Part I - Evolution of Learning Processes
Published online by Cambridge University Press: 26 May 2022
Summary
A summary is not available for this content so a preview has been provided. Please use the Get access link above for information on how to access this content.
- Type
- Chapter
- Information
- Evolution of Learning and Memory Mechanisms , pp. 13 - 282Publisher: Cambridge University PressPrint publication year: 2022
References
References
Amano, H., & Maruyama, I. N. (2011). Aversive olfactory learning and associative long-term memory in Caenorhabditis elegans. Learning & Memory, 18, 654–665. https://doi.org/10.1101/lm.2224411CrossRefGoogle ScholarPubMed
Ardiel, E. L., Giles, A. C., Yu, A. J., Lindsay, T. H., Lockery, S. R., & Rankin, C. H. (2016). Dopamine receptor DOP-4 modulates habituation to repetitive photoactivation of a C. elegans polymodal nociceptor. Learning & Memory, 23, 495–503. https://doi.org/10.1101/lm.041830.116CrossRefGoogle Scholar
Ardiel, E. L., McDiarmid, T. A., Timbers, T. A., Lee, K. C. Y., Safaei, J., Pelech, S. L., & Rankin, C. H. (2018). Insights into the roles of CMK-1 and OGT-1 in interstimulus interval-dependent habituation in Caenorhabditis elegans. Proceedings of the Royal Society B: Biological Sciences, 285, 20182084. https://doi.org/10.1098/rspb.2018.2084CrossRefGoogle ScholarPubMed
Ardiel, E. L., Yu, A. J., Giles, A. C., & Rankin, C. H. (2017). Habituation as an adaptive shift in response strategy mediated by neuropeptides. npj Science of Learning, 2, 9. https://doi.org/10.1038/s41539–017-0011-8CrossRefGoogle ScholarPubMed
Bargmann, C. I. (2006). Chemosensation in C. elegans. WormBook, ed. The C. elegans research community. https://doi.org/10.1895/wormbook.1.123.1, www.wormbook.org.CrossRefGoogle Scholar
Beck, C. D., & Rankin, C. H. (1995). Heat shock disrupts long-term memory consolidation in Caenorhabditis elegans. Learning & Memory, 2(3–4), 161–177. https://doi.org/10.1101/lm.2.3-4.161CrossRefGoogle ScholarPubMed
Beets, I., Janssen, T., Meelkop, E., Temmerman, L., Suetens, N., Rademakers, S., … Schoofs, L. (2012). Vasopressin/oxytocin-related signaling regulates gustatory associative learning in C. elegans. Science, 338, 543–545. https://doi.org/10.1126/science.1226860CrossRefGoogle ScholarPubMed
Bernhard, N., & van der Kooy, D. (2000). A behavioral and genetic dissection of two forms of olfactory plasticity in Caenorhabditis elegans: Adaptation and habituation. Learning and Memory, 7, 199–212. https://doi.org/10.1101/lm.7.4.199CrossRefGoogle ScholarPubMed
Biron, D., Wasserman, S., Thomas, J. H., Samuel, A. D. T., & Sengupta, P. (2008). An olfactory neuron responds stochastically to temperature and modulates Caenorhabditis elegans thermotactic behavior. Proceedings of the National Academy of Sciences, 105, 11002–11007. https://doi.org/10.1073/pnas.0805004105CrossRefGoogle ScholarPubMed
Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics, 77(1), 71–94. www.ncbi.nlm.nih.gov/pubmed/4366476CrossRefGoogle ScholarPubMed
Byrne, J. H., & Hawkins, R. D. (2015). Nonassociative learning in invertebrates. Cold Spring Harbor Perspectives in Biology, 7, a021675. https://doi.org/10.1101/cshperspect.a021675CrossRefGoogle ScholarPubMed
The C. elegans Sequencing Consortium. (1998). Genome sequence of the nematode C. elegans: A platform for investigating biology. Science, 282, 2012–2018. https://doi.org/10.1126/science.282.5396.2012CrossRefGoogle Scholar
Chen, Z., Hendricks, M., Cornils, A., Maier, W., Alcedo, J., & Zhang, Y. (2013). Two insulin-like peptides antagonistically regulate aversive olfactory learning in C. elegans. Neuron, 77, 572–585. https://doi.org/10.1016/j.neuron.2012.11.025CrossRefGoogle ScholarPubMed
Cheung, B. H. H., Cohen, M., Rogers, C., Albayram, O., & De Bono, M. (2005). Experience-dependent modulation of C. elegans behavior by ambient oxygen. Current Biology, 15, 905–917. https://doi.org/10.1016/j.cub.2005.04.017CrossRefGoogle ScholarPubMed
Chew, Y. L., Tanizawa, Y., Cho, Y., Zhao, B., Yu, A. J., Ardiel, E. L., … Schafer, W. R. (2018). An afferent neuropeptide system transmits mechanosensory signals triggering sensitization and arousal in C. elegans. Neuron, 99, 1233–1246.e6. https://doi.org/10.1016/j.neuron.2018.08.003CrossRefGoogle ScholarPubMed
Clark, D. A., Biron, D., Sengupta, P., & Samuel, A. D. T. (2006). The AFD sensory neurons encode multiple functions underlying thermotactic behavior in Caenorhabditis elegans. Journal of Neuroscience, 26, 7444–7451. https://doi.org/10.1523/JNEUROSCI.1137-06.2006CrossRefGoogle ScholarPubMed
Das, S., Sadanandappa, M. K., Dervan, A., Larkin, A., Lee, J. A., Sudhakaran, I. P., … Ramaswamia, M. (2011). Plasticity of local GABAergic interneurons drives olfactory habituation. Proceedings of the National Academy of Sciences, 108(36): E646–E654. https://doi.org/10.1073/pnas.1106411108CrossRefGoogle ScholarPubMed
Fenk, L. A., & de Bono, M. (2017). Memory of recent oxygen experience switches pheromone valence in Caenorhabditis elegans. Proceedings of the National Academy of Sciences, 114, 4195–4200. https://doi.org/10.1073/pnas.1618934114CrossRefGoogle ScholarPubMed
Gray, J. M., Hill, J. J., & Bargmann, C. I. (2005). A circuit for navigation in Caenorhabditis elegans. Proceedings of the National Academy of Sciences, 102, 3184–3191. https://doi.org/10.1073/pnas.0409009101CrossRefGoogle ScholarPubMed
Groves, P. M., & Thompson, R. F. (1970). Habituation: A dual-process theory. Psychological Review, 77(5), 419–450. www.ncbi.nlm.nih.gov/pubmed/4319167CrossRefGoogle ScholarPubMed
Hart, A. C., Kass, J., Shapiro, J. E., & Kaplan, J. M. (1999). Distinct signaling pathways mediate touch and osmosensory responses in a polymodal sensory neuron. Journal of Neuroscience, 19, 1952–1958. https://doi.org/10.1523/jneurosci.19-06-01952.1999CrossRefGoogle Scholar
Hedgecock, E. M., & Russell, R. L. (1975). Normal and mutant thermotaxis in the nematode Caenorhabditis elegans. Proceedings of the National Academy of Sciences, 72, 4061–4065. https://doi.org/10.1073/pnas.72.10.4061CrossRefGoogle ScholarPubMed
Hong, M., Ryu, L., Ow, M. C., Kim, J., Je, A. R., Chinta, S., … Kim, K. (2017). Early pheromone experience modifies a synaptic activity to influence adult pheromone responses of C. elegans. Current Biology, 27, 3168–3177.e3. https://doi.org/10.1016/j.cub.2017.08.068CrossRefGoogle ScholarPubMed
Hukema, R. K., Rademakers, S., & Jansen, G. (2008). Gustatory plasticity in C. elegans involves integration of negative cues and NaCl taste mediated by serotonin, dopamine, and glutamate. Learning and Memory, 15, 829–836. https://doi.org/10.1101/lm.994408CrossRefGoogle Scholar
Jin, X., Pokala, N., & Bargmann, C. I. (2016). Distinct circuits for the formation and retrieval of an imprinted olfactory memory. Cell, 164, 632–643. https://doi.org/10.1016/j.cell.2016.01.007CrossRefGoogle ScholarPubMed
Kano, T., Brockie, P. J., Sassa, T., Fujimoto, H., Kawahara, Y., Iino, Y., … Maricq, A. V. (2008). Memory in Caenorhabditis elegans is mediated by NMDA-type ionotropic glutamate receptors. Current Biology, 18, 1010–1015. https://doi.org/10.1016/j.cub.2008.05.051CrossRefGoogle ScholarPubMed
Kauffman, A. L., Ashraf, J. M., Corces-Zimmerman, M. R., Landis, J. N., & Murphy, C. T. (2010). Insulin signaling and dietary restriction differentially influence the decline of learning and memory with age. PLoS Biology, 8, e1000372. https://doi.org/10.1371/journal.pbio.1000372CrossRefGoogle ScholarPubMed
Kindt, K. S., Quast, K. B., Giles, A. C., De, S., Hendrey, D., Nicastro, I., … Schafer, W. R. (2007). Dopamine mediates context-dependent modulation of sensory plasticity in C. elegans. Neuron, 55, 662–676. https://doi.org/10.1016/j.neuron.2007.07.023CrossRefGoogle ScholarPubMed
Kodama, E., Kuhara, A., Mohri-Shiomi, A., Kimura, K. D., Okumura, M., Tomioka, M., … Mori, I. (2006). Insulin-like signaling and the neural circuit for integrative behavior in C. elegans. Genes and Development, 20, 2955–2960. https://doi.org/10.1101/gad.1479906CrossRefGoogle ScholarPubMed
Kuhara, A., & Mori, I. (2006). Molecular physiology of the neural circuit for calcineurin-dependent associative learning in Caenorhabditis elegans. Journal of Neuroscience, 26, 9355–9364. https://doi.org/10.1523/JNEUROSCI.0517-06.2006CrossRefGoogle ScholarPubMed
Kuhara, A., Okumura, M., Kimata, T., Tanizawa, Y., Takano, R., Kimura, K. D., … Mori, I. (2008). Temperature sensing by an olfactory neuron in a circuit controlling behavior of C. elegans. Science, 320, 803–807. https://doi.org/10.1126/science.1148922CrossRefGoogle Scholar
Landry, C. D., Kandel, E. R., & Rajasethupathy, P. (2013). New mechanisms in memory storage: PiRNAs and epigenetics. Trends in Neurosciences, 36, 534–542. https://doi.org/10.1016/j.tins.2013.05.004CrossRefGoogle ScholarPubMed
Lau, H. L., Timbers, T. A, Mahmoud, R., & Rankin, C. H. (2013). Genetic dissection of memory for associative and non-associative learning in Caenorhabditis elegans. Genes, Brain and Behavior, 12, 210–223. https://doi.org/10.1111/j.1601-183X.2012.00863.xCrossRefGoogle ScholarPubMed
Lee, K., & Mylonakis, E. (2017). An intestine-derived neuropeptide controls avoidance behavior in Caenorhabditis elegans. Cell Reports, 20, 2501–2512. https://doi.org/10.1016/j.celrep.2017.08.053CrossRefGoogle ScholarPubMed
Li, C., Timbers, T. A., Rose, J. K., Bozorgmehr, T., McEwan, A., & Rankin, C. H. (2013). The FMRFamide-related neuropeptide FLP-20 is required in the mechanosensory neurons during memory for massed training in C. elegans. Learning & Memory, 20, 103–108. https://doi.org/10.1101/lm.028993.112CrossRefGoogle ScholarPubMed
Lim, J. P., Fehlauer, H., Das, A., Saro, G., Glauser, D. A., Brunet, A., & Goodman, M. B. (2018). Loss of CaMKI function disrupts salt aversive learning in C. elegans. Journal of Neuroscience, 38, 6114–6129. https://doi.org/10.1523/JNEUROSCI.1611-17.2018CrossRefGoogle ScholarPubMed
Lorenz, K. Z. (1981). The foundations of ethology. Springer Vienna. https://doi.org/10.1007/978-3-7091-3671-3CrossRefGoogle Scholar
Mita, K., Yamagishi, M., Fujito, Y., Lukowiak, K., & Ito, E. (2014). An increase in insulin is important for the acquisition conditioned taste aversion in Lymnaea. Neurobiology of Learning and Memory, 116, 132–138. https://doi.org/10.1016/j.nlm.2014.10.006CrossRefGoogle ScholarPubMed
Mohri, A., Kodama, E., Kimura, K. D., Koike, M., Mizuno, T., & Mori, I. (2005). Genetic control of temperature preference in the nematode Caenorhabditis elegans. Genetics, 169, 1437–1450. https://doi.org/10.1534/genetics.104.036111CrossRefGoogle ScholarPubMed
Moore, R. S., Kaletsky, R., & Murphy, C. T. (2019). Piwi/PRG-1 Argonaute and TGF-β mediate transgenerational learned pathogenic avoidance. Cell, 177, 1827–1841.e12. https://doi.org/10.1016/j.cell.2019.05.024CrossRefGoogle ScholarPubMed
Mori, I., & Ohshima, Y. (1995). Neural regulation of thermotaxis in Caenorhabditis elegans. Nature, 376(6538), 344–348. https://doi.org/10.1038/376344a0CrossRefGoogle ScholarPubMed
Morrison, G. E., & van der Kooy, D. (2001). A mutation in the AMPA-type glutamate receptor, glr-1, blocks olfactory associative and nonassociative learning in Caenorhabditis elegans. Behavioral Neuroscience, 115, 640–649. https://doi.org/10.1037/0735-7044.115.3.640CrossRefGoogle ScholarPubMed
Morrison, G. E., Wen, J. Y. M., Runciman, S., & van der Kooy, D. (1999). Olfactory associative learning in Caenorhabditis elegans is impaired in lrn-1 and lrn-2 mutants. Behavioral Neuroscience, 113, 358–367. https://doi.org/10.1037//0735-7044.113.2.358CrossRefGoogle ScholarPubMed
Nishijima, S., & Maruyama, I. N. (2017). Appetitive olfactory learning and long-term associative memory in Caenorhabditis elegans. Frontiers in Behavioral Neuroscience, 11, 80. https://doi.org/10.3389/fnbeh.2017.00080CrossRefGoogle ScholarPubMed
Nuttley, W. M., Atkinson-Leadbeater, K. P., & van der Kooy, D. (2002). Serotonin mediates food-odor associative learning in the nematode Caenorhabditis elegans. Proceedings of the National Academy of Sciences, 99, 12449–12454. https://doi.org/10.1073/pnas.192101699CrossRefGoogle Scholar
Nuttley, W. M., Harbinder, S., & van der Kooy, D. (2001). Regulation of distinct attractive and aversive mechanisms mediating benzaldehyde chemotaxis in Caenorhabditis elegans. Learning and Memory, 8, 170–181. https://doi.org/10.1101/lm.36501CrossRefGoogle ScholarPubMed
Ohnishi, N., Kuhara, A., Nakamura, F., Okochi, Y., & Mori, I. (2011). Bidirectional regulation of thermotaxis by glutamate transmissions in Caenorhabditis elegans. EMBO Journal, 30, 1376–1388. https://doi.org/10.1038/emboj.2011.13CrossRefGoogle ScholarPubMed
Peymen, K., Watteyne, J., Borghgraef, C., Van Sinay, E., Beets, I., & Schoofs, L. (2019). Myoinhibitory peptide signaling modulates aversive gustatory learning in Caenorhabditis elegans. PLOS Genetics, 15, e1007945. https://doi.org/10.1371/journal.pgen.1007945CrossRefGoogle ScholarPubMed
Pierce-Shimomura, J. T., Faumont, S., Gaston, M. R., Pearson, B. J., & Lockery, S. R. (2001). The homeobox gene lim-6 is required for distinct chemosensory representations in C. elegans. Nature, 410, 694–698. https://doi.org/10.1038/35070575CrossRefGoogle ScholarPubMed
Pinsker, H., Kupfermann, I., Castellucci, V., & Kandel, E. (1970). Habituation and dishabituation of the gill-withdrawal reflex in Aplysia. Science, 167, 1740–1742. https://doi.org/10.1126/science.167.3926.1740CrossRefGoogle ScholarPubMed
Ramaswami, M. (2014). Network plasticity in adaptive filtering and behavioral habituation. Neuron, 82, 1216–1229. https://doi.org/10.1016/j.neuron.2014.04.035CrossRefGoogle ScholarPubMed
Rankin, C. H., Abrams, T., Barry, R. J., Bhatnagar, S., Clayton, D. F., Colombo, J., … Thompson, R. F. (2009). Habituation revisited: An updated and revised description of the behavioral characteristics of habituation. Neurobiology of Learning and Memory, 92, 135–138. https://doi.org/10.1016/j.nlm.2008.09.012CrossRefGoogle ScholarPubMed
Rankin, C. H., Beck, C. D., & Chiba, C. M. (1990). Caenorhabditis elegans: A new model system for the study of learning and memory. Behavioural Brain Research, 37, 89–92. https://doi.org/10.1016/0166-4328(90)90074-OCrossRefGoogle Scholar
Rankin, C. H., & Broster, B. S. (1992). Factors affecting habituation and recovery from habituation in the nematode Caenorhabditis elegans. Behavioral Neuroscience, 106, 239–249. https://doi.org/10.1037/0735-7044.106.2.239CrossRefGoogle ScholarPubMed
Rankin, C. H., & Wicks, S. R. (2000). Mutations of the Caenorhabditis elegans brain-specific inorganic phosphate transporter eat-4 affect habituation of the tap-withdrawal response without affecting the response itself. Journal of Neuroscience, 20, 4337–4344.CrossRefGoogle Scholar
Remy, J. J., & Hobert, O. (2005). Neuroscience: An interneuronal chemoreceptor required for olfactory imprinting in C. elegans. Science, 309, 787–790. https://doi.org/10.1126/science.1114209CrossRefGoogle Scholar
Rose, J. K., Kaun, K. R., Chen, S. H., & Rankin, C. H. (2003). GLR-1, a non-NMDA glutamate receptor homolog, is critical for long-term memory in Caenorhabditis elegans. Journal of neuroscience, 23, 9595–9599. https://doi.org/10.1523/JNEUROSCI.23-29-09595.2003CrossRefGoogle ScholarPubMed
Rose, J. K., Kaun, K. R., & Rankin, C. H. (2002). A new group-training procedure for habituation demonstrates that presynaptic glutamate release contributes to long-term memory in Caenorhabditis elegans. Learning and Memory, 9, 130–137. https://doi.org/10.1101/lm.46802CrossRefGoogle ScholarPubMed
Rose, J. K., & Rankin, C. H. (2006). Blocking memory reconsolidation reverses memory-associated changes in glutamate receptor expression. Journal of Neuroscience, 26, 11582–11587. https://doi.org/10.1523/JNEUROSCI.2049-06.2006CrossRefGoogle ScholarPubMed
Saeki, S., Yamamoto, M., & Iino, Y. (2001). Plasticity of chemotaxis revealed by paired presentation of a chemoattractant and starvation in the nematode Caenorhabditis elegans. Journal of Experimental Biology, 204(10), 1757–1764. https://doi.org/10.1242/jeb.204.10.1757CrossRefGoogle ScholarPubMed
Sakai, N., Iwata, R., Yokoi, S., Butcher, R. A., Clardy, J., Tomioka, M., & Iino, Y. (2013). A sexually conditioned switch of chemosensory behavior in C. elegans. PLoS ONE, 8(7): e68676. https://doi.org/10.1371/journal.pone.0068676CrossRefGoogle ScholarPubMed
Sammut, M., Cook, S. J., Nguyen, K. C. Q., Felton, T., Hall, D. H., Emmons, S. W., … Barrios, A. (2015). Glia-derived neurons are required for sex-specific learning in C. elegans. Nature, 526(7573), 385–390. https://doi.org/10.1038/nature15700CrossRefGoogle ScholarPubMed
Schulenburg, H., & Félix, M. A. (2017). The natural biotic environment of Caenorhabditis elegans. Genetics, 206, 55–86. https://doi.org/10.1534/genetics.116.195511CrossRefGoogle ScholarPubMed
Sulston, J. E., Schierenberg, E., White, J. G., & Thomson, J. N. (1983). The embryonic cell lineage of the nematode Caenorhabditis elegans. Developmental Biology, 100, 64–119. https://doi.org/10.1016/0012-1606(83)90201-4CrossRefGoogle ScholarPubMed
Timbers, T. A., Giles, A. C., Ardiel, E. L., Kerr, R. A., & Rankin, C. H. (2013). Intensity discrimination deficits cause habituation changes in middle-aged Caenorhabditis elegans. Neurobiology of Aging, 34, 621–631. https://doi.org/10.1016/j.neurobiolaging.2012.03.016CrossRefGoogle ScholarPubMed
Timbers, T. A., & Rankin, C. H. (2011). Tap withdrawal circuit interneurons require CREB for long-term habituation in Caenorhabditis elegans. Behavioral Neuroscience, 125, 560–566. https://doi.org/10.1037/a0024370CrossRefGoogle ScholarPubMed
Tomioka, M., Adachi, T., Suzuki, H., Kunitomo, H., Schafer, W. R., & Iino, Y. (2006). The Insulin/PI 3-Kinase pathway regulates salt chemotaxis learning in Caenorhabditis elegans. Neuron, 51, 613–625. https://doi.org/10.1016/j.neuron.2006.07.024CrossRefGoogle ScholarPubMed
Torayama, I., Ishihara, T., & Katsura, I. (2007). Caenorhabditis elegans integrates the signals of butanone and food to enhance chemotaxis to butanone. Journal of Neuroscience, 27, 741–750. https://doi.org/10.1523/JNEUROSCI.4312-06.2007CrossRefGoogle ScholarPubMed
Wen, J. Y. M., Kumar, N., Morrison, G., Rambaldini, G., Runciman, S., Rousseau, J., & Van Der Kooy, D. (1997). Mutations that prevent associative learning in C. elegans. Behavioral Neuroscience, 111, 354–368. https://doi.org/10.1037/0735-7044.111.2.354CrossRefGoogle ScholarPubMed
White, J. G., Southgate, E., Thomson, J. N., & Brenner, S. (1986). The structure of the nervous system of the nematode Caenorhabditis elegans. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 314, 1–340.Google ScholarPubMed
Wicks, S. R., & Rankin, C. H. (1995). Integration of mechanosensory stimuli in Caenorhabditis elegans. Journal of Neuroscience, 15, 2434–2444.CrossRefGoogle ScholarPubMed
Wu, T., Duan, F., Yang, W., Liu, H., Caballero, A., Fernandes de Abreu, D. A., … Zhang, Y. (2019). Pheromones modulate learning by regulating the balanced signals of two insulin-like peptides. Neuron, 104, 1095–1109.e5. https://doi.org/10.1016/j.neuron.2019.09.006CrossRefGoogle ScholarPubMed
Yamazoe-Umemoto, A., Fujita, K., Iino, Y., Iwasaki, Y., & Kimura, K. D. (2015). Modulation of different behavioral components by neuropeptide and dopamine signalings in non-associative odor learning of Caenorhabditis elegans. Neuroscience Research, 99, 22–33. https://doi.org/10.1016/j.neures.2015.05.009CrossRefGoogle ScholarPubMed
Zhang, X., & Zhang, Y. (2012). DBL-1, a TGF-β, is essential for Caenorhabditis elegans aversive olfactory learning. Proceedings of the National Academy of Sciences USA, 109, 17081–17086. https://doi.org/10.1073/pnas.1205982109CrossRefGoogle ScholarPubMed
Zhang, Y., Lu, H., & Bargmann, C. I. (2005). Pathogenic bacteria induce aversive olfactory learning in Caenorhabditis elegans. Nature, 438, 179–184. https://doi.org/10.1038/nature04216CrossRefGoogle ScholarPubMed
References
Almaguer-Melian, W., Rojas-Reyes, Y., Alvare, A., Rosillo, J. C., Frey, J. U., & Bergado, J. A. (2005). Long-term potentiation in the dentate gyrus in freely moving rats is reinforced by intraventricular application of norepinephrine, but not oxotremorine. Neurobiology of Learning & Memory, 83, 72–78. https://doi.org/10.1016/j.nlm.2004.08.002CrossRefGoogle Scholar
Bailey, C. H., Giustetto, M., Huang, Y. Y., Hawkins, R. D., & Kandel, E. R. (2000). Is heterosynaptic modulation essential for stabilizing Hebbian plasticity and memory? Nature Reviews Neuroscience, 1, 11–20. https://doi.org/10.1038/35036191CrossRefGoogle ScholarPubMed
Baldwin, J. M. (1896). A new factor in evolution. American Naturalist, 30, 441–451.CrossRefGoogle Scholar
Berriman, J. S., Kay, M. C., Reed, D. C., Rassweiler, A., Goldstein, D. A., & Wright, W. G. (2015). Shifts in attack behavior of an important kelp forest predator within marine reserves. Marine Ecology Progress Series, 522, 193–201. https://doi.org/10.3354/meps11157CrossRefGoogle Scholar
Bertness, M. D., Garrity, S. D., & Levings, S. C. (1981). Predation pressure and gastropod foraging: A tropical-temperate comparison. Evolution, 35, 995–1007. https://doi.org/10.2307/2407870Google ScholarPubMed
Blumstein, D. T. (2006). The multipredator hypothesis and the evolutionary persistence of antipredator behavior. Ethology, 112, 209–217. https://doi.org/10.1111/j.1439-0310.2006.01209.xCrossRefGoogle Scholar
Bornancin, L., Bonnard, I., Mills, S., & Banaigs, B. (2017). Chemical mediation as a structuring element in marine gastropod predator–prey interactions. Natural Product Reports, 34, 644–676. https://doi.org/10.1039/C6NP00097ECrossRefGoogle ScholarPubMed
Bouchet, P., Rocroi, J.-P., Hausdorf, B., Kaim, A., Kano, Y., Nützel, A., Parkhaev, Pavel, Schrödl, Michael, & Strong, E. E. (2017). Revised classification, nomenclator and typification of gastropod and monoplacophoran families. Malacologia, 61, 1–526. https://doi.org/10.4002/040.061.0201CrossRefGoogle Scholar
Byers, J. A. (1997). American pronghorn: Social adaptations and the ghosts of predators past. University of Chicago Press.Google Scholar
Byrne, J. H., & Kandel, E. R. (1996). Presynaptic facilitation revisited: State and time dependence. Journal of Neuroscience, 16, 425–435. https://doi.org/10.1523/JNEUROSCI.16-02-00425CrossRefGoogle ScholarPubMed
Carefoot, T. H. (1987). Aplysia: Its biology and ecology. Oceanography & Marine Biology, 25, 167–284. <Go to ISI>://WOS:A1987K531000005Google Scholar
Carew, T. J. (2000). Behavioral neurobiology: The cellular organization of natural behavior. Sinauer.Google Scholar
Carew, T. J., Hawkins, R. D., & Kandel, E. R. (1983). Differential classical conditioning of a defensive withdrawal reflex in Aplysiida californica. Science, 219, 397–400. https://doi.org/10.1126/science.6681571CrossRefGoogle Scholar
Chitwood, R. A., Li, Q., & Glanzman, D. L. (2001). Serotonin facilitates AMPA-type responses in isolated siphon motor neurons of Aplysia in culture. Journal of Physiology-London, 534, 501–510. https://doi.org/10.1111/j.1469-7793.2001.00501.xCrossRefGoogle ScholarPubMed
Cimino, G., & Ghiselin, M. T. (2009). Chemical defense and the evolution of opisthobranch gastropods. Proceedings of the California Academy of Sciences, 60, 175.Google Scholar
Cleary, L. J., Byrne, J. H., & Frost, W. N. (1995). Role of interneurons in defensive withdrawal reflexes in Aplysia. Learning & Memory, 2, 133–151. https://doi.org/10.1101/lm.2.3.133CrossRefGoogle ScholarPubMed
Cleary, L. J., Lee, W. L., & Byrne, J. H. (1998). Cellular correlates of long-term sensitization in Aplysia. Journal of Neuroscience, 18, 5988–5998. https://doi.org/10.1523/JNEUROSCI.18-15-05988CrossRefGoogle ScholarPubMed
Crook, R. J., Dickson, K., Hanlon, R. T., & Walters, E. T. (2014). Nociceptive sensitization reduces predation risk. Current Biology, 24, 1121–1125. https://doi.org/10.1016/j.cub.2014.03.043CrossRefGoogle ScholarPubMed
Derby, C. D. (2007). Escape by inking and secreting: Marine molluscs avoid predators through a rich array of chemicals and mechanisms. Biological Bulletin, 213, 274–289. https://doi.org/10.2307/25066645CrossRefGoogle ScholarPubMed
Derby, C. D., & Aggio, J. F. (2011). The neuroecology of chemical defenses. Integrative & Comparative Biology, 51, 771–780. https://doi.org/10.1093/icb/icr063CrossRefGoogle ScholarPubMed
Ding, L., & Perkel, D. J. (2004). Long-term potentiation in an avian basal ganglia nucleus essential for vocal learning. Journal of Neuroscience, 24, 488–494. https://doi.org/10.1523/JNEUROSCI.4358-03.2004CrossRefGoogle Scholar
Eliot, L. S., Hawkins, R. D., Kandel, E. R., & Schacher, S. (1994). Pairing-specific, activity-dependent presynaptic facilitation at Aplysia sensory-motor neuron synapses in isolated cell-culture. Journal of Neuroscience, 14, 368–383. https://doi.org/10.1523/JNEUROSCI.14-01-00368CrossRefGoogle ScholarPubMed
Erixon, N. J., Demartini, L. J., & Wright, W. G. (1999). Dissociation between sensitization and learning-related neuromodulation in an aplysiid species. Journal of Comparative Neurology, 408, 506–514.3.0.CO;2-P>CrossRefGoogle Scholar
Estes, J. A., & Steinberg, P. D. (1988). Predation, herbivory, and kelp evolution. Paleobiology, 14, 19–36. https://doi.org/10.1017/S0094837300011775CrossRefGoogle Scholar
Frost, W. N., Clark, G. A., & Kandel, E. R. (1988). Parallel processing of short-term memory for sensitization in Aplysia. Journal of Neurobiology, 19, 297–334. https://doi.org/10.1002/neu.480190402CrossRefGoogle ScholarPubMed
Gillette, R. (2006). Evolution and function in serotonergic systems. Integrative & Comparative Biology, 46, 838–846. https://doi.org/10.1093/icb/icl024CrossRefGoogle ScholarPubMed
Glanzman, D. L. (1995). The cellular basis of classical conditioning in Aplysia californica: It’s less simple than you think. Trends in Neurosciences, 18, 30–36. https://doi.org/10.1016/0166-2236(95)93947-VCrossRefGoogle Scholar
Glanzman, D. L. (2008). New tricks for an old slug: The critical role of postsynaptic mechanisms in learning and memory in Aplysia. In Sossin, W. S., Lacaille, J. C., Castellucci, V. F., & Belleville, S. (Eds.), Essence of memory (Vol. 169, pp. 277–292). Elsevier. https://doi.org/10.1016/S0079-6123(07)00017-9CrossRefGoogle Scholar
Glanzman, D. L. (2010). Common mechanisms of synaptic plasticity in vertebrates and invertebrates. Current Biology, 20(1), R31–R36.CrossRefGoogle ScholarPubMed
Glanzman, D. L., Mackey, S. L., Hawkins, R. D., Dyke, A. M., Lloyd, P. E., & Kandel, E. R. (1989). Depletion of serotonin in the nervous system of Aplysia reduces the behavioral enhancement of gill withdrawal as well as the heterosynaptic facilitation produced by tail shock. Journal of Neuroscience, 9, 4200–4213. https://doi.org/10.1523/JNEUROSCI.09-12-04200.1989CrossRefGoogle ScholarPubMed
Harley, C. W. (2007). Norepinephrine and the dentate gyrus. In Scharfman, H. E. (Ed.), Dentate Gyrus: A Comprehensive Guide to Structure, Function, and Clinical Implications (Vol. 163, pp. 299–318). Elsevier. https://doi.org/10.1016/S0079-6123(07)63018-0CrossRefGoogle Scholar
Himstead, A., & Wright, W. G. (2018). Precise foraging schedule in an intertidal euopisthobranch mollusk. Marine & Freshwater Behaviour and Physiology, 51, 131–141. https://doi.org/10.1080/10236244.2018.1505430CrossRefGoogle Scholar
Hoover, B. A., Nguyen, H., Thompson, L., & Wright, W. G. (2006). Associative memory in three aplysiids: Correlation with heterosynaptic modulation. Learning & Memory, 13, 820–826. https://doi.org/10.1101/lm.284006CrossRefGoogle ScholarPubMed
Jami, S. A., Wright, W. G., & Glanzman, D. L. (2007). Differential classical conditioning of the gill-withdrawal reflex in Aplysia recruits both NMDA receptor-dependent enhancement and NMDA receptor-dependent depression of the reflex. Journal of Neuroscience, 27, 3064–3068. https://doi.org/10.1523/jneurosci.2581-06.2007CrossRefGoogle ScholarPubMed
Jing, J., Vilim, F. S., Cropper, E. C., & Weiss, K. R. (2008). Neural analog of arousal: Persistent conditional activation of a feeding modulator by serotonergic initiators of locomotion. Journal of Neuroscience, 28, 12349–12361. https://doi.org/10.1523/jneurosci.3855-08.2008CrossRefGoogle ScholarPubMed
Kandel, E. R. (1976). Cellular basis of behavior: An introduction to behavioral neurobiology. Freeman.Google Scholar
Kandel, E. R. (2012). The molecular biology of memory: cAMP, PKA, CRE, CREB-1, CREB-2, and CPEB. Molecular Brain, 5: 14. https://doi.org/10.1186/1756-6606-5-14.CrossRefGoogle ScholarPubMed
Kandel, E. R., Klein, M., Hochner, B., Shuster, M., Siegelbaum, S. A., Hawkins, R. D., Glanzman, D. L., Castellucci, V. F., and Abrams, T. W. (1987). Synaptic modulation and learning: New insights into synaptic transmission from the study of behavior. In Edelman, G. & Gall, W. E. (Eds.), Synaptic function (pp. 472–518). John Wiley & Sons. https://doi.org/10.1002/hup.470050111Google Scholar
Kandel, E. R., & Schwartz, J. H. (1982). Molecular biology of learning: Modulation of transmitter release. Science, 218, 433–443. https://doi.org/10.1126/science.6289442CrossRefGoogle ScholarPubMed
Krug, P. J. (2011). Patterns of speciation in marine gastropods: A review of the phylogenetic evidence for localized radiations in the sea. American Malacological Bulletin, 29, 169–186. https://doi.org/10.4003/006.029.0210CrossRefGoogle Scholar
Lahti, D. C., Johnson, N. A., Ajie, B. C., Otto, S. P., Hendry, A. P., Blumstein, D. T., Coss, R. G., Donohue, K., and Foster, S. A. (2009). Relaxed selection in the wild. Trends in Ecology & Evolution, 24, 487–496. https://doi.org/10.1016/j.tree.2009.03.010CrossRefGoogle ScholarPubMed
LeDoux, J. E. (2000). Emotion circuits in the brain. Annual Review of Neuroscience, 23, 155–184. https://doi.org/10.1146/annurev.neuro.23.1.155CrossRefGoogle Scholar
Lynch, M. A. (2004). Long-term potentiation and memory. Physiological Reviews, 84, 87–136. https://doi.org/10.1152/physrev.00014.2003CrossRefGoogle ScholarPubMed
Mackey, S., & Carew, T. J. (1983). Locomotion in Aplysia: Triggering by serotonin and modulation by bag-cell extract. Journal of Neuroscience, 3, 1469–1477. https://doi.org/10.1523/JNEUROSCI.03-07-01469.1983CrossRefGoogle ScholarPubMed
Marcus, E. A., Nolen, T. G., Rankin, C. H., & Carew, T. J. (1988). Behavioral dissociation of dishabituation, sensitization and inhibition in Aplysia. Science, 241, 210–213. https://doi.org/10.1126/science.3388032CrossRefGoogle ScholarPubMed
Marinesco, P., & Carew, T. J. (2002). Serotonin release evoked by tail nerve stimulation in the CNS of Aplysia: Characterization and relationship to heterosynaptic plasticity. Journal of Neuroscience, 22, 2299–2312. https://doi.org/10.1523/JNEUROSCI.22-06-02299.2002CrossRefGoogle ScholarPubMed
Marinesco, S., Duran, K. L., & Wright, W. G. (2003). Evolution of learning in three aplysiid species: Differences in heterosynaptic plasticity contrast with conservation in serotonergic pathways. Journal of Physiology-London, 550, 241–253. https://doi.org/10.1113/jphysiol.2003.038356CrossRefGoogle ScholarPubMed
Marinesco, S., Wickremasinghe, N., Kolkman, K. E., & Carew, T. J. (2004). Serotonergic modulation in Aplysia. II. Cellular and behavioral consequences of increased serotonergic tone. Journal of Neurophysiology, 92, 2487–2496. https://doi.org/10.1152/jn.00210.2004CrossRefGoogle ScholarPubMed
Martin, S. J., Grimwood, P. D., & Morris, R. G. M. (2000). Synaptic plasticity and memory: An evaluation of the hypothesis. Annual Review of Neuroscience, 23, 649–711. https://doi.org/10.1146/annurev.neuro.23.1.649CrossRefGoogle ScholarPubMed
Mason, M. J., Watkins, A. J., Wakabayashi, J., Buechler, J., Pepino, C., Brown, M., & Wright, W. G. (2014). Connecting model species to nature: Predator-induced long-term sensitization in Aplysia californica. Learning & Memory, 21, 363–367. https://doi.org/10.1101/lm.034330.114CrossRefGoogle ScholarPubMed
Nature Research Highlights (2010) Animal behaviour: Lobster shock. Nature 467, 8.CrossRefGoogle Scholar
Owen, G. R., & Brenner, E. A. (2012). Mapping molecular memory: Navigating the cellular pathways of learning. Cellular & Molecular Neurobiology, 32, 919–941. https://doi.org/10.1007/s10571-012-9836-0CrossRefGoogle Scholar
Paine, R. T. (1966). Food web complexity and species diversity. American Naturalist, 100, 65–75. https://doi.org/10.1086/282400CrossRefGoogle Scholar
Palmer, A. R. (1979). Fish predation and the evolution of gastropod shell sculpture: Experimental and geographic evidence. Evolution, 33, 697–713. https://doi.org/10.2307/2407792CrossRefGoogle ScholarPubMed
Papini, M. R. (2002). Pattern and process in the evolution of learning. Psychological Review, 109, 186–201. https://doi.org/10.1037/0033-295X.109.1CrossRefGoogle ScholarPubMed
Pennings, S. C., Nadeau, M. T., & Paul, V. J. (1993). Selectivity and growth of the generalist herbivore, Dolabella auricularia feeding upon complementary resources. Ecology, 74, 879–890. https://doi.org/10.2307/1940813CrossRefGoogle Scholar
Pennings, S. C., & Paul, V. J. (1993). Sequestration of dietary secondary metabolites by 3 species of sea hares-location, specificity, and dynamics. Marine Biology, 117, 535–546. https://doi.org/10.1007/BF00349763CrossRefGoogle Scholar
Pennings, S. C., Paul, V. J., Dunbar, D. C., Hamann, M. T., Lumbang, W. A., Novack, B., & Jacobs, R. S. (1999). Unpalatable compounds in the marine gastropod Dolabella auricularia: Distribution and effect of diet. Journal of Chemical Ecology, 25(4), 735–755. Retrieved from <Go to ISI>://WOS:000080123000005CrossRefGoogle Scholar
Perrot-Minnot, M. J., Banchetry, L., & Cézilly, F. (2017). Anxiety-like behaviour increases safety from fish predation in an amphipod crustacea. Royal Society Open Science, 4, 171558. https://doi.org/10.1098/rsos.171558CrossRefGoogle Scholar
Ricketts, E. F., Calvin, J., & Hedgpeth, J. W. (1992). Between Pacific tides (5th ed.). Stanford University Press.Google Scholar
Schultz, W. (1998). Predictive reward signal of dopamine neurons. Journal of Neurophysiology, 80, 1–27. https://doi.org/10.1152/jn.1998.80.1.1CrossRefGoogle ScholarPubMed
Senter, P. (2010). Vestigial skeletal structures in dinosaurs. Journal of Zoology, 280, 60–71. https://doi.org/10.1111/j.1469-7998.2009.00640.xCrossRefGoogle Scholar
Stopfer, M., & Carew, T. J. (1988). Development of sensitization in the escape locomotion system in Aplysia. Journal of Neuroscience, 8, 223–230. https://doi.org/10.1523/JNEUROSCI.08-01-00223.1988CrossRefGoogle ScholarPubMed
Takagi, K. K., Ono, N., & Wright, W. G. (2010). Interspecific variation in palatability suggests cospecialization of antipredator defenses in a sea hare. Marine Ecology Progress Series, 416, 137–144. https://doi.org/10.3354/meps08738CrossRefGoogle Scholar
Tetreault, I., & Ambrose, R. F. (2007). Temperate marine reserves enhance targeted but not untargeted fishes in multiple no-take maps. Ecological Applications, 17, 2251–2267. https://doi.org/10.1890/06-0161.1CrossRefGoogle ScholarPubMed
Vermeij, G. J. (1994). The evolutionary interaction among species: Selection, escalation, and coevolution. Annual Review of Ecology & Systematics, 25, 219–236. https://doi.org/10.1146/annurev.es.25.110194.001251CrossRefGoogle Scholar
Vermeij, G. J. (2013). On escalation. Annual Review of Earth & Planetary Sciences, 41, 1–19. https://doi.org/10.1146/annurev-earth-050212-124123CrossRefGoogle Scholar
Walker, S. E., & Brett, C. E. (2002). Post-Paleozoic patterns in marine predation: Was there a Mesozoic and Cenozoic marine predatory revolution? Paleontological Society Papers, 8, 119–194. https://doi.org/10.1017/S108933260000108XCrossRefGoogle Scholar
Walters, E. T. (1987). Site-specific sensitization of defensive reflexes in Aplysia: A simple model of long-term hyperalgesia. Journal of Neuroscience, 7, 400–407. https://doi.org/10.1523/JNEUROSCI.07-02-00400.1987CrossRefGoogle ScholarPubMed
Walters, E. T. (1991). A functional, cellular, and evolutionary model of nociceptive plasticity in Aplysia. Biological Bulletin, 180, 241–251. https://doi.org/10.2307/1542394CrossRefGoogle ScholarPubMed
Walters, E. T. (1994). Injury-related behavior and neuronal plasticity: An evolutionary perspective on sensitization, hyperalgesia, and analgesia. International Review of Neurobiology, 36, 325–427. https://doi.org/10.1016/S0074-7742(08)60307-4CrossRefGoogle ScholarPubMed
Walters, E. T. (2018). Nociceptive biology of molluscs and arthropods: evolutionary clues about functions and mechanisms potentially related to pain. Frontiers in Physiology, 9, 1049.CrossRefGoogle Scholar
Walters, E. T. (2019). Adaptive mechanisms driving maladaptive pain: How chronic ongoing activity in primary nociceptors can enhance evolutionary fitness after severe injury. Philosophical Transactions of the Royal Society B-Biological Sciences, 374, 20190277. https://doi.org/10.1098/rstb.2019.0277CrossRefGoogle ScholarPubMed
Watkins, A. J., Goldstein, D. A., Lee, L. C., Pepino, C. J., Tillett, S. L., Ross, F. E., Wilder, E. L., and Wright, W. G. (2010). Lobster attack induces sensitization in the sea hare, Aplysia californica. Journal of Neuroscience, 30, 11028–11031. https://doi.org/10.1523/JNEUROSCI.1317-10.2010CrossRefGoogle ScholarPubMed
West-Eberhard, M. J. (1989). Phenotypic plasticity and the origins of diversity. Annual Review of Ecology and Systematics, 20(1), 249–278.CrossRefGoogle Scholar
West-Eberhard, M. J. (2003). Developmental plasticity and evolution. Oxford University Press.CrossRefGoogle Scholar
White, J. A., Ziv, I., Cleary, L. J., Baxter, D. A., & Byrne, J. H. (1993). The role of interneurons in controlling the tail-withdrawal reflex. Journal of Neurophysiology, 70, 1777–1786. https://doi.org/10.1152/jn.1993.70.5.1777CrossRefGoogle ScholarPubMed
Wright, W. G. (1998). Evolution of nonassociative learning: Behavioral analysis of a phylogenetic lesion. Neurobiology of Learning & Memory, 69, 326–337. https://doi.org/10.1006/nlme.1998.3829CrossRefGoogle ScholarPubMed
Wright, W. G. (2000). Neuronal and behavioral plasticity in evolution: Experiments in a model lineage. Bioscience, 50, 883–894. https://doi.org/10.1006/nlme.1998.3829CrossRefGoogle Scholar
Wright, W. G., Jones, K., Sharp, P., & Maynard, B. (1995). Widespread anatomical projections of the serotonergic modulatory neuron, CB1, in Aplysia. Invertebrate Neuroscience 1, 173–183. https://doi.org/10.1007/bf02331914CrossRefGoogle ScholarPubMed
Wright, W. G., Kirschman, D., Rozen, D., & Maynard, B. (1996). Phylogenetic analysis of learning-related neuromodulation in molluscan mechanosensory neurons. Evolution, 50, 2248–2263. https://doi.org/10.1111/j.1558-5646.1996.tb03614.xGoogle ScholarPubMed
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, 93–96. https://doi.10.1126/science.206.4414.93CrossRefGoogle ScholarPubMed
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 Scholar
Alghamdi, A., Dalton, L., Phillis, A., Rosato, E., & Mallon, E. B. (2008). Immune response impairs learning in free-flying bumble-bees. Biology Letters, 4, 479–481. https://doi.org/10.1098/rsbl.2008.0331CrossRefGoogle ScholarPubMed
Applewhite, P. B. (1968). Non-local nature of habituation in a rotifer and protozoan. Nature, 217, 287–288. https://doi.org/10.1038/217287a0CrossRefGoogle 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, 85–92. https://doi.org/10.1016/j.jinsphys.2018.07.001CrossRefGoogle ScholarPubMed
Armus, H. L., Montgomery, A. R., & Gurney, R. L. (2006). Discrimination learning and extinction in Paramecia (P. caudatum). Psychological Reports, 98, 705–711. https://doi.org/10.2466%2Fpr0.98.3.705-711CrossRefGoogle Scholar
Bailey, N. W., & Zuk, M. (2009). Field crickets change mating preferences using remembered social information. Biology Letters, 5, 449–451. https://doi.org/10.1098/rsbl.2009.0112CrossRefGoogle ScholarPubMed
Bernays, E. A. (1993). Aversion learning and feeding. In Papaj, D. R. & Lewis, A. C. (Eds.), Insect learning (pp. 1–17). 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. 61–80). The MIT Press.Google 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, 168–172. https://doi.org/10.1098/rsbl.2010.1056CrossRefGoogle ScholarPubMed
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.2018.0368CrossRefGoogle ScholarPubMed
Campbell, H. R., & Strausfeld, N. J. (2001). Learned discrimination of pattern orientation in walking flies. Journal of Experimental Biology, 204, 1–14.CrossRefGoogle ScholarPubMed
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/10.1186/1475-2875-11-27CrossRefGoogle ScholarPubMed
Coolen, I., Dangles, O., & Casas, J. (2005). Social learning in noncolonial insects? Current Biology, 21, 1931–1935. 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, 229–240. https://doi.org/10.1111/eea.12129CrossRefGoogle Scholar
Decker, S., McConnaughey, S., & Page, T. L. (2007). Circadian regulation of insect olfactory learning. Proceedings of the National Academy of Sciences, 104, 15905–15910. https://doi.org/10.1073/pnas.0702082104CrossRefGoogle ScholarPubMed
DesJardins, N., & Tibbetts, E. A. (2018). Sex differences in face but not colour learning in Polistes fuscatus paper wasps. Animal Behaviour, 140, 1–6. 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, 195–200. https://doi.org/10.1007/s002650050553CrossRefGoogle Scholar
Dukas, R. (2008). Evolutionary biology of insect learning. Annual Review of Entomology, 53, 145–160. 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, 2637–2640. 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, 536–543. 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, 1067–1076. 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.0177581CrossRefGoogle ScholarPubMed
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.2014.00043CrossRefGoogle ScholarPubMed
Fukushi, T. (1989). Learning and discrimination of coloured papers in the walking blowfly, Lucilia cuprina. Journal of Comparative Physiology A, 166, 57–64. 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/srep38427CrossRefGoogle ScholarPubMed
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.0058693CrossRefGoogle ScholarPubMed
Giurfa, M. (2013). Cognition with few neurons: Higher-order learning in insects. Trends in Neurosciences, 36, 285–294. https://doi.org/10.1016/j.tins.2012.12.011CrossRefGoogle ScholarPubMed
Giurfa, M. (2015). Learning and cognition in insects. Wiley Interdisciplinary Reviews: Cognitive Science, 6, 383–395. https://doi.org/10.1002/wcs.1348Google ScholarPubMed
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, 737–741. https://doi.org/10.1016/0022-1910(78)90071-9CrossRefGoogle 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. 647–649). 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, 177–184. https://doi.org/10.1016/j.tree.2014.01.004CrossRefGoogle ScholarPubMed
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, 224–232. 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, 595–600. https://doi.org/10.1007/s00114-007-0233-3CrossRefGoogle ScholarPubMed
Haralson, J. V., Groff, C. I., & Haralson, S. J. (1975). Classical conditioning in the sea anemone, Cribrina xanthogrammica. Physiology & Behavior, 15, 455–460. https://doi.org/10.1016/0031-9384(75)90259-0CrossRefGoogle ScholarPubMed
Hoedjes, K. M., & Smid, H. M. (2014). Natural variation in long-term memory formation among Nasonia parasitic wasp species. Behavioural Processes, 105, 40–45. https://doi.org/10.1016/j.beproc.2014.02.014CrossRefGoogle ScholarPubMed
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, 1–64. https://doi.org/10.1016/S0065-3454(08)60045-5CrossRefGoogle Scholar
Hollis, K. L. (1997). Contemporary research on Pavlovian conditioning: A “new” functional analysis. American Psychologist, 52, 956–965. https://psycnet.apa.org/doi/10.1037/0003-066X.52.9.956CrossRefGoogle ScholarPubMed
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 Scholar
Hollis, K. L., & Guillette, L. M. (2011). Associative learning in insects: Evolutionary models, mushroom bodies, and a neuroscientific conundrum. Comparative Cognition & Behavior Reviews, 6, 24–45. https://psycnet.apa.org/doi/10.3819/ccbr.2011.60004CrossRefGoogle 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, 1–18.CrossRefGoogle 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, 68–82. 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, 219–225. https://psycnet.apa.org/doi/10.1037/0735-7036.111.3.219CrossRefGoogle Scholar
Iqbal, J., & Mueller, U. (2007). Virus infection causes specific learning deficits in honeybee foragers. Proceedings of the Royal Society B, 274, 1517–1521. 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, 1121–1129. https://doi.org/10.1007/s00359-005-0035-zCrossRefGoogle ScholarPubMed
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, 363–370. https://doi.org/10.1007/s00359-006-0192-8CrossRefGoogle ScholarPubMed
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.1000569CrossRefGoogle ScholarPubMed
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, 163–173. 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, 205–215. 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, 635–636. 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.34348CrossRefGoogle ScholarPubMed
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, 1449–1459. https://doi.org/10.1111/evo.13498CrossRefGoogle Scholar
Loomis, W. F. (2014). Cell signaling during development of Dictyostelium. Developmental Biology, 391, 1–16. https://doi.org/10.1016/j.ydbio.2014.04.001CrossRefGoogle ScholarPubMed
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, E448–E457. https://doi.org/10.1073/pnas.1709037115CrossRefGoogle ScholarPubMed
Loukola, O. J., Perry, C. J., Coscos, L., & Chittka, L. (2017). Bumblebees show cognitive flexibility by improving on an observed complex behavior. Science, 355, 833–836. 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, 19–27. https://doi.org/10.1101/lm.1146009CrossRefGoogle ScholarPubMed
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, 30–36. https://doi.org/10.1016/j.nlm.2011.08.010CrossRefGoogle ScholarPubMed
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, 479–526. 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, 218–223. https://doi.org/10.1242/jeb.074898Google ScholarPubMed
Mingee, C. M. (2013). Retention of a brightness discrimination task in Paramecia, P. caudatum. International Journal of Comparative Psychology, 26, 202–212. https://escholarship.org/uc/item/5428c5xnCrossRefGoogle Scholar
Nelson, M. C. (1971). Classical conditioning in the blowfly (Phormia regina): Associative and excitatory factors. Journal of Comparative and Physiological Psychology, 77, 353–368. https://psycnet.apa.org/doi/10.1037/h0031882CrossRefGoogle ScholarPubMed
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, 543–556. https://doi.org/10.1002/ece3.1379CrossRefGoogle ScholarPubMed
Nöbel, S., Allain, M., Isabel, G., & Danchin, E. (2018). Mate copying in Drosophila melanogaster males. Animal Behaviour, 141, 9–15. 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, 417–420. https://doi.org/10.1101/lm.031427.113CrossRefGoogle ScholarPubMed
Perlman, R. L., & Pastan, I. (1971). The role of cyclic AMP in bacteria. Current Topics in Cellular Regulation, 3, 117–134.CrossRefGoogle Scholar
Perry, C. J., Barron, A. B., & Cheng, K. (2013). Invertebrate learning and cognition: Relating phenomena to neural substrate. WIREs Cognitive Science, 4, 561–582. https://doi.org/10.1002/wcs.1248CrossRefGoogle ScholarPubMed
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.2016.0246CrossRefGoogle ScholarPubMed
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, 335–341.Google Scholar
Quinn, W. G., Harris, W. A., & Benzer, S. (1974). Conditioned behavior in Drosophila melanogaster. Proceedings of the National Academy of Sciences, 71, 708–712. 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, R486–R488. https://doi.org/10.1016/j.cub.2009.04.047CrossRefGoogle Scholar
Rains, G. C., Utley, S. L., & Lewis, W. J. (2006). Behavioral monitoring of trained insects for chemical detection. Biotechnology Progress, 22, 2–8. 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, 1–14. https://doi.org/10.3389/fnbeh.2016.00105CrossRefGoogle ScholarPubMed
Raubenheimer, D., & Blackshaw, J. (1994). Locusts learn to associate visual stimuli with drinking. Journal of Insect Behavior, 7, 569–575. https://psycnet.apa.org/doi/10.1007/BF02025450CrossRefGoogle Scholar
Raubenheimer, D., & Tucker, D. (1997). Associative learning by locusts: Pairing of visual cues with consumption of protein and carbohydrate. Animal Behaviour, 54, 1449–1459. https://doi.org/10.1006/anbe.1997.0542CrossRefGoogle ScholarPubMed
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, 91–98. https://doi.org/10.1098/rspb.2010.1337CrossRefGoogle ScholarPubMed
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, 137–146. https://doi.org/10.1093/sleep/34.2.137CrossRefGoogle ScholarPubMed
Shirakawa, T., Gunji, Y.-P., & Miyake, Y. (2011). An associative learning experiment using the plasmodium of Physarum polycephalum. Nano Communication Networks, 2, 99–105. https://doi.org/10.1016/j.nancom.2011.05.002CrossRefGoogle 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, 1539–1546. 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, 81–89. https://doi.org/10.1901/jeab.2010.93-81CrossRefGoogle Scholar
Srinivasan, M. V. (2010). Honey bees as a model for vision, perception, and cognition. Annual Review of Entomology, 55, 267–284. https://doi.org/10.1146/annurev.ento.010908.164537CrossRefGoogle ScholarPubMed
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, 16–26. https://doi.org/10.1111/eea.12590CrossRefGoogle Scholar
Thellier, M., & Lüttge, U. (2012). Plant memory: A tentative model. Plant Biology, 15, 1–12. https://doi.org/10.1111/j.1438-8677.2012.00674.xCrossRefGoogle ScholarPubMed
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, 595–603. https://doi.org/10.1086/696848CrossRefGoogle ScholarPubMed
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 Scholar
Verzijden, M. N., & Svensson, E. I. (2016). Interspecific interactions and learning variability jointly drive geographic differences in mate preferences. Evolution, 70, 1896–1903. https://doi.org/10.1111/evo.12982CrossRefGoogle ScholarPubMed
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, 333–344. https://doi.org/10.1016/j.cub.2017.12.015CrossRefGoogle ScholarPubMed
Vinauger, C., & Lazzari, C. R. (2015). Circadian modulation of learning ability in a disease vector insect, Rhodinus prolixus. Journal of Experimental Biology, 218, 3110–3117. 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.0001125CrossRefGoogle ScholarPubMed
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, 283–298. https://doi.org/10.1111/bij.12841CrossRefGoogle 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, 1139–1145. https://doi.org/10.1016/j.anbehav.2013.09.002CrossRefGoogle 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 ScholarPubMed
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), 1–8. https://doi.org/10.1093/jisesa/iew108CrossRefGoogle 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/ncomms4102CrossRefGoogle ScholarPubMed
References
Adami, C., Ofria, C., & Collier, T. C. (2000). Evolution of biological complexity. Proceedings of the National Academy of Sciences, 97(9), 4463–4468. https://doi.org/10.1073/pnas.97.9.4463CrossRefGoogle ScholarPubMed
Brand, P., & Ramírez, S. R. (2017). The evolutionary dynamics of the odorant receptor gene family in corbiculate bees. Genome Biology and Evolution, 9(8), 2023–2036. https://doi.org/10.1093/gbe/evx149CrossRefGoogle ScholarPubMed
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), 1294–1304. https://doi.org/10.1111/j.1558-5646.2008.00376.xCrossRefGoogle ScholarPubMed
Burnham, T. C., Dunlap, A. S., & Stephens, D. W. (2015). Experimental evolution and economics. Sage OPEN (October–December) 1–17. https://doi.org/10.1177/2158244015612524CrossRefGoogle Scholar
Dall, S., Giraldeau, L., Olsson, O., McNamara, J., & Stephens, D. W. (2005). Information and its use by animals in evolutionary ecology. Trends in Ecology & Evolution, 20(4), 187–193. https://doi.org/10.1016/j.tree.2005.01.010CrossRefGoogle ScholarPubMed
Davis, R. L., & Zhong, Y. (2017). The biology of forgetting – A perspective. Neuron, 95(3), 490–503. https://doi.org/10.1016/j.neuron.2017.05.039CrossRefGoogle ScholarPubMed
Domjan, M., Cusato, B., & Krause, M. (2004). Learning with arbitrary versus ecological conditioned stimuli: Evidence from sexual conditioning. Psychonomic Bulletin & Review, 11(2), 232–246. https://doi.org/10.3758/bf03196565CrossRefGoogle ScholarPubMed
Dunlap, A. S., McLinn, C. M., MacCormick, H. A., Scott, M. E., & Kerr, B. (2009). Why some memories do not last a lifetime: Dynamic long-term retrieval in changing environments. Behavioral Ecology, 20(5), 1096–1105. https://doi.org/10.1093/beheco/arp102CrossRefGoogle Scholar
Dunlap, A. S., Nielsen, M. E., Dornhaus, A., & Papaj, D. R. (2016). Foraging bumble bees weigh the reliability of personal and social information. Current Biology, 26(9), 1195–1199. https://doi.org/10.1016/j.cub.2016.03.009CrossRefGoogle ScholarPubMed
Dunlap, A. S., & Stephens, D. W. (2009). Components of change in the evolution of learning and unlearned preference. Proceedings of the Royal Society B: Biological Sciences, 276(1670), 3201–3208. https://doi.org/10.1098/rspb.2009.0602CrossRefGoogle ScholarPubMed
Dunlap, A. S., & Stephens, D. W. (2012). Tracking a changing environment: optimal sampling, adaptive memory and overnight effects. Behavioural Processes, 89(2), 86–94. https://doi.org/10.1016/j.beproc.2011.10.005CrossRefGoogle ScholarPubMed
Dunlap, A. S., & Stephens, D. W. (2014). Experimental evolution of prepared learning. Proceedings of the National Academy of Sciences, 111(32), 11750–11755. https://doi.org/10.1073/pnas.1404176111CrossRefGoogle ScholarPubMed
Dunlap, A. S., & Stephens, D. W. (2016). Reliability, uncertainty, and costs in the evolution of animal learning. Current Opinion in Behavioral Sciences, 12, 73–79. https://doi.org/10.1016/j.cobeha.2016.09.010CrossRefGoogle Scholar
Dwyer, D. M. (2015). Experimental evolution of sensitivity to a stimulus domain alone is not an example of prepared learning. Proceedings of the National Academy of Sciences, 112(5), E385. https://doi.org/10.1073/pnas.1420871112CrossRefGoogle Scholar
Farris, S. M., & Schulmeister, S. (2011). Parasitoidism, not sociality, is associated with the evolution of elaborate mushroom bodies in the brains of hymenopteran insects. Proceedings of the Royal Society B: Biological Sciences, 278(1707), 940–951. https://doi.org/10.1098/rspb.2010.2161CrossRefGoogle Scholar
Fawcett, T. W., Fallenstein, B., Higginson, A. D., Houston, A. I., Mallpress, D. E. W., Trimmer, P. C., & McNamara, J. M. (2014). The evolution of decision rules in complex environments. Trends in Cognitive Sciences, 18(3), 153–161. https://doi.org/10.1016/j.tics.2013.12.012CrossRefGoogle ScholarPubMed
Ferrari, M. C. O., Vrtělová, J., Brown, G. E., & Chivers, D. P. (2012). Understanding the role of uncertainty on learning and retention of predator information. Animal Cognition, 15(5), 807–813. https://doi.org/10.1007/s10071-012-0505-yCrossRefGoogle ScholarPubMed
Garcia, J., & Koelling, R. A. (1966). Relation of cue to consequence in avoidance learning. Psychonomic Science, 4(1), 123–124. https://doi.org/10.3758/bf03342209CrossRefGoogle Scholar
Garland, T., & Rose, M.R. (2009). Experimental evolution: Concepts, methods, and applications of selection experiments (1st ed.). University of California Press.CrossRefGoogle Scholar
Hauser, F. E., & Chang, B. S. W. (2017). Insights into visual pigment adaptation and diversity from model ecological and evolutionary systems. Current Opinion in Genetics & Development, 47, 110–120. https://doi.org/10.1016/j.gde.2017.09.005CrossRefGoogle ScholarPubMed
Kikuchi, D. W., & Pfennig, D. W. (2013). Imperfect mimicry and the limits of natural selection. The Quarterly Review of Biology, 88(4), 297–315. https://doi.org/10.1086/673758CrossRefGoogle ScholarPubMed
Knudsen, E. I. (2007). Fundamental components of attention. Annual Review of Neuroscience, 30(1), 57–78. https://doi.org/10.1146/annurev.neuro.30.051606.094256CrossRefGoogle ScholarPubMed
Köksal, F., Domjan, M., & Weisman, G. (1994). Blocking of the sexual conditioning of differentially effective conditioned stimulus objects. Animal Learning & Behavior, 22, 103–111.CrossRefGoogle Scholar
Koops, M. A. (2004). Reliability and the value of information. Animal Behaviour, 67(1), 103–111. https://doi.org/10.1016/j.anbehav.2003.02.008CrossRefGoogle Scholar
Kotrschal, A., Corral-Lopez, A., Amcoff, M., & Kolm, N. (2014). A larger brain confers a benefit in a spatial mate search learning task in male guppies. Behavioral Ecology, 26(2), 527–532. https://doi.org/10.1093/beheco/aru227CrossRefGoogle Scholar
Kotrschal, A., Rogell, B., Bundsen, A., Svensson, B., Zajitschek, S., Brännström, I., Immler, S., Maklakov, A. A., & Kolm, N. (2013). Artificial selection on relative brain size in the guppy reveals costs and benefits of evolving a larger brain. Current Biology, 23(2), 168–171. https://doi.org/10.1016/j.cub.2012.11.058CrossRefGoogle ScholarPubMed
Kraaijeveld, K., Oostra, V., Liefting, M., Wertheim, B., de Meijer, E., & Ellers, J. (2018). Regulatory and sequence evolution in response to selection for improved associative learning ability in Nasonia vitripennis. BMC Genomics, 19(1), 1–15. https://doi.org/10.1186/s12864-018-5310-9CrossRefGoogle ScholarPubMed
Kraemer, P. J., & Golding, J. M. (1997). Adaptive forgetting in animals. Psychonomic Bulletin & Review, 4(4), 480–491. https://doi.org/10.3758/bf03214337CrossRefGoogle Scholar
Krause, M. A., Cusato, B., & Domjan, M. (2003). Extinction of conditioned sexual responses in male Japanese quail (Coturnix japonica): Role of species typical cues. Journal of Comparative Psychology, 117, 76–86.CrossRefGoogle ScholarPubMed
Leadbeater, E., & Dawson, E. H. (2017). A social insect perspective on the evolution of social learning mechanisms. Proceedings of the National Academy of Sciences, 114(30), 7838–7845. https://doi.org/10.1073/pnas.1620744114CrossRefGoogle ScholarPubMed
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), 1449–1459. https://doi.org/10.1111/evo.13498CrossRefGoogle Scholar
Linwick, D., Patterson, J., & Overmier, J. B. (1981). On inferring selective association: Methodological considerations. Animal Learning & Behavior, 9(4), 508–512. https://doi.org/10.3758/bf03209782CrossRefGoogle Scholar
LoLordo, V. M. (1979). Selective associations. In Dickinson, A. and Boakes, R. A. (Eds.), Mechanisms of learning and motivation: A memorial volume to Jerzy Konorski (pp. 367–398). Lawrence Erlbaum..Google Scholar
Maharaj, G., Horack, P., Yoder, M., & Dunlap, A. S. (2018). Influence of preexisting preference for color on sampling and tracking behavior in bumble bees. Behavioral Ecology, 30(1), 150–158. https://doi.org/10.1093/beheco/ary140CrossRefGoogle Scholar
Marcus, M., Burnham, T. C., Stephens, D. W., & Dunlap, A. S. (2017). Experimental evolution of color preference for oviposition in Drosophila melanogaster. Journal of Bioeconomics, 20(1), 125–140. https://doi.org/10.1007/s10818-017-9261-zCrossRefGoogle Scholar
McNamara, J. M., & Houston, A. I. (1987). Memory and the efficient use of information. Journal of Theoretical Biology, 125(4), 385–395. https://doi.org/10.1016/s0022-5193(87)80209-6CrossRefGoogle ScholarPubMed
Mery, F., & Kawecki, T. J. (2002). Experimental evolution of learning ability in fruit flies. Proceedings of the National Academy of Sciences, 99(22), 14274–14279. https://doi.org/10.1073/pnas.222371199CrossRefGoogle ScholarPubMed
Mery, F., & Kawecki, T. J. (2003). A fitness cost of learning ability in Drosophila melanogaster. Proceedings of the Royal Society of London B Biological Sciences, 270, 2465–2469. https://doi.org/10.1098/rspb.2003.2548CrossRefGoogle ScholarPubMed
Mery, F., & Kawecki, T. J. (2004). The effect of learning on experimental evolution of resource preference in Drosophila melanogaster. Evolution, 58(4), 757. https://doi.org/10.1554/03-540CrossRefGoogle ScholarPubMed
Mery, F., Pont, J., Preat, T., & Kawecki, T. J. (2007). Experimental evolution of olfactory memory in Drosophila melanogaster. Physiological and Biochemical Zoology, 80(4), 399–405. https://doi.org/10.1086/518014CrossRefGoogle ScholarPubMed
Miller, S. E., Legan, A. W., Henshaw, M. T., Ostevik, K. L., Samuk, K., Uy, F. M., & Sheehan, M. J. (2020). Evolutionary dynamics of recent selection on cognitive abilities. Proceedings of the National Academy of Sciences, 117(6), 3045–3052. https://doi.org/10.1073/pnas.1918592117CrossRefGoogle ScholarPubMed
Morand-Ferron, J. (2017). Why learn? The adaptive value of associative learning in wild populations. Current Opinion in Behavioral Sciences, 16, 73–79.CrossRefGoogle Scholar
Oberling, P., Bristol, A. S., Matute, H., & Miller, R. R. (2000). Biological significance attenuates overshadowing, relative validity, and degraded contingency effects. Animal Learning & Behavior, 28, 172–186.CrossRefGoogle Scholar
Pontes, A. C., Mobley, R. B., Ofria, C., Adami, C., & Dyer, F. C. (2020). The evolutionary origin of associative learning. The American Naturalist, 195(1), E1–E19. https://doi.org/10.1086/706252CrossRefGoogle ScholarPubMed
Reader, S. M. (2016). Animal social learning: Associations and adaptations. F1000Research, 5, 2120. https://doi.org/10.12688/f1000research.7922.1CrossRefGoogle ScholarPubMed
Rescorla, R. A. & Wagner, A. R. (1972). A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. In Black, A. H. & Prokasy, W. F. (Eds.), Classical conditioning II: Current research and theory (pp. 64–99). Appleton-Century-Crofts.Google Scholar
Riffell, J. (2020). The neuroecology of insect-plant interactions: The importance of physiological state and sensory integration. Current Opinion in Insect Science, 42, 118–124. https://doi.org/10.1016/j.cois.2020.10.007CrossRefGoogle ScholarPubMed
Rubi, T. L., & Stephens, D. W. (2015). Should receivers follow multiple signal components? An economic perspective. Behavioral Ecology, 27(1), 36–44. https://doi.org/10.1093/beheco/arv121CrossRefGoogle Scholar
Rubi, T. L., & Stephens, D. W. (2016). Why complex signals matter, sometimes. In Bee, M. & Miller, C. (Eds.), Psychological mechanisms in animal communication. Animal signals and communication (Vol. 5, pp. 119–136). Springer. https://doi.org/10.1007/978-3-319-48690-1_5CrossRefGoogle Scholar
Seligman, M. E. (1970). On the generality of the laws of learning. Psychological Review, 77(5), 406–418. https://doi.org/10.1037/h0029790CrossRefGoogle Scholar
Silva, F. J. (2018). The puzzling persistence of “neutral” conditioned stimuli. Behavioural Processes, 157, 80–90. https://doi.org/10.1016/j.beproc.2018.07.004CrossRefGoogle ScholarPubMed
Snell-Rood, E. C., & Steck, M. (2015). Experience drives the development of movement-cognition correlations in a butterfly. Frontiers in Ecology and Evolution, 3, 63–73. https://doi.org/10.3389/fevo.2015.00021CrossRefGoogle Scholar
Stevens, M. (2013). Sensory ecology, behaviour, and evolution (Illustrated ed.). Oxford University Press.CrossRefGoogle Scholar
Van Damme, S., De Fruyt, N., Watteyne, J., Kenis, S., Peumen, K., Schoofs, L., & Beets, I. (2021). Neuromodulatory pathways in learning and memory: Lessons from invertebrates. Journal of Neuroendocrinology, 33(1), e1291. https://doi.org/10.1111/jne.12911CrossRefGoogle ScholarPubMed
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), 1–10. http://dx.doi.org/10.1098/rstb.2017.0280CrossRefGoogle ScholarPubMed
Brandes, C. (1988). Estimation of heritability of learning behavior in honeybees (Apis mellifera capensis). Behavior Genetics, 18(1), 119–132. https://doi.org/10.1007/BF01067081CrossRefGoogle 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), 1–9. https://doi.org/10.3389/fevo.2018.00160CrossRefGoogle 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), 1294–1304. https://doi.org/10.1111/j.1558-5646.2008.00376.xCrossRefGoogle ScholarPubMed
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, 44–66. 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), 275–285. https://doi.org/10.1023/A:1012227308783CrossRefGoogle Scholar
Cheng, K., & Wignall, A. E. (2006). Honeybees (Apis mellifera) holding on to memories: Response competition causes retroactive interference effects. Animal Cognition, 9(2), 141–150. https://doi.org/10.1007/s10071-005-0012-5CrossRefGoogle ScholarPubMed
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), 1–11. https://doi.org/10.1038/srep23571CrossRefGoogle ScholarPubMed
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), 1447–1459. https://doi.org/10.1093/beheco/arv088CrossRefGoogle Scholar
DeWitt, T. J., Sih, A., & Wilson, D. S. (1998). Costs and limits of phenotypic plasticity. Trends in Ecology & Evolution, 13(2), 77–81. https://doi.org/10.1016/S0169-5347(97)01274-3CrossRefGoogle ScholarPubMed
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), 1–12. https://doi.org/10.1098/rstb.2017.0282CrossRefGoogle ScholarPubMed
Dukas, R. (2008a). Evolutionary biology of insect learning. Annual Review of Entomology, 53, 145–160. https://doi.org/10.1146/annurev.ento.53.103106.093343CrossRefGoogle ScholarPubMed
Dukas, R. (2008b). Learning decreases heterospecific courtship and mating in fruit flies. Biology Letters, 4(6), 645–647. 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), 2637–2640. 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, 536–543. https://doi.org/10.1093/beheco/11.5.536CrossRefGoogle 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, 157–166. 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), 11750–11755. https://doi.org/10.1073/pnas.1404176111CrossRefGoogle ScholarPubMed
Dunlap, A. S., & Stephens, D. W. (2016). Reliability, uncertainty, and costs in the evolution of animal learning. Current Opinion in Behavioral Sciences, 12, 73–79. https://doi.org/10.1016/j.cobeha.2016.09.010CrossRefGoogle 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), 513–523. https://doi.org/10.1111/j.2007.0030-1299.15462.xCrossRefGoogle Scholar
Ellers, J., & Liefting, M. (2015). Extending the integrated phenotype: Covariance and correlation in plasticity of behavioural traits. Current Opinion in Insect Science, 9, 31–35. https://doi.org/10.1016/j.cois.2015.05.013CrossRefGoogle ScholarPubMed
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), 613–628. https://doi.org/10.1111/j.1420-9101.2004.00691.xCrossRefGoogle ScholarPubMed
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), 475–484. https://doi.org/10.1007/s00359-014-0905-3CrossRefGoogle 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), 1–10. https://doi.org/10.1038/s41598-017-00389-0CrossRefGoogle ScholarPubMed
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), 527–534. https://doi.org/10.1006/anbe.2000.1635CrossRefGoogle 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), 210–212. https://doi.org/10.1038/nature05764CrossRefGoogle ScholarPubMed
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/10.1037/0033-2909.127.1.45CrossRefGoogle 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), 207–214. https://doi.org/10.1016/j.tree.2015.01.012CrossRefGoogle ScholarPubMed
van Grunsven, R. H. A., & Liefting, M. (2015). How to maintain ecological relevance in ecology. Trends in Ecology & Evolution, 30(10), 563–564. https://doi.org/10.1016/j.tree.2015.07.010CrossRefGoogle ScholarPubMed
Haberkern, H., & Jayaraman, V. (2016). Studying small brains to understand the building blocks of cognition. Current Opinion in Neurobiology, 37, 59–65. https://doi.org/10.1016/j.conb.2016.01.007CrossRefGoogle ScholarPubMed
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), 349–352. https://doi.org/10.1111/een.12204CrossRefGoogle 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), 784–785. https://doi.org/10.1016/0003-3472(77)90130-0CrossRefGoogle 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), 889–897. https://doi.org/10.1098/rspb.2010.2199CrossRefGoogle ScholarPubMed
Hoedjes, K. M., & Smid, H. M. (2014). Natural variation in long-term memory formation among Nasonia parasitic wasp species. Behavioural Processes, 105, 40–45. 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), 542–550. https://doi.org/10.1038/hdy.2014.66CrossRefGoogle ScholarPubMed
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), 879–887. https://doi.org/10.1111/j.1601-183X.2012.00823.xCrossRefGoogle ScholarPubMed
Holliday, M., & Hirsch, J. (1986). A comment on the evidence for learning in diptera. Behavior Genetics, 16(4), 439–447. https://doi.org/10.1007/BF01074263CrossRefGoogle ScholarPubMed
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), 245–261. 0003-0147/2001/15703-0001$03.00CrossRefGoogle ScholarPubMed
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/s12864-018-5310-9CrossRefGoogle ScholarPubMed
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), 353–361. https://doi.org/10.1007/s00442-015-3346-yCrossRefGoogle 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), 4015–4023. https://doi.org/10.1098/rspb.2012.1457CrossRefGoogle ScholarPubMed
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), 1449–1459. https://doi.org/10.1111/evo.13498CrossRefGoogle Scholar
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), 851–861. https://doi.org/10.1007/s10071-019-01281-2CrossRefGoogle ScholarPubMed
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, 25–31. https://doi.org/10.1016/j.anbehav.2020.07.026CrossRefGoogle Scholar
Lofdahl, K. L., Holliday, M., & Hirsch, J. (1992). Selection for conditionability in Drosophila melanogaster. Journal of Comparative Psychology, 106(2), 172–183. https://doi.org/10.1037/0735-7036.106.2.172CrossRefGoogle ScholarPubMed
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), 1–9. https://doi.org/10.1098/rstb.2017.0297CrossRefGoogle ScholarPubMed
McNamara, J. M., & Houston, A. I. (1987). Memory and the efficient use of information. Journal of Theoretical Biology, 125(4), 385–395. https://doi.org/10.1016/S0022-5193(87)80209-6CrossRefGoogle ScholarPubMed
Mery, F. (2013). Natural variation in learning and memory. Current Opinion in Neurobiology, 23(1), 52–56. https://doi.org/10.1016/j.conb.2012.09.001CrossRefGoogle ScholarPubMed
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), 13051–13055. https://doi.org/10.1073/pnas.0702923104CrossRefGoogle ScholarPubMed
Mery, F., & Kawecki, T. J. (2002). Experimental evolution of learning ability in fruit flies. Proceedings of the National Academy of Sciences, 99(22), 14274–14279. https://doi.org/10.1073/pnas.222371199CrossRefGoogle ScholarPubMed
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), 2465–2469. https://doi.org/10.1098/rspb.2003.2548CrossRefGoogle ScholarPubMed
Mery, F., Pont, J., Preat, T., & Kawecki, T. J. (2007). Experimental evolution of olfactory memory in Drosophila melanogaster. Physiological and Biochemical Zoology, 80(4), 399–405. https://doi.org/10.1086/518014CrossRefGoogle ScholarPubMed
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), 845–856. https://doi.org/10.1038/nrg2207CrossRefGoogle ScholarPubMed
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), 367–389. https://doi.org/10.1111/brv.12174CrossRefGoogle ScholarPubMed
Népoux, V., Haag, C. R., & Kawecki, T. J. (2010). Effects of inbreeding on aversive learning in Drosophila. Journal of Evolutionary Biology, 23(11), 2333–2345. https://doi.org/10.1111/j.1420-9101.2010.02094.xCrossRefGoogle ScholarPubMed
Papaj, D. R., & Lewis, A. C. (1993). Insect learning: Ecology and evolutionary perspectives (Papaj, D. R. & Lewis, A. C. (eds.)). Chapman & Hall.CrossRefGoogle 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), 1702–1709. 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, 111–118. https://doi.org/10.1016/j.cobeha.2017.05.011CrossRefGoogle Scholar
Perry, C. J., & Chittka, L. (2019). How foresight might support the behavioral flexibility of arthropods. Current Opinion in Neurobiology, 54, 171–177. https://doi.org/10.1016/j.conb.2018.10.014CrossRefGoogle ScholarPubMed
Price, T. D., & Schluter, D. (1991). On the low heritability of life-history traits. Evolution, 45(4), 853–861. https://doi.org/10.2307/2409693CrossRefGoogle ScholarPubMed
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), 1–14. https://doi.org/10.1098/rstb.2015.0184CrossRefGoogle 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), 803–808. https://doi.org/10.1098/rspb.2007.1652CrossRefGoogle ScholarPubMed
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), 241–256. https://doi.org/10.1127/entom.gen/28/2006/241CrossRefGoogle Scholar
Rowe, C., & Healy, S. D. (2014). Measuring variation in cognition. Behavioral Ecology, 25(6), 1287–1292. 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), 649–658. https://doi.org/10.1007/s10340-016-0798-8CrossRefGoogle Scholar
Snell-Rood, E. C., Davidowitz, G., & Papaj, D. R. (2011). Reproductive tradeoffs of learning in a butterfly. Behavioral Ecology, 22(2), 291–302. https://doi.org/10.1093/beheco/arq169CrossRefGoogle Scholar
Stamps, J. A. (2016). Individual differences in behavioural plasticities. Biological Reviews, 91(2), 534–567. https://doi.org/10.1111/brv.12186CrossRefGoogle ScholarPubMed
Stephens, D. W. (1991). Change, regularity, and value in the evolution of animal learning. Behavioral Ecology, 2, 77–89. https://doi.org/https://doi.org/10.1093/beheco/2.1.77CrossRefGoogle Scholar
Thornton, A., & Lukas, D. (2012). Individual variation in cognitive performance: Developmental and evolutionary perspectives. Philosophical Transactions of the Royal Society B, 367(1603), 2773–2783. 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.1214CrossRefGoogle ScholarPubMed
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), 1–10. https://doi.org/10.1101/pdb.emo134Google Scholar
Werren, J. H., Richards, S.