[go: up one dir, main page]
More Web Proxy on the site http://driver.im/ Skip to main content
Springer Nature Link
Log in

Behavioural plasticity: an interaction between evolution and experience

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
£29.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • 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 487–509

    Google Scholar 

  • Ancel LW (2000) Undermining the Baldwin expediting effect: does phenotypic plasticity accelerate evolution? Theor Popul Biol 58:307–319

    Article  CAS  PubMed  Google Scholar 

  • Anderson RW (1995) Learning and evolution: a quantitative genetics approach. J Theor Biol 175:89–101

    Article  CAS  PubMed  Google Scholar 

  • Attwell D, Laughlin SB (2001) An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 21:1133–1145

    Article  CAS  PubMed  Google Scholar 

  • Baldwin JM (1896) A new factor in evolution. Am Nat 30:441–451

    Article  Google Scholar 

  • 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 54:568–590

    Article  PubMed  Google Scholar 

  • Bateson P, Mameli M (2007) The innate and the acquired: useful clusters or a residual distinction from folk biology? Dev Psychobiol 49:818–831

    Article  PubMed  Google Scholar 

  • 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 34–41

  • 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 82–97

    Google Scholar 

  • Biegler R, McGregor A, Krebs JR, Healy SD (2001) A larger hippocampus is associated with longer-lasting spatial memory. Proc Natl Acad Sci USA 98:6941–6944

    Article  CAS  PubMed  Google Scholar 

  • Bolhuis JJ (1991) Mechanisms of avian imprinting: a review. Biol Rev Camb Philos Soc 66:303–345

    Article  CAS  PubMed  Google Scholar 

  • Bolles RC (1970) Species-specific defense reactions and avoidance learning. Psychol Rev 77:32–48

    Article  Google Scholar 

  • Bourret RB, Stock AM (2002) Molecular information processing: lessons from bacterial chemotaxis. J Biol Chem 277:9625–9628

    Article  CAS  PubMed  Google Scholar 

  • Boyd R, Richerson PJ (1985) Culture and the evolutionary process. University of Chicago Press, Chicago

    Google Scholar 

  • Boyd R, Richerson PJ (1988) The evolution of reciprocity in sizable groups. J Theor Biol 132:337–356

    Article  CAS  PubMed  Google Scholar 

  • Brelands K, Brelands M (1961) The misbehavior of organisms. Am Psychol 16:681–684

    Article  Google Scholar 

  • Brown C, Laland KN (2003) Social learning in fishes: a review. Fish Fish 4:280–288

    Google Scholar 

  • Burns JG, Rodd FH (2008) Hastiness, brain size and predation regime affect the performance of wild guppies in a spatial memory task. Anim Behav 76:911–922

    Article  Google Scholar 

  • Changizi MA (2003) Relationship between number of muscles, behavioral repertoire size, and encephalization in mammals. J Theor Biol 220:157–168

    Article  PubMed  Google Scholar 

  • 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 5:1413–1420

    Article  CAS  PubMed  Google Scholar 

  • Dall SRX, Cuthill IC (1997) The information costs of generalism. Oikos 80:197–202

    Article  Google Scholar 

  • 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 273:693–699

    Article  CAS  Google Scholar 

  • de Meester L (1996) Evolutionary potential and local genetic differentiation in a phenotypically plastic trait of a cyclical parthenogen, daphnia magna. Evolution 50:1293–1298

    Article  Google Scholar 

  • DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81

    Article  Google Scholar 

  • Domjam M, Wilson NE (1972) Specificity of cue to consequence in aversion learning in the rat. Psychon Sci 26:143–145

    Google Scholar 

  • Dukas R (1998a) Cognitive ecology. University of Chicago Press, Chicago

    Google Scholar 

  • 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 129–174

    Google Scholar 

  • Dukas R (1999) Costs of memory: ideas and predictions. J Theor Biol 197:41–50

    Article  CAS  PubMed  Google Scholar 

  • Dukas R (2008) Learning decreases heterospecific courtship and mating in fruit flies. Biol Lett 4:645–647

    Article  PubMed  Google Scholar 

  • 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 187–204

    Google Scholar 

  • Galef BG, Whiskin EE (2001) Interaction of social and individual learning in food preferences of Norway rats. Anim Behav 62:41–46

    Article  Google Scholar 

  • Garcia J, Koelling RA (1966) Relation of cue to consequence in avoidance learning. Psychon Sci 4:123–124

    Google Scholar 

  • Girvan JR, Braithwaite VA (1998) Population differences in spatial learning in three-spined sticklebacks. Proc R Soc Biol Sci Ser B 265:913–918

    Article  Google Scholar 

  • Grant BR, Grant PR (1996) Cultural inheritance of song and its role in the evolution of Darwin’s finches. Evolution 50:2471–2487

    Article  Google Scholar 

  • Gronenberg W, Liebig J (1999) Smaller brains and optic lobes in reproductive workers of the ant Harpegnathos. Naturwissenschaften 86:343–345

    Article  CAS  Google Scholar 

  • Gumbert A (2000) Color choices by bumble bees (Bombus terrestris): innate preferences and generalization after learning. Behav Ecol Sociobiol 48:36–43

    Article  Google Scholar 

  • 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 2:174

    Article  PubMed  Google Scholar 

  • Healy SD, Rowe C (2007) A critique of comparative studies of brain size. Proc R Soc B Biol Sci 274:453–464

    Article  Google Scholar 

  • Heyes CM (1994) Social learning in animals: categories and mechanisms. Biol Rev 69:207–231

    Article  CAS  PubMed  Google Scholar 

  • Hinton GE, Nowlan SJ (1987) How learning can guide evolution. Complex Systems 1:495–502

    Google Scholar 

  • 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 16:607–615

    Article  PubMed  Google Scholar 

  • Isabel G, Pascual A, Preat T (2004) Exclusive consolidated memory phases in Drosophila. Science 304:1024–1027

    Article  CAS  PubMed  Google Scholar 

  • Isler K, van Schaik CP (2006) Metabolic costs of brain size evolution. Biol Lett 2:557–560

    Article  PubMed  Google Scholar 

  • Iwaniuk AN, Nelson JE (2003) Developmental differences are correlated with relative brain size in birds: a comparative analysis. Can J Zool 81:1913–1928

    Article  Google Scholar 

  • Jachner A (2001) Anti-predator behaviour of naive compared with experienced juvenile roach. J Fish Biol 59:1313–1322

    Google Scholar 

  • 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 87:6349–6352

    Article  CAS  PubMed  Google Scholar 

  • 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 205–220

    Google Scholar 

  • Johnston TD (1982) Selective costs and benefits in the evolution of learning. Adv Study Behav 12:65–106

    Article  Google Scholar 

  • Julian GE, Gronenberg W (2002) Reduction of brain volume correlates with behavioral changes in queen ants. Brain Behav Evol 60:152–164

    Article  PubMed  Google Scholar 

  • Kats LB, Dill LM (1998) The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394

    Google Scholar 

  • Lachlan RF, Servedio MR (2004) Song learning accelerates allopatric speciation. Evolution 58:2049–2063

    CAS  PubMed  Google Scholar 

  • Laughlin SB (2001) Energy as a constraint on the coding and processing of sensory information. Curr Opin Neurobiol 11:475–480

    Article  CAS  PubMed  Google Scholar 

  • Laughlin SB, van Steveninck RRD, Anderson JC (1998) The metabolic cost of neural information. Nat Neurosci 1:36–41

    Article  CAS  PubMed  Google Scholar 

  • Laverty TM, Plowright RC (1988) Flower handling by bumblebees: a comparison of specialists and generalists. Anim Behav 36:733–740

    Article  Google Scholar 

  • 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 107–128

    Chapter  Google Scholar 

  • Magurran AE (1986) The development of shoaling behavior in the European minnow, Phoxinus phoxinus. J Fish Biol 29:159–169

    Article  Google Scholar 

  • Marino L (2005) Big brains do matter in new environments. Proc Natl Acad Sci USA 102:5306–5307

    Article  CAS  PubMed  Google Scholar 

  • 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 135–144

    Google Scholar 

  • Mery F, Kawecki TJ (2002) Experimental evolution of learning ability in fruit flies. Proc Natl Acad Sci USA 99:14274–14279

    Article  CAS  PubMed  Google Scholar 

  • Mery F, Kawecki TJ (2004a) The effect of learning on experimental evolution of resource preference in Drosophila melanogaster. Evolution 58:757–767

    PubMed  Google Scholar 

  • Mery F, Kawecki TJ (2004b) An operating cost of learning in Drosophila melanogaster. Anim Behav 68:589–598

    Article  Google Scholar 

  • Mery F, Kawecki TJ (2005) A cost of long-term memory in Drosophila. Science 308:1148

    Article  CAS  PubMed  Google Scholar 

  • Moran NA (1992) The evolutionary maintenance of alternative phenotypes. Am Nat 139:971–989

    Article  Google Scholar 

  • Morgan CL (1896) On modification and variation. Science 4:733–740

    Article  PubMed  CAS  Google Scholar 

  • Moscovitch A, Lolordo VM (1968) Role of safety in pavlovian backward fear conditioning procedure. J Comp Physiol Psychol 66: 673

    Google Scholar 

  • Nelson DA (2000) A preference for own-subspecies’ song guides vocal learning in a song bird. Proc Natl Acad Sci USA 97:13348–13353

    Article  CAS  PubMed  Google Scholar 

  • Niven JE, Anderson JC, Laughlin SB (2007) Fly photoreceptors demonstrate energy-information trade-offs in neural coding. PLoS Biol 5:828–840

    Article  CAS  Google Scholar 

  • Odling-Smee L, Braithwaite VA (2003) The influence of habitat stability on landmark use during spatial learning in the three-spined stickleback. Anim Behav 65:701–707

    Article  Google Scholar 

  • 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 133–153

    Google Scholar 

  • Papaj DR, Prokopy RJ (1989) Ecological and evolutionary aspects of learning in phytophagous insects. Annu Rev Entomol 34:315–350

    Article  Google Scholar 

  • Pigliucci M (2005) Evolution of phenotypic plasticity: where are we going now? Trends Ecol Evol 20:481–486

    Article  PubMed  Google Scholar 

  • Pitnick S, Jones KE, Wilkinson GS (2006) Mating system and brain size in bats. Proc R Soc B Biol Sci 273:719–724

    Article  Google Scholar 

  • Podos J, Huber SK, Taft B (2004) Bird song: the interface of evolution and mechanism. Annu Rev Ecol Evol Syst 35:55–87

    Article  Google Scholar 

  • 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 116:515–522

    Article  PubMed  Google Scholar 

  • Ratcliffe JM, Fenton MB, Galef BG (2003) An exception to the rule: common vampire bats do not learn taste aversions. Anim Behav 65:385–389

    Article  Google Scholar 

  • Relyea RA (2001) The relationship between predation risk and antipredator responses in larval anurans. Ecology 82:541–554

    Article  Google Scholar 

  • Reznick DN, Ghalambor CK (2005) Selection in nature: experimental manipulations of natural populations. Integr Comp Biol 45:456–462

    Article  Google Scholar 

  • 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 105:3404–3409

    Article  CAS  PubMed  Google Scholar 

  • Robinson BW, Dukas R (1999) The influence of phenotypic modifications on evolution: the Baldwin effect and modern perspectives. Oikos 85:582–589

    Article  Google Scholar 

  • Rosenzweig MR, Bennett EL (1996) Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav Brain Res 78:57–65

    Article  CAS  PubMed  Google Scholar 

  • Roudez RJ, Glover T, Weis JS (2008) Learning in an invasive and a native predatory crab. Biol Invasions 10:1191–1196

    Article  Google Scholar 

  • Sacher GA, Staffeldt EF (1974) Relation of gestation time to brain weight for placental mammals: implications for theory of vertebrate growth. Am Nat 108:593–615

    Article  Google Scholar 

  • 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 23:93–102

    Article  PubMed  Google Scholar 

  • Sherry DF, Hoshooley JS (2009) The seasonal hippocampus of food-storing birds. Behav Processes 80:334–338

    Article  PubMed  Google Scholar 

  • Shettleworth SJ (1998) Cognition, evolution, and behavior. Oxford University Press, New York

    Google Scholar 

  • 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 274:1539–1546

    Article  Google Scholar 

  • 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 173:615–631

    Article  PubMed  Google Scholar 

  • Snell-Rood EC, Papaj DR, Gronenberg W (2009) Brain size: a global or induced cost of learning? Brain Behav Evol 73:111–128

    Article  PubMed  Google Scholar 

  • 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 1843–1864

    Google Scholar 

  • Sol D (2009) Revisiting the cognitive buffer hypothesis for the evolution of large brains. Biol Lett 5:130–133

    Article  PubMed  Google Scholar 

  • 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 102:5460–5465

    Article  CAS  PubMed  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Stephens D (1991) Change, regularity, and value in the evolution of animal learning. Behav Ecol 2:77–89

    Article  Google Scholar 

  • Sullivan KA (1988) Age-specific profitability and prey choice. Anim Behav 36:613–615

    Article  Google Scholar 

  • Tanimoto H, Heisenberg M, Gerber B (2004) Event timing turns punishment to reward. Nature 430:983

    Article  CAS  PubMed  Google Scholar 

  • 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 118:242–247

    Article  Google Scholar 

  • Van Buskirk J (2002) Phenotypic lability and the evolution of predator-induced plasticity in tadpoles. Evolution 56:361–370

    PubMed  Google Scholar 

  • van Praag H, Kempermann G, Gage FH (2000) Neural consequences of environmental enrichment. Nat Rev Neurosci 1:191–198

    Article  PubMed  CAS  Google Scholar 

  • West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New York

    Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Laboratoire Evolution Génome et Spéciation, UPR9034, Centre National de la Recherche Scientifique and Université Paris-Sud 11, 91198, Gif sur Yvette Cedex, France

    Frederic Mery & James G. Burns

Authors
  1. Frederic Mery
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. James G. Burns
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Frederic Mery.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mery, F., Burns, J.G. Behavioural plasticity: an interaction between evolution and experience. Evol Ecol 24, 571–583 (2010). https://doi.org/10.1007/s10682-009-9336-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-009-9336-y

Keywords

Search

Navigation