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Octopamine-like immunoreactive neurons in the brain and subesophageal ganglion of the parasitic wasps Nasonia vitripennis and N. giraulti

Abstract

Octopamine is an important neuromodulator in the insect nervous system, influencing memory formation, sensory perception and motor control. In this study, we compare the distribution of octopamine-like immunoreactive neurons in two parasitic wasp species of the Nasonia genus, N. vitripennis and N. giraulti. These two species were previously described as differing in their learning and memory formation, which raised the question as to whether morphological differences in octopaminergic neurons underpinned these variations. Immunohistochemistry in combination with confocal laser scanning microscopy was used to reveal and compare the somata and major projections of the octopaminergic neurons in these wasps. The brains of both species showed similar staining patterns, with six different neuron clusters being identified in the brain and five different clusters in the subesophageal ganglion. Of those clusters found in the subesophageal ganglion, three contained unpaired neurons, whereas the other three consisted in paired neurons. The overall pattern of octopaminergic neurons in both species was similar, with no differences in the numbers or projections of the ventral unpaired median (VUM) neurons, which are known to be involved in memory formation in insects. In one other cluster in the brain, located in-between the optic lobe and the antennal lobe, we detected more neurons in N. vitripennis compared with N. giraulti. Combining our results with findings made previously in other Hymenopteran species, we discuss possible functions and some of the ultimate factors influencing the evolution of the octopaminergic system in the insect brain.

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References

  • Agarwal M, Giannoni Guzmán M, Morales-Matos C, Del Valle Díaz RA, Abramson CI, Giray T (2011) Dopamine and octopamine influence avoidance learning of honey bees in a place preference assay. PLoS ONE 6:e25371

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • Berg M van den, Duivenvoorde L, Wang GH, 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

  • Bleeker MAK, Van der Zee B, Smid HM (2006) Octopamine-like immunoreactivity in the brain and suboesophageal ganglion of two parasitic wasps, Cotesia glomerata and Cotesia rubecula. Anim Biol 56:247–257

    Article  Google Scholar 

  • Brandt R, Rohlfing T, Rybak J, Krofczik S, Maye A, Westerhoff M, Hege HC, Menzel R (2005) Three-dimensional average-shape atlas of the honeybee brain and its applications. J Comp Neurol 492:1–19

    PubMed  Article  Google Scholar 

  • Bräunig P (1991) Suboesophageal DUM neurons innervate the principal neuropiles of the locust brain. Philos Trans R Soc Lond B Biol Sci 332:221–240

    Article  Google Scholar 

  • Burke CJ, Huetteroth W, Owald D, Perisse E, Krashes MJ, Das G, Gohl D, Silies M, Certel S, Waddell S (2012) Layered reward signalling through octopamine and dopamine in Drosophila. Nature 492:433–437

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • Busch S, Selcho M, Ito K, Tanimoto H (2009) A map of octopaminergic neurons in the Drosophila brain. J Comp Neurol 513:643–667

    PubMed  Article  Google Scholar 

  • Cardona A, Saalfeld S, Schindelin J, Arganda-Carreras I, Preibisch S, Longair M, Tomancak P, Hartenstein V, Douglas RJ (2012) TrakEM2 software for neural circuit reconstruction. PLoS ONE 7:e38011

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • Dacks AM, Christensen TA, Agricola HJ, Wollweber L, Hildebrand JG (2005) Octopamine-immunoreactive neurons in the brain and subesophageal ganglion of the hawkmoth Manduca sexta. J Comp Neurol 488:255–268

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • Darling DC, Werren JH (1990) Biosystematics of Nasonia (Hymenoptera: pteromalidae): two new species reared from birds nests in North America. Ann Ent Soc Am 83:352–370

    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

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • Eckert M, Rapus J, Nurnberger A, Penzlin H (1992) The octopaminergic system within the ventral nerve cord of the American cockroach. Acta Biol Hung 43:201–211

    PubMed  CAS  Google Scholar 

  • Evans PD (1980) Biogenic amines in the insect nervous system. Adv Insect Physiol 15:317–473

    Article  CAS  Google Scholar 

  • Farooqui T (2007) Octopamine-mediated neuromodulation of insect senses. Neurochem Res 32:1511–1529

    PubMed  Article  CAS  Google Scholar 

  • Farooqui T (2012) Review of octopamine in insect nervous systems. Open Access Insect Physiol 4:1–17

    Article  CAS  Google Scholar 

  • Farooqui T, Robinson K, Vaessin H, Smith BH (2003) Modulation of early olfactory processing by an octopaminergic reinforcement pathway in the honeybee. J Neurosci 23:5370–5380

    PubMed  CAS  Google Scholar 

  • Farris SM, Schulmeister S (2011) Parasitoidism, not sociality, is associated with the evolution of elaborate mushroom bodies in the brains of hymenopteran insects. Proc Biol Sci 278:940–951

    PubMed  Article  PubMed Central  Google Scholar 

  • Giurfa M (2006) Associative learning: the instructive function of biogenic amines. Curr Biol 16:R892–R895

    PubMed  Article  CAS  Google Scholar 

  • Hammer M (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366:59–63

    PubMed  Article  CAS  Google Scholar 

  • Hammer M (1997) The neural basis of associative reward learning in honeybees. Trends Neurosci 20:245–252

    PubMed  Article  CAS  Google Scholar 

  • Hammer M, Menzel R (1998) Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn Mem 5:146–156

    PubMed  CAS  PubMed Central  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 LE, Smid HM (2011) Natural variation in learning rate and memory dynamics in parasitoid wasps: opportunities for converging ecology and neuroscience. Proc Biol Sci 278:889–897

    PubMed  Article  PubMed Central  Google Scholar 

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

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • Hoedjes KH, Smid HM, Vet LEM, Werren JH (2014) Introgression study reveals two quantitative trait loci involved in interspecific variation in memory retention among Nasonia wasp species. Heredity (in press)

  • Homberg U, Seyfarth J, Binkle U, Monastirioti M, Alkema MJ (2013) Identification of distinct tyraminergic and octopaminergic neurons innervating the central complex of the desert locust, Schistocerca gregaria. J Comp Neurol 521:2025–2041

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • Jefferis GS, Potter CJ, Chan AM, Marin EC, Rohlfing T, Maurer CR, Luo L (2007) Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128:1187–1203

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • Klappenbach M, Kaczer L, Locatelli F (2013) Dopamine interferes with appetitive long-term memory formation in honey bees. Neurobiol Learn Mem 106:230–237

    PubMed  Article  CAS  Google Scholar 

  • Konings PN, Vullings HG, Geffard M, Buijs RM, Diederen JH, Jansen WF (1988) Immunocytochemical demonstration of octopamine-immunoreactive cells in the nervous system of Locusta migratoria and Schistocerca gregaria. Cell Tissue Res 251:371–379

    PubMed  Article  CAS  Google Scholar 

  • Koon AC, Ashley J, Barria R, DasGupta S, Brain R, Waddell S, Alkema MJ, Budnik V (2011) Autoregulatory and paracrine control of synaptic and behavioral plasticity by octopaminergic signaling. Nat Neurosci 14:190–199

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • Krashes MJ, DasGupta S, Vreede A, White B, Armstrong JD, Waddell S (2009) A neural circuit mechanism integrating motivational state with memory expression in Drosophila. Cell 139:416–427

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • Kreissl S, Eichmuller S, Bicker G, Rapus J, Eckert M (1994) Octopamine-like immunoreactivity in the brain and subesophageal ganglion of the honeybee. Comp Neurol 348:583–595

    Article  CAS  Google Scholar 

  • Kruidhof HM, Rijk M de, Hoffmann D, Harvey JA, Vet LEM, Soler R (2013) Effect of belowground herbivory on parasitoid associative learning of plant odours. Oikos 122:1094–1100

  • Liu C, Plaçais PY, Yamagata N, Pfeiffer BD, Aso Y, Friedrich AB, Siwanowicz I, Rubin GM, Preat T, Tanimoto H (2012) A subset of dopamine neurons signals reward for odour memory in Drosophila. Nature 488:512–516

    PubMed  Article  CAS  Google Scholar 

  • Lynch JA, Desplan C (2006) A method for parental RNA interference in the wasp Nasonia vitripennis. Nat Protocol 1:486–494

    Article  CAS  Google Scholar 

  • Menzel R (2012) The honeybee as a model for understanding the basis of cognition. Nat Rev Neurosci 13:758–768

    PubMed  Article  CAS  Google Scholar 

  • Monastirioti M, Gorczyca M, Rapus J, Eckert M, White K, Budnik V (1995) Octopamine immunoreactivity in the fruit fly Drosophila melanogaster. J Comp Neurol 356:275–287

    PubMed  Article  CAS  Google Scholar 

  • Monastirioti M, Linn CEJ, White K (1996) Characterization of Drosophila tyramine beta-hydroxylase gene and isolation of mutant flies lacking octopamine. J Neurosci 16:3900–3911

    PubMed  CAS  Google Scholar 

  • Mons N, Geffard M (1987) Specific antisera against the catecholamines—L-3,4-dihydroxyphenylalanine, dopamine, noradrenaline, and octopamine tested by an enzyme-linked-immunosorbent-assay. J Neurochem 48:1826–1833

    PubMed  Article  CAS  Google Scholar 

  • Niehuis O, Gibson JD, Rosenberg MS, Pannebakker BA, Koevoets T, Judson AK, Desjardins CA, Kennedy K, Duggan D, Beukeboom LW, Zande L van de, Shuker DM, Werren JH, Gadau J (2010) Recombination and its impact on the genome of the haplodiploid parasitoid wasp Nasonia. PLoS ONE 5:e8597

  • Pannebakker BA, Niehuis O, Hedley A, Gadau J, Shuker DM (2010) The distribution of microsatellites in the Nasonia parasitoid wasp genome. Ins Mol Biol 19:91–98

    Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Perry CJ, Barron AB (2013) Neural mechanisms of reward in insects. Annu Rev Entomol 58:543–562

    PubMed  Article  CAS  Google Scholar 

  • Peters RS (2010) Host range and offspring quantities in natural populations of Nasonia vitripennis (Walker, 1836) (Hymenoptera: Chalcidoidea: Pteromalidae). J Hymenopteran Res 19:128–138

    Google Scholar 

  • Pflüger H-J, Stevenson PA (2005) Evolutionary aspects of octopaminergic systems with emphasis on arthropods. Arthropod Struct Dev 34:379–396

    Article  Google Scholar 

  • Rehder V (1989) Sensory pathways and motoneurons of the proboscis reflex in the subesophageal ganglion of the honey bee. J Comp Neurol 279:499–513

    PubMed  Article  CAS  Google Scholar 

  • Roeder T (1999) Octopamine in invertebrates. Prog Neurobiol 59:533–561

    PubMed  Article  CAS  Google Scholar 

  • Roeder T (2005) Tyramine and octopamine: ruling behavior and metabolism. Annu Rev Entomol 50:447–477

    PubMed  Article  CAS  Google Scholar 

  • Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682

    PubMed  Article  CAS  Google Scholar 

  • Schröter U, Malun D, Menzel R (2007) Innervation pattern of suboesophageal ventral unpaired median neurones in the honeybee brain. Cell Tissue Res 327:647–667

    PubMed  Article  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 

  • Schwaerzel M, Monastirioti M, Scholz H, Friggi Grelin F, Birman S, Heisenberg M (2003) Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 23:10495–10502

    PubMed  CAS  Google Scholar 

  • Sinakevitch I, Strausfeld NJ (2006) Comparison of octopamine-like immunoreactivity in the brains of the fruit fly and blow fly. J Comp Neurol 494:460–475

    PubMed  Article  CAS  Google Scholar 

  • Sinakevitch I, Niwa M, Strausfeld NJ (2005) Octopamine-like immunoreactivity in the honey bee and cockroach: comparable organization in the brain and subesophageal ganglion. J Comp Neurol 488:233–254

    PubMed  Article  CAS  Google Scholar 

  • Smid HM (1998) Transfer of a male accessory gland peptide to the female during mating in Leptinotarsa decemlineata. Invertebr Reprod Dev 34:47–53

    Article  CAS  Google Scholar 

  • Smid HM, Bleeker MAK, Loon JJA van, Vet LEM (2003) Three-dimensional organization of the glomeruli in the antennal lobe of the parasitoid wasps Cotesia glomerata and C. rubecula. Cell Tissue Res 312:237–248

  • Smid HM, Wang G, Bukovinszky T, Steidle JL, Bleeker MA, Loon JJ van, Vet LE (2007) Species-specific acquisition and consolidation of long-term memory in parasitic wasps. Proc R Soc Lond B Biol Sci 274:1539–1546

  • Spivak M, Masterman R, Ross R, Mesce KA (2003) Hygienic behavior in the honey bee (Apis mellifera L.) and the modulatory role of octopamine. J Neurobiol 55:341–354

    PubMed  Article  CAS  Google Scholar 

  • Spörhase-Eichmann U, Vullings HG, Buijs RM, Hörner M, Schürmann FW (1992) Octopamine-immunoreactive neurons in the central nervous system of the cricket, Gryllus bimaculatus. Cell Tissue Res 268:287–304

    PubMed  Article  Google Scholar 

  • Stern M, Thompson KSJ, Zhou P, Watson DG, Midgley JM, Gewecke M, Bacon JP (1995) Octopaminergic neurons in the locust brain—morphological, biochemical and electrophysiological characterization of potential modulators of the visual-system. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 177:611–625

  • Stevenson PA, Spörhase-Eichmann U (1995) Localization of octopaminergic neurones in insects. Comp Biochem Physiol A Physiol 110:203–215

    PubMed  Article  CAS  Google Scholar 

  • Suver MP, Mamiya A, Dickinson MH (2012) Octopamine neurons mediate flight-induced modulation of visual processing in Drosophila. Curr Biol 22:2294–2302

    PubMed  Article  CAS  Google Scholar 

  • Tamo C, Ricard I, Held M, Davison AC, Turlings TCJ (2006) A comparison of naive and conditioned responses of three generalist endoparasitoids of lepidopteran larvae to host-induced plant odours. Anim Biol 56:205–220

    Article  Google Scholar 

  • Turlings TCJ, Wäckers FL, Vet LEM, Lewis WJ, Tumlinson JH (1993) Learning of host-finding cues by hymenopterous parasitoids. In: Papaj DR, Lewis AC (eds) Insect learning: ecological and evolutionary perspectives. Chapman & Hall, New York, pp 51–78

    Chapter  Google Scholar 

  • Unoki S, Matsumoto Y, Mizunami M (2005) Participation of octopaminergic reward system and dopaminergic punishment system in insect olfactory learning revealed by pharmacological study. Eur J Neurosci 22:1409–1416

    PubMed  Article  Google Scholar 

  • Vergoz V, Roussel E, Sandoz JC, Giurfa M (2007) Aversive learning in honeybees revealed by the olfactory conditioning of the sting extension reflex. PLoS ONE 2:e288

    PubMed  Article  PubMed Central  Google Scholar 

  • Verlinden H, Vleugels R, Marchal E, Badisco L, Pflüger H-J, Blenau W, Broeck JV (2010) The role of octopamine in locusts and other arthropods. J Insect Physiol 56:854–867

    PubMed  Article  CAS  Google Scholar 

  • Vet LEM, Lewis WJ, Cardé RT (1995) Parasitoid foraging and learning. In: Cardé RT, Bell WJ (eds) Chemical ecology of insects. Chapman & Hall, New York, pp 65-101

    Chapter  Google Scholar 

  • Waddell S (2013) Reinforcement signalling in Drosophila; dopamine does it all after all. Curr Opin Neurobiol 23:324–329

    PubMed  Article  CAS  Google Scholar 

  • Werren JH, Loehlin DW (2009) The parasitoid wasp Nasonia: an emerging model system with haploid male genetics. Cold Spring Harb Protoc 2009:pdb.emo134

    PubMed  PubMed Central  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Wong AM, Wang JW, Axel R (2002) Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109:229–241

    PubMed  Article  CAS  Google Scholar 

  • Woude E van der, Smid HM, Chittka L, Huigens ME (2013) Breaking Haller’s rule: brain-body size isometry in a minute parasitic wasp. Brain Behav Evol 81:86–92

  • Wright GA, Mustard JA, Simcock NK, Ross-Taylor AA, McNicholas LD, Popescu A, Marion-Poll F (2010) Parallel reinforcement pathways for conditioned food aversions in the honeybee. Curr Biol 20:2234–2240

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  • Wu CL, Shih MF, Lai JS, Yang HT, Turner GC, Chen L, Chiang AS (2011) Heterotypic gap junctions between two neurons in the Drosophila brain are critical for memory. Curr Biol 21:848–854

    PubMed  Article  CAS  Google Scholar 

  • Wu CL, Shih MF, Lee PT, Chiang AS (2013) An octopamine-mushroom body circuit modulates the formation of anesthesia-resistant memory in Drosophila. Curr Biol 23:2346–2354

    PubMed  Article  CAS  Google Scholar 

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Acknowledgments

We are grateful to Jack Werren (University of Rochester, N.Y., USA) and Bart Pannebakker (Wageningen University, Genetics) for sending Nasonia lines, to Emma van der Woude and Mark Boumans (Wageningen University, Entomology) for preparing some of the confocal stacks and to Henk Schipper (Wageningen University, Animal Sciences) for use of the confocal laser scanning microscope.

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Haverkamp, A., Smid, H.M. Octopamine-like immunoreactive neurons in the brain and subesophageal ganglion of the parasitic wasps Nasonia vitripennis and N. giraulti . Cell Tissue Res 358, 313–329 (2014). https://doi.org/10.1007/s00441-014-1960-3

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  • DOI: https://doi.org/10.1007/s00441-014-1960-3

Keywords

  • Octopamine
  • Brain
  • Learning
  • Insect
  • Nasonia
  • Parasitic wasp