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Early memory in the parasitoid wasp Nasonia vitripennis

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Abstract

We studied early memory in Nasonia vitripennis, a parasitoid of fly pupae and emerging model organism for ecological questions in the context of learning. After associative training consisting of one drilling experience in a host in the presence of cinnamon, females showed a preference to cinnamon for at least 24 h. To study sensitisation, wasps were trained by one drilling in a host without cinnamon. These wasps were not attracted to cinnamon immediately afterwards. Obviously, sensitisation is not involved in early memory. Wasps that were anaesthetised by CO2 directly after associative training did not react to cinnamon 30–45 min later, but after 1 and 24 h. CO2 treatment ≥5 min after training did not erase the reaction to cinnamon. This indicates the existence of four early memory phases. (a) One phase <5 min after training, in which CO2 has to be applied to become effective. (b) One subsequent phase which is resistant to CO2. (c) One phase <1 h in which memory can be erased by CO2 treatment directly after training. (d) One phase 1–24 h not affected by CO2 treatment. Together with earlier data this enables us to establish a complete memory structure for N. vitripennis.

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Abbreviations

ARM:

Anaesthesia-resistant memory

ASM:

Anaesthesia-sensitive memory

d:

Day(s)

eSTM:

Early short-term memory

h:

Hour(s)

L:D:

Light:dark

lSTM:

Late short-term memory

LTM:

Long-term memory

min:

Minute(s)

mg:

Milligram

n.s.:

Not significant

p :

Level of probability

s:

Seconds

References

  • Abdel-latief M, Garbe L-A, Koch M, Ruther J (2008) An epoxide hydrolase involved in the biosynthesis of an insect sex attractant and its use to localize the production site. PNAS 105:8914–8919

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Abraham R (1985) Nasonia vitripennis an insect from Birds’ Nests. Entomol Gen 10:121–124

    Article  Google Scholar 

  • Barco A, Bailey CH, Kandel ER (2006) Common molecular mechanisms in explicit and implicit memory. J Neurochem 97:1520–1533. doi:10.1111/j.1471-4159.2006.03870.x

    Article  CAS  PubMed  Google Scholar 

  • Bertossa RC, van Dijk J, Diao W, Saunders D, Beukeboom LW (2013) Circadian rhythms differ between sexes and closely related species of Nasonia wasps. PLoS ONE 8:e60167. doi:10.1371/journal.pone.0060167

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Burton-Chellew MN, Koevoets T, Grillenberger BK, Sykes EM, Underwood SL, Bijlsma K, Gadau J, van de Zande L, Beukeboom LW, West SA, Shuker DM (2008) Facultative sex ratio adjustment in natural populations of wasps: cues of local mate competition and the precision of adaptation. Am Nat 172:393–404

    Article  PubMed  Google Scholar 

  • Collatz J, Müller C, Steidle JLM (2006) Protein-synthesis dependent long-term memory induced by one single, non-spaced training in a parasitic wasp. Learn Mem 13:263–266. doi:10.1101/lm.192506

    Article  CAS  PubMed  Google Scholar 

  • Collatz J, Fuhrmann A, Selzer P, Oehme RM, Hartelt K, Kimmig P, Meiners T, Mackenstedt U, Steidle JLM (2010) Being a parasitoid of parasites: Host finding in the tick wasp Ixodiphagus hookeri by odours from mammals. Entomol Exp Appl 134:131–137

    Article  Google Scholar 

  • Collett T (2008) Insect behaviour: learning for the future. Curr Biol 18:131–134

    Article  Google Scholar 

  • Davis RL (2005) Olfactory memory formation in Drosophila: From molecular to systems neuroscience. Ann Rev Neurosci 28:275–302. doi:10.1146/annurev.neuro.28.061604.135651

    Article  CAS  PubMed  Google Scholar 

  • del Valle Fathala M, Iribarren L, Kunert MC, Maldonado H (2009a) A field model of learning: 1. Short-term memory in the crab Chasmagnathus granulatus. J Comp Physiol A 196:61–75

    Google Scholar 

  • del Valle Fathala M, Kunert MC, Maldonado H (2009b) A field model of learning: 2. Long-term memory in the crab Chasmagnathus granulatus. J Comp Physiol A 196:77–84

    Google Scholar 

  • Desjardins CA, Perfectti F, Bartos JD, Enders LS, Werren JH (2010) The genetic basis of interspecies host preference differences in the model parasitoid Nasonia. Heredity 104:270–277

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • DeZazzo J, Tully T (1995) Dissection of memory formation: from behavioural pharmacology to molecular genetics. Trends Neurosci 18:212–218. doi:10.1016/0166-2236(95)93905-D

    Article  CAS  PubMed  Google Scholar 

  • Domjan M (1998) The principles of learning and behaviour. Brooks/Cole Publishing Company, Pacific Grove

    Google Scholar 

  • Dudai Y (2002) Memory from A to Z. Keywords, concepts and beyond. Oxford University Press, Oxford

  • Eisenhardt D (2006) Learning and memory formation in the honeybee (Apis mellifera) and its dependency on the cAMP-protein kinase A pathway. Anim Biol 56:259–278

    Article  Google Scholar 

  • Erber J (1976) Retrograde amnesia in honeybees (Apis mellifera carnica). J Comp Physiol Psychol 90:41–46

    Article  CAS  PubMed  Google Scholar 

  • Erber J, Masuhr T, Menzel R (1980) Localization of short-term memory in the brain of the bee, Apis mellifera. Physiol Entomol 5:343–358

    Article  Google Scholar 

  • Gandolfi M, Mattiacci L, Dorn S (2003) Preimaginal learning determines adult response to chemical stimuli in a parasitic wasp. Proc R Soc Lond B 270:2623–2629. doi:10.1098/rspb.2003.2541

    Article  Google Scholar 

  • Hawkins RD, Kandel ER, Bailey CH (2006) Molecular mechanisms of memory storage in Aplysia. Biol Bull 210:174–191

    Article  CAS  PubMed  Google Scholar 

  • Hilker M, McNeil J (2008) Chemical and behavioral ecology in insect parasitoids: how to behave optimally in a complex odorous environment. In: Wajnberg E, Bernstein C, van Alphen J (eds) Behavioral ecology of insect parasitoids. Blackwell, Malden, USA, pp 92–112

    Chapter  Google Scholar 

  • Hoedjes KM, Smid HM (2014) Natural variation in long-term memory formation among Nasonia parasitic wasp species. Behav Process 105:40–45

    Article  Google Scholar 

  • Hoedjes KM, Kruidhof HM, Huigens ME, Dicke M, Vet LEM, Smid HM (2011) Natural variation in learning rate and memory dynamics in parasitoid wasps: opportunities for converging ecology and neuroscience. Proc R Soc Lond B 278:889–897

    Article  Google Scholar 

  • Hoedjes KM, Steidle JLM, Werren JH, Vet LEM, Smid HM (2012) High-throughput olfactory conditioning and memory retention test show variation in Nasonia parasitic wasps. Genes Brain Behav 11:879–887

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kaiser L, Perez-Maluf R, Sandoz JC, Pham-Delegue MH (2003) Dynamics of odour learning in Leptopilina boulardi, a hymenopterous parasitoid. Anim Behav 66:1077–1084

    Article  Google Scholar 

  • Kandel ER (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science 294:1030–1038. doi:10.1126/science.1067020

    Article  CAS  PubMed  Google Scholar 

  • König K, Krimmer E, Brose S, Gantert C, Buschlüter I, König C, Klopfstein S, Wendt I, Baur H, Krogmann L, Steidle JLM (2015) Does early learning drive ecological divergence during speciation processes in parasitoid wasps? Proc R Soc B 282: 20141850. http://dx.doi.org/10.1098/rspb.2014.1850

  • Krashes MJ, Waddell S (2008) Rapid consolidation to a radish and protein synthesis-dependent long-term memory after single-session appetitive olfactory conditioning in Drosophila. J Neurosci 28:3103–3113

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lafferty KD, Kuris AM (2002) Trophic strategies, animal diversity and body size. Trends Ecol Evol 17:507–513. doi:10.1016/S0169-5347(02)02615-0

    Article  Google Scholar 

  • Loehlin D, Enders LS, Werren JH (2010) Evolution of sex-specific wing shape at the widerwing locus in four species of Nasonia. Heredity 104:260–269. doi:10.1038/hdy.2009.146

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lynch JA, El-Sherif E, Brown SJ (2012) Comparisons of the embryonic development of Drosophila, Nasonia, and Tribolium. WIREs Dev Biol 1:16–39. doi:10.1002/wdev.3

    Article  CAS  Google Scholar 

  • Menzel R (1999) Memory dynamics in the honeybee. J Comp Physiol 185:323–340. doi:10.1007/s003590050392

    Article  Google Scholar 

  • Mery F (2013) Natural variation in learning and memory. Curr Opin Neurobiol 23:52–56

    Article  CAS  PubMed  Google Scholar 

  • Müller U (2012) The molecular signalling processes underlying olfactory learning and memory formation in honeybees. Apidologie 43:322–333

    Article  Google Scholar 

  • Müller C, Collatz J, Wieland R, Steidle JLM (2005) Associative learning and memory duration in the parasitic wasp Lariophagus distinguendus. Anim Biol 56:221–232

    Article  Google Scholar 

  • Niehuis O, Buellesbach J, Gibson JD, Pothmann D, Hanner C, Mutti NS, Judson A, Gadau J, Ruther J, Schmitt T (2013) Behavioural and genetic analyses of Nasonia shed light on the evolution of sex pheromones. Nature 494:345–348

    Article  CAS  PubMed  Google Scholar 

  • Pannebakker BA, Trivedi U, Blaxter MA, Watt R, Shuker DM (2013) The transcriptomic basis of oviposition behaviour in the parasitoid wasp Nasonia vitripennis. PLoS ONE 8:e68608

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Papaj DR, Vet LEM (1990) Odor learning and foraging successs in the parasitoid, Leptopilina heterotoma. J Chem Ecol 16:3137–3150

    Article  CAS  PubMed  Google Scholar 

  • Quinn WG, Dudai Y (1976) Memory phases in Drosophila. Nature 262:576–577

    Article  CAS  PubMed  Google Scholar 

  • Rose SPR (2000) God’s organism? The chick as a model system for memory studies. Learn Mem 7:1–17

    Article  CAS  PubMed  Google Scholar 

  • Schurmann D, Collatz J, Hagenbucher S, Ruther J, Steidle JLM (2009) Olfactory host finding, intermediate memory and its potential ecological adaptation in Nasonia vitripennis. Naturwissenschaften 96:383–391

    Article  CAS  PubMed  Google Scholar 

  • Schurmann D, Sommer C, Schinko APB, Greschista M, Smid H, Steidle JLM (2012) Demonstration of long-term memory in the parasitic wasp Nasonia vitripennis. Entomol Exp Appl 143:199–206

    Article  Google Scholar 

  • Steidle JLM (1998) Learning pays off: Influence of experience on host finding and parasitism in Lariophagus distinguendus (Hymenoptera: Pteromalidae). Ecol Ent 23:451–456

    Article  Google Scholar 

  • Steidle JLM, Schöller M (1997) Olfactory host location and learning in the granary weevil parasitoid Lariophagus distinguendus (Hymenoptera: Pteromalidae). J Ins Behav 10:331–342

    Article  Google Scholar 

  • Steidle JLM, van Loon JJA (2002) Chemoecology of parasitoid and predator oviposition behavior. In: Hilker M, Meiners T (eds) Chemoecology of insect eggs and egg deposition. Blackwell, London, pp 291–317. doi:10.1002/9780470760253.ch11

  • Steidle JLM, van Loon JJA (2003) Dietary specialization and infochemical use in carnivorous arthropods: testing a concept. Entomol Exp Appl 108:133–148. doi:10.1046/j.1570-7458.2003.00080.x

    Article  Google Scholar 

  • Steidle JLM, Steppuhn A, Ruther J (2003) Specific foraging kairomones used by a generalist parasitoid. J Chem Ecol 29:131–143

    Article  CAS  PubMed  Google Scholar 

  • Steinberg S, Dicke M, Vet LEM, Wanningen R (1992) Response of the braconid parasitoid Cotesia (=Apanteles) glomerata to volatile infochemicals: Effects of bioassay set-up, parasitoid age and experience and barometric flux. Entomol Exp Appl 63:163–175

    Article  CAS  Google Scholar 

  • Steiner S, Ruther J (2009) Mechanism and behavioral context of male sex pheromone release in Nasonia vitripennis. J Chem Ecol 35:416–421

    Article  CAS  PubMed  Google Scholar 

  • Tully T, Preat T, Boynton SC, Del Vecchio M (1994) Genetic dissection of consolidated memory in Drosophila. Cell 79:35–47

    Article  CAS  PubMed  Google Scholar 

  • van den Berg M, Duivenvoorde L, Wang G, Tribuhl S, Bukovinszky T, Vet LEM, Dicke M, Smid HM (2011) Natural variation in learning and memory dynamics studied by artificial selection on learning rate in parasitic wasps. Anim Behav 81:325–333

    Article  Google Scholar 

  • van der Merwe JS (1943) Investigations on the biology and ecology of Mormoniella vitripennis Walk. (Pteromalidae Hym.). J Ent Soc S Africa 6:48–64

    Google Scholar 

  • van Emden HF, Sponagl B, Wagner E, Baker T, Ganguly S, Douloumpaka S (1996) Hopkins ‘host selection principle’, another nail in its coffin. Physiol Entomol 21:325–328. doi:10.1111/j.1365-3032.1996.tb00873.xvan

    Article  Google Scholar 

  • Vinson SB (1991) Chemical signals used by parasitoids. Redia 74:15–42

    Google Scholar 

  • Werren JH, Richards S, Desjardins CA, Niehuis O, Gadau J et al (2010) Functional and evolutionary insights from the genomes of three parasitoid. Nasonia species. Science 327:343–348

    CAS  Google Scholar 

  • Whiting AR (1967) The Biology of the Parasitic Wasp Mormoniella vitripennis. Q Rev Biol 42:333–406

    Article  Google Scholar 

  • Xia SZ, Liu L, Feng CH, Guo AK (1997) Memory consolidation in Drosophila operant visual learning. Learn Mem 4:205–218

    Article  CAS  PubMed  Google Scholar 

  • Xia SZ, Feng CH, Guo AK (1998) Multiple-phase model of memory consolidation confirmed by behavioral and pharmacological analyses of operant conditioning in Drosophila. Pharmacol Biochem Behav 60:809–816

    Article  CAS  PubMed  Google Scholar 

  • Xia SZ, Feng CH, Guo AK (1999) Temporary amnesia induced by cold anesthesia and hypoxia in Drosophila. Physiol Behav 65:617–623

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We wish to thank Claudia Häußermann, Farina Kleinbeck, Elias Roller, Lisa Speigl and Nadine Weyhing for performing olfactometer experiments during a student course. The experiments comply with the current law of the country in which they were performed. The procedures and experiments described in this paper respect the ethical standards in the Helsinki Declaration of 1975, as revised in 2000 (5), as well as the national law.

Conflict of interest

All authors declare that they have no conflict of interests.

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Authors and Affiliations

  1. Institut für Zoologie, Fachgebiet Tierökologie 220c, Universität Hohenheim, Garbenstr. 30, 70593, Stuttgart, Germany

    Daria Schurmann, Dominic Kugel & Johannes L. M. Steidle

  2. Sterntalerweg 29, 97084, Würzburg, Germany

    Daria Schurmann

  3. Rudolf-Brenner-Straße 20, 70619, Stuttgart, Germany

    Dominic Kugel

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  1. Daria Schurmann
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Correspondence to Johannes L. M. Steidle.

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Schurmann, D., Kugel, D. & Steidle, J.L.M. Early memory in the parasitoid wasp Nasonia vitripennis . J Comp Physiol A 201, 375–383 (2015). https://doi.org/10.1007/s00359-015-0989-4

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  • DOI: https://doi.org/10.1007/s00359-015-0989-4

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