AN EYE FOR DETAIL: SELECTIVE SEXUAL IMPRINTING IN ZEBRA FINCHES
Nancy Tyler Burley
Department of Ecology and Evolutionary Biology, University of California-Irvine, California 92697-2525 E-mail: [email protected]
Search for more papers by this authorNancy Tyler Burley
Department of Ecology and Evolutionary Biology, University of California-Irvine, California 92697-2525 E-mail: [email protected]
Search for more papers by this authorAbstract
Abstract To investigate the idea that sexual imprinting creates incipient reproductive isolation between phenotypically diverging populations, I performed experiments to determine whether colony-reared zebra finches would imprint on details of artificial white crests. In the first experiment, adults in one breeding colony wore white crests with a vertical black stripe, while in another colony adults wore crests having a horizontal black stripe; except for their crests, breeders possessed wild-type plumage and conformation. Offspring of both sexes reared in these colonies developed mate preferences for opposite-sexed birds wearing the crest type with which they were reared; neither sex developed a social preference for crested individuals of the same sex. In a second experiment, females reared by crested parents preferred crested males versus males with red leg bands, while control females (reared in a colony of wild-type, uncrested birds) preferred red-banded males in the same test. Results of a third experiment that used sexually dimorphic crest phenotypes indicate that both sexes of offspring imprinted on maternal crest patterns. Results support the hypothesis that sexual imprinting can facilitate isolation both by engendering a preference for population-typical traits and by prioritizing such an imprinting-based preference over species-typical preferences for other traits used in mate choice. Comparison with results of other recent studies indicates that imprinting tendencies of both sexes vary with the characteristics of traits presented as an imprinting stimuli. Tendency to imprint may vary with the perceived information content (e.g., kin, sex, or population indicator) of parental traits, a process dubbed selective sexual imprinting.
Literature Cited
- Albert, A. Y. K. 2005. Mate choice, sexual imprinting, and speciation: a test of a one-allele isolating mechanism in sympatric sticklebacks. Evolution 59: 927–931.
- Armstrong, E. A. 1965. Bird display and behavior: an introduction to the study of bird psychology. Dover, New York .
- Andersson, M. 1994. Sexual selection. Monographs in Behavior and Ecology. Princeton Univ. Press, Princeton , NJ .
- Basolo, A. 1998. Evolutionary change in a receiver bias: a comparison of female preference functios. Proc. R. Soc. Lond. B 265: 2223–2228.
- Bateson, P. 1978. Sexual imprinting and optimal outbreeding. Nature 273: 659–660.
- Bereczkei, T., P. Gyuris, and G. E. Weisfeld. 2004. Sexual imprinting in human mate choice. Proc. R. Soc. Lond. B 271: 1129–1134.
-
Bischof, H.-J.
1994. Sexual imprinting as a two-stage process. Pp. 82–97
in
J. A. Hogan and
J. J. Bolhuis, eds.
Causal mechanisms of behavioural development. Cambridge Univ. Press,
Cambridge
,
U.K.
10.1017/CBO9780511565120.006 Google Scholar
- Burley, N. 1985. The organization of behavior and the evolution of sexually selected traits. Pp. 22–44 in P. A. Gowaty, D. W. Mock, eds. Avian monogamy. Ornithology Monograph 37. American Ornithologists' Union, Washington, DC.
- Burley, N. 1986a. Sexual selection for aesthetic traits in species with biparental care. Am. Nat. 127: 415–445.
- Burley, N. 1986b. Comparison of the band-colour preferences of two species of estrildid finches. Anim. Behav. 34: 1732–1741.
- Burley, N. 1988. The differential allocation hypothesis: an experimental test. Am. Nat. 132: 611–628.
- Burley, N. 2006. Oedipus, yes; Electra, no: sex differences in sexual imprinting on artificial crests in zebra finches. Behav. Ecol. In press.
- Burley, N., and P. J. Bartels. 1990. Phenotypic similarities of sibling zebra finches. Anim. Behav. 39: 174–180.
- Burley, N., and C. B. Coopersmith. 1987. Bill color preferences of zebra finches. Ethology 76: 133–151.
- Burley, N. T., and V. S. Foster. 2006. Variation in female choice of mates: condition influences selectivity. Anim. Behav. In press.
- Burley, N. T., and R. Symanski. 1998. “A taste for the beautiful”: latent aesthetic mate preferences for white crests in two species of Australian grassfinches. Am. Nat. 152: 792–802.
- Burley, N., G. Krantztberg, and P. Radman. 1982. Influence of colour-banding on the conspecific preferences of zebra finches. Anim. Behav. 30: 444–455.
- Burley, N., R. A. Zann, S. C. Tidemann, and E. B. Male. 1989. Sex ratios of zebra finches. Emu 89: 83–92.
- Burley, N., C. Minor, and C. Strachan. 1990. Social preferences of zebra finches for siblings, cousins and non-kin. Anim. Behav. 39: 775–784.
- Calkins, J. D., and N. T. Burley. 2003. Mate choice for multiple ornaments in the California quail, Callipepla californica. Anim. Behav. 65: 69–81.
- Clayton, N. S. 1987. Song tutor choice in zebra finches. Anim. Behav. 35: 714–721.
- Clayton, N. S. 1988. Song discrimination learning in zebra finches. Anim. Behav. 36: 1016–1024.
- Clayton, N. S. 1990. Subspecies recognition and song learning in zebra finches. Anim. Behav. 40: 1009–1017.
- Coyne, J. A., and H. A. Orr. 2004. Speciation. Sinauer, Sunderland , MA .
- Darwin, C. 1871. The descent of man and selection in relation to sex. John Murray, London .
- de Kogel, C. H., and H. J. Prijs. 1996. Effects of brood size manipulations on sexual attractiveness of offspring in the zebra finch. Anim. Behav. 51: 699–708.
- Dooling, R. J., S. D. Brown, K. Manabe, and E. F. Powell. 1996. The perceptual foundations of vocal learning in budgerigars. Pp. 113–137 in C. F. Moss and S. J. Shettleworth, eds. Neuroethological studies of cognitive and perceptual processes. Westview Press, Boulder , CO .
- Dukas, R. 1998. Evolutionary ecology of learning. Pp. 129–174 in R. Dukas, ed. Cognitive ecology: the evolutionary ecology of information processing and decision making. Univ. of Chicago Press, Chicago .
- Düttmann, H., H.-H. Bergmann, and W. Engländer. 1998. Development of behavior. Pp. 223–246 in J. M. Stark and R. E. Ricklefs, eds. Avian growth and development. Cambridge Univ. Press, Cambridge , U.K.
- Galef, B. G., Jr., and C. Allen. 1995. A new model for studying behavioral traditions in animals. Anim. Behav. 50: 705–717.
- Grant, P. R., and B. R. Grant. 1997a. Genetics and the origin of bird species. Proc. Natl. Acad. Sci. USA 94: 7768–7775.
- Grant, P. R., and B. R. Grant. 1997b. Hybridization, sexual imprinting and mate choice. Am. Nat. 149: 1–28.
- Hansen, B. T., and T. Slagsvold. 2004. Early learning affects social dominance: interspecifically cross-fostered tits become subdominant. Behav. Ecol. 15: 262–268.
- Hess, E. H. 1973. Imprinting: early experience and the developmental psychobiology of attachment. Van Nostrand Reinhold, New York .
- Hörster, A., E. Curio, and K. Witte. 2000. No sexual imprinting on red bill as a novel trait. Behaviour 137: 1223–1239.
- Houtman, A. M. 1990. Sexual selection in the zebra finch (Poephila guttata). Ph.D. diss., University of Oxford, Oxford, U.K.
- Immelmann, K. 1975. Ecological significance of imprinting and early learning. Annu. Rev. Ecol. Syst. 6: 15–37.
- Immelmann, K. 1985. Sexual imprinting in zebra finches: mechanisms and biological significance. Pp. 156–172 in V. D. Ilyichev and U. M. Gavrilov, eds. Proceedings of the XVIII International Ornithological Congress. Nauka, Moscow .
- Immelmann, K., and S. J. Suomi. 1981. Sensitive phases in development. Pp. 395–431 in K. Immelmann, G. W. Barlow, L. Petrinovich, and M. Main, eds. Behavioural development. Cambridge Univ. Press, Cambridge , U.K.
- Irwin, D. E., and T. Price. 1999. Sexual imprinting, learning, and speciation. Heredity 82: 347–354.
- Kalmus, H., and J. Maynard Smith. 1966. Some evolutionary consequences of pegmatic mating systems (imprinting). Am. Nat. 100: 619–635.
- Kendrick, K. M., M. R. Hinton, K. Atkins, M. A. Haupt, and J. D. Skinner. 1998. Mothers determine sexual preferences. Nature 395: 229–230.
- Kruijt, J. P. 1985. On the development of social attachments in birds. Neth. J. Zool. 35: 45–62.
- Kruijt, J. P., and G. B. Meeuwissen. 1993. Consolidation and modification of sexual preferences in adult male zebra finches. Neth. J. Zool. 43: 68–79.
- Laland, K. N. 1994. On the evolutionary consequences of sexual imprinting. Evolution 48: 477–489.
- Lehman, L., and N. Perrin. 2002. Altruism, dispersal, and phenotype-matching kin recognition. Am. Nat. 159: 451–468.
- Lickliter, R. 1993. Timing and the development of perinatal perceptual organization. Pp. 105–123 in G. Turkewitz and D. A. Devenny, eds. Developmental time and timing L. Erlbaum Associates, Hillsdale , NY .
-
Lorenz, K.
1935. Der Kumpan in der Umwelt des Vogels.
J. Ornithol.
83: 137–213, 289–413.
10.1007/BF01905355 Google Scholar
- Nelson, D. A. 2000. A preference for own-subspecies' song guides vocal learning in a song bird. Proc. Natl. Acad. Sci. USA 97: 13348–13353.
- Oyama, S. 1993. Constraints and development. Neth. J. Zool. 43: 6–16.
- Payne, R. B. 1973. Behavior, mimetic songs and song dialects, and relationships of the parasitic indigobirds (Vidua) of Africa. Ornithol. Monogr. 11: 1–133.
- Payne, R. B., L. L. Payne, J. L. Woods, and M. D. Sorenson. 2000. Imprinting and the origin of parasite-host species associations in brood-parasitic indigobirds, Vidua chalybeata. Anim. Behav. 59: 69–81.
- Plenge, M., E. Curio, and K. Witte. 2000. Sexual imprinting supports the evolution of novel male traits by transference of a preference for the colour red. Behaviour 137: 741–758.
- Price, D. K., and N. T. Burley. 1993. Constraints on the evolution of attractive traits: genetic (co)variance of zebra finch bill colour. Heredity 71: 405–412.
- Price, D. K., and N. T. Burley. 1994. Constraints on the evolution of attractive traits: selection in male and female zebra finches. Am. Nat. 144: 908–934.
- Rogers, C. 1977. Zebra finches. John Bartholomew and Son, Edinburgh .
- Schutz, F. 1965. Sexual Pragung bei Anatiden. Z. Tierpsychol. 22: 50–103.
- Shapiro, J. L. 1980. Species identification in birds: a review and synthesis. Pp. 69–111 in M. A. Roy, ed. Species identity and attachment: a phylogenetic evaluation. Garland STPM Press, New York .
- Sokal, R. R., and F. J. Rohlf. 1981. Biometry. 2nd ed. W. H. Freeman, New York .
- ten Cate, C. 1984. The influence of social relations on the development of species recognition in zebra finch males. Behaviour 91: 263–295.
- ten Cate, C. 2000. How learning mechanisms might affect evolutionary processes. Trends. Ecol. Evol. 15: 179–181.
- ten Cate, C., and P. Bateson. 1988. Sexual selection: the evolution of conspicuous characteristics in birds by means of imprinting. Evolution 42: 1355–1358.
- ten Cate, C., and D. R. Vos. 1999. Sexual imprinting and evolutionary process in birds: a reassessment. Adv. Stud. Behav. 28: 1–31.
- Vos, D. R. 1995a. Sexual imprinting in zebra-finch females: Do females develop a preference for males that look like their father Ethology 99: 252–262.
- Vos, D. R. 1995b. The role of sexual imprinting for sex recognition in zebra finches: a difference between males and females. Anim. Behav. 50: 645–653.
- Vos, D. R., J. Prijs, and C. ten Cate. 1993. Sexual imprinting in zebra finch males: a differential effect of successive and simultaneous experience with two colour morphs. Behaviour 126: 137–154.
- Weisman, R., S. Shackleton, L. Ratcliffe, D. Weary, and P. Boag. 1994. Sexual preferences of female zebra finches: imprinting on beak colour. Behaviour 128: 15–24.
- Witte, K., and N. Sawka. 2003. Sexual imprinting on a novel trait in the dimorphic zebra finch: sexes differ. Anim. Behav. 65: 195–203.
-
Zann, R. A.
1996. The zebra finch: a synthesis of field and laboratory studies. Oxford Univ. Press,
Oxford
,
U.K.
10.1093/oso/9780198540793.001.0001 Google Scholar