title: Learning-induced gene expression in the heads of two Nasonia species that differ in long-term memory formation.
abstract: BACKGROUND
  Cellular processes underlying memory formation are evolutionary conserved, but natural variation in memory dynamics between animal species or populations is common. The genetic basis of this fascinating phenomenon is poorly understood. Closely related species of Nasonia parasitic wasps differ in long-term memory (LTM) formation: N. vitripennis will form transcription-dependent LTM after a single conditioning trial, whereas the closely-related species N. giraulti will not. Genes that were differentially expressed (DE) after conditioning in N. vitripennis, but not in N. giraulti, were identified as candidate genes that may regulate LTM formation.
  
  
  RESULTS
  RNA was collected from heads of both species before and immediately, 4 or 24 hours after conditioning, with 3 replicates per time point. It was sequenced strand-specifically, which allows distinguishing sense from antisense transcripts and improves the quality of expression analyses. We determined conditioning-induced DE compared to naïve controls for both species. These expression patterns were then analysed with GO enrichment analyses for each species and time point, which demonstrated an enrichment of signalling-related genes immediately after conditioning in N. vitripennis only. Analyses of known LTM genes and genes with an opposing expression pattern between the two species revealed additional candidate genes for the difference in LTM formation. These include genes from various signalling cascades, including several members of the Ras and PI3 kinase signalling pathways, and glutamate receptors. Interestingly, several other known LTM genes were exclusively differentially expressed in N. giraulti, which may indicate an LTM-inhibitory mechanism. Among the DE transcripts were also antisense transcripts. Furthermore, antisense transcripts aligning to a number of known memory genes were detected, which may have a role in regulating these genes.
  
  
  CONCLUSIONS
  This study is the first to describe and compare expression patterns of both protein-coding and antisense transcripts, at different time points after conditioning, of two closely related animal species that differ in LTM formation. Several candidate genes that may regulate differences in LTM have been identified. This transcriptome analysis is a valuable resource for future in-depth studies to elucidate the role of candidate genes and antisense transcription in natural variation in LTM formation.
authors.affiliation: Laboratory of Entomology, Plant Sciences Group, Wageningen University, P.O. box 8031, 6700AP, Wageningen, The Netherlands. katja.hoedjes@unil.ch.|Department of Ecology and Evolution, University of Lausanne, Le Biophore, CH-1015, Lausanne, Switzerland. katja.hoedjes@unil.ch.
authors.forename: Katja M
authors.initials: KM
authors.lastname: Hoedjes
authors.affiliation: Laboratory of Entomology, Plant Sciences Group, Wageningen University, P.O. box 8031, 6700AP, Wageningen, The Netherlands. hansm.smid@wur.nl.
authors.forename: Hans M
authors.initials: HM
authors.lastname: Smid
authors.affiliation: PRI Bioscience, Plant Research International, P.O. box 619, 6700AP, Wageningen, The Netherlands. elio.schijlen@wur.nl.
authors.forename: Elio G W M
authors.initials: EG
authors.lastname: Schijlen
authors.affiliation: Laboratory of Entomology, Plant Sciences Group, Wageningen University, P.O. box 8031, 6700AP, Wageningen, The Netherlands. l.vet@nioo.knaw.nl.|Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), P.O. Box 50, 6700 AB, Wageningen, The Netherlands. l.vet@nioo.knaw.nl.
authors.forename: Louise E M
authors.initials: LE
authors.lastname: Vet
authors.affiliation: Department of Terrestrial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), P.O. Box 50, 6700 AB, Wageningen, The Netherlands. j.f.a.vanvugt-2@umcutrecht.nl.|Department of Neurology, University Medical Center Utrecht, P.O. Box 85500, 3508 GA, Utrecht, The Netherlands. j.f.a.vanvugt-2@umcutrecht.nl.
authors.forename: Joke J F A
authors.initials: JJ
authors.lastname: van Vugt
mesh_terms: D017398:Alternative Splicing; D000818:Animals; D001921:Brain / Q000378:metabolism*; D005260:Female; D005421:Flavoring Agents / Q000494:pharmacology; D006927:Hymenoptera / Q000235:genetics* / Q000378:metabolism; D057567:Memory, Long-Term / Q000187:drug effects / Q000502:physiology*; D009812:Odorants; D020320:Oligoribonucleotides, Antisense / Q000378:metabolism; D012313:RNA / Q000032:analysis / Q000302:isolation & purification / Q000378:metabolism; D034622:RNA Interference; D062085:RNA, Long Noncoding / Q000032:analysis / Q000302:isolation & purification / Q000378:metabolism; D017423:Sequence Analysis, RNA; D059467:Transcriptome
chemical_list: D005421:Flavoring Agents; D020320:Oligoribonucleotides, Antisense; D062085:RNA, Long Noncoding; D012313:RNA