Skip to main content Accessibility help
×
Hostname: page-component-76fb5796d-r6qrq Total loading time: 0 Render date: 2024-04-26T11:06:56.216Z Has data issue: false hasContentIssue false

5 - Evolutionary Processes Shaping Learning Ability in Insects

from Part I - Evolution of Learning Processes

Published online by Cambridge University Press:  26 May 2022

Mark A. Krause
Affiliation:
Southern Oregon University
Karen L. Hollis
Affiliation:
Mount Holyoke College, Massachusetts
Mauricio R. Papini
Affiliation:
Texas Christian University
Get access

Summary

Insects demonstrate an impressive repertoire of learned behaviors and are specifically suitable for studies on evolutionary processes because of their high fecundity and short life span. In this chapter I focus on the evolutionary processes that shape learning ability in insects on the relatively short-term evolutionary scale. For cognitive traits and behavior to evolve under direct natural selection the following requirements must be met: (1) variation in cognitive ability between individuals, (2) this variation is heritable, and (3) this variation is related to fitness (reproduction or survival) in specific environments. First, I describe natural variation in learning ability and how this variation can be maintained in natural populations. Second, I discuss work on heritability of cognition, as well as related studies on artificial selection and experimental evolution. Finally, I discuss the benefits and costs of learning in relation to fitness.

Type
Chapter
Information
Publisher: Cambridge University Press
Print publication year: 2022

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Boogert, N. J., Madden, J. R., Morand-Ferron, J., & Thornton, A. (2018). Measuring and understanding individual differences in cognition. Philosophical Transactions of the Royal Society B, 373(1756), 110. http://dx.doi.org/10.1098/rstb.2017.0280Google Scholar
Brandes, C. (1988). Estimation of heritability of learning behavior in honeybees (Apis mellifera capensis). Behavior Genetics, 18(1), 119132. https://doi.org/10.1007/BF01067081Google Scholar
de Bruijn, J. A. C., Vet, L. E. M., & Smid, H. M. (2018). Costs of persisting unreliable memory: Reduced foraging efficiency for free-flying parasitic wasps in a wind tunnel. Frontiers in Ecology and Evolution, 6(160), 19. https://doi.org/10.3389/fevo.2018.00160Google Scholar
Burger, J. M. S., Kolss, M., Pont, J., & Kawecki, T. J. (2008). Learning ability and longevity: A symmetrical evolutionary trade-off in Drosophila. Evolution, 62(6), 12941304. https://doi.org/10.1111/j.1558-5646.2008.00376.xGoogle Scholar
Callahan, H. S., Maughan, H., & Steiner, U. K. (2008). Phenotypic plasticity, costs of phenotypes, and costs of plasticity: Toward an integrative view. Annals of the New York Academy of Sciences, 1133, 4466. https://doi.org/10.1196/annals.1438.008CrossRefGoogle ScholarPubMed
Chandra, S. B. C., Hunt, G. J., Cobey, S., & Smith, B. H. (2001). Quantitative trait loci associated with reversal learning and latent inhibition in honeybees (Apis mellifera). Behavior Genetics, 31(3), 275285. https://doi.org/10.1023/A:1012227308783CrossRefGoogle ScholarPubMed
Cheng, K., & Wignall, A. E. (2006). Honeybees (Apis mellifera) holding on to memories: Response competition causes retroactive interference effects. Animal Cognition, 9(2), 141150. https://doi.org/10.1007/s10071-005-0012-5Google Scholar
Christiansen, I. C., Szin, S., & Schausberger, P. (2016). Benefit-cost trade-offs of early learning in foraging predatory mites Amblyseius swirskii. Scientific Reports, 6(23571), 111. https://doi.org/10.1038/srep23571Google Scholar
Croston, R., Branch, C. L., Kozlovsky, D. Y., Dukas, R., & Pravosudov, V. V. (2015). Heritability and the evolution of cognitive traits. Behavioral Ecology, 26(6), 14471459. https://doi.org/10.1093/beheco/arv088Google Scholar
Darwin, C. (1859). On the origin of species. John Murray.Google Scholar
DeWitt, T. J., Sih, A., & Wilson, D. S. (1998). Costs and limits of phenotypic plasticity. Trends in Ecology & Evolution, 13(2), 7781. https://doi.org/10.1016/S0169-5347(97)01274-3Google Scholar
Dougherty, L. R., & Guillette, L. M. (2018). Linking personality and cognition: A meta-analysis. Philosophical Transactions of the Royal Society B: Biological Sciences, 373(1756), 112. https://doi.org/10.1098/rstb.2017.0282Google Scholar
Dukas, R. (2008a). Evolutionary biology of insect learning. Annual Review of Entomology, 53, 145160. https://doi.org/10.1146/annurev.ento.53.103106.093343Google Scholar
Dukas, R. (2008b). Learning decreases heterospecific courtship and mating in fruit flies. Biology Letters, 4(6), 645647. https://doi.org/10.1098/rsbl.2008.0437CrossRefGoogle ScholarPubMed
Dukas, R., & Bernays, E. A. (2000). Learning improves growth rate in grasshoppers. Proceedings of the National Academy of Sciences, 97(6), 26372640. https://doi.org/10.1073/pnas.050461497CrossRefGoogle ScholarPubMed
Dukas, R., & Duan, J. J. (2000). Potential fitness consequences of associative learning in a parasitoid wasp. Behavioral Ecology, 11, 536543. https://doi.org/10.1093/beheco/11.5.536Google Scholar
Dunlap, A. S., Austin, M. W., & Figueiredo, A. (2019). Components of change and the evolution of learning in theory and experiment. Animal Behaviour, 147, 157166. https://doi.org/10.1016/j.anbehav.2018.05.024CrossRefGoogle Scholar
Dunlap, A. S., & Stephens, D. W. (2014). Experimental evolution of prepared learning. Proceedings of the National Academy of Sciences, 111(32), 1175011755. https://doi.org/10.1073/pnas.1404176111Google Scholar
Dunlap, A. S., & Stephens, D. W. (2016). Reliability, uncertainty, and costs in the evolution of animal learning. Current Opinion in Behavioral Sciences, 12, 7379. https://doi.org/10.1016/j.cobeha.2016.09.010Google Scholar
Eliassen, S., Jørgensen, C., Mangel, M., & Giske, J. (2017). Exploration or exploitation: Life expectancy changes the value of learning in foraging strategies. Oikos, 116(3), 513523. https://doi.org/10.1111/j.2007.0030-1299.15462.xGoogle Scholar
Ellers, J., & Liefting, M. (2015). Extending the integrated phenotype: Covariance and correlation in plasticity of behavioural traits. Current Opinion in Insect Science, 9, 3135. https://doi.org/10.1016/j.cois.2015.05.013Google Scholar
Ernande, B., & Dieckmann, U. (2004). The evolution of phenotypic plasticity in spatially structured environments: Implications of intraspecific competition, plasticity costs and environmental characteristics. Journal of Evolutionary Biology, 17(3), 613628. https://doi.org/10.1111/j.1420-9101.2004.00691.xGoogle Scholar
Evans, L. J., & Raine, N. E. (2014). Foraging errors play a role in resource exploration by bumble bees (Bombus terrrestris). Journal of Comparative Physiology A, 200(6), 475484. https://doi.org/10.1007/s00359-014-0905-3Google Scholar
Evans, L. J., Smith, K. E., & Raine, N. E. (2017). Fast learning in free-foraging bumble bees is negatively correlated with lifetime resource collection. Scientific Reports, 7(1), 110. https://doi.org/10.1038/s41598-017-00389-0Google Scholar
Ferguson, H. J., Cobey, S., & Smith, B. H. (2001). Sensitivity to a change in reward is heritable in the honeybee, Apis mellifera. Animal Behaviour, 61(3), 527534. https://doi.org/10.1006/anbe.2000.1635Google Scholar
Fitzpatrick, M. J., Feder, E., Rowe, L., & Sokolowski, M. B. (2007). Maintaining a behaviour polymorphism by frequency-dependent selection on a single gene. Nature, 447(7141), 210212. https://doi.org/10.1038/nature05764Google Scholar
Gosling, S. D. (2001). From mice to men: What can we learn about personality from animal research? In Psychological Bulletin (Vol. 127, Issue 1, pp. 45–86). https://doi.org/10.1037/0033-2909.127.1.45Google Scholar
Griffin, A. S., Guillette, L. M., & Healy, S. D. (2015). Cognition and personality: An analysis of an emerging field. Trends in Ecology & Evolution, 30(4), 207214. https://doi.org/10.1016/j.tree.2015.01.012Google Scholar
van Grunsven, R. H. A., & Liefting, M. (2015). How to maintain ecological relevance in ecology. Trends in Ecology & Evolution, 30(10), 563564. https://doi.org/10.1016/j.tree.2015.07.010Google Scholar
Haberkern, H., & Jayaraman, V. (2016). Studying small brains to understand the building blocks of cognition. Current Opinion in Neurobiology, 37, 5965. https://doi.org/10.1016/j.conb.2016.01.007Google Scholar
Hallgrímsson, B., & Hall, B. K. (2005). Variation – A central concept in biology (Hallgrímsson, B. & Hall, B. K. (eds.)). Elsevier. https://doi.org/10.1016/B978-0-12-088777-4.X5000-5Google Scholar
Harvey, J. A., Malcicka, M., & Ellers, J. (2015). Integrating more biological and ecological realism into studies of multitrophic interactions. Ecological Entomology, 40(4), 349352. https://doi.org/10.1111/een.12204Google Scholar
Hirsch, J., & McCauley, L. A. (1977). Successful replication of, and selective breeding for, classical conditioning in the blowfly Phormia regina. Animal Behaviour, 25(3), 784785. https://doi.org/10.1016/0003-3472(77)90130-0Google Scholar
Hoedjes, K. M., Kruidhof, H. M., Huigens, M. E., Dicke, M., Vet, L. E. M., & Smid, H. M. (2011). Natural variation in learning rate and memory dynamics in parasitoid wasps: opportunities for converging ecology and neuroscience. Proceedings of the Royal Society B, 278(1707), 889897. https://doi.org/10.1098/rspb.2010.2199Google Scholar
Hoedjes, K. M., & Smid, H. M. (2014). Natural variation in long-term memory formation among Nasonia parasitic wasp species. Behavioural Processes, 105, 4045. https://doi.org/10.1016/j.beproc.2014.02.014CrossRefGoogle ScholarPubMed
Hoedjes, K. M., Smid, H. M., Vet, L. E. M., & Werren, J. H. (2014). Introgression study reveals two quantitative trait loci involved in interspecific variation in memory retention among Nasonia wasp species. Heredity, 113(6), 542550. https://doi.org/10.1038/hdy.2014.66Google Scholar
Hoedjes, K. M., Steidle, J. L. M., Werren, J. H., Vet, L. E. M., & Smid, H. M. (2012). High-throughput olfactory conditioning and memory retention test show variation in Nasonia parasitic wasps. Genes, Brain and Behavior, 11(7), 879887. https://doi.org/10.1111/j.1601-183X.2012.00823.xGoogle Scholar
Holliday, M., & Hirsch, J. (1986). A comment on the evidence for learning in diptera. Behavior Genetics, 16(4), 439447. https://doi.org/10.1007/BF01074263Google Scholar
Hoppitt, W., Samson, J., Laland, K. N., & Thornton, A. (2012). Identification of learning mechanisms in a wild meerkat population. PLoS ONE, 7(8), e42044. https://doi.org/10.1371/journal.pone.0042044CrossRefGoogle Scholar
Kingsolver, J. G., Hoekstra, H. E., Hoekstra, J. M., Berrigan, D., Vignieri, S. N., Hill, C. E., Hoang, A., Gibert, P., & Beerli, P. (2001). The strength of phenotypic selection in natural populations. The American Naturalist, 157(3), 245261. 0003-0147/2001/15703-0001$03.00Google Scholar
Kraaijeveld, K., Oostra, V., Liefting, M., Wertheim, B., Meijer, E. de, & Ellers, J. (2018). Regulatory and sequence evolution in response to selection for improved associative learning ability in Nasonia vitripennis. BMC Genomics, 19, 892. https://doi.org/doi.org/10.1186/s12864-018-5310-9Google Scholar
Kruidhof, H. M., Roberts, A. L., Magdaraog, P., Muñoz, D., Gols, R., Vet, L. E. M., Hoffmeister, T. S., & Harvey, J. A. (2015). Habitat complexity reduces parasitoid foraging efficiency, but does not prevent orientation towards learned host plant odours. Oecologia, 179(2), 353361. https://doi.org/10.1007/s00442-015-3346-yGoogle Scholar
Lagasse, F., Moreno, C., Preat, T., & Mery, F. (2012). Functional and evolutionary trade-offs co-occur between two consolidated memory phases in Drosophila melanogaster. Proceedings of the Royal Society B, 279(1744), 40154023. https://doi.org/10.1098/rspb.2012.1457Google Scholar
Liefting, M., Hoedjes, K. M., Le Lann, C., Smid, H. M., & Ellers, J. (2018). Selection for associative learning of color stimuli reveals correlated evolution of this learning ability across multiple stimuli and rewards. Evolution, 72(7), 14491459. https://doi.org/10.1111/evo.13498CrossRefGoogle ScholarPubMed
Liefting, M., Rohmann, J. L., Le Lann, C., & Ellers, J. (2019). What are the costs of learning? Modest trade-offs and constitutive costs do not set the price of fast associative learning ability in a parasitoid wasp. Animal Cognition, 22(5), 851861. https://doi.org/10.1007/s10071-019-01281-2Google Scholar
Liefting, M., Verwoerd, L., Dekker, M. L., Hoedjes, K. M., & Ellers, J. (2020). Strain differences rather than species differences contribute to variation in associative learning ability in Nasonia. Animal Behaviour, 168, 2531. https://doi.org/10.1016/j.anbehav.2020.07.026Google Scholar
Lofdahl, K. L., Holliday, M., & Hirsch, J. (1992). Selection for conditionability in Drosophila melanogaster. Journal of Comparative Psychology, 106(2), 172183. https://doi.org/10.1037/0735-7036.106.2.172Google Scholar
Madden, J. R., Langley, E. J. G., Whiteside, M. A., Beardsworth, C. E., & Van Horik, J. O. (2018). The quick are the dead: Pheasants that are slow to reverse a learned association survive for longer in the wild. Philosophical Transactions of the Royal Society B, 373(1756), 19. https://doi.org/10.1098/rstb.2017.0297Google Scholar
McNamara, J. M., & Houston, A. I. (1987). Memory and the efficient use of information. Journal of Theoretical Biology, 125(4), 385395. https://doi.org/10.1016/S0022-5193(87)80209-6Google Scholar
Mery, F. (2013). Natural variation in learning and memory. Current Opinion in Neurobiology, 23(1), 5256. https://doi.org/10.1016/j.conb.2012.09.001Google Scholar
Mery, F., Belay, A. T., So, A. K.-C., Sokolowski, M. B., & Kawecki, T. J. (2007). Natural polymorphism affecting learning and memory in Drosophila. Proceedings of the National Academy of Sciences, 104(32), 1305113055. https://doi.org/10.1073/pnas.0702923104Google Scholar
Mery, F., & Kawecki, T. J. (2002). Experimental evolution of learning ability in fruit flies. Proceedings of the National Academy of Sciences, 99(22), 1427414279. https://doi.org/10.1073/pnas.222371199Google Scholar
Mery, F., & Kawecki, T. J. (2003). A fitness cost of learning ability in Drosophila melanogaster. Proceedings of the Royal Society of London B, 270(1532), 24652469. https://doi.org/10.1098/rspb.2003.2548Google Scholar
Mery, F., Pont, J., Preat, T., & Kawecki, T. J. (2007). Experimental evolution of olfactory memory in Drosophila melanogaster. Physiological and Biochemical Zoology, 80(4), 399405. https://doi.org/10.1086/518014Google Scholar
Mitchell-Olds, T., Willis, J. H., & Goldstein, D. B. (2007). Which evolutionary processes influence natural genetic variation for phenotypic traits? Nature Reviews Genetics, 8(11), 845856. https://doi.org/10.1038/nrg2207Google Scholar
Morand-Ferron, J., Cole, E. F., & Quinn, J. L. (2016). Studying the evolutionary ecology of cognition in the wild: A review of practical and conceptual challenges. Biological Reviews, 91(2), 367389. https://doi.org/10.1111/brv.12174Google Scholar
Népoux, V., Haag, C. R., & Kawecki, T. J. (2010). Effects of inbreeding on aversive learning in Drosophila. Journal of Evolutionary Biology, 23(11), 23332345. https://doi.org/10.1111/j.1420-9101.2010.02094.xGoogle Scholar
Papaj, D. R., & Lewis, A. C. (1993). Insect learning: Ecology and evolutionary perspectives (Papaj, D. R. & Lewis, A. C. (eds.)). Chapman & Hall.Google Scholar
Pasquier, G., & Grüter, C. (2016). Individual learning performance and exploratory activity are linked to colony foraging success in a mass-recruiting ant. Behavioral Ecology, 27(6), 17021709. https://doi.org/10.1093/beheco/arw079Google Scholar
Perry, C. J., Barron, A. B., & Chittka, L. (2017). The frontiers of insect cognition. Current Opinion in Behavioral Sciences, 16, 111118. https://doi.org/10.1016/j.cobeha.2017.05.011Google Scholar
Perry, C. J., & Chittka, L. (2019). How foresight might support the behavioral flexibility of arthropods. Current Opinion in Neurobiology, 54, 171177. https://doi.org/10.1016/j.conb.2018.10.014Google Scholar
Price, T. D., & Schluter, D. (1991). On the low heritability of life-history traits. Evolution, 45(4), 853861. https://doi.org/10.2307/2409693Google Scholar
Quinn, J. L., Cole, E. F., Reed, T. E., & Morand-Ferron, J. (2016). Environmental and genetic determinants of innovativeness in a natural population of birds. Philosophical Transactions of the Royal Society B, 371(1690), 114. https://doi.org/10.1098/rstb.2015.0184Google Scholar
Raine, N. E., & Chittka, L. (2008). The correlation of learning speed and natural foraging success in bumble-bees. Proceedings of the Royal Society B, 275(1636), 803808. https://doi.org/10.1098/rspb.2007.1652Google Scholar
Raine, N. E., Ings, T. C., Ramos-Rodriguez, O., & Chittka, L. (2006). Intercolony variation in learning performance of a wild British bumblebee population (Hymenoptera: Apidae: Bombus terrestris audax). Entomologia Generalis, 28(4), 241256. https://doi.org/10.1127/entom.gen/28/2006/241Google Scholar
Rowe, C., & Healy, S. D. (2014). Measuring variation in cognition. Behavioral Ecology, 25(6), 12871292. https://doi.org/10.1093/beheco/aru090CrossRefGoogle Scholar
Sepúlveda, D. A., Zepeda-Paulo, F., Ramírez, C. C., Lavandero, B., & Figueroa, C. C. (2017). Loss of host fidelity in highly inbred populations of the parasitoid wasp Aphidius ervi (Hymenoptera: Braconidae). Journal of Pest Science, 90(2), 649658. https://doi.org/10.1007/s10340-016-0798-8Google Scholar
Snell-Rood, E. C., Davidowitz, G., & Papaj, D. R. (2011). Reproductive tradeoffs of learning in a butterfly. Behavioral Ecology, 22(2), 291302. https://doi.org/10.1093/beheco/arq169Google Scholar
Stamps, J. A. (2016). Individual differences in behavioural plasticities. Biological Reviews, 91(2), 534567. https://doi.org/10.1111/brv.12186Google Scholar
Stephens, D. W. (1991). Change, regularity, and value in the evolution of animal learning. Behavioral Ecology, 2, 7789. https://doi.org/https://doi.org/10.1093/beheco/2.1.77Google Scholar
Thornton, A., & Lukas, D. (2012). Individual variation in cognitive performance: Developmental and evolutionary perspectives. Philosophical Transactions of the Royal Society B, 367(1603), 27732783. https://doi.org/10.1098/rstb.2012.0214CrossRefGoogle ScholarPubMed
Versace, E., & Reisenberger, J. (2015). Large-scale assessment of olfactory preferences and learning in Drosophila melanogaster: behavioral and genetic components. PeerJ, 3, e1214. https://doi.org/10.7717/peerj.1214Google Scholar
Werren, J. H., & Loehlin, D. W. (2009). The parasitoid wasp Nasonia: An emerging model system with haploid male genetics. Cold Spring Harbor Protocols, 4(10), 110. https://doi.org/10.1101/pdb.emo134Google Scholar
Werren, J. H., Richards, S., Desjardins, C. A., Niehuis, O., Gadau, J., Colbourne, J. K., Beukeboom, L. W., Desplan, C., Elsik, C. G., Grimmelikhuijzen, C. J. P., Kitts, P., Lynch, J. A., Murphy, T., Oliveira, D. C. S. G., Smith, C. D., van de Zande, L., Worley, K. C., Zdobnov, E. M., Aerts, M., … Gibbs, R. A. (2010). Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science, 327(5963), 343348. https://doi.org/10.1126/science.1178028Google Scholar
Zrelec, V., Zini, M., Guarino, S., Mermoud, J., Oppliger, J., Valtat, A., Zeender, V., & Kawecki, T. J. (2013). Drosophila rely on learning while foraging under seminatural conditions. Ecology and Evolution, 3(12), 41394148. https://doi.org/10.1002/ece3.783Google Scholar
Zwoinska, M. K., Lind, M. I., Cortazar‐Chinarro, M., Ramsden, M., & Maklakov, A. A. (2016). Selection on learning performance results in the correlated evolution of sexual dimorphism in life history. Evolution, 70(2), 342357. https://doi.org/10.1111/evo.12862Google Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×