1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Entomology
  4. Volume 53, 2008
  5. Article

Annual Review of Entomology

Volume 53, 2008

Evolutionary Biology of Insect Learning

Abstract

Learning and memory, defined as the acquisition and retention of neuronal representations of new information, are ubiquitous among insects. Recent research indicates that a variety of insects rely extensively on learning for all major life activities including feeding, predator avoidance, aggression, social interactions, and sexual behavior. There is good evidence that individuals within an insect species exhibit genetically based variation in learning abilities and indirect evidence linking insect learning to fitness. Although insects rely on innate behavior to successfully manage many types of variation and unpredictability, learning may be superior to innate behavior when dealing with features unique to time, place, or individuals. Among insects, social learning, which can promote the rapid spread of novel behaviors, is currently known only from a few well-studied examples in social Hymenoptera. The prevalence and importance of social learning in insects are still unknown. Similarly, we know little about ecological factors that may have promoted enhanced learning abilities in insects, and whether learning has significantly contributed to speciation in insects.

Keyword(s): bees, ecology, evolution, fruit flies, grasshoppers, memory
Loading

Article metrics loading...

/content/journals/10.1146/annurev.ento.53.103106.093343
2008-01-07
2025-04-20
Loading full text...

Full text loading...

/deliver/fulltext/en/53/1/annurev.ento.53.103106.093343.html?itemId=/content/journals/10.1146/annurev.ento.53.103106.093343&mimeType=html&fmt=ahah

Literature Cited

  1. Abisgold JD, Simpson SJ. 1.  1988. The effect of dietary-protein levels and hemolymph composition on the sensitivity of the maxillary palp chemoreceptors of locusts. J. Exp. Biol. 135:215–29 [Google Scholar]
  2. Aceves-Pina EO, Quinn WG. 2.  1979. Learning in normal and mutant Drosophila larvae. Science 206:93–96 [Google Scholar]
  3. Alcock J. 3.  2005. Animal Behavior Sunderland, MA: Sinauer, 8th. ed. [Google Scholar]
  4. Alexander RD, Marshall DC, Cooley JR. 4.  1997. Evolutionary perspectives on insect mating. The Evolution of Mating Systems in Insects and Arachnids JC Choe, BJ Crespi 4–31 New York: Cambridge Univ. Press [Google Scholar]
  5. Alloway TM. 5.  1972. Learning and memory in insects. Annu. Rev. Entomol. 17:43–56 [Google Scholar]
  6. Anderson JR. 6.  2000. Learning and Memory New York: Wiley [Google Scholar]
  7. Andersson M. 7.  1994. Sexual Selection Princeton, NJ: Princeton Univ. Press [Google Scholar]
  8. Armstrong JD, de-Belle JS, Wang ZS, Kaiser K. 8.  1998. Metamorphosis of the mushroom bodies: large-scale rearrangements of the neural substrates for associative learning and memory in Drosophila. Learn. Mem. 5:102–14 [Google Scholar]
  9. Baldwin JM. 9.  1896. A new factor in evolution. Am. Nat. 30:441–51 [Google Scholar]
  10. Barron AB, Corbet SH. 10.  1999. Preimaginal conditioning in Drosophila revisited. Anim. Behav. 58:621–28 [Google Scholar]
  11. Barrows EM, Bell WJ, Michener CD. 11.  1975. Individual odor differences and their social functions in insects. Proc. Natl. Acad. Sci. USA 72:2824–28 [Google Scholar]
  12. Bateman AJ. 12.  1948. Intra-sexual selection in Drosophila. Heredity 2:349–68 [Google Scholar]
  13. Beekman M, Ratnieks FLW. 13.  2000. Long-range foraging by the honeybee, Apis mellifera L. Funct. Ecol. 14:490–96 [Google Scholar]
  14. Behmer ST, Elias DO, Bernays EA. 14.  1999. Post-ingestive feedbacks and associative learning regulate the intake of unsuitable sterols in a generalist grasshopper. J. Exp. Biol. 202:739–48 [Google Scholar]
  15. Brandes C. 15.  1991. Genetic differences in learning behavior in honeybees (Apis mellifera capensis). Behav. Genet. 21:271–94 [Google Scholar]
  16. Brandes C, Frisch B, Menzel R. 16.  1988. Time-course of memory formation differs in honey bee lines selected for good and poor learning. Anim. Behav. 36:981–85 [Google Scholar]
  17. Burns JG, Thomson JD. 17.  2006. A test of spatial memory and movement patterns of bumblebees at multiple spatial and temporal scales. Behav. Ecol. 17:48–55 [Google Scholar]
  18. Butcher LM, Kennedy JKJ, Plomin R. 18.  2006. Generalist genes and cognitive neuroscience. Curr. Opin. Neurobiol. 16:145–51 [Google Scholar]
  19. Capaldi EA, Smith AD, Osborne JL, Fahrbach SE, Farris SM et al.19.  2000. Ontogeny of orientation flight in the honeybee revealed by harmonic radar. Nature 403:537–40 [Google Scholar]
  20. Cartar RV. 20.  2004. Resource-tracking by bumble bees: responses to plant-level differences in quality. Ecology 85:2764–71 [Google Scholar]
  21. Chandra SBC, Hosler JS, Smith BH. 21.  2000. Heritable variation for latent inhibition and its correlation with reversal learning in honeybees (Apis mellifera). J. Comp. Psychol. 114:86–97 [Google Scholar]
  22. Chapman RF. 22.  1998. The Insects Cambridge, UK: Cambridge Univ. Press [Google Scholar]
  23. Collett TS, Collett M. 23.  2002. Memory use in insect visual navigation. Nat. Rev. Neurosci. 3:542–52 [Google Scholar]
  24. Coyne JA, Orr HA. 24.  1989. Patterns of speciation in Drosophila. Evolution 43:362–81 [Google Scholar]
  25. Davis RL. 25.  2005. Olfactory memory formation in Drosophila: from molecular to systems neuroscience. Annu. Rev. Neurosci. 28:275–302 [Google Scholar]
  26. Dornhaus A, Chittka L. 26.  1999. Evolutionary origins of bee dances. Nature 401:38 [Google Scholar]
  27. Dubnau J, Chiang A-S, Tully T. 27.  2003. Neural substrates of memory: from synapse to system. J. Neurobiol. 54:238–53 [Google Scholar]
  28. Dubnau J, Tully T. 28.  1998. Gene discovery in Drosophila: new insights for learning and memory. Annu. Rev. Neurosci. 21:407–44 [Google Scholar]
  29. Dudai Y. 29.  2002. Memory from A to Z: Keywords, Concepts, and Beyond Oxford: Oxford Univ. Press [Google Scholar]
  30. Dukas R. 30.  1998. Constraints on information processing and their effects on behavior. Cognitive Ecology R Dukas 89–127 Chicago: Univ. Chicago Press [Google Scholar]
  31. Dukas R. 31.  1998. Evolutionary ecology of learning. Cognitive Ecology R Dukas 129–74 Chicago: Univ. Chicago Press [Google Scholar]
  32. Dukas R. 32.  1999. Costs of memory: ideas and predictions. J. Theor. Biol. 197:41–50 [Google Scholar]
  33. Dukas R. 33.  1999. Ecological relevance of associative learning in fruit fly larvae. Behav. Ecol. Sociobiol. 45:195–200 [Google Scholar]
  34. Dukas R. 34.  2004. Evolutionary biology of animal cognition. Annu. Rev. Ecol. Evol. Syst. 35:347–74 [Google Scholar]
  35. Dukas R. 35.  2004. Male fruit flies learn to avoid interspecific courtship. Behav. Ecol. 15:695–98 [Google Scholar]
  36. Dukas R. 36.  2005. Experience improves courtship in male fruit flies. Anim. Behav. 69:1203–9 [Google Scholar]
  37. Dukas R. 37.  2005. Learning affects mate choice in female fruit flies. Behav. Ecol. 16:800–4One in a series of papers documenting the adaptive significance of learning in the context of sexual behavior in insects. [Google Scholar]
  38. Dukas R. 38.  2006. Learning in the context of sexual behavior in insects. Anim. Biol. 56:125–41 [Google Scholar]
  39. Dukas R, Bernays EA. 39.  2000. Learning improves growth rate in grasshoppers. Proc. Natl. Acad. Sci. USA 97:2637–40 [Google Scholar]
  40. Dukas R, Clark CW, Abbott K. 40.  2006. Courtship strategies of male insects: When is learning advantageous?. Anim. Behav. 72:1395–404 [Google Scholar]
  41. Dukas R, Visscher PK. 41.  1994. Lifetime learning by foraging honey bees. Anim. Behav. 48:1007–12 [Google Scholar]
  42. Dyer FC. 42.  1998. Cognitive ecology of navigation. Cognitive Ecology R Dukas 201–60 Chicago: Univ. Chicago Press [Google Scholar]
  43. Dyer FC. 43.  2002. The biology of the dance language. Annu. Rev. Entomol. 47:917–49 [Google Scholar]
  44. Eisenbach M, Lengeler JW. 44.  2004. Chemotaxis London: Imperial College Press499 pp. [Google Scholar]
  45. Ejima A, Smith BPC, Lucas C, Levine JD, Griffith LC. 45.  2005. Sequential learning of pheromonal cues modulates memory consolidation in trainer-specific associative courtship conditioning. Curr. Biol. 15:194–206 [Google Scholar]
  46. Fabre J-H, Teixeira de Mattos A, Miall B. 46.  1918. The Wonders of Instinct New York: The Century Co322 pp. [Google Scholar]
  47. Farina WM, Gruter C, Diaz PC. 47.  2005. Social learning of floral odours inside the honeybee hive. Proc. R. Soc. London Sci. Ser. B 272:1923–28 [Google Scholar]
  48. Folkers E. 48.  1982. Visual learning and memory of Drosophila melanogaster wild type C—S and the mutants dunce1, amnesiac, turnip and rutabaga. J. Insect Physiol. 28:535–39 [Google Scholar]
  49. Franks NR, Richardson T. 49.  2006. Teaching in tandem-running ants. Nature 439:153The first report of teaching in a nonhuman animal. [Google Scholar]
  50. Free JB. 50.  1970. Insect Pollination of Crops London: Academic [Google Scholar]
  51. Free JB. 51.  1987. Pheromones of Social Bees London: Chapman and Hall [Google Scholar]
  52. Galef BG, Laland KN. 52.  2005. Social learning in animals: empirical studies and theoretical models. Bioscience 55:489–99 [Google Scholar]
  53. Gandolfi M, Mattiacci L, Dorn S. 53.  2003. Preimaginal learning determines adult response to chemical stimuli in a parasitic wasp. Proc. R. Soc. London B 270:2623–29 [Google Scholar]
  54. Gerber B, Scherer S, Neuser K, Michels B, Hendel T et al.54.  2004. Visual learning in individually assayed Drosophila larvae. J. Exp. Biol. 207:179–88 [Google Scholar]
  55. Gould JL. 55.  1975. Honey bee recruitment. Science 189:685–93 [Google Scholar]
  56. Hall JC. 56.  1994. The mating of a fly. Science 264:1702–14 [Google Scholar]
  57. 57.  Heyes CM, Galef BG. 1996. Social Learning in Animals San Diego, CA: Academic [Google Scholar]
  58. Holliday M, Hirsch J. 58.  1986. A comment on the evidence for learning in Diptera. Behav. Genet. 16:439–47 [Google Scholar]
  59. 59.  Howard DJ, Berlocher SH. 1998. Endless Forms: Species and Speciation New York: Oxford Univ. Press470 pp. [Google Scholar]
  60. Jaenike J. 60.  1982. Environmental modification of oviposition behavior in Drosophila. Am. Nat. 119:784–802 [Google Scholar]
  61. Koshland D. 61.  1980. Bacterial Chemotaxis as a Model Behavioral System New York: Raven [Google Scholar]
  62. Kovas Y, Plomin R. 62.  2006. Generalist genes: implications for the cognitive sciences. Trends Cogn. Sci. 10:198–203 [Google Scholar]
  63. Laverty TM. 63.  1994. Bumble bee learning and flower morphology. Anim. Behav. 47:531–45 [Google Scholar]
  64. Leadbeater E, Chittka L. 64.  2005. A new mode of information transfer in foraging bumblebees?. Curr. Biol. 15:R447–R48 [Google Scholar]
  65. Lee JC, Bernays EA. 65.  1990. Food tastes and toxic effects: associative learning by the polyphagous grasshopper Schistocerca americana (Drury) (Orthoptera: Acrididae). Anim. Behav. 39:163–73 [Google Scholar]
  66. Lefebvre L, Whittle P, Lascaris E, Finkelstein A. 66.  1997. Feeding innovations and forebrain size in birds. Anim. Behav. 53:549–60 [Google Scholar]
  67. Lehrer M. 67.  1993. Why do bees turn back and look?. J. Comp. Physiol. A 172:549–63 [Google Scholar]
  68. Lewis WL, Takasu K. 68.  1990. Use of learned odours by a parasitic wasp in accordance with host and food needs. Nature 348:635–36 [Google Scholar]
  69. Linn C, Feder JL, Nojima S, Dambroski HR, Berlocher SH, Roelofs W. 69.  2003. Fruit odor discrimination and sympatric host race formation in Rhagoletis. Proc. Natl. Acad. Sci. USA 100:11490–93 [Google Scholar]
  70. Liu G, Seiler H, Wen A, Zars T, Ito K et al.70.  2006. Distinct memory traces for two visual features in the Drosophila brain. Nature 439:551–56 [Google Scholar]
  71. Lofdahl KL, Holliday M, Hirsch J. 71.  1992. Selection for conditionability in Drosophila melanogaster. J. Comp. Psychol. 106:172–83 [Google Scholar]
  72. Manoli DS, Meissner GW, Baker BS. 72.  2006. Blueprints for behavior: genetic specification of neural circuitry for innate behaviors. Trends Neurosci. 29:444–51 [Google Scholar]
  73. Markow TA. 73.  1988. Reproductive behavior of Drosophila melanogaster and D. nigrospiracula in the field and in the laboratory. J. Comp. Psychol. 102:169–73 [Google Scholar]
  74. Mayr E. 74.  1963. Animal Species and Evolution Cambridge, MA: Harvard Univ. Press [Google Scholar]
  75. Mayr E. 75.  1974. Behavior programs and evolutionary strategies. Am. Sci. 62:650–59 [Google Scholar]
  76. McGuire TR, Hirsch J. 76.  1977. Behavior genetic analysis of Formia regina: conditioning, reliable individual differences, and selection. Proc. Natl. Acad. Sci. USA 74:5193–97 [Google Scholar]
  77. Menzel R, Erber J, Masuhr T. 77.  1974. Learning and memory in the honeybee. Experimental Analysis of Insect Behavior L Barton-Browne 195–217 Berlin: Springer-Verlag [Google Scholar]
  78. Menzel R, Muller U. 78.  1996. Learning and memory in honeybees: from behavior to neural substrates. Annu. Rev. Neurosci. 19:379–404 [Google Scholar]
  79. Mery F, Kawecki TJ. 79.  2002. Experimental evolution of learning ability in fruit flies. Proc. Natl. Acad. Sci. USA 99:14274–79 [Google Scholar]
  80. Mery F, Kawecki TJ. 80.  2003. A fitness cost of learning ability in Drosophila melanogaster. Proc. R. Soc. London Sci. Ser. B 270:2465–69 [Google Scholar]
  81. Mery F, Kawecki TJ. 81.  2004. An operating cost of learning in Drosophila melanogaster. Anim. Behav. 68:589–98 [Google Scholar]
  82. Mery F, Kawecki TJ. 82.  2005. A cost of long-term memory in Drosophila. Science 308:1148One in a series of papers quantifying the cost of learning. [Google Scholar]
  83. Minckley RL, Wcislo WT, Yanega D, Buchmann SL. 83.  1994. Behavior and phenology of a specialist bee (Dieunomia) and sunflower (Helianthus) pollen availability. Ecology 75:1406–19 [Google Scholar]
  84. Nuttley WM, Atkinson-Leadbeater KP, van der Kooy D. 84.  2002. Serotonin mediates food-odor associative learning in the nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 99:12449–54 [Google Scholar]
  85. Olson DJ, Kamil AC, Balda RP, Nims PJ. 85.  1995. Performance of four seed-caching corvid species in operant tests of nonspatial and spatial memory. J. Comp. Psychol. 109:173–81 [Google Scholar]
  86. Papaj DR, Lewis AC. 86.  1993. Insect Learning New York: Chapman and Hall [Google Scholar]
  87. Papaj DR, Prokopy RJ. 87.  1989. Ecological and evolutionary aspects of learning in phytophagous insects. Annu. Rev. Entomol. 34:315–50 [Google Scholar]
  88. Papaj DR, Vet LEM. 88.  1990. Odor learning and foraging success in the parasitoid, Leptopilina heterotoma. J. Chem. Ecol. 16:3137–49 [Google Scholar]
  89. Quinn WG, Harris WA, Benzer S. 89.  1974. Conditioned behavior in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 71:708–12 [Google Scholar]
  90. Ratcliffe JM, Fenton MB, Galef BG. 90.  2003. An exception to the rule: Common vampire bats do not learn taste aversions. Anim. Behav. 65:385–89 [Google Scholar]
  91. Raubenheimer D, Tucker D. 91.  1997. Associative learning by locusts: pairing of visual cues with consumption of protein and carbohydrate. Anim. Behav. 54:1449–59 [Google Scholar]
  92. Ray S. 92.  1999. Survival of olfactory memory through metamorphosis in the fly Musca domestica. Neurosci. Lett. 259:37–40 [Google Scholar]
  93. Reader SM, Laland KN. 93.  2002. Social intelligence, innovation, and enhanced brain size in primates. Proc. Natl. Acad. Sci. USA 99:4436–41 [Google Scholar]
  94. Reinhardt JF. 94.  1952. Some responses of honey bees to alfalfa flowers. Am. Nat. 86:257–75 [Google Scholar]
  95. Riley JR, Greggers U, Smith AD, Reynolds DR, Menzel R. 95.  2005. The flight paths of honeybees recruited by the waggle dance. Nature 435:205–7 [Google Scholar]
  96. Rosenthal R, Fode KL. 96.  1963. The effect of experimenter bias on the performance of the albino rat. Behav. Sci. 8:183–89 [Google Scholar]
  97. Schippers M-P, Dukas R, Smith RW, Wang J, Smolen K, McClelland GB. 97.  2006. Lifetime performance in foraging honeybees: behaviour and physiology. J. Exp. Biol. 209:3828–36 [Google Scholar]
  98. Seeley TD. 98.  1996. The Wisdom of the Hive Cambridge, MA: Harvard Univ. Press [Google Scholar]
  99. Siegel RW, Hall JC. 99.  1979. Conditioned courtship in Drosophila and its mediation by association of chemical cues. Proc. Natl. Acad. Sci. USA 76:3430–34 [Google Scholar]
  100. Simpson SJ, Raubenheimer D. 100.  2000. The hungry locust. Adv. Study Behav. 29:1–44 [Google Scholar]
  101. Smid HM, Wang G, Bukovinszky T, Steidle JLM, Bleeker MAK et al.101.  2007. Species-specific acquisition and consolidation of long-term memory in parasitic wasps. Proc. R. Soc. London Ser. B 274:1539–46 [Google Scholar]
  102. Spieth HT. 102.  1974. Courtship behavior in Drosophila. Annu. Rev. Entomol. 19:383–406 [Google Scholar]
  103. Staddon JER. 103.  1983. Adaptive Behavior and Learning Cambridge, MA: Cambridge Univ. Press [Google Scholar]
  104. Strausfeld NJ, Hansen L, Li YS, Gomez RS, Ito K. 104.  1998. Evolution, discovery, and interpretations of arthropod mushroom bodies. Learn. Mem. 5:11–37 [Google Scholar]
  105. Tautz J, Sandeman DC. 105.  2003. Recruitment of honeybees to nonscented food sources. J. Comp. Physiol. A 189:293–300 [Google Scholar]
  106. Tempel BL, Bonini N, Dawson DR, Quinn WG. 106.  1983. Reward learning in normal and mutant Drosophila. Proc. Natl. Acad. Sci. USA 80:1482–86 [Google Scholar]
  107. Thornton A, McAuliffe K. 107.  2006. Teaching in wild meerkats. Science 313:227–29 [Google Scholar]
  108. Thorpe W, Jones F. 108.  1937. Olfactory conditioning in a parasitic insect and its relation to the problem of host selection. Proc. R. Soc. London Sci. Ser. B 124:56–81 [Google Scholar]
  109. Tibbetts EA. 109.  2002. Visual signals of individual identity in the wasp Polistes fuscatus. Proc. R. Soc. London Sci. Ser. B 269:1423–28 [Google Scholar]
  110. Tully T. 110.  1996. Discovery of genes involved with learning and memory: an experimental synthesis of Hirschian and Benzerian perspectives. Proc. Natl. Acad. Sci. USA 93:13460–67 [Google Scholar]
  111. Tully T, Cambiazo V, Kruse L. 111.  1994. Memory through metamorphosis in normal and mutant Drosophila. J. Neurosci. 14:68–74 [Google Scholar]
  112. Vet LEM, Lewis WJ, Carde RT. 112.  1995. Parasitoid foraging and learning. Chemical Ecology of Insects 2 RT Carde, WJ Bell 65–101 New York: Chapman and Hall [Google Scholar]
  113. Visscher PK, Seeley TD. 113.  1982. Foraging strategy of honeybee colonies in a temperate deciduous forest. Ecology 63:1790–801 [Google Scholar]
  114. von Frisch K. 114.  1967. The Dance Language and Orientation of Bees Cambridge, MA: Harvard Univ. Press [Google Scholar]
  115. Wackers FL, Lewis WJ. 115.  1999. A comparison of color-, shape- and pattern-learning by the hymenopteran parasitoid Microplitis croceipes. J. Comp. Physiol. A 184:387–93 [Google Scholar]
  116. Waddell S, Quinn WG. 116.  2001. Flies, genes, and learning. Annu. Rev. Neurosci. 24:1283–309 [Google Scholar]
  117. Wcislo WT. 117.  1987. The role of learning in the mating biology of a sweat bee Lasioglossum zephyrum (Hymenoptera, Halictidae). Behav. Ecol. Sociobiol. 20:179–85 [Google Scholar]
  118. Wertheim B, van Baalen E-JA, Dicke M, Vet LEM. 118.  2005. Pheromone-mediated aggregation in nonsocial arthropods: an evolutionary ecological perspective. Annu. Rev. Entomol. 50:321–46 [Google Scholar]
  119. West-Eberhard MJ. 119.  2003. Developmental Plasticity and Evolution Oxford: Oxford Univ. Press794 pp. [Google Scholar]
  120. Wolf R, Heisenberg M. 120.  1991. Basic organization of operant behavior as revealed in Drosophila flight orientation. J. Comp. Physiol. A 169:699–705 [Google Scholar]
  121. Worden BD, Papaj DR. 121.  2005. Flower choice copying in bumblebees. Biol. Lett. 1:504–7 [Google Scholar]
  122. Wright WG, Kirschman D, Rozen D, Maynard B. 122.  1996. Phylogenetic analysis of learning-related neuromodulation in molluscan mechanosensory neurons. Evolution 50:2248–63 [Google Scholar]
  123. Yurkovic A, Wang O, Basu AC, Kravitz EA. 123.  2006. Learning and memory associated with aggression in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA 103:17519–24A report suggesting learning-mediated individual recognition in fruit flies. [Google Scholar]
  124. Zhang Y, Lu H, Bargmann CI. 124.  2005. Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature 438:179–84A study suggesting associative learning in a classic simple model animal. [Google Scholar]
/content/journals/10.1146/annurev.ento.53.103106.093343
Loading
  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error