나므로, 비가중적 요소도 암컷이 배우자를 선택하는데 있어 기여를 할 것으로 예상된다.

Keywords

Acknowledgement

Supported by : 한국연구재단

References

  1. 김익수∙최 윤∙이충렬∙이용주∙김병직∙김지현. 2005. 한국어류대도감. 교학사, 615pp.
  2. 김화선∙김유희∙조재윤∙윤길하∙하봉석. 1999. 천연산 각시붕어(Rhodeus uyekii) 혼인색의 색소 조성. 한국수산학회지, 32: 520-524
  3. 송호복∙권오길. 1995. 줄납자루, Acheilognathus yamatsutae Mori (Cyprinidae)의 산란 조건. 한국어류학회지, 7: 18-24.
  4. 안철민. 1995a 각시붕어, Rhodeus uyekii의 생식주기. 한국어류학회지, 7: 33-42.
  5. 안철민. 1995b 각시붕어, Rhodeus uyekii의 생식주기에 미치는 광주기와 수온의 영향. 한국어류학회지, 7: 43-55.
  6. 채병수. 2001. 각시붕어, Rhodeus uyekii의 (Pisces: Cyprinidae)의 산란관의 신장. 한국어류학회지, 13: 111-116.
  7. Agbali, M., M. Reichard, A. Bryjova, J. Bryja and C. Smith. 2010. Mate choice for nonadditive genetic benefits correlate with MHC dissimilarity in the rose bitterling (Rhodeus ocellatus). Evolution, 64: 1683-1696. https://doi.org/10.1111/j.1558-5646.2010.00961.x
  8. Andersson, M. 1994. Sexual selection. Princeton University Press, 624pp.
  9. Akai, Y. and R. Arai. 1998. Rhodeus sinensis, a senior synonym of R. lighti and R. uyekii (Acheilognathinae, Cyprinidae). Ichthyol. Res., 45: 105-110. https://doi.org/10.1007/BF02678582
  10. Barber, I., S. a. Arnott, V. a. Braithwaite, J. Andrew and F. a. Huntingford 2001. Indirect fitness consequences of mate choice in sticklebacks: offspring of brighter males grow slowly but resist parasitic infections. Proc. Roy. Soc. Lond. B., 268: 71-6. https://doi.org/10.1098/rspb.2000.1331
  11. Baube, C. 1997. Manipulations of signaling environment affect male competitive success in three-spined sticklebacks. Anim. Behav., 53: 819-833. https://doi.org/10.1006/anbe.1996.0347
  12. Boake, C.R.B. 1989. Repeatability: its role in evolutionary studies of mating behavior. Evol. Ecol., 3: 173-182. https://doi.org/10.1007/BF02270919
  13. Candolin, U. 2003. The use of multiple cues in mate choice. Biol. Rev., 78: 575-595. https://doi.org/10.1017/S1464793103006158
  14. Casalini, M., M. Agbali, M. Reichard, M. Konecna, A. Bryjova and C. Smith. 2009. Male dominance, female mate choice, and intersexual conflict in the rose bitterling (Rhodeus ocellatus). Evolution, 63: 366-376. https://doi.org/10.1111/j.1558-5646.2008.00555.x
  15. Eberhard, W.G. 1996. Female control: sexual selection by cryptic female choice. Princeton University Press, 472pp.
  16. Endler, J. A. 1980. Natural selection on color patterns in Poecilia reticulata. Evolution, 34: 76-91. https://doi.org/10.2307/2408316
  17. Fox, D. 1976. Animal Biochromes and Structural Colours. University of California Press, 433pp.
  18. Godin, J-G. J. and L.A. Dugatkin. 1995. Variability and repeatability of female mating preference in the guppy. Anim. Behav., 49: 1427-1433. https://doi.org/10.1016/0003-3472(95)90063-2
  19. Goodwin, T.W. 1984. The biochemistry of the carotenoids: animal, vol. 2. Chapman and Hall. 224pp.
  20. Grether, F.G. 2000. Carotenoid limitation and mate preference evolution: a test of the indicator hypothesis in Guppies (Poecilia reticulate). Evolution, 54: 1712-1724. https://doi.org/10.1111/j.0014-3820.2000.tb00715.x
  21. Griggio, M., C. Biard, D.J. Penn and H. Hoi. 2011. Female house sparrows "count on" male genes: experimental evidence for MHC-dependent mate preference in birds. BMC Evol. Biol., 11: 44. https://doi.org/10.1186/1471-2148-11-44
  22. Hamilton, W.D. and M. Zuk. 1982. Heritable true fitness and bright birds: a role for parasites? Science, 218: 384-387. https://doi.org/10.1126/science.7123238
  23. Hill, G.E. and R. Montgomerie. 1994. Plumage colour signals nutritional condition in the house finch. Proc. Roy. Soc. Lond. B., 258: 47-52. https://doi.org/10.1098/rspb.1994.0140
  24. Houde, A.E. and A.J. Torio. 1992. Effect of parasitic infection on male color pattern and female choice in guppies. Behav. Ecol., 3: 346-351. https://doi.org/10.1093/beheco/3.4.346
  25. Hughes, K.A., F.H. Rodd and D.N. Reznick. 2005. Genetic and environmental effects on secondary sex traits in guppies (Poecilia reticulata). J. Evol. Biol., 18: 35-45. https://doi.org/10.1111/j.1420-9101.2004.00806.x
  26. Jennions, M.D. and M. Petrie. 1997. Variation in mate choice and mating preferences: a review of causes and consequences. Biol. Rev., 72: 283-327. https://doi.org/10.1017/S0006323196005014
  27. Johnstone, R.A. 1996. Multiple display in animal communication: 'backup signals' and 'multiple messages'. Philos. Trans. R. Soc. Lond. B. Biol. Sci., 351: 329-338. https://doi.org/10.1098/rstb.1996.0026
  28. Jordan, W.C. and M.W. Bruford. 1998. New perspectives on mate choice and the MHC. Heredity, 81: 127-133. https://doi.org/10.1046/j.1365-2540.1998.00428.x
  29. Kodric-Brown, A. 1989. Dietary carotenoids and male mating success in the guppy: an environmental component to female choice. Behav. Ecol. Sociobiol., 25: 393-401. https://doi.org/10.1007/BF00300185
  30. Kirkpatrick, M. and M. Ryan. 1991. The evolution of mating preferences and the paradox of the lek. Nature, 350: 33-38. https://doi.org/10.1038/350033a0
  31. Kokko, H., R. Brooks, M.D. Jennions and J. Morley. 2003. The evolution of mate choice and mating biases. Proc. Roy. Soc. Lond. B., 270: 653-664. https://doi.org/10.1098/rspb.2002.2235
  32. Kokko, H., M.D. Jennions and R. Brooks. 2006. Unifying and testing models of sexual selection. Ann. Rev. Ecol. Evol. Syst., 37: 43-66. https://doi.org/10.1146/annurev.ecolsys.37.091305.110259
  33. Mays Jr, H.L. and G.E. Hill. 2004. Choosing mates: good genes versus genes that are a good fit. Trends Ecol. Evol.,19: 554-559. https://doi.org/10.1016/j.tree.2004.07.018
  34. Milinski, M. and T.C.M. Bakker. 1990. Female sticklebacks use male coloration in mate choice and hence avoid parasitized males. Nature, 344: 330-333. https://doi.org/10.1038/344330a0
  35. Milinski, M., S. Griffiths, K.M. Wegner, T.B.H. Reusch, A. Haas- Assenbaum and T. Boehm. 2005. Mate choice decision of stickleback females predictably modified by MHC peptide ligands. Proc. Nat. Acad. Sci., 102: 4414-4418. https://doi.org/10.1073/pnas.0408264102
  36. Moller, A.P. 1990. Parasites and sexual selection: Current status of the Hamilton and Zuk hypothesis. J. Evol. Biol., 3: 319-328. https://doi.org/10.1046/j.1420-9101.1990.3050319.x
  37. Moller, A.P. 1994. Repeatability of female choice in a monogamous swallow. Anim. Behav., 47: 643-648. https://doi.org/10.1006/anbe.1994.1087
  38. Moller, A.P. and A. Pomiankowski. 1993. Why have birds got multiple sexual ornaments? Behav. Ecol. Sociobiol., 32: 167-176.
  39. Neff, B.D. and T.E. Pitcher. 2005. Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Mol. Ecol., 14: 19-38.
  40. Nicoletto, P.F. 1991. The relationship between male ornamentation and swimming performance in the guppy, Poecilia reticulata. Behav. Ecol. Sociobiol., 28: 365-370. https://doi.org/10.1007/BF00164386
  41. Putnam, M. 1992. A review of the nature, function, variability, and supply of pigments in salmonid fish. pp. 245-263 in N. Depauw and J. Joyce, eds. Aquaculture and the environment. European Aquaculture Society, Gent, Belgium.
  42. Reichard, M., H. Liu and C. Smith. 2007. The co-evolutionary relationship between bitterling fishes and freshwater mussels: insights from interspecific comparisons. Evol. Ecol. Res., 9: 239-259.
  43. Reichard, M., J. Bryja, M. Ondrackova, M. Davidova, P. Kaniewska and C. Smith. 2005. Sexual selection for male dominance reduces opportunities for female mate choice in the Europe-an bitterling (Rhodeus sericeus). Mol. Ecol., 14: 1533-1542. https://doi.org/10.1111/j.1365-294X.2005.02534.x
  44. Reinhold, K. 2002. Modelling the evolution of female choice strategies under inbreeding conditions. Genetica, 116: 189-195. https://doi.org/10.1023/A:1021253014088
  45. Reusch, T.B.H., M.A. Haberli, P.B. Aeschlimann and M. Milinski. 2001. Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism. Nature, 414: 300-302. https://doi.org/10.1038/35104547
  46. Rowe, L. and D. Houle. 1996. The lek paradox and the capture of genetic variance by condition dependent traits. Proc. Roy. Soc. Lond. B., 263: 1415-1421. https://doi.org/10.1098/rspb.1996.0207
  47. Schiedt, K. 1989 New aspects of carotenoid metabolism in animals. In Carotenoids: chemistry and biology (ed. N.I. Krinsky, M.M. Mathews-Roth & R.F. Taylor), pp. 247-268. New York: Plenum Press.
  48. Spence, R. and C. Smith. 2006. Mating preference of female zebrafish, Danio rerio, in relation to male dominance. Behav. Ecol., 17: 779-783. https://doi.org/10.1093/beheco/arl016
  49. Suk, H.Y. and J.C. Choe. 2008. Dynamic female preference for multiple signals in Rhinogobius brunneus. Behav. Ecol. Sociobiol., 62: 945-951. https://doi.org/10.1007/s00265-007-0519-7
  50. Tomkins, J.L., J. Radwan, J.S. Kotiaho and T. Tregenza. 2004. Genic capture and resolving the lek paradox. Trends Ecol. Evol., 19: 323-328. https://doi.org/10.1016/j.tree.2004.03.029
  51. Tregenza, T. and N. Wedell. 2000. Genetic compatibility, mate choice and patterns of parentage: invited review. Mol. Ecol., 9: 1013-1027. https://doi.org/10.1046/j.1365-294x.2000.00964.x
  52. van Doorn, G.S. and F.J. Weissing. 2004. The evolution of female preferences for multiple indicators of quality. Amer. Nat., 164: 173-186. https://doi.org/10.1086/422203
  53. van Oosterhout, C., R.E. Trigg, G.R. Carvalho, A.E. Magurran, L. Hauser and P.W. Shaw. 2003. Inbreeding depression and genetic load of sexually selected traits: how the guppy lost its spots. J. Evol. Biol., 16: 273-281. https://doi.org/10.1046/j.1420-9101.2003.00511.x
  54. Widemo, F. and S.A. Saeher. 1999. Beauty is in the eye of the beholder: causes and consequences of variation in mating preferences. Trends Ecol. Evol., 14: 26-31. https://doi.org/10.1016/S0169-5347(98)01531-6
  55. Zahavi, A. 1975. Mate selection - a selection for a handicap. J. Theo. Biol., 53: 205-214. https://doi.org/10.1016/0022-5193(75)90111-3
  56. Zuk, M., R. Thornhill, J.D. Ligon, K. Johnson, S. Austad, S.H. Ligon, N. Thornhill and C. Costin. 1990. The role of male ornaments and courtship behavior in female mate choice of red jungle fowl. Amer. Nat., 136: 459-473. https://doi.org/10.1086/285107