Evolutionary Ecology

, Volume 19, Issue 3, pp 303–320 | Cite as

Perceptual Processes and the Maintenance of Polymorphism Through Frequency-dependent Predation

  • David Punzalan
  • F. Helen Rodd
  • Kimberly A. Hughes
Evolutionary Perspective


One of the key challenges of both ecology and evolutionary biology is to understand the mechanisms that maintain diversity. Negative frequency-dependent selection is a powerful mechanism for maintaining variation in the population as well as species diversity in the community. There are a number of studies showing that this type of selection, where individuals of a rare type (i.e. a rare morph or a rare species) experience higher survival than those of more common type(s). However, it is still not clear how frequency-dependent selection operates. Search image formation has been invoked as a possible, proximate explanation. Although the conceptual link between search image and frequency-dependent predation is often assumed in ecological and evolutionary studies, a review of the literature reveals a paucity of evidence demonstrating the occurrence of both in a natural predator-prey system. Advances in the field of psychology strongly support the existence of search image, yet these findings are not fully recognized in the realm of ecology and evolutionary biology, in part, we feel because of confusion and inconsistencies in terminology. Here we try to simplify the language, clarify the advances in the study of frequency-dependent predation and search image, and suggest avenues for future research. We feel that the investigations of both proximate (perceptual mechanisms) and ultimate (pattern of predation) processes are necessary to fully understand the importance of individual behavioural processes for mediating evolutionary and ecological diversity.


apostatic selection diversity frequency-dependent selection polymorphism predation search image switching variation 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abrams, P.A. 1999The adaptive dynamics of consumer choiceAm. Nat1538397CrossRefGoogle Scholar
  2. Allen, J.A. 1972Evidence for stabilizing selection and apostatic selection in wild blackbirdsNature237348349CrossRefPubMedGoogle Scholar
  3. Allen, J.A. 1988aFrequency-dependent selection by predatorsPhil. Trans. R. Soc. Lond. B319485503Google Scholar
  4. Allen, J.A. 1988bReflexive selection is apostatic selectionOikos51251253Google Scholar
  5. Allen, J.A. 1989Searching for search imageTrends Evol. Ecol4361CrossRefGoogle Scholar
  6. Allen, J.A., Clarke, B.C. 1968Evidence for apostatic selection by wild PasserinesNature220501502PubMedGoogle Scholar
  7. Allen, J.A., Clarke, B.C. 1984Frequency dependent selection: homage to E.B. PoultonBiol. J. Linn. Soc231518Google Scholar
  8. Allen, J.A., Raison, H.E., Weale, M.E. 1998The influence of density on frequency-dependent selection by wild birds feeding on artificial preyProc. Roy. Soc. Lond. B26510311035CrossRefGoogle Scholar
  9. Ayala, F.J., Campbell, C.A. 1974Frequency-dependent selectionAnnu. Rev. Ecol. Syst5115138CrossRefGoogle Scholar
  10. Barton, N.H., Turelli, M. 1989Evolutionary quantitative genetics: how little do we knowAnn. Rev. Genet23337370PubMedGoogle Scholar
  11. Blough, P.M. 1991Selective attention and search images in pigeonsJ. Exp. Psych. Anim. Behav. Proc17292298CrossRefGoogle Scholar
  12. Blough, P.M. 1992Detectability and choice during visual search – joint effects of sequential priming and discriminabilityAnim. Learn. Behav20293300Google Scholar
  13. Blough, P.M., Lacourse, D.M. 1994Sequential priming in visual search – contributions of stimulus-driven facilitation and learned expectanciesAnim. Learn. Behav22275281Google Scholar
  14. Bond, A.B. 1983Visual search and selection of natural stimuli in the pigeon: the attention threshold hypothesisJ. Exp. Psych. Anim. Behav. Proc9292306CrossRefGoogle Scholar
  15. Bond, A.B., Kamil, A.C. 1998Apostatic selection by blue jays produces balanced polymorphism in virtual preyNature395594595CrossRefGoogle Scholar
  16. Bond, A.B., Kamil, A.C. 2002Visual predators select for crypticity and polymorphism in virtual preyNature415609613CrossRefPubMedGoogle Scholar
  17. Bond, A.B., Riley, D.A. 1991Searching image in the pigeon – test of 3 hypothetical mechanismsEthology87203224Google Scholar
  18. Cain, A.J., Sheppard, P.M. 1954Natural selection in CepaeaGenetics3989116Google Scholar
  19. Carvalho, G.R., Shaw, P.W., Magurran, A.E., Seghers, B.H. 1991Marked genetic-divergence revealed by allozymes among populations of the guppy Poecilia reticulata (Poeciliidae), in TrinidadBiol. J. linn. Soc42389405Google Scholar
  20. Castillo, R.A., Cordero, C., Domínguez, C.A. 2002Are reward polymorphisms subject to frequency- and density-dependent selection? Evidence from a monoecious species pollinated by deceitJ. Evol. Biol15544552CrossRefGoogle Scholar
  21. Charnov, E.L. 1976Optimal foraging: the marginal value theoremTheor. Pop. Biol9129136CrossRefGoogle Scholar
  22. Charlesworth, B. 1987

    The heritability of fitness

    Bradbury, J.W.Andersson, M.B. eds. Sexual Selection: Testing the AlternativesJohn WileyChichester, United Kingdom2140
    Google Scholar
  23. Chase, A.R., Hill, W. 1999Reliable operant apparatus for fish: audio stimulus generator, response button, and pellet-dispensing nippleBehav. Res. Meth. Ins. C31470478Google Scholar
  24. Clarke, B.C. 1962a

    Balanced polymorphism and the diversity of sympatric species

    Nichols, D. eds. Taxonomy and GeographyOxfordSystematics Association4770
    Google Scholar
  25. Clarke, B.C. 1962bNatural selection in mixed populations of two polymorphic snailsHeredity17319345Google Scholar
  26. Clarke, B.C. 1969The evidence for apostatic selectionHeredity24347352PubMedGoogle Scholar
  27. Clarke, B.C., O’Donald, P. 1964Frequency-dependent selectionHeredity19201206Google Scholar
  28. Cook, L.M. 1998A two-stage model for Cepaea polymorphismPhil. Trans. R. Soc. Lond B35315771593CrossRefGoogle Scholar
  29. Cook, L.M., Miller, P. 1976Density-dependent selection on polymorphic prey – some dataAm. Nat111594598CrossRefGoogle Scholar
  30. Cooper, J.M 1984Apostatic selection on prey that match the backgroundBiol. J. Linn. Soc23221228Google Scholar
  31. Coppinger, R.P. 1969The effect of experience and novelty on avian feeding behaviour with reference to the evolution of warning coloration in butterflies. Part I. Reactions of wild-caught adult blue jays to novel insectsBehaviour354560Google Scholar
  32. Coppinger, R.P. 1970The effect of experience and novelty on avian feeding behaviour with reference to the evolution of warning coloration in butterflies. Part II. Reactions of naïve birds to novel insectsAm. Nat104323335CrossRefGoogle Scholar
  33. Croze, H.J. 1970Searching images in carrion crowsZ. Tierpsychol. Beiheft5185Google Scholar
  34. Curio, E. 1976The Ethology of PredationSpringer-VerlagBerlinGoogle Scholar
  35. Dawkins, M. 1971aPerceptual changes in chicks: another look at the ‘search image’ conceptAnim. Behav19566574Google Scholar
  36. Dawkins, M. 1971bShifts of ‘attention’ in chicks during feedingAnim. Behav19571582Google Scholar
  37. Fockert, J.W., Rees, G., Frith, C.D., Lavie, N. 2001The role of working memory in visual selective attentionScience29118031806CrossRefPubMedGoogle Scholar
  38. Dukas, R. 2002Behavioural and ecological consequences of limited attentionPhil. Trans. R. Soc. Lond. B35715391547CrossRefGoogle Scholar
  39. Dukas, R., Ellner, S. 1993Information processing and prey detectionEcology7413371346Google Scholar
  40. Dukas, R., Kamil, A.C. 2001Limited attention: the constraint underlying search imageBehav. Ecol12192199CrossRefGoogle Scholar
  41. Dukas, R., Real, L. 1993Learning constraints and floral choice behaviour in bumblebeesAnim. Behav46637644CrossRefGoogle Scholar
  42. Endler, J.A. 1978A predator’s view of animal color patternsEvol. Biol11319364Google Scholar
  43. Endler, J.A. 1980Natural selection on color patterns in Poecilia reticulataEvolution347691Google Scholar
  44. Endler, J.A. 1983Natural and sexual selection on color-patterns in poeciliid fishesEnviron. Biol. Fishes9173190CrossRefGoogle Scholar
  45. Endler, J.A. 1988Frequency-dependent predation, crypsis and aposematic colorationPhil. Trans. R. Soc. Lond. B319505523Google Scholar
  46. Endler, J.A. 1995Multiple-trait coevolution and environmental gradients in guppiesTrends Ecol. Evol102229CrossRefGoogle Scholar
  47. Endler, J.A. and Mielke, P.W. (2005). Comparing entire colour patterns as birds see them. Biol. J. Linn. Soc. (in press)Google Scholar
  48. Fajen, A., Breden, F. 1992Mitochondrial-DNA sequence variation among natural populations of the Trinidad Guppy, Poecilia reticulataEvolution4614571465Google Scholar
  49. Falconer, D.S. 1981Introduction to quantitative genetics2LongmanLondonGoogle Scholar
  50. Farr, J.A. 1977Male rarity or novelty, female choice behavior and sexual selection in the guppy Poecilia reticulata Peters (Pisces: Poeciliidae)Evolution31162168Google Scholar
  51. Fowlie, M.K., Kruger, O. 2003The evolution of plumage polymorphism in birds of prey and owls: the apostatic selection hypothesis revisitedJ. Evol. Biol16577583CrossRefPubMedGoogle Scholar
  52. Galeotti, P., Robolini, D., Dunn, P.O., Fasola, M. 2003Colour polymorphism in birds: causes and functionsJ. Evol. Biol16635646CrossRefPubMedGoogle Scholar
  53. Gee, P., Stephenson, D., Wright, D.E. 1994Temporal discrimination-learning of operant feeding in goldfish (Carassius auratus)J. Exp. Anal. Behav62113Google Scholar
  54. Gendron, R.P. 1986Searching for cryptic prey: evidence for optimal search rates and the formation of search images in quail (Colinus virginianus)Anim. Behav34898912Google Scholar
  55. Gendron, R.P. 1987Models and mechanisms of frequency-dependent predationAm. Nat130603623CrossRefGoogle Scholar
  56. Gendron, R.P., Staddon, J. 1983Searching for cryptic prey: the effects of search rateAm. Nat121172186CrossRefGoogle Scholar
  57. Gigord, L.D.B., Macnair, M.R., Smithson, A. 2001Negative frequency-dependent selection maintains a dramatic flower color polymorphism in the rewardless orchid Dactylorhiza sambucina (L.) SooProc. Nat. Acad. Sci9862536255CrossRefPubMedGoogle Scholar
  58. Gillespie, R.G., Oxford, G.S. 1998Selection on the colour polymorphism in Hawaiian happy-face spiders: evidence from genetic structure and temporal fluctuationsEvolution52775783Google Scholar
  59. Gillespie, R.G., Tabashnik, B.E. 1990Maintaining a happy face: stable color polymorphism in the spider Theridion grallator (Araneae, Theridiidae)Heredity656774Google Scholar
  60. Glanville, P.W., Allen, J.A. 1997Protective polymorphism in populations of computer-simulated moth-like preyOikos80565571Google Scholar
  61. Goulson, D. 2000Are insects flower constant because they use search images to find flowers?Oikos88547552CrossRefGoogle Scholar
  62. Greenwood, J.J.D. 1969Apostatic selection and population densityHeredity24157161Google Scholar
  63. Greenwood, J.J.D. 1984The functional basis of frequency-dependent food selectionBiol. J. Linn. Soc23177199Google Scholar
  64. Greenwood, J.J.D. 1985Frequency-dependent selection by seed-predatorsOikos44195210Google Scholar
  65. Greenwood, J.J.D., Elton, R.A. 1979Analysing experiments on frequency-dependent selection by predatorsJ. Anim. Ecol48721737Google Scholar
  66. Greenwood, J.J.D., Wood, E.M., Batchelor, S. 1981Apostatic selection of distasteful preyHeredity472734Google Scholar
  67. Greenwood, J.J.D., Cotton, P.A., Wilson, D.A. 1989Frequency-dependent selection on aposematic prey: some experimentsBiol. J. Linn. Soc36213226Google Scholar
  68. Grether, G.F., Millie, D.F., Bryant, M.J., Reznick, D.N., Mayea, W. 2001Rain forest canopy cover, resource availability, and life history evolution in guppiesEcology8215461559Google Scholar
  69. Guilford, T., Dawkins, M.S. 1987Search images not proven: a reappraisal of some recent evidenceAnim. Behav3518381845Google Scholar
  70. Haldane, J.B.S. 1955On the biochemistry of heterosis, and the stability of polymorphismProc. Roy. Soc. Lond. B144217220Google Scholar
  71. Harvey, P.H., Jordan, C.A., Allen, J.A. 1974Selection behaviour of wild blackbirds at high prey densitiesHeredity32401404PubMedGoogle Scholar
  72. Holling, C.S. 1959The components of predation as revealed by a study of small-mammal predation of the European pine sawflyCan. Entomol91293320Google Scholar
  73. Holt, R.D. 1984Spatial heterogeneity, indirect interactions and the coexistence of prey speciesAm. Nat124377406CrossRefGoogle Scholar
  74. Horsley, D.T., Lynch, B.M., Greenwood, J.J.D., Hardman, B., Mosley, S. 1979Frequency-dependent selection by birds when the density of prey is highJ. Anim. Ecol48483490Google Scholar
  75. Houde, A.E. 1992Sex-linked heritability of a sexually selected character in a natural population of Poecilia reticulataHeredity69229235Google Scholar
  76. Hughes, K.A., Linh, D., Rodd, F.H., Reznick, D.N. 1999Familiarity leads to female mate preference for novel males in the guppy, Poecilia reticulataAnim. Behav5819CrossRefPubMedGoogle Scholar
  77. Hughes, R.N., Croy, M.I. 1993An experimental analysis of frequency-dependent predation (switching) in the 15-spined stickleback, Spinachia spinachiaJ. Anim. Ecol62341352Google Scholar
  78. Jones, J.S., Leith, B., Rawlings, B. 1977Polymorphism in Cepaea – a problem with too many solutionsAnn. Rev. Ecol. Syst8109143CrossRefGoogle Scholar
  79. Joron, M., Mallett, J. 1998Diversity in mimicry: paradox or paradigm?Trends Ecol. Evol13461466CrossRefGoogle Scholar
  80. Jormalainen, V., Merilaita, S., Tuomi, J. 1995Differential predation on sexes affects color polymorphism of the isopod Idotea baltica (Pallas)Biol. J. Linn Soc554568CrossRefGoogle Scholar
  81. Kono, H., Reid, P.J., Kamil, A.C. 1998The effect of background cuing on prey detectionAnim. Behav56963972CrossRefPubMedGoogle Scholar
  82. Krebs, J.R. 1973

    Behavioural aspects of predation

    Bateson, P.P.G.Klopfer, P.H. eds. Perspectives in EthologyPlenum PressNew York-London73111
    Google Scholar
  83. Kunzler, R., Bakker, T.C.M. 2001Female preferences for single and combined traits in computer animated stickleback malesBehav. Ecol12681685CrossRefGoogle Scholar
  84. Langley, C.M. 1996Search images: selective attention to specific visual features of preyJ. Exp. Psych. Anim. Behav. Proc22152163CrossRefGoogle Scholar
  85. Langley, C.M., Riley, D.A., Bond, A.B., Goel, N. 1996Visual search for natural grains in pigeons (Columba livia): search images and selective attentionJ. Exp. Psych. Anim. Behav. Proc22139151CrossRefGoogle Scholar
  86. Lawrence, E.S. 1985Evidence for search image in blackbirds Turdus merula: long-term learningAnim. Behav3313011309Google Scholar
  87. Lawrence, E.S., Allen, J.A. 1983On the term ‘search image’Oikos40313314Google Scholar
  88. Lewontin, R.C. 1974The genetic basis of evolutionary changeColumbia University PressNew YorkGoogle Scholar
  89. Li, C.C. 1962On ‘reflexive selection’Science136262263MathSciNetGoogle Scholar
  90. Lindström, L., Alatalo, R.V., Lyytinen, A., Mappes, J. 2001Strong antiapostatic selection against novel rare aposematic preyProc. Natl. Acad. Sci. USA9891819184CrossRefPubMedGoogle Scholar
  91. MacDougall, A., Dawkins, M.S. 1998Predator discrimination and the benefits of Mullerian mimicryAnim. Behav5512811288CrossRefPubMedGoogle Scholar
  92. Mallet, J., Joron, M. 1999Evolution of diversity in warning colour and mimicry: polymorphisms, shifting balance, and speciationAnnu. Rev. Ecol. Syst30201233CrossRefGoogle Scholar
  93. Manly, B.F.J. 1972Tables for the analysis of selective predation experimentsRes. Pop. Ecol147481Google Scholar
  94. Manly, B.F.J. 1973A linear model for frequency-dependent selection by predatorsRes. Pop. Ecol14137150Google Scholar
  95. Manly, B.F.J. 1974A model for certain types of selection experimentsBiometrics30281294Google Scholar
  96. Manly, B.F.J., Miller, P., Cook, L.M. 1972Analysis of a selective predation experimentAm. Nat106719736CrossRefGoogle Scholar
  97. Mappes, J., Alatalo, R.V. 1997Effects of novelty and gregariousness in survival of aposematic preyBehav. Ecol8174177Google Scholar
  98. Marples, N.M., Roper, T.J., Harper, D.G.C. 1998Responses of wild birds to novel prey: evidence of dietary conservatismOikos83161165Google Scholar
  99. May, R.M. 1977Predators that switchNature269103104CrossRefPubMedGoogle Scholar
  100. Merilaita, S., Tuomi, J., Jormalainen, V. 1999Optimisation of cryptic colorations in heterogeneous habitatsBiol. J. Linn. Soc67151161CrossRefGoogle Scholar
  101. Merilaita, S., Lyytinen, A., Mappes, J. 2001Selection for cryptic coloration in a visually heterogeneous habitatProc. Roy. Soc. Lond. B26819251929CrossRefGoogle Scholar
  102. Moment, G.B. 1962Reflexive selection: a possible answer to an old puzzleScience136262263MathSciNetGoogle Scholar
  103. Morgan, R.A., Brown, J.S. 1996Using giving-up densities to detect search imagesAm. Nat14810591074CrossRefGoogle Scholar
  104. Morris, M.R., Nicoletto, P.F., Hesselman, E. 2003A polymorphism in female preference for a polymorphic male trait in the swordtail Xiphophorus corteziAnim. Behav654552CrossRefGoogle Scholar
  105. Murdoch, W.W. 1969Switching in general predators: experiments on predator specificity and stability of prey populationsEcol. Monogr39335353Google Scholar
  106. Murdoch, W.W., Oaten, A. 1975Predation and population stabilityAdv. Ecol. Res91131Google Scholar
  107. Murdoch, W.W., Avery, S., Smyth, M.B. 1975Switching in predatory fishEcology5610941105Google Scholar
  108. Owen, D.F., Whiteley, D. 1986Reflexive selection: moment’s hypothesis resurrectedOikos47117120Google Scholar
  109. Owen, D.F., Whitely, D. 1989Evidence that reflexive polymorphisms are maintained by visual selection by predatorsOikos55130133Google Scholar
  110. Owen, D.F., Wiegert, R.G. 1962Balanced polymorphism in the meadow spittle-bug Philaenus spumariusAm. Nat96353359CrossRefGoogle Scholar
  111. Parkyn, D.C., Austin, J.D., Hawryshyn, C.W. 2003Acquisition of polarized-light orientation in salmonids under laboratory conditionsAnim. Behav65893904CrossRefGoogle Scholar
  112. Paulson, D.R. 1973Predator polymorphism and apostatic selectionEvolution27269277Google Scholar
  113. Pietrewicz, A.T., Kamil, A.C. 1977Visual detection of cryptic prey by Blue Jays (Cyanocitta cristata)Science195580582Google Scholar
  114. Pietrewicz, A.T., Kamil, A.C. 1979Search image formation in the Blue Jay (Cyanocitta cristata)Science20413321333Google Scholar
  115. Plaisted, K.C. 1997The effect of interstimulus interval on the discrimination of cryptic targetsJ. Exp. Psych. Anim. Behav. Proc23248259CrossRefGoogle Scholar
  116. Plaisted, K.C., Mackintosh, N.J. 1995Visual search for cryptic stimuli in pigeons: implications for the search image and search rate hypothesesAnim. Behav5012191232CrossRefGoogle Scholar
  117. Popham, E.J. 1941The variation in the colour of certain species of Arctocorisa (Hemiptera, Corixidae) and its significanceProc. Zool. Soc. Lond. A111135172Google Scholar
  118. Poulton, E.B. 1884Notes upon, or suggested by, the colours, markings, and protective attitudes of certain lepidopterous larvae and pupae, and of a hymenopterous larvaTrans. Entomol. Soc. Lond18842760Google Scholar
  119. Pyke, G.H., Pulliam, H.R., Charnov, E.L. 1977Optimal foraging: a selective review of theory and testsQuart. Rev. Biol52137154CrossRefGoogle Scholar
  120. Rausher, M.D. 1978Search image for leaf shape in a butterflyScience20010711073Google Scholar
  121. Rees, G., Frith, C.D., Lavie, N. 1997Modulating irrelevant motion perception by varying attentional load in an unrelated taskScience27816161619CrossRefPubMedGoogle Scholar
  122. Reid, D.G. 1987Natural selection for apostasy and crypsis acting on the shell polymorphism of a mangrove snail, Littoraria filosa (Sowerby) (Gastropoda: Littorinidae)Biol. J. Linn. Soc30124Google Scholar
  123. Reid, P.J., Shettleworth, S.J. 1992Detection of cryptic prey: search image or search rate?J. Exp. Psych. Anim. Behav. Proc18273286CrossRefGoogle Scholar
  124. Reznick, D.N., Butler, M.J.,IV, Rodd, F.H., Ross, P.N. 1996Life history evolution in guppies (Poecilia reticulata) 6: differential mortality as a mechanism for natural selectionEvolution5016511660Google Scholar
  125. Reznick, D.N., Shaw, F.H., Rodd, F.H., Shaw, R.G. 1997Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata)Science27519341937CrossRefPubMedGoogle Scholar
  126. Reznick, D.N., Butler, M.J.,IV, Rodd, F.H 2001Life history evolution in guppies 7: the comparative ecology of high and low predation environmentsAm. Nat157126140CrossRefGoogle Scholar
  127. Rodd, F.H., Reznick, D.N 1997Variation in the demography of guppy populations: the importance of predation and life historiesEcology78405418Google Scholar
  128. Rohwer, S 1983Formalizing the avoidance-image hypothesis: critique of an earlier predictionAuk100971974Google Scholar
  129. Roughgarden, J., Feldman, M 1975Species packing and predation pressureEcology56489492Google Scholar
  130. Rowland, W.J 1999Studying visual cues in fish behavior: a review of ethological techniques. 1999Environ. Biol. Fishes56285305CrossRefGoogle Scholar
  131. Royama, T 1970Factors governing the hunting behaviour and selection of food by the great tit (Parus major L.)J. Anim. Ecol39619659Google Scholar
  132. Sevenster, P., FeuthBrujin, E., Huisman, J.J. 1995Temporal structure in stickleback behaviourBehaviour13212671284pt. 15–16Google Scholar
  133. Sherratt, T.N., Harvey, I.F. 1993Frequency-dependent food selection by arthropods: a reviewBiol. J. Linn. Soc48167186CrossRefGoogle Scholar
  134. Sherratt, T.N., MacDougall, A.D. 1995Some population consequences of variation in preference among individual predatorsBiol. J. Linn. Soc5593107CrossRefGoogle Scholar
  135. Shigemiya, Y. 2004Reversible frequency-dependent predation of a puffer, Takifugu niphobles (Pisces: Tetraodontidae), related to spatial distribution of colour-polymorphic preyBiol. J. Linn. Soc8197202CrossRefGoogle Scholar
  136. Smithson, A., MacNair, M.R. 1997Negative frequency-dependent selection by pollinators on artificial flowers without rewardsEvolution51715723Google Scholar
  137. Spinks, J.A., Zhang, J.X., Fox, P.T., Gao, J.H., Tan, L.H 2004More workload on the central executive of working memory, less attention capture by novel visual distractors: evidence from an fMRI studyNeuroImage23517524CrossRefPubMedGoogle Scholar
  138. Thompson, T. 1966Operant and classically-conditioned aggressive behaviour in Siamese fighting fishAm. Zool66291966PubMedGoogle Scholar
  139. Thompson, V. 1984Polymorphism under apostatic and aposematic selectionHeredity53677686Google Scholar
  140. Tinbergen, L. 1960The natural control of insects in pinewoods. Factors influencing the intensity of predation by songbirdsArch. Neer. Zool13265343Google Scholar
  141. Weale, M.E., Allen, J.A 1989Massive polymorphism – how do we test for frequency-dependence?Oikos55133134Google Scholar
  142. Weale, M.E., Whitwell, D., Raison, H.E., Raymond, D.L., Allen, J.A 2000The influence of density on frequency-dependent food selection: a comparison of four experiments with wild birdsOecologia124391395CrossRefGoogle Scholar
  143. Whiteley, D.A.A., Owen, D.F., Smith, D.A.S 1997Massive polymorphism and natural selection in Donacilla cornea (Poll, 1791) (Bivalvia: Mesodesmatidae)Biol. J. Linn. Soc62475494CrossRefGoogle Scholar
  144. Willis, A.J., McEwan, J.W.T., Greenwood, J.J.D., Elton, R.A. 1980Food selection by chicks-effects of color, density and frequency of food typesAnim. Behav28874879Google Scholar
  145. Winge, O 1922One-sided masculine and sex-linked inheritance in Lebistes reticulatusJ. Genet12145162Google Scholar
  146. Winge, O., Ditlevsen, E. 1947Colour inheritance and sex-determination in LebistesHeredity16583Google Scholar
  147. Wright, S 1948On the roles of directed and random changes in gene frequency in the genetics of natural populationsEvolution2279294Google Scholar
  148. Vane-Wright, R.I., Ackery, P.R., Smiles, R.L. 1975The distribution, polymorphism and mimicry of Heliconius telesiphe (Doubleday) and the species of Podotricha Michener (Lepidoptera: Heliconiinae)Trans. Roy. Entomol. Soc. Lond126611636Google Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  • David Punzalan
    • 1
  • F. Helen Rodd
    • 1
  • Kimberly A. Hughes
    • 2
  1. 1.Department of ZoologyUniversity of TorontoOntarioCanada
  2. 2.Department of Animal BiologyUniversity of Illinois at Urbana-ChampaignUrbanaUSA

Personalised recommendations