Population Ecology

, 52:15 | Cite as

Evolutionary ecology of learning: insights from fruit flies

  • Tadeusz J. Kawecki
Special Feature: Review Rapid Adaptation


Ecologically and evolutionarily oriented research on learning has traditionally been carried out on vertebrates and bees. While less sophisticated than those animals, fruit flies (Drosophila) are capable of several forms of learning, and have the advantage of a short generation time, which makes them an ideal system for experimental evolution studies. This review summarizes the insights into evolutionary questions about learning gained in the last decade from evolutionary experiments on Drosophila. These experiments demonstrate that Drosophila has the genetic potential to evolve a substantially improved learning performance in ecologically relevant learning tasks. In at least one set of selected populations, the improved learning generalized to a task other than that used to impose selection, involving a different behavior, different stimuli, and a different sensory channel for the aversive reinforcement. This improvement in learning ability was associated with reductions in other fitness-related traits, such as larval competitive ability and lifespan, pointing to evolutionary trade-offs for improved learning. These trade-offs were confirmed by other evolutionary experiments where a reduction in learning performance was observed as a correlated response to selection for tolerance to larval nutritional stress or for delayed aging. Such trade-offs could be one reason why fruit flies have not fully used up their evolutionary potential for learning. Finally, another evolutionary experiment with Drosophila provided the first direct evidence for the long-standing idea that learning can under some circumstances accelerate and in others slow down genetically based evolutionary change. These results demonstrate the usefulness of fruit flies as a model system to address evolutionary questions about learning.


Behavior Drosophila Experimental evolution Learning Memory Trade-offs 



This work reported here was supported by the Swiss National Science Foundation, the Roche Research Foundation and the Velux Foundation.


  1. Anderson RW (1995) Learning and evolution: a quantitative genetics approach. J Theor Biol 175:89–101CrossRefPubMedGoogle Scholar
  2. Baldwin JM (1896) A new factor in evolution. Am Nat 30(441–451):536–553CrossRefGoogle Scholar
  3. Beecher MD, Brenowitz EA (2005) Functional aspects of song learning in songbirds. Trends Ecol Evol 20:143–149CrossRefPubMedGoogle Scholar
  4. Bleeker MAK, Smid HM, Steidle JLM, Kruidhof HM, Van Loon JJA, Vet LEM (2006) Differences in memory dynamics between two closely related parasitoid wasp species. Anim Behav 71:1343–1350CrossRefGoogle Scholar
  5. Boesch C, Marchesi P, Marchesi N, Fruth B, Joulian F (1994) Is nut cracking in wild chimpanzees a cultural behavior. J Hum Evol 26:325–338CrossRefGoogle Scholar
  6. Bolhuis JJ (2005) Function and mechanism in neuroecology: looking for clues. Anim Biol 55:457–490CrossRefGoogle Scholar
  7. Borenstein E, Meilijson I, Ruppin E (2006) The effect of phenotypic plasticity on evolution in multipeaked fitness landscapes. J Evol Biol 19:1555–1570CrossRefPubMedGoogle Scholar
  8. Burger JMS, Kolss M, Pont J, Kawecki TJ (2008) Learning ability and longevity: a symmetrical evolutionary trade-off in Drosophila. Evolution 62:1294–1304CrossRefPubMedGoogle Scholar
  9. Chittka L, Thomson JD (1997) Sensori-motor learning and its relevance for task specialization in bumble bees. Behav Ecol Sociobiol 41:385–398CrossRefGoogle Scholar
  10. Davis RL (2005) Olfactory memory formation in Drosophila: from molecular to systems neuroscience. Annu Rev Neurosci 28:275–302CrossRefPubMedGoogle Scholar
  11. Dukas R (2004a) Evolutionary biology of animal cognition. Annu Rev Ecol Evol Syst 35:347–374CrossRefGoogle Scholar
  12. Dukas R (2004b) Male fruit flies learn to avoid interspecific courtship. Behav Ecol 15:695–698CrossRefGoogle Scholar
  13. Dukas R, Bernays EA (2000) Learning improves growth rate in grasshoppers. Proc Natl Acad Sci USA 97:2637–2640CrossRefPubMedGoogle Scholar
  14. Dyer AG, Rosa MGP, Reser DH (2008) Honeybees can recognise images of complex natural scenes for use as potential landmarks. J Exp Biol 211:1180–1186CrossRefPubMedGoogle Scholar
  15. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longman, HarlowGoogle Scholar
  16. Fontanari JF, Meir R (1990) The effect of learning on the evolution of asexual populations. Complex Syst 4:401–414Google Scholar
  17. Gittleman JL, Harvey PH (1980) Why are distasteful prey not cryptic? Nature 286:149–150CrossRefGoogle Scholar
  18. Healy SD, Braithwaite VA (2000) Cognitive ecology: a field of substance? Trends Ecol Evol 15:22–26CrossRefPubMedGoogle Scholar
  19. Hewitt JK, Fulker DW, Hewitt CA (1983) Genetic architecture of olfactory discriminative avoidance conditioning in Drosophila melanogaster. J Comp Psychol 97:52–58CrossRefPubMedGoogle Scholar
  20. Hinton GE, Nowlan SJ (1987) How learning can guide evolution. Complex Syst 1:495–502Google Scholar
  21. Ihalainen E, Lindstrom L, Mappes J, Puolakkainen S (2008) Can experienced birds select for Mullerian mimicry? Behav Ecol 19:362–368CrossRefGoogle Scholar
  22. Johnston TD (1982) Selective costs and benefits in the evolution of learning. Adv Study Behav 12:65–106CrossRefGoogle Scholar
  23. Kamil AC, Jones JE (1997) The seed-storing corvid Clark’s nutcracker learns geometric relationships among landmarks. Nature 390:276–279CrossRefGoogle Scholar
  24. Kolss M, Kawecki TJ (2008) Reduced learning ability as a consequence of evolutionary adaptation to nutritional stress in Drosophila melanogaster. Ecol Entomol 33:583–588CrossRefGoogle Scholar
  25. Kolss M, Kraaijeveld AR, Mery F, Kawecki TJ (2006) No trade-off between learning ability and parasitoid resistance in Drosophila melanogaster. J Evol Biol 19:1359–1363CrossRefPubMedGoogle Scholar
  26. Laughlin SB (2001) Energy as a constraint on the coding and processing of sensory information. Curr Opin Neurobiol 11:475–480CrossRefPubMedGoogle Scholar
  27. Lofdahl KL, Holliday M, Hirsch J (1992) Selection for conditionability in Drosophila melanogaster. J Comp Psychol 106:172–183CrossRefPubMedGoogle Scholar
  28. Macphail EM, Bolhuis JJ (2001) The evolution of intelligence: adaptive specialization versus general process. Biol Rev 76:341–364CrossRefPubMedGoogle Scholar
  29. Merkle T, Wehner R (2008) Landmark guidance and vector navigation in outbound desert ants. J Exp Biol 211:3370–3377CrossRefPubMedGoogle Scholar
  30. Mery F, Kawecki TJ (2002) Experimental evolution of learning ability in fruit flies. Proc Natl Acad Sci USA 99:14274–14279CrossRefPubMedGoogle Scholar
  31. Mery F, Kawecki TJ (2003) A fitness cost of learning ability in Drosophila melanogaster. Proc R Soc Lond B Biol Sci 270:2465–2469CrossRefGoogle Scholar
  32. Mery F, Kawecki TJ (2004) The effect of learning on experimental evolution of resource preference in Drosophila melanogaster. Evolution 58:757–767PubMedGoogle Scholar
  33. Mery F, Pont J, Preat T, Kawecki TJ (2007) Experimental evolution of olfactory memory in Drosophila melanogaster. Physiol Biochem Zool 80:399–405CrossRefPubMedGoogle Scholar
  34. Nakamichi M, Kato E, Kojima Y, Itoigawa N (1998) Carrying and washing of grass roots by free-ranging Japanese macaques at Katsuyama. Folia Primatol 69:35–40CrossRefPubMedGoogle Scholar
  35. Odling-Smee LC, Boughman JW, Braithwaite VA (2008) Sympatric species of three spine stickleback differ in their performance in a spatial learning task. Behav Ecol Sociobiol 62:1935–1945CrossRefGoogle Scholar
  36. Ohman A, Dimberg U (1978) Facial expressions as conditioned stimuli for electrodermal responses: case of preparedness. J Pers Soc Psychol 36:1251–1258CrossRefPubMedGoogle Scholar
  37. Ono Y, Hayashi I, Matsushima T (2002) Visual memory of shapes in quail chicks: discrimination among 2-dimensional objects. Zool Sci 19:719–725CrossRefPubMedGoogle Scholar
  38. Osborn HF (1896) Ontogenic and phylogenic variation. Science 4:786–789CrossRefPubMedGoogle Scholar
  39. Paenke I, Sendhoff B, Kawecki TJ (2007) Influence of plasticity and learning on evolution under directional selection. Am Nat 170:E47–E58CrossRefPubMedGoogle Scholar
  40. Papaj DR (1994) Optimizing learning and its effect on evolutionary change in behavior. In: Real LA (ed) Behavioral mechanisms in evolutionary biology. University of Chicago Press, Chicago, pp 133–154Google Scholar
  41. Potter DA, Held DW (1999) Absence of food-aversion learning by a polyphagous scarab, Popillia japonica, following intoxication by geranium, Pelargonium × hortorum. Entomol Exp Appl 91:83–88CrossRefGoogle Scholar
  42. Raine NE, Chittka L (2008) The correlation of learning speed and natural foraging success in bumble-bees. Proc R Soc Lond B Biol Sci 275:803–808CrossRefGoogle Scholar
  43. Reader SM, Laland KN (2002) Social intelligence, innovation, and enhanced brain size in primates. Proc Natl Acad Sci USA 99:4436–4441CrossRefPubMedGoogle Scholar
  44. Reif M, Linsenmair KE, Heisenberg M (2002) Evolutionary significance of courtship conditioning in Drosophila melanogaster. Anim Behav 63:143–155CrossRefGoogle Scholar
  45. Rescorla RA (1988) Behavioral studies of Pavlovian conditioning. Annu Rev Neurosci 11:329–352CrossRefPubMedGoogle Scholar
  46. Roff DA, Fairbairn DJ (2007) The evolution of trade-offs: where are we? J Evol Biol 20:433–447CrossRefPubMedGoogle Scholar
  47. Schlichting CD, Pigliucci M (1998) Phenotypic evolution. A reaction norm perspective. Sinauer, SunderlandGoogle Scholar
  48. Seppanen JT, Forsman JT (2007) Interspecific social learning: novel preference can be acquired from a competing species. Curr Biol 17:1248–1252CrossRefPubMedGoogle Scholar
  49. Shettleworth SJ (1999) Cognition, evolution, and behavior. Oxford University Press, OxfordGoogle Scholar
  50. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  51. Wittman AB, Wall LL (2007) The evolutionary origins of obstructed labor: bipedalism, encephalization, and the human obstetric dilemma. Obstet Gynecol Surv 62:739–748CrossRefPubMedGoogle Scholar

Copyright information

© The Society of Population Ecology and Springer 2009

Authors and Affiliations

  1. 1.Department of Ecology and EvolutionUniversity of LausanneLausanneSwitzerland

Personalised recommendations