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3 - Learning in Insects: Perspectives and Possibilities

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
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Summary

We provide a brief overview of current research on the behavioral ecology of learning in insects, emphasizing the function of learning in their ability to find food, locate hosts, avoid danger, and secure mates. In addition, we outline two important issues facing the current study of insect learning. One issue is the need, not only to recognize, but also to understand the role of plasticity and variation in the expression of learning, including the impacts of circadian rhythm, intraspecific and interspecific genetic differences, sex, development and environmental context. A second issue is the vexing question of homology versus homoplasy in the underlying mechanisms of learning in insects, other invertebrates and single-celled organisms.

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Publisher: Cambridge University Press
Print publication year: 2022

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References

Abramson, C. I., & Chicas-Mosier, A. M. (2016). Learning in plants: Lessons from Mimosa pudica. Frontiers in Psychology, 7, 417. https://doi.org/10.3389/fpsyg.2016.00417CrossRefGoogle ScholarPubMed
Aceves-Piña, E. O., & Quinn, W. G. (1979). Learning in normal and mutant Drosophila larvae. Science, 206, 9396. https://doi.10.1126/science.206.4414.93Google Scholar
Alem, S., Perry, C. J., Zhu, X., Loukola, O. J., Ingraham, T., Søvik, E., & Chittka, L. (2016). Associative mechanisms allow for social learning and cultural transmission of string pulling in an insect. PLoS Biology, 14(10), e1002564. https://doi.org/10.1371/journal.pbio.1002564CrossRefGoogle ScholarPubMed
Alghamdi, A., Dalton, L., Phillis, A., Rosato, E., & Mallon, E. B. (2008). Immune response impairs learning in free-flying bumble-bees. Biology Letters, 4, 479481. https://doi.org/10.1098/rsbl.2008.0331Google Scholar
Applewhite, P. B. (1968). Non-local nature of habituation in a rotifer and protozoan. Nature, 217, 287288. https://doi.org/10.1038/217287a0Google Scholar
Arenas, A., & Roces, F. (2018). Appetitive and aversive learning of plants odors inside different nest compartments by foraging leaf-cutting ants. Journal of Insect Physiology, 109, 8592. https://doi.org/10.1016/j.jinsphys.2018.07.001Google Scholar
Armus, H. L., Montgomery, A. R., & Gurney, R. L. (2006). Discrimination learning and extinction in Paramecia (P. caudatum). Psychological Reports, 98, 705711. https://doi.org/10.2466%2Fpr0.98.3.705-711CrossRefGoogle ScholarPubMed
Bailey, N. W., & Zuk, M. (2009). Field crickets change mating preferences using remembered social information. Biology Letters, 5, 449451. https://doi.org/10.1098/rsbl.2009.0112Google Scholar
Bernays, E. A. (1993). Aversion learning and feeding. In Papaj, D. R. & Lewis, A. C. (Eds.), Insect learning (pp. 117). Routledge, Chapman & Hall. https://doi.org/10.1007/978-1-4615-2814-2_1Google Scholar
Bitterman, M. E. (2000). Cognitive evolution: A psychological perspective. In Heyes, C. & Huber, L. (Eds.), The evolution of cognition (pp. 6180). The MIT Press.CrossRefGoogle Scholar
Blackawton, P. S., Airzee, S., Allen, A., Baker, S., Berrow, A., Blair, C., Churchill, M., Coles, J., Cumming, R. F.-J., Fraquelli, L., Hackford, C., Hinton Mellor, A., Hutchcroft, M., Ireland, B., Jewsbury, D., Littlejohns, A., Littlejohns, G. M., Lotto, M., McKeown, J., … Lotto, R. B. (2011). Blackawton bees. Biology Letters, 7, 168172. https://doi.org/10.1098/rsbl.2010.1056Google Scholar
Blackiston, D. J., Casey, E. S., & Weiss, M. R. (2008). Retention of memory through metamorphosis: Can a moth remember what it learned as a caterpillar? PLoS ONE, 3(3), e1736. https://doi.org/10.1371/journal.pone.0001736CrossRefGoogle ScholarPubMed
Boisseau, R. P., Vogel, D., & Dussutour, A. (2016). Habituation in non-neural organisms: Evidence from slime moulds. Proceedings of the Royal Society B, 283, 20160446. https://doi.org/10.1098/rspb.2016.0446CrossRefGoogle ScholarPubMed
Boussard, A. Delescluse, J., Pérez-Escudero, A., & Dussutour, A. (2019). Memory inception and preservation in slime moulds: The quest for a common mechanism. Philosophical Transactions of the Royal Society B, 374, 20180368. https://doi.org/10.1098/rstb.2018.0368Google Scholar
Campbell, H. R., & Strausfeld, N. J. (2001). Learned discrimination of pattern orientation in walking flies. Journal of Experimental Biology, 204, 114.Google Scholar
Chilaka, N., Perkins, E., & Tripet, F. (2012). Visual and olfactory associative learning in the malaria vector Anopheles gambiae sensu stricto. Malaria Journal, 11, 27. https://doi.org/10.1186/1475-2875-11-27Google Scholar
Coolen, I., Dangles, O., & Casas, J. (2005). Social learning in noncolonial insects? Current Biology, 21, 19311935. https://doi.org/10.1016/j.cub.2005.09.015CrossRefGoogle Scholar
Danci, A., Hrabar, M., Ikoma, S., Schaefer, P. W., & Gries, G. (2013). Learning provides mating opportunities for males of a parasitoid wasp. Entomologia Experimentalis et Applicata, 149, 229240. https://doi.org/10.1111/eea.12129Google Scholar
Decker, S., McConnaughey, S., & Page, T. L. (2007). Circadian regulation of insect olfactory learning. Proceedings of the National Academy of Sciences, 104, 1590515910. https://doi.org/10.1073/pnas.0702082104Google Scholar
DesJardins, N., & Tibbetts, E. A. (2018). Sex differences in face but not colour learning in Polistes fuscatus paper wasps. Animal Behaviour, 140, 16. https://doi.org/10.1016/j.anbehav.2018.03.012CrossRefGoogle Scholar
Dukas, R. (1999). Ecological relevance of associative learning in fruit fly larvae. Behavioral Ecology and Sociobiology, 45, 195200. https://doi.org/10.1007/s002650050553Google Scholar
Dukas, R. (2008). Evolutionary biology of insect learning. Annual Review of Entomology, 53, 145160. https://doi.org/10.1146/annurev.ento.53.103106.093343CrossRefGoogle ScholarPubMed
Dukas, R., & Bernays, E. A. (2000). Learning improves growth rate in grasshoppers. Ecology, 97, 26372640. https://doi.org/10.1073/pnas.050461497Google ScholarPubMed
Dukas, R., & Duan, J. J. (2000). Potential fitness consequences of associative learning in parasitoid wasps. Behavioral Ecology, 11, 536543. https://doi.org/10.1093/beheco/11.5.536CrossRefGoogle Scholar
Durisko, Z., & Dukas, R. (2013). Effects of early-life experience on learning ability in fruit flies. Ethology, 119, 10671076. https://doi.org/10.1111/eth.12168CrossRefGoogle Scholar
Froissart, L., Giurfa, M., Sauzet, S., & Desouhant, E. (2017). Cognitive adaptation in asexual and sexual wasps living in contrasted environments. PLoS ONE,12(5), e0177581. https://doi.org/10.1371/journal.pone.0177581Google Scholar
Fropf, R., Zhang, J., Tanenhaus, A. K., Fropf, W. J., Siefkes, E., & Yin, J. C. P. (2014). Time of day influences memory formation and dCREB2 proteins in Drosophila. Frontiers in Systems Neuroscience, 8, 43. https://doi.org/10.3389/fnsys.2014.00043Google Scholar
Fukushi, T. (1989). Learning and discrimination of coloured papers in the walking blowfly, Lucilia cuprina. Journal of Comparative Physiology A, 166, 5764. https://doi.org/10.1007/BF00190210CrossRefGoogle ScholarPubMed
Gagliano, M., Vyazovskiy, V. V., Borbély, A. A., Grimonprez, M., & Depczynski, M. (2016). Learning by association in plants. Scientific Reports, 6, 38427. https://doi.org/10.1038/srep38427Google Scholar
Garren, M. V., Sexauer, S. B., & Page, T. L. (2013). Effect of circadian phase on memory acquisition and recall: Operant conditioning vs. classical conditioning. PLoS ONE 8(3), e58693. https://doi.org/10.1371/journal.pone.0058693Google Scholar
Giurfa, M. (2013). Cognition with few neurons: Higher-order learning in insects. Trends in Neurosciences, 36, 285294. https://doi.org/10.1016/j.tins.2012.12.011Google Scholar
Giurfa, M. (2015). Learning and cognition in insects. Wiley Interdisciplinary Reviews: Cognitive Science, 6, 383395. https://doi.org/10.1002/wcs.1348Google Scholar
Goldsmith, C. M., Hepburn, H. R., & Mitchell, D. (1978). Retention of an associative learning task after metamorphosis in Locusta migratoria migratorioides. Journal of Insect Physiology, 24, 737741. https://doi.org/10.1016/0022-1910(78)90071-9Google Scholar
Gong, Z., Tan, K., & Nieh, J. C. (2018). First demonstration of olfactory learning and long-term memory in honey bee queens. Journal of Experimental Biology, 221, jeb177303. https://doi.org/10.5281/zenodo.1148794CrossRefGoogle ScholarPubMed
Greenspan, R. J. (2007). Afterword: Universality and brain mechanisms. In North, G. & Greenspan, R. J. (Eds.), Invertebrate neurobiology (pp. 647649). Cold Spring Harbor Laboratory Press.Google Scholar
Grüter, C., & Leadbeater, E. (2014). Insights from insects about adaptive social information use. Trends in Ecology & Evolution, 29, 177184. https://doi.org/10.1016/j.tree.2014.01.004Google Scholar
Guillette, L. M., Hollis, K. L., & Markarian, A. (2009). Learning in a sedentary insect predator: Antlions (Neuroptera: Myrmeleontidae) anticipate a long wait. Behavioural Processes, 80, 224232. https://doi.org/10.1016/j.beproc.2008.12.015CrossRefGoogle Scholar
Gutiérrez-Ibáñez, C., Villagra, C. A., & Niemeyer, H. M. (2007). Pre-pupation behaviour of the aphid parasitoid Aphidius ervis (Haliday) and its consequences for pre-imaginal learning. Naturwissenschaften, 94, 595600. https://doi.org/10.1007/s00114-007-0233-3Google Scholar
Haralson, J. V., Groff, C. I., & Haralson, S. J. (1975). Classical conditioning in the sea anemone, Cribrina xanthogrammica. Physiology & Behavior, 15, 455460. https://doi.org/10.1016/0031-9384(75)90259-0Google 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.2014.02.014Google Scholar
Hollis, K. L. (1982). Pavlovian conditioning of signal-centered action patterns and autonomic behavior: A biological analysis of function. Advances in the Study of Behavior, 12, 164. https://doi.org/10.1016/S0065-3454(08)60045-5Google Scholar
Hollis, K. L. (1997). Contemporary research on Pavlovian conditioning: A “new” functional analysis. American Psychologist, 52, 956965. https://psycnet.apa.org/doi/10.1037/0003-066X.52.9.956Google Scholar
Hollis, K. L., Cogswell, H., Snyder, K., Guillette, L. M., & Nowbahari, E. (2011). Specialized learning in antlions (Neuroptera: Myrmeleontidae), pit-digging predators, shortens vulnerable larval stage. PLoS ONE, 6(3), e17958. https://doi.org/10.1371/journal.pone.0017958CrossRefGoogle ScholarPubMed
Hollis, K. L., & Guillette, L. M. (2011). Associative learning in insects: Evolutionary models, mushroom bodies, and a neuroscientific conundrum. Comparative Cognition & Behavior Reviews, 6, 2445. https://psycnet.apa.org/doi/10.3819/ccbr.2011.60004Google Scholar
Hollis, K. L., & Guillette, L. M. (2015). What associative learning in insects tells us about models for the evolution of learning. International Journal of Comparative Psychology, 28, 118.Google Scholar
Hollis, K. L., Harrsch, F. A., & Nowbahari, E. (2015). Ants vs. antlions: An insect model for studying the role of learned ad hard-wired behavior in coevolution. Learning & Behavior, 50, 6882. https://doi.org/10.1016/j.lmot.2014.11.003Google Scholar
Hollis, K. L., Pharr, V. L., Dumas, M. J., Britton, G. B., & Field, J. (1997). Classical conditioning provides paternity advantage for territorial male blue gouramis (Trichogaster trichopterus). Journal of Comparative Psychology, 111, 219225. https://psycnet.apa.org/doi/10.1037/0735-7036.111.3.219Google Scholar
Iqbal, J., & Mueller, U. (2007). Virus infection causes specific learning deficits in honeybee foragers. Proceedings of the Royal Society B, 274, 15171521. https://doi.org/10.1098/rspb.2007.0022CrossRefGoogle ScholarPubMed
Jones, J. C., Helliwell, P., Beekman, M., Maleszka, R., & Oldroyd, B. P. (2005). The effects of rearing temperature on developmental stability and learning and memory in the honey bee, Apis mellifera. Journal of Comparative Physiology A, 191, 11211129. https://doi.org/10.1007/s00359-005-0035-zGoogle Scholar
Kacsoh, B. Z., Bozler, J., & Bosco, G. (2018). Drosophila species learn dialects through communal living. PLoS Genetics, 14(7), e1007430. https://doi.org/10.1371/journal.pgen.1007430CrossRefGoogle ScholarPubMed
König, K., Krimmer, E., Brose, S., Gantert, C., Buschlüter, I., König, C., Klopfstein, S., Wendt, I., Baur, H., Krogmann, L., & Steidle, J. L. M. (2015). Does early learning drive ecological divergence during speciation processes in parasitoid wasps? Proceedings of the Royal Society B, 282, 20141850. https://doi.org/10.1098/rspb.2014.1850CrossRefGoogle ScholarPubMed
Kralj, J., Brockmann, A., Fuchs, S., & Tautz, J. (2007). The parasitic mite Varroa destructor affects non-associative learning in honey bee foragers, Apis mellifera L. Journal of Comparative Physiology A, 193, 363370. https://doi.org/10.1007/s00359-006-0192-8Google Scholar
Kramer, J. M., Kochinke, K., Oortveld, M. A. W., Marks, H., Kramer, D., de Jong, E. K., Asztalos, Z., Westwood, J. T., Stunnenberg, H. G., Sokolowski, M. B., Keleman, K., Zhou, H., van Bokhoven, H., & Schenck, A. (2011). Epigenetic regulation of learning and memory by Drosophila EHMT/G9a. PLoS Biology, 9(1), e1000569. https://doi.org/10.1371/journal.pbio.1000569Google Scholar
Lee, J. C., & Bernays, E. A. (1990). Food tastes and toxic effects: Associative learning by the polyphagous grasshopper Schistocerca americana (Drury) (Orthoptera: Acricicae). Animal Behaviour, 39, 163173. https://doi.org/10.1371/journal.pbio.1000569CrossRefGoogle Scholar
Lehmann, M., Gustav, D., & Galizia, C. G. (2011). The early bee catches the flower – Circadian rhythmicity influences learning performance in honey bees, Apis mellifera. Behavioral Ecology and Sociobiology, 65, 205215. https://doi.org/10.1007/s00265-010-1026-9CrossRefGoogle ScholarPubMed
Lewis, W. J., & Takasu, K. (1990). Use of learned odours by a parasitic wasp in accordance with host and food needs. Nature, 348, 635636. https://psycnet.apa.org/doi/10.1038/348635a0CrossRefGoogle Scholar
Li, X., Ishimoto, H., & Kamikouchi, A. (2018). Auditory experience controls the maturation of song discrimination and sexual response in Drosophila. eLife, 7, e34348. https://doi.org/10.7554/eLife.34348Google 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, 14491459. https://doi.org/10.1111/evo.13498Google Scholar
Loomis, W. F. (2014). Cell signaling during development of Dictyostelium. Developmental Biology, 391, 116. https://doi.org/10.1016/j.ydbio.2014.04.001Google Scholar
Louis, T., Stahl, A., Boto, T., & Tomchik, S. M. (2018). Cyclic AMP-dependent plasticity underlies rapid changes in odor coding associated with reward learning. Proceedings of the National Academy of Sciences, 115, E448E457. https://doi.org/10.1073/pnas.1709037115Google Scholar
Loukola, O. J., Perry, C. J., Coscos, L., & Chittka, L. (2017). Bumblebees show cognitive flexibility by improving on an observed complex behavior. Science, 355, 833836. https://doi.org/10.1126/science.aag2360CrossRefGoogle Scholar
Lunau, K., An, L., Donda, M., Hohmann, M., Sermon, L., & Stegmanns, V. (2018). Limitations of learning in the proboscis reflex of the flower visiting syrphid fly Eristalis tenax. PLoS ONE 13(3), e0194167. https://doi.org/10.1371/journal.pone.0194167CrossRefGoogle ScholarPubMed
Lyons, L. C., & Roman, G. (2009). Circadian modulation of short-term memory in Drosophila. Learning and Memory, 16, 1927. https://doi.org/10.1101/lm.1146009Google Scholar
Matsumoto, C. S., Matsumoto, Y., Watanabe, H., Nishino, H., & Mizunami, M. (2012). Context-dependent olfactory learning monitored by activities of salivary neurons in cockroaches. Neurobiology of Learning and Memory, 97, 3036. https://doi.org/10.1016/j.nlm.2011.08.010Google Scholar
McGuire, T. R. (1984). Learning in three species of Diptera: The blow fly Phormia regina, the fruit fly, Drosophila melanogaster, and the house fly, Musca domestica. Behaviour Genetics, 14, 479526. https://doi.org/10.1007/BF01065445CrossRefGoogle Scholar
Menda, G., Uhr, J. H., Wyttenbach, R. A., Vermeylen, F. M., Smith, D. M., Harrington, L. C., & Hoy, R. R. (2013). Associative learning in the dengue vector mosquito, Aedes aegypti: Avoidance of a previously attractive odor or surface color that is paired with an aversive stimulus. Journal of Experimental Biology, 216, 218223. https://doi.org/10.1242/jeb.074898Google Scholar
Mingee, C. M. (2013). Retention of a brightness discrimination task in Paramecia, P. caudatum. International Journal of Comparative Psychology, 26, 202212. https://escholarship.org/uc/item/5428c5xnGoogle Scholar
Nelson, M. C. (1971). Classical conditioning in the blowfly (Phormia regina): Associative and excitatory factors. Journal of Comparative and Physiological Psychology, 77, 353368. https://psycnet.apa.org/doi/10.1037/h0031882Google Scholar
Nepoux, V., Babin, A., Haag, C., Kawecki, T. J., & Le Rouzic, A. (2015). Quantitative genetics of learning ability and resistance to stress in Drosophila melanogaster. Ecology and Evolution, 5, 543556. https://doi.org/10.1002/ece3.1379Google Scholar
Nöbel, S., Allain, M., Isabel, G., & Danchin, E. (2018). Mate copying in Drosophila melanogaster males. Animal Behaviour, 141, 915. https://doi.org/10.1016/j.anbehav.2018.04.019CrossRefGoogle Scholar
North, G., & Greenspan, R. J. (2007). Invertebrate neurobiology. Cold Spring Laboratory Press.Google Scholar
Perez, M., Rolland, U., Giurfa, M., & d’Ettorre, P. (2013). Sucrose responsiveness, learning success, and task specialization in ants. Learning & Memory, 20, 417420. https://doi.org/10.1101/lm.031427.113Google Scholar
Perlman, R. L., & Pastan, I. (1971). The role of cyclic AMP in bacteria. Current Topics in Cellular Regulation, 3, 117134.Google Scholar
Perry, C. J., Barron, A. B., & Cheng, K. (2013). Invertebrate learning and cognition: Relating phenomena to neural substrate. WIREs Cognitive Science, 4, 561582. https://doi.org/10.1002/wcs.1248Google Scholar
Piiroinen, S., & Goulson, D. (2016). Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honeybees and bumblebees. Proceedings of the Royal Society B, 283, 20160246. https://doi.org/10.1098/rspb.2016.0246Google Scholar
Prokopy, R. J., Reynolds, A. H., & Ent, L.-J. van der (1998). Can Rhagoletis pomonella flies (Diptera: Tephritidae) learn to associate presence of food on foliage with foliage colour? European Journal of Entomology, 95, 335341.Google Scholar
Quinn, W. G., Harris, W. A., & Benzer, S. (1974). Conditioned behavior in Drosophila melanogaster. Proceedings of the National Academy of Sciences, 71, 708712. https://doi.org/10.1073/pnas.71.3.708CrossRefGoogle ScholarPubMed
Raine, N. E. (2009). Cognitive ecology: Environmental dependence of the fitness costs of learning. Current Biology, 19, R486R488. https://doi.org/10.1016/j.cub.2009.04.047Google Scholar
Rains, G. C., Utley, S. L., & Lewis, W. J. (2006). Behavioral monitoring of trained insects for chemical detection. Biotechnology Progress, 22, 28. https://doi.org/10.1021/bp050164pCrossRefGoogle ScholarPubMed
Ramírez, G., Fagundez, C., Grosso, J. P., Argibay, P., Arenas, A., & Farina, W. M. (2016). Odor experiences during preimaginal stages cause behavioral and neural plasticity in adult honeybees. Frontiers in Behavioral Neuroscience, 10, 114. https://doi.org/10.3389/fnbeh.2016.00105Google Scholar
Raubenheimer, D., & Blackshaw, J. (1994). Locusts learn to associate visual stimuli with drinking. Journal of Insect Behavior, 7, 569575. https://psycnet.apa.org/doi/10.1007/BF02025450Google Scholar
Raubenheimer, D., & Tucker, D. (1997). Associative learning by locusts: Pairing of visual cues with consumption of protein and carbohydrate. Animal Behaviour, 54, 14491459. https://doi.org/10.1006/anbe.1997.0542Google Scholar
Reaume, C. J., Sokolowski, M. B., & Mery, F. (2011). A natural genetic polymorphism affects retroactive interference in Drosophila melanogaster. Proceedings of the Royal Society B, 278, 9198. https://doi.org/10.1098/rspb.2010.1337Google Scholar
Resh, V. H., & Cardé, R. T. (Eds.). (2003). Encyclopedia of insects. Elsevier Science, Academic Press.Google Scholar
Saigusa, T., Tero, A., Nakagaki, T., & Kuramoto, Y. (2008). Amoebae anticipate periodic events. Physical Review Letters, 100, 018101. https://doi.org/10.1103/PhysRevLett.100.018101CrossRefGoogle ScholarPubMed
Seugnet, L., Suzuki, Y., Donlea, J. M., Gottschalk, L., & Shaw, P. J. (2011). Sleep deprivation during early-adult development results in long-lasting learning deficits in adult Drosophila. Sleep, 34, 137146. https://doi.org/10.1093/sleep/34.2.137Google Scholar
Shirakawa, T., Gunji, Y.-P., & Miyake, Y. (2011). An associative learning experiment using the plasmodium of Physarum polycephalum. Nano Communication Networks, 2, 99105. https://doi.org/10.1016/j.nancom.2011.05.002Google Scholar
Smid, H. M., Wang, G., Bukovinszky, T., Steidle, J. L. M., Bleeker, M. A. K., van Loon, J. J. A., & Vet, L. E. M. (2007). Species-specific acquisition and consolidation of long-term memory in parasitic wasps. Proceeding of the Royal Society B, 274, 15391546. https://doi.org/10.1098/rspb.2007.0305Google ScholarPubMed
Sokolowski, M. B. C., Disma, G., & Abramson, C. I. (2010). A paradigm for operant conditioning in blow flies (Phormia terrae novae Robineau-Desvoidy, 1830). Journal of the Experimental Analysis of Behavior, 93, 8189. https://doi.org/10.1901/jeab.2010.93-81Google Scholar
Srinivasan, M. V. (2010). Honey bees as a model for vision, perception, and cognition. Annual Review of Entomology, 55, 267284. https://doi.org/10.1146/annurev.ento.010908.164537Google Scholar
Stejskal, K., Streinzer, M., Dyer, A., Paulus, H. F., & Spaethe, J. (2015). Functional significance of labellum pattern variation in a sexually deceptive orchid (Ophrys heldreichii): Evidence of individual signature learning effects. PLoS ONE, 10(11), e0142971. https://doi.org/10.1371/journal.pone.0142971CrossRefGoogle Scholar
Stockton, D. G., Martini, X., Pratt, J. M., & Stelinski, L. L. (2016). The influence of learning on host plant preference in a significant phytopathogen vector, Diaphorina citri. PLoS ONE, 11(3), e0149815. https://doi.org/10.1371/journal.pone.0149815CrossRefGoogle Scholar
Stockton, D. G., Pescitelli, L. E., Martini, X., & Stelinski, L. L. (2017). Female mate preference in an invasive phytopathogen vector: How learning may influence mate choice and fecundity in Diaphorina citri. Entomologia Experimentalis et Applicata, 164, 1626. https://doi.org/10.1111/eea.12590Google Scholar
Thellier, M., & Lüttge, U. (2012). Plant memory: A tentative model. Plant Biology, 15, 112. https://doi.org/10.1111/j.1438-8677.2012.00674.xGoogle Scholar
Tibbetts, E. A., Injaian, A., Sheehan, M. J., & Desjardins, N. (2018). Intraspecific variation in learning: Worker wasps are less able to learn and remember individual conspecific faces than queen wasps. American Naturalist, 191, 595603. https://doi.org/10.1086/696848Google Scholar
Tomberlin, J. K., Rains, G. C., Allan, S. A., Sanford, M. R., & Lewis, W. J. (2006). Associative learning of odor with food- or blood-meal by Culex quinquefasciatus Say (Diptera: Culicidae). Naturwissenschaften, 93, 551. https://doi.org/10.1007/s00114-006-0143-9CrossRefGoogle ScholarPubMed
Verzijden, M. N., & Svensson, E. I. (2016). Interspecific interactions and learning variability jointly drive geographic differences in mate preferences. Evolution, 70, 18961903. https://doi.org/10.1111/evo.12982Google Scholar
Vinauger, C., Lahondère, C., Wolff, G. H., Locke, L. T., Liaw, J. E., Parrish, J. Z., Akbari, O. S., Dickinson, M. H., & Riffell, J. A. (2018). Modulation of host learning in Aedes aegypti mosquitoes. Current Biology, 28, 333344. https://doi.org/10.1016/j.cub.2017.12.015Google Scholar
Vinauger, C., & Lazzari, C. R. (2015). Circadian modulation of learning ability in a disease vector insect, Rhodinus prolixus. Journal of Experimental Biology, 218, 31103117. https://doi.org/10.1242/jeb.119057Google Scholar
Vogel, D., & Dussutour, A. (2016). Direct transfer of learned behavior via cell fusion in non-neural organisms. Proceedings of the Royal Society B, 283, 20162382. https://doi.org/10.1098/rspb.2016.2382CrossRefGoogle ScholarPubMed
Wang, X., Green, D. S., Roberts, S. P., & de Belle, S. (2007). Thermal disruption of mushroom body development and odor learning in Drosophila. PLoS ONE, 2(11), e0177581. https://doi.org/10.1371/journal.pone.0001125Google Scholar
Weinstein, A. M., Davis, B. J., Menz, M. H. M., Dixon, K. W., & Phillips, R. D. (2016). Behaviour of sexually deceived ichneumonid wasps and its implications for pollination in Cryptostylis (Orchidaceae). Biological Journal of the Linnean Society, 119, 283298. https://doi.org/10.1111/bij.12841Google Scholar
Westerman, E. L., & Monteiro, A. (2013). Odour influences whether females learn to prefer or to avoid wing patterns of male butterflies. Animal Behaviour, 86, 11391145. https://doi.org/10.1016/j.anbehav.2013.09.002Google Scholar
Williams-Simon, P. A., Posey, C., Mitchell, S., Ng’oma, E., Mrkvicka, J. A., Zars, T., & King, E. G. (2019). Multiple genetic loci affect place learning and memory performance in Drosophila melanogaster. Genes, Brains and Behavior, 18, e12581. https://doi.org/10.1111/gbb.12581Google Scholar
Wilson, J. K., & Woods, H. A. (2016). Innate and learned olfactory responses in a wild population of the egg parasitoid Trichogramma (Hymenoptera: Trichogrammatidae). Journal of Insect Science, 16(1), 18. https://doi.org/10.1093/jisesa/iew108Google Scholar
Zhang, H., Lin, M., Shi, H., Ji, W., Huang, L., Zhang, X., Shen, S., Gao, R., Wu, S., Tian, C., Yang, Z., Zhang, G., He, S., Wang, H., Saw, T., Chen, Y., & Ouyang, Q. (2014). Programming a Pavlovian-like conditioning circuit in Escherichia coli. Nature Communications, 5, 3102. https://doi.org/10.1038/ncomms4102Google Scholar

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