Evolutionary Ecology

, Volume 24, Issue 3, pp 571–583 | Cite as

Behavioural plasticity: an interaction between evolution and experience

  • Frederic MeryEmail author
  • James G. Burns
Original Paper


Animals adjust their behaviour in response to complex environmental conditions. This form of plasticity requires the formation of association between information and an appropriate behavioural response. Such a connection is the result of a complex interaction between evolutionary pre-programmed cue-response behaviour (innate behavioural response) and cumulated lifetime experience (learning). The evolution of learning and innate behavioural responses is likely to depend on their respective fitness costs and benefits. However, as natural selection will indirectly affect each form through global behavioural plasticity, it is critical to understand how each form interacts with the other. The inclusion of innate behavioural plasticity and learning in behaviour is likely to result in more than the mere sum of each plastic form. In this review we investigate the costs and benefits of learning and innate behavioural responses and the effect of one on the other in their evolution. We highlight the need for more explicit study of the interaction between innate behavioural response and learning in natural systems for a better understanding of behavioural plasticity.


Information Costs Benefits Environmental heterogeneity 



We thank N. Kohn and C. Reaume for useful comments on the manuscript. The work was supported by an ATIP Grant from the Life Sciences Division of the Centre National de la Recherche Scientifique and from the European Research Council under the European Community’s Seventh Framework Programme (FP7/2007–2013)/ERC Grant agreement no 209540.


  1. Ackley D, Littman M (1990) Interactions between learning and evolution. In: Langton CG, Taylor C, Farmer JD, Rasmussen S (eds) 2nd workshop on artificial life. Santa Fe, Nm, pp 487–509Google Scholar
  2. Ancel LW (2000) Undermining the Baldwin expediting effect: does phenotypic plasticity accelerate evolution? Theor Popul Biol 58:307–319CrossRefPubMedGoogle Scholar
  3. Anderson RW (1995) Learning and evolution: a quantitative genetics approach. J Theor Biol 175:89–101CrossRefPubMedGoogle Scholar
  4. Attwell D, Laughlin SB (2001) An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21:1133–1145CrossRefPubMedGoogle Scholar
  5. Baldwin JM (1896) A new factor in evolution. Am Nat 30:441–451CrossRefGoogle Scholar
  6. Barrickman NL, Bastian ML, Isler K, van Schaik CP (2008) Life history costs and benefits of encephalization: a comparative test using data from long-term studies of primates in the wild. J Hum Evol 54:568–590CrossRefPubMedGoogle Scholar
  7. Bateson P, Mameli M (2007) The innate and the acquired: useful clusters or a residual distinction from folk biology? Dev Psychobiol 49:818–831CrossRefPubMedGoogle Scholar
  8. Belew RK (1989) When both individuals and populations search: Adding simple learning to the genetic algorithm. In: Schaffer JD, Fairfax VA (eds) 3rd International Conf on Genetic Algorithms, pp 34–41Google Scholar
  9. Berrigan D, Scheiner SM (2004) Modeling the evolution of phenotypic plasticity. In: DeWitt TJ, Scheiner SM (eds) Phenotypic plasticity: functional and conceptual approaches. Oxford University Press, Oxford, pp 82–97Google Scholar
  10. Biegler R, McGregor A, Krebs JR, Healy SD (2001) A larger hippocampus is associated with longer-lasting spatial memory. Proc Natl Acad Sci USA 98:6941–6944CrossRefPubMedGoogle Scholar
  11. Bolhuis JJ (1991) Mechanisms of avian imprinting: a review. Biol Rev Camb Philos Soc 66:303–345CrossRefPubMedGoogle Scholar
  12. Bolles RC (1970) Species-specific defense reactions and avoidance learning. Psychol Rev 77:32–48CrossRefGoogle Scholar
  13. Bourret RB, Stock AM (2002) Molecular information processing: lessons from bacterial chemotaxis. J Biol Chem 277:9625–9628CrossRefPubMedGoogle Scholar
  14. Boyd R, Richerson PJ (1985) Culture and the evolutionary process. University of Chicago Press, ChicagoGoogle Scholar
  15. Boyd R, Richerson PJ (1988) The evolution of reciprocity in sizable groups. J Theor Biol 132:337–356CrossRefPubMedGoogle Scholar
  16. Brelands K, Brelands M (1961) The misbehavior of organisms. Am Psychol 16:681–684CrossRefGoogle Scholar
  17. Brown C, Laland KN (2003) Social learning in fishes: a review. Fish Fish 4:280–288Google Scholar
  18. Burns JG, Rodd FH (2008) Hastiness, brain size and predation regime affect the performance of wild guppies in a spatial memory task. Anim Behav 76:911–922CrossRefGoogle Scholar
  19. Changizi MA (2003) Relationship between number of muscles, behavioral repertoire size, and encephalization in mammals. J Theor Biol 220:157–168CrossRefPubMedGoogle Scholar
  20. Crusio WE, Schwegler H, Brust I (1993) Covariations between hippocampal mossy fibres and working and reference memory in spatial and non-spatial radial maze tasks in mice. Eur J Neurosci 5:1413–1420CrossRefPubMedGoogle Scholar
  21. Dall SRX, Cuthill IC (1997) The information costs of generalism. Oikos 80:197–202CrossRefGoogle Scholar
  22. Davies NB, Madden JR, Butchart SHM, Rutila J (2006) A host-race of the cuckoo Cuculus canorus with nestlings attuned to the parental alarm calls of the host species. Proc R Soc B Biol Sci 273:693–699CrossRefGoogle Scholar
  23. de Meester L (1996) Evolutionary potential and local genetic differentiation in a phenotypically plastic trait of a cyclical parthenogen, daphnia magna. Evolution 50:1293–1298CrossRefGoogle Scholar
  24. DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81CrossRefGoogle Scholar
  25. Domjam M, Wilson NE (1972) Specificity of cue to consequence in aversion learning in the rat. Psychon Sci 26:143–145Google Scholar
  26. Dukas R (1998a) Cognitive ecology. University of Chicago Press, ChicagoGoogle Scholar
  27. Dukas R (1998b) Evolutionary ecology of learning. In: Dukas R (ed) Cognitive ecology: the evolutionary ecology of information processing and decision making. University of Chicago Press, Chicago, pp 129–174Google Scholar
  28. Dukas R (1999) Costs of memory: ideas and predictions. J Theor Biol 197:41–50CrossRefPubMedGoogle Scholar
  29. Dukas R (2008) Learning decreases heterospecific courtship and mating in fruit flies. Biol Lett 4:645–647CrossRefPubMedGoogle Scholar
  30. Fuller JL (1979) Fuller BWS lines: history and results. In: Hahn ME, Jensen C, Dudek BC (eds) Development and evolution of brain size: behavioral implications. Academic Press, New York, pp 187–204Google Scholar
  31. Galef BG, Whiskin EE (2001) Interaction of social and individual learning in food preferences of Norway rats. Anim Behav 62:41–46CrossRefGoogle Scholar
  32. Garcia J, Koelling RA (1966) Relation of cue to consequence in avoidance learning. Psychon Sci 4:123–124Google Scholar
  33. Girvan JR, Braithwaite VA (1998) Population differences in spatial learning in three-spined sticklebacks. Proc R Soc Biol Sci Ser B 265:913–918CrossRefGoogle Scholar
  34. Grant BR, Grant PR (1996) Cultural inheritance of song and its role in the evolution of Darwin’s finches. Evolution 50:2471–2487CrossRefGoogle Scholar
  35. Gronenberg W, Liebig J (1999) Smaller brains and optic lobes in reproductive workers of the ant Harpegnathos. Naturwissenschaften 86:343–345CrossRefGoogle Scholar
  36. Gumbert A (2000) Color choices by bumble bees (Bombus terrestris): innate preferences and generalization after learning. Behav Ecol Sociobiol 48:36–43CrossRefGoogle Scholar
  37. Haier R, Karama S, Leyba L, Jung R (2009) MRI assessment of cortical thickness and functional activity changes in adolescent girls following three months of practice on a visual-spatial task. BMC Res Notes 2:174CrossRefPubMedGoogle Scholar
  38. Healy SD, Rowe C (2007) A critique of comparative studies of brain size. Proc R Soc B Biol Sci 274:453–464CrossRefGoogle Scholar
  39. Heyes CM (1994) Social learning in animals: categories and mechanisms. Biol Rev 69:207–231CrossRefPubMedGoogle Scholar
  40. Hinton GE, Nowlan SJ (1987) How learning can guide evolution. Complex Systems 1:495–502Google Scholar
  41. Hourcade B, Perisse E, Devaud J-M, Sandoz J-C (2009) Long-term memory shapes the primary olfactory center of an insect brain. Learn Mem 16:607–615CrossRefPubMedGoogle Scholar
  42. Isabel G, Pascual A, Preat T (2004) Exclusive consolidated memory phases in Drosophila. Science 304:1024–1027CrossRefPubMedGoogle Scholar
  43. Isler K, van Schaik CP (2006) Metabolic costs of brain size evolution. Biol Lett 2:557–560CrossRefPubMedGoogle Scholar
  44. Iwaniuk AN, Nelson JE (2003) Developmental differences are correlated with relative brain size in birds: a comparative analysis. Can J Zool 81:1913–1928CrossRefGoogle Scholar
  45. Jachner A (2001) Anti-predator behaviour of naive compared with experienced juvenile roach. J Fish Biol 59:1313–1322Google Scholar
  46. Jacobs LF, Gaulin SJC, Sherry DF, Hoffman GE (1990) Evolution of spatial cognition—sex-specific patterns of spatial-behaviour predict hippocampal size. Proc Natl Acad Sci USA 87:6349–6352CrossRefPubMedGoogle Scholar
  47. Jensen C (1979) Learning performance in mice genetically selected for brain weight: Problems of generality. In: Hahn ME, Jensen C, Dudek BC (eds) Development and evolution of brain size: behavioral implications. Academic Press, New York, pp 205–220Google Scholar
  48. Johnston TD (1982) Selective costs and benefits in the evolution of learning. Adv Study Behav 12:65–106CrossRefGoogle Scholar
  49. Julian GE, Gronenberg W (2002) Reduction of brain volume correlates with behavioral changes in queen ants. Brain Behav Evol 60:152–164CrossRefPubMedGoogle Scholar
  50. Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394Google Scholar
  51. Lachlan RF, Servedio MR (2004) Song learning accelerates allopatric speciation. Evolution 58:2049–2063PubMedGoogle Scholar
  52. Laughlin SB (2001) Energy as a constraint on the coding and processing of sensory information. Curr Opin Neurobiol 11:475–480CrossRefPubMedGoogle Scholar
  53. Laughlin SB, van Steveninck RRD, Anderson JC (1998) The metabolic cost of neural information. Nat Neurosci 1:36–41CrossRefPubMedGoogle Scholar
  54. Laverty TM, Plowright RC (1988) Flower handling by bumblebees: a comparison of specialists and generalists. Anim Behav 36:733–740CrossRefGoogle Scholar
  55. Lefebvre L, Giraldeau LA (1996) Is social learning an adaptive specialization? In: Galef BG, Heyes CM (eds) Social learning in animals: the roots of culture. Academic Press, New York, pp 107–128CrossRefGoogle Scholar
  56. Magurran AE (1986) The development of shoaling behavior in the European minnow, Phoxinus phoxinus. J Fish Biol 29:159–169CrossRefGoogle Scholar
  57. Marino L (2005) Big brains do matter in new environments. Proc Natl Acad Sci USA 102:5306–5307CrossRefPubMedGoogle Scholar
  58. Mayley G (1997) Guiding or hiding: explorations into the effects of learning on the rate of evolution. In: Husbands P, Harvey I (eds) 4th European conference on artificial life (ECAL97). Brighton, England, pp 135–144Google Scholar
  59. Mery F, Kawecki TJ (2002) Experimental evolution of learning ability in fruit flies. Proc Natl Acad Sci USA 99:14274–14279CrossRefPubMedGoogle Scholar
  60. Mery F, Kawecki TJ (2004a) The effect of learning on experimental evolution of resource preference in Drosophila melanogaster. Evolution 58:757–767PubMedGoogle Scholar
  61. Mery F, Kawecki TJ (2004b) An operating cost of learning in Drosophila melanogaster. Anim Behav 68:589–598CrossRefGoogle Scholar
  62. Mery F, Kawecki TJ (2005) A cost of long-term memory in Drosophila. Science 308:1148CrossRefPubMedGoogle Scholar
  63. Moran NA (1992) The evolutionary maintenance of alternative phenotypes. Am Nat 139:971–989CrossRefGoogle Scholar
  64. Morgan CL (1896) On modification and variation. Science 4:733–740CrossRefPubMedGoogle Scholar
  65. Moscovitch A, Lolordo VM (1968) Role of safety in pavlovian backward fear conditioning procedure. J Comp Physiol Psychol 66: 673Google Scholar
  66. Nelson DA (2000) A preference for own-subspecies’ song guides vocal learning in a song bird. Proc Natl Acad Sci USA 97:13348–13353CrossRefPubMedGoogle Scholar
  67. Niven JE, Anderson JC, Laughlin SB (2007) Fly photoreceptors demonstrate energy-information trade-offs in neural coding. PLoS Biol 5:828–840CrossRefGoogle Scholar
  68. Odling-Smee L, Braithwaite VA (2003) The influence of habitat stability on landmark use during spatial learning in the three-spined stickleback. Anim Behav 65:701–707CrossRefGoogle Scholar
  69. Papaj DR (1994) Optimizing learning and its effects on evolutionary change. In: Real L (ed) Behavioral mechanisms in evolutionary ecology. University of Chicago Press, Chicago, pp 133–153Google Scholar
  70. Papaj DR, Prokopy RJ (1989) Ecological and evolutionary aspects of learning in phytophagous insects. Annu Rev Entomol 34:315–350CrossRefGoogle Scholar
  71. Pigliucci M (2005) Evolution of phenotypic plasticity: where are we going now? Trends Ecol Evol 20:481–486CrossRefPubMedGoogle Scholar
  72. Pitnick S, Jones KE, Wilkinson GS (2006) Mating system and brain size in bats. Proc R Soc B Biol Sci 273:719–724CrossRefGoogle Scholar
  73. Podos J, Huber SK, Taft B (2004) Bird song: the interface of evolution and mechanism. Annu Rev Ecol Evol Syst 35:55–87CrossRefGoogle Scholar
  74. Pravosudov VV, Clayton NS (2002) A test of the adaptive specialization hypothesis: population differences in caching, memory, and the hippocampus in black—capped chickadees (Poecile atricapilla). Behav Neurosci 116:515–522CrossRefPubMedGoogle Scholar
  75. Ratcliffe JM, Fenton MB, Galef BG (2003) An exception to the rule: common vampire bats do not learn taste aversions. Anim Behav 65:385–389CrossRefGoogle Scholar
  76. Relyea RA (2001) The relationship between predation risk and antipredator responses in larval anurans. Ecology 82:541–554CrossRefGoogle Scholar
  77. Reznick DN, Ghalambor CK (2005) Selection in nature: experimental manipulations of natural populations. Integr Comp Biol 45:456–462CrossRefGoogle Scholar
  78. Riffell JA, Alarcon R, Abrell L, Davidowitz G, Bronstein JL, Hildebrand JG (2008) Behavioral consequences of innate preferences and olfactory learning in hawkmoth-flower interactions. Proc Natl Acad Sci USA 105:3404–3409CrossRefPubMedGoogle Scholar
  79. Robinson BW, Dukas R (1999) The influence of phenotypic modifications on evolution: the Baldwin effect and modern perspectives. Oikos 85:582–589CrossRefGoogle Scholar
  80. Rosenzweig MR, Bennett EL (1996) Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav Brain Res 78:57–65CrossRefPubMedGoogle Scholar
  81. Roudez RJ, Glover T, Weis JS (2008) Learning in an invasive and a native predatory crab. Biol Invasions 10:1191–1196CrossRefGoogle Scholar
  82. Sacher GA, Staffeldt EF (1974) Relation of gestation time to brain weight for placental mammals: implications for theory of vertebrate growth. Am Nat 108:593–615CrossRefGoogle Scholar
  83. Sasaki K, Fox SF, Duvall D (2009) Rapid evolution in the wild: changes in body size, life-history traits, and behavior in hunted populations of the Japanese mamushi snake. Conserv Biol 23:93–102CrossRefPubMedGoogle Scholar
  84. Sherry DF, Hoshooley JS (2009) The seasonal hippocampus of food-storing birds. Behav Processes 80:334–338CrossRefPubMedGoogle Scholar
  85. Shettleworth SJ (1998) Cognition, evolution, and behavior. Oxford University Press, New YorkGoogle Scholar
  86. Smid HM, Bukovinszky T, Wang G, Steidle JLM, Bleeker MAK, van Loon JJA, Vet LEM (2007) Species-specific acquisition and consolidation of long-term memory in parasitic wasps. Proc R Soc Biol Sci Ser B 274:1539–1546CrossRefGoogle Scholar
  87. Snell-Rood EC, Papaj DR (2009) Patterns of phenotypic plasticity in common and rare environments: a study of host use and color learning in the cabbage white butterfly Pieris rapae. Am Nat 173:615–631CrossRefPubMedGoogle Scholar
  88. Snell-Rood EC, Papaj DR, Gronenberg W (2009) Brain size: a global or induced cost of learning? Brain Behav Evol 73:111–128CrossRefPubMedGoogle Scholar
  89. Sokoloff L (1960) The metabolism of the central nervous system in vivo. In: Field L, Magoun H, Hall VE (eds) Handbook of physiology. American Physiological Society, Washington, pp 1843–1864Google Scholar
  90. Sol D (2009) Revisiting the cognitive buffer hypothesis for the evolution of large brains. Biol Lett 5:130–133CrossRefPubMedGoogle Scholar
  91. Sol D, Duncan RP, Blackburn TM, Cassey P, Lefebvre L (2005) Big brains, enhanced cognition, and response of birds to novel environments. Proc Natl Acad Sci USA 102:5460–5465CrossRefPubMedGoogle Scholar
  92. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  93. Stephens D (1991) Change, regularity, and value in the evolution of animal learning. Behav Ecol 2:77–89CrossRefGoogle Scholar
  94. Sullivan KA (1988) Age-specific profitability and prey choice. Anim Behav 36:613–615CrossRefGoogle Scholar
  95. Tanimoto H, Heisenberg M, Gerber B (2004) Event timing turns punishment to reward. Nature 430:983CrossRefPubMedGoogle Scholar
  96. Turner AM, Fetterolf SA, Bernot RJ (1999) Predator identity and consumer behavior: differential effects of fish and crayfish on the habitat use of a freshwater snail. Oecologia 118:242–247CrossRefGoogle Scholar
  97. Van Buskirk J (2002) Phenotypic lability and the evolution of predator-induced plasticity in tadpoles. Evolution 56:361–370PubMedGoogle Scholar
  98. van Praag H, Kempermann G, Gage FH (2000) Neural consequences of environmental enrichment. Nat Rev Neurosci 1:191–198CrossRefPubMedGoogle Scholar
  99. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New YorkGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  1. 1.Laboratoire Evolution Génome et Spéciation, UPR9034Centre National de la Recherche Scientifique and Université Paris-Sud 11Gif sur Yvette CedexFrance

Personalised recommendations