Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-22T16:26:50.813Z Has data issue: false hasContentIssue false

2 - Adaptive Evolution of Learning and Memory in a Model Lineage

from Part I - Evolution of Learning Processes

Published online by Cambridge University Press:  26 May 2022

By
William G. Wright
Edited by
Mark A. Krause ,
Karen L. Hollis  and
Mauricio R. Papini
Mark A. Krause
Affiliation:
Southern Oregon University
Karen L. Hollis
Affiliation:
Mount Holyoke College, Massachusetts
Mauricio R. Papini
Affiliation:
Texas Christian University
Get access

Summary

Although reductionistic studies of mechanisms of learning in a broad range of model species have advanced our understanding of neural mechanisms, our integrated understanding of mechanisms, behavior, ecology, and evolution of learning remains patchy. A more wholistic research approach in a model lineage of species related to the sea hare, Aplysia californica, has revealed a complete loss of mechanisms of sensitization in one sea-hare genus, Dolabrifera, with concomitant changes in its behavior and ecology. A partial loss of sensitization via different mechanisms in a sister genus, Phyllaplysia, provides further information for our evolving understanding of the evolution of learning and memory. Does a relatively specific “change in diet” hypothesis, or a more universal “generalist versus specialist” hypothesis better predict the patterns? Further analyses of sensitization in a half-dozen additional sea-hare genera will distinguish the predictive powers of these and other synthetic evolutionary theories.

Type
Chapter
Information
Evolution of Learning and Memory Mechanisms , pp. 33 - 51
Publisher: Cambridge University Press
Print publication year: 2022

Access options

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

References

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/10.1038/35036191Google Scholar
Baldwin, J. M. (1896). A new factor in evolution. American Naturalist, 30, 441–451.Google 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/meps11157Google 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 Scholar
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.xGoogle 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/C6NP00097EGoogle Scholar
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/10.4002/040.061.0201Google 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.xGoogle Scholar
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.2.3.133Google Scholar
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.2014.03.043Google Scholar
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/icr063Google Scholar
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.4358-03.2004Google 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.Google 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
Futuyma, D., & Kirkpatrick, M. (2017). Evolution. Sinauer.Google Scholar
Gillette, R. (2006). Evolution and function in serotonergic systems. Integrative & Comparative Biology, 46, 838–846. https://doi.org/10.1093/icb/icl024Google Scholar
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 ScholarPubMed
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)00017-9Google Scholar
Glanzman, D. L. (2010). Common mechanisms of synaptic plasticity in vertebrates and invertebrates. Current Biology, 20(1), R31–R36.Google Scholar
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.09-12-04200.1989Google Scholar
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/10.1080/10236244.2018.1505430Google 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.2581-06.2007Google Scholar
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.3855-08.2008Google Scholar
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
Kay, A. (1979). Hawaiian marine shells. Bernice Pauahi Bishop Museum.Google Scholar
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.2009.03.010Google Scholar
LeDoux, J. E. (2000). Emotion circuits in the brain. Annual Review of Neuroscience, 23, 155–184. https://doi.org/10.1146/annurev.neuro.23.1.155Google Scholar
Lynch, M. A. (2004). Long-term potentiation and memory. Physiological Reviews, 84, 87–136. https://doi.org/10.1152/physrev.00014.2003Google Scholar
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.03-07-01469.1983Google Scholar
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.22-06-02299.2002Google Scholar
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.2003.038356Google Scholar
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.23.1.649Google Scholar
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.034330.114Google Scholar
Nature Research Highlights (2010) Animal behaviour: Lobster shock. Nature 467, 8.Google 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/s10571-012-9836-0Google Scholar
Paine, R. T. (1966). Food web complexity and species diversity. American Naturalist, 100, 65–75. https://doi.org/10.1086/282400Google 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/10.2307/2407792Google Scholar
Papini, M. R. (2002). Pattern and process in the evolution of learning. Psychological Review, 109, 186–201. https://doi.org/10.1037/0033-295X.109.1Google Scholar
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/10.2307/1940813Google 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/BF00349763Google 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.171558Google 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.1998.80.1.1Google Scholar
Senter, P. (2010). Vestigial skeletal structures in dinosaurs. Journal of Zoology, 280, 60–71. https://doi.org/10.1111/j.1469-7998.2009.00640.xGoogle 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.08-01-00223.1988Google Scholar
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/10.1890/06-0161.1Google Scholar
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.25.110194.001251Google Scholar
Vermeij, G. J. (2013). On escalation. Annual Review of Earth & Planetary Sciences, 41, 1–19. https://doi.org/10.1146/annurev-earth-050212-124123Google 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/S108933260000108XGoogle 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.07-02-00400.1987Google Scholar
Walters, E. T. (1991). A functional, cellular, and evolutionary model of nociceptive plasticity in Aplysia. Biological Bulletin, 180, 241–251. https://doi.org/10.2307/1542394Google Scholar
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)60307-4Google Scholar
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 ScholarPubMed
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.2019.0277Google Scholar
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.Google 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.1998.3829Google Scholar
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.1998.3829Google 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/bf02331914Google Scholar
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

Save book to Kindle

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

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

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

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

Available formats
×

Save book to Google Drive

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

Available formats
×