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Ontogeny of Nestmate Recognition in Social Hymenoptera

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Social Recognition in Invertebrates

Abstract

The ability to discriminate between friends and foes is a central feature of social life. In social insects, nestmate recognition is mediated by colony specific cuticular hydrocarbons (CHCs) (label) that are perceived by an individual and compared with its neural representation of the colony odour (template). Although numerous advances have been made in understanding the identity, origin and production of recognition cues in social hymenoptera, relatively little is known about the ontogeny of nestmate recognition, and the learning processes that might be involved. It appears that wasps and bees learn the recognition cues required for template formation from their nest/comb odour, while ants learn principally from their nestmates. In general, the referent template is learned during the early stages of adult life, although pre-imaginal learning might play a role. The CHC blend can change over time; cue-exchange among nestmates is therefore needed to reduce chemical variability among individuals and to integrate environmental compounds into the colony odour. As a result of this process, the referent template is updated during life. This relative plasticity of the recognition system can be exploited by insect social parasites to integrate themselves within the host colonies and to fool host workers about their real identity. By studying the chemical integration strategies of social parasites new insights on the ontogeny of nestmate recognition could be acquired. However, further studies are needed to reveal the neural substrates implicated in learning and memory at different stages of social insect life to better understand how and when template formation occurs.

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References

  • Akino T, Yamamura K, Wakamura S, Yamaoka R (2004) Direct behavioral evidence for hydrocarbons as nestmate recognition cues in Formica japonica (Hymenoptera: Formicidae). Appl Entomol Zool 39:381–387

    CAS  Google Scholar 

  • Baracchi D, Petrocelli I, Cusseau G, Pizzocaro L, Teseo S, Turillazzi S (2013) Facial markings in the hover wasps: quality signals and familiar recognition cues in two species of Stenogastrinae. Anim Behav 85(1):203–212

    Google Scholar 

  • Baracchi D, Petrocelli I, Chittka L, Ricciardi G, Turillazzi S (2015) Speed and accuracy in nest-mate recognition: a hover wasp prioritizes face recognition over colony odour cues to minimize intrusion by outsiders. Proc R Soc B 282(1802):2014–2750  

    Google Scholar 

  • Blatrix R, Sermage C (2005) Role of early experience in ant enslavement: a comparative analysis of a host and a non-host species. Fron Zool 2(1):13

    Google Scholar 

  • Berton F, Lenoir A, Nowbahari E, Barreau S (1991) Ontogeny of queen attraction to workers in the ant Cataglyphis cursor (Hymenoptera: Formicidae). Insect Soc 38:293–305

    Google Scholar 

  • Boomsma JJ, d’Ettorre P (2013) Nice to kin and nasty to non-kin: revisiting Hamilton’s early insights on eusociality. Biol Lett 9(6):20130444

    PubMed Central  PubMed  Google Scholar 

  • Bos N, d’Ettorre P (2012) Recognition of social identity in ants. Front Psychol 3:83

    Google Scholar 

  • Bos N, Grinsted L, Holman L (2011) Wax on, wax off: nest soil facilitates in direct transfer of recognition cues between ant nestmates. PLoSONE 6:e19435

    CAS  Google Scholar 

  • Boulay R, Lenoir A (2001) Social isolation of mature workers affects nestmate recognition in the ant Camponotus fellah. Behav Process 55:67–73

    Google Scholar 

  • Boulay R, Hefetz H, Soroker V, Lenoir A (2000) Camponotus fellah colony integration: worker individuality necessitates frequent hydrocarbon exchanges. Anim Behav 59:1127–1133

    PubMed  Google Scholar 

  • Boulay R, Katzav-Gozansky T, Vander Meer RK, Hefetz A (2003) Colony insularity through queen control on worker social motivation in ants. Proc R Soc Lond B 270:971–977

    Google Scholar 

  • Brandstaetter AS, Rössler W, Kleineidam CJ (2011) Friends and foes from an ant brain’s point of view—neuronal correlates of colony odors in a social insect. PLoS ONE 6(6):e21383

    PubMed Central  CAS  PubMed  Google Scholar 

  • Brandt M, Heinze J, Schmitt T, Foitzik S (2005) A chemical level in the coevolutionary arms race between an ant social parasite and its hosts. J Evol Biol 18:576–586

    CAS  PubMed  Google Scholar 

  • Breed MD, Stiller TM (1992) Honey bee, Apis mellifera, nestmate discrimination: hydrocarbons effects and the evolutionary implications of comb choice. Anim Behav 43:875–883

    Google Scholar 

  • Breed MD, Butler L, Stiller TM (1985) Kin discrimination by workers in genetically mixed groups. Proc Natl Acad Sci USA 82:3058–3061

    PubMed Central  CAS  PubMed  Google Scholar 

  • Breed MD, Stiller TM, Moor MJ (1988) The ontogeny of kin discrimination cues in the honey bee, Apis mellifera. Behav Genet 18(4):439–448

    Google Scholar 

  • Breed MD, Garry MF, Pearce AN, Bjostad L, Hibbard B, Page RE (1995) The role of wax comb in honeybee nestmate recognition: genetic effects on comb discrimination, acquisition of comb cues by bees, and passage of cues among individuals. Anim Behav 50:489–496

    Google Scholar 

  • Breed MD, Leger EA, Pearce AN, Wang YJ (1998) Comb wax effects on the ontogeny of honey bee nestmate recognition. Anim Behav 55:13–20

    PubMed  Google Scholar 

  • Breed MD, Perry S, Bjostad LB (2004) Testing the blank state hypothesis: why honey bee colonies accept young bees Insect Soc 51:12–16

    Google Scholar 

  • Bruschini C, Cervo R, Turillazzi S (2010) Pheromones in social wasps. In: Litwack G (ed) Vitamins and hormones, vol 83. Academic Press, Burlington, pp 447–492

    Google Scholar 

  • Buczkowski G, Kumar R, Suib SL, Silverman J (2005) Diet-related modification of cuticular hydrocarbon profiles of the Argentine ant, Linepithema humile, diminishes intercolony aggression. J Chem Ecol 31: 829–843

    Google Scholar 

  • Cappa F, Bruschini C, Cipollini M, Pieraccini G, Cervo R (2014) Sensing the intruder: a quantitative threshold for recognition cues perception in honeybees. Naturwiss 101:149–152

    Google Scholar 

  • Carlin N, Hölldobler B (1983) Nestmate and kin recognition in interspecific mixed colonies of ants. Science 222:1027–1029

    Google Scholar 

  • Carlin N, Hölldobler B (1986) The kin recognition system of carpenter ants (Camponotus spp.). I. Hierarchical cues in small colonies. Behav Ecol Sociobiol 19:123–134

    Google Scholar 

  • Carlin NF, Schwartz PH (1989) Pre-imaginal experience and nestmate brood recognition in the carpenter ant, Camponotus floridanus. Anim Behav 38:89–95

    Google Scholar 

  • Carlin NF, Halpern R, Hölldobler B, Schwartz P (1987) Early learning and the recognition of conspecific cocoons by carpenter ants (Camponotus spp.). Ethology 75:306–316

    Google Scholar 

  • Carpenter JM (1996) Phylogeny and biogeography. In: Turillazzi S, West-Eberhard MJ (eds) Natural history and evolution of paper wasps. Oxford University Press, Oxford, pp 18–57

    Google Scholar 

  • Caubet Y, Jaisson P, Lenoir A (1992) Preimaginal induction of adult behaviour in insects. Q J Exp Psychol B 44B:165–178

    Google Scholar 

  • Cayre M, Strambi C, Charpin P, Augier R, Meyer MR, Edwards JS, Strambi A (1996) Neurogenesis in adult insect mushroom bodies. J Comp Neurol 371:300–331

    CAS  PubMed  Google Scholar 

  • Cervo R (2006) Polistes wasps and their social parasites: an overview. Ann Zool Fenn 43:550–563

    Google Scholar 

  • Cervo R, Dani FR (1996) Social parasitism and its evolution in Polistes. In: Turillazzi S, West Eberhard MJ (eds) Natural history and the evolution of paper wasps. Oxford University Press, Oxford, pp 98–112

    Google Scholar 

  • Cervo R, Turillazzi S (1989) Nest exchange experiments in Polistes gallicus (L.) (Hymenoptera Vespidae). Ethol Ecol Evol 1(2): 185–193

    Google Scholar 

  • Cervo R, Dani FR, Zanetti P, Massolo A, Turillazzi S (2002) Chemical nestmate recognition in a stenogastrine wasp, Liostenogaster flavolineata (Hymenoptera: Vespidae). Ethol Ecol Evol 14:351–363

    Google Scholar 

  • Cervo R, Dani FR, Cotoneschi C, Scala C, Lotti I, Strassmann JE, Queller DC, Turillazzi S (2008) Why are larvae of the social parasite wasp Polistes sulcifer not removed from the host nest? Behav Ecol Sociobiol 62(8):1319–1331

    Google Scholar 

  • Châline N, Sandoz JC, Martin SJ, Ratnieks FLW, Jones GR (2005) Learning and discrimination of individual cuticular hydrocarbons by honeybees (Apis mellifera). Chem Senses 30:327–335

    PubMed  Google Scholar 

  • Cini A, Gioli L, Cervo R (2009) A quantitative threshold for nestmate recognition in a paper social wasp. Biol Lett 5:459–461

    PubMed Central  PubMed  Google Scholar 

  • Cobb M, Domain I (2000) Olfactory learning in individually assayed Drosophila larvae. Proc R Soc Lond B 267:2119–2125

    CAS  Google Scholar 

  • Corbet SA (1985) Insect Chemosensory Responses—a chemical legacy hypothesis. Ecol Entomol 10(2):143–153

    Google Scholar 

  • Costanzi E, Bagnères AG, Lorenzi MC (2013) Changes in the hydrocarbon proportions of colony odor and their consequences on nestmate recognition in social wasps. PLoS ONE 8(5):e65107

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cotoneschi C, Dani FR, Cervo R, Sledge MF, Turillazzi S (2007) Polistes dominulus (Hymenoptera: Vespidae) larvae have their own chemical signatures. J Insect Physiol 53:954–963

    CAS  PubMed  Google Scholar 

  • Couvillon MJ, Caple JP, Endsor SL, Kärcher M, Russell TE, Storey DE, Ratnieks FLW (2007) Nest-mate recognition template of guard honeybees (Apis mellifera) is modified by wax comb transfer. Biol Lett 3:228–230

    PubMed Central  PubMed  Google Scholar 

  • Crozier RH, Dix MW (1979) Analysis of two genetic models for the innate components of colony odor in social Hymenoptera. Behav Ecol Sociobiol 47:217–224

    Google Scholar 

  • Crozier RH, Pamilo P (1996) Evolution of social insect colonies. Oxford University Press, Oxford

    Google Scholar 

  • Dahbi A, Lenoir A (1998) Nest separation and the dynamics of the Gestalt odor in the polydomous ant Cataglyphis iberica (Hymenoptera, Formicidae). Behav Ecol Sociobiol 42:349–355

    Google Scholar 

  • Dahbi A, Cerdá X, Lenoir A (1998) Ontogeny of colonial hydrocarbon label in callow workers of the ant Cataglyphis iberica. Comptes Rendus de l’Académie des Sciences—Series III—Sciences de la Vie 321:395–402

    Google Scholar 

  • Dahbi A, Hefetz A, Cerdá X, Lenoir A (1999) Trophallaxis mediates uniformity of colony odor in Cataglyphis iberica ants (Hymenoptera, Formicidae). J Insect Behav 12:559–567

    Google Scholar 

  • Dani FR (2006) Cuticular lipids as semiochemicals in paper wasps and other social insects. Ann Zool Fenn 43:500–514

    Google Scholar 

  • Dani FR, Cervo R, Turillazzi S (1992) Abdomen stroking behaviour and its possible functions in Polistes dominulus (Christ) (Hymenoptera Vespidae). Behav Process 28:51–58

    CAS  Google Scholar 

  • Dani FR, Jones GR, Destri S, Spencer SH, Turillazzi S (2001) Deciphering the recognition signature within the cuticular chemical profile of paper wasps. Anim Behav 62:165–171

    Google Scholar 

  • Dani FR, Jones GR, Corsi S, Beard R, Pradella D, Turillazzi S (2005) Nestmate recognition cues in the honey bee: differential importance of cuticular alkanes and alkenes. Chem Senses 30:477–489

    CAS  PubMed  Google Scholar 

  • Dapporto L, Pansolli C, Turillazzi S (2004) Hibernation clustering and its consequences for associative nest foundation in Polistes dominulus (Hymenoptera Vespidae). Behav Ecol Sociobiol 56:315–321

    Google Scholar 

  • Dapporto L, Sledge MF, Turillazzi S (2005) Dynamics of cuticular chemical profiles of Polistes dominulus workers in orphaned nests. J Insect Physiol 51:969–973

    CAS  PubMed  Google Scholar 

  • Dapporto L, Santini A, Dani FR, Turillazzi S (2007) Workers of a Polistes paper wasp detect the presence of their queen by chemical cues. Chem Senses 32(8):795–802

    CAS  PubMed  Google Scholar 

  • Dawkins R (1976) The selfish gene. Oxford University Press, NewYork

    Google Scholar 

  • Downs SG, Ratnieks FLW (2000) Adaptive shifts in honey bee (Apis mellifera L.) guarding behavior support predictions of the acceptance threshold model. Behav Ecol 9:326–333

    Google Scholar 

  • Dettner K, Liepert C (1994) Chemical mimicry and camouflage. Ann Rev Entomol 39(1):129–154

    CAS  Google Scholar 

  • d’Ettorre P, Errard C (1999) Trophallaxie proctodéale chez la fourmi esclavagiste Polyergus rufescens. Actes Coll Insectes Soc 12:61–64

    Google Scholar 

  • d’Ettorre P, Heinze J (2005) Individual recognition in ant queens. Curr Biol 15:2170–2174

    PubMed  Google Scholar 

  • d’Ettorre P, Lenoir A (2010) Nestmate recognition. In: Lach L, Parr CL, Abbott KL (eds) Ant ecology. Oxford University Press, Oxford, pp 194–209

    Google Scholar 

  • d’Ettorre P, Mondy N, Lenoir A, Errard C (2002) Blending in with the crowd: social parasites integrate into their host colonies using a flexible chemical signature. Proc R Soc Lond B 269:1911–1918

    Google Scholar 

  • d’Ettorre P, Wenseleers T, Dawson J, Hutchinson S, Boswell T, Ratnieks FLW (2006) Wax combs mediate nestmate recognition by guard honey bees. Anim Behav 71:773–779

    Google Scholar 

  • Dreier S, d’Ettorre P (2009) Social context predicts recognition systems in ant queens. J Evol Biol 22(3):644–649

    CAS  PubMed  Google Scholar 

  • Dreier S, van Zweden JS, d’Ettorre P (2007) Long term memory of individual identity in ant queens. Biol Lett 17:459–462

    Google Scholar 

  • Erber J, Masuhr TH, Menzel R (1980) Localization of short-term memory in the brain of the bee, Apis mellifera. Behav Neural Biol 62:259–263

    Google Scholar 

  • Errard C (1994a) Development of interspecific recognition behavior in the ants Manica rubida and Formica selysi (Hymenoptera: Formicidae) reared in mixed-species groups. J Insect Behav 7:83–99

    Google Scholar 

  • Errard C (1994b) Long-term memory involved in nestmate recognition in ants. Anim Behav 48:263–271

    Google Scholar 

  • Errard C, Fresneau D, Heinze J, Francoeur A, Lenoir A (1997) Social organization in the guest-ant Formicoxenus provancheri. Ethology 103:149–159

    Google Scholar 

  • Errard C, Hefetz A, Jaisson P (2006) Social discrimination tuning in ants: template formation and chemical similarity. Behav Ecol Sociobiol 59(3):353–363

    Google Scholar 

  • Espelie KE, Hermann HR (1990) Surface lipid of the social wasp Polistes annularis (L.) and its nest and nest pedicel. J Chem Ecol 16:1841–1852

    CAS  PubMed  Google Scholar 

  • Espelie KE, Wenzel JW, Chang G (1990) Surface lipids of social wasp Polistes metricus say and its nest and pedicel and their relation to nestmate recognition. J Chem Ecol 16:2229–2241

    CAS  PubMed  Google Scholar 

  • Fahrbach SE, Strande JL, Robinson GE (1995) Neurogenesis is absent in the brains of adult honey bees and does not explain behavioural neuroplasticity. Neurosci Lett 197:145–148

    CAS  PubMed  Google Scholar 

  • Farris SM, Robinson GE, Davis RL, Fahrbach SE (1999) Larval and pupal development of the mushroom bodies in the honey bee. Apis mellifera J Comp Neurol 414:97–113

    CAS  Google Scholar 

  • Fénéron R, Jaisson P (1995) Ontogeny of nestmate brood recognition in a primitive ant, Ectatomma tubercalutum Olivier (Ponerinae). Anim Behav 50(1):9–14

    Google Scholar 

  • Foitzik S, DeHeer CJ, Hunjan DN, Herbers JM (2001) Coevolution in host-parasite systems: behavioural strategies of slave-making ants and their hosts. Proc R Soc Lond B 268:1139–1146

    CAS  Google Scholar 

  • Foubert E, Nowbahari E (2008) Memory span for heterospecific individuals’odors in an ant, Cataglyphis cursor. Learn Behav 36:319–326

    PubMed  Google Scholar 

  • Gamboa GJ (1988) Sister, aunt-niece, and cousin recognition by social wasps. Behav Genet 18:409–423

    CAS  PubMed  Google Scholar 

  • Gamboa GJ (2004) Kin recognition in eusocial wasps. Ann Zool Fennici 41:789–808

    Google Scholar 

  • Gamboa GJ, Reeve HK, Pfennig DW (1986a) The evolution and ontogeny of nestmate recognition in social wasps. A Rev Entomol 31:431–454

    Google Scholar 

  • Gamboa GJ, Reeve HK, Ferguson I, Wacker TL (1986b) Nestmate recognition in social wasps: the origin and acquisition of recognition odours. Anim Behav 34:685–695

    Google Scholar 

  • Getz WM, Smith KB (1983) Genetic kin recognition: honey bees discriminate between full and half sisters. Nature 302:147–148

    Google Scholar 

  • Getz WM, Smith KB (1986) Honey bee kin recognition: learning self and nestmate phenotypes. Anim Behav 34:1617–1626

    Google Scholar 

  • Greene MJ, Gordon DM (2003) Social insects cuticular hydrocarbons inform task decisions. Nature 423:32

    CAS  PubMed  Google Scholar 

  • Gronenberg W, Heeren S, Hölldobler B (1996) Age-dependent and task-related morphological changes in the brain and the mushroom bodies of the ant Camponotus floridanus. J Exp Biol 199:2011–2019

    PubMed  Google Scholar 

  • Guerrieri FJ, Nehring V, Jørgensen CG, Nielsen J, Galizia CG, d’Ettorre P (2009) Ants recognize foes and not friends. Proc R Soc B 276:2461–2468

    PubMed Central  CAS  PubMed  Google Scholar 

  • Guerrieri FJ, d’Ettorre P, Devaud JM, Giurfa M (2011) Long- term olfactory memories are stabilised via protein synthesis in Camponotus fellah ants. J Exp Biol 214:3300–3304

    CAS  PubMed  Google Scholar 

  • Hadley NF (1994) Water relations of terrestrial arthropods. Academic Press, San Diego

    Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behaviour. J Theor Biol 7:1–50

    CAS  PubMed  Google Scholar 

  • Hamilton WD (1987) Discrimination nepotism: expectable, common, overlooked. In: Fletcher DJC, Michener CD (eds) Kin recognition in animals. Wiley, New York, pp 417–437

    Google Scholar 

  • Harano K, Sasaki M (2006) Renewal process of nestmate recognition template in European honeybee Apis mellifera L. (Hymenoptera: Apidae). Appl Entomol Zool 41(2): 325–330

    Google Scholar 

  • Hare JF, Alloway TM (2001) Prudent Protomognathus and despotic Leptothorax duloticus: differential costs of ant slavery. Proc Natl Acad Sci USA 98:12093–12096

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hefetz A (2007) The evolution of hydrocarbon pheromone parsimony in ants (Hymenoptera: Formicidae)—interplay of colony odor uniformity and odor idiosyncrasy: a review. Myrmecol News 10:59–68

    Google Scholar 

  • Heimbeck G, Bugnon V, Gendre N, Häberlin C, Stocker RF (1999) Smell and taste perception in D. melanogaster larva: toxin expression studies in chemosensory neurons. J Neurosci 19:6599–6609

    CAS  PubMed  Google Scholar 

  • Heisenberg M (1994) Central brain function in insects: genetic studies on the mushroom bodies and central complex in Drosophila. Forts Zool 39:30–39

    Google Scholar 

  • Heisenberg M (1998) What do the mushroom bodies do for the insect brain? Intro Learn Mem 5(1):1–10

    CAS  Google Scholar 

  • Hepper PG (1987) The amniotic fluid: an important priming role in kin recognition. Anim Behav 35(5):1343–1346

    Google Scholar 

  • Hepper PG, Waldman B (1992) Embryonic olfactory learning in frogs. Q J Exp Psychol B 44(3–4): 179–197

    Google Scholar 

  • Hepper PG (2003) Prenatal psychological and behavioural development. In: Valsiner J, Connolly KJ (eds) The handbook of developmental psychology. Sage, London, pp 91–114

    Google Scholar 

  • Hölldobler B, Michener CD (1980) Mechanisms of identification and discrimination in social Hymenoptera. In: Markl H (ed) Evolution of social behavior: hypotheses and empirical tests. VC, Weinheim, pp 35–58

    Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Belknap Press, Cambridge, p 732

    Google Scholar 

  • Holman L, Jørgensen CG, Nielsen J, d’Ettorre P (2010) Identification of an ant queen pheromone regulating worker sterility. Proc R Soc B 277(1701):3793–3800

    PubMed Central  CAS  PubMed  Google Scholar 

  • Holman L, Leroy C, Jørgensen C, Nielsen J, d’Ettorre P (2013) Are queen ants inhibited by their own pheromone? Regulation of productivity via negative feedback. Behav Ecol 24(2):380–385

    Google Scholar 

  • Holmes WG, Sherman PW (1982) The ontogeny of kin recognition in two species of ground squirrels. Am Zool 22:491–517

    Google Scholar 

  • Hudson R (1993) Olfactory imprinting. Current Opin Neurobiol 3(4):548–552

    CAS  Google Scholar 

  • Ichinose K, Lenoir A (2010) Hydrocarbons detection levels in ants. Insect Soc 57:453–455

    Google Scholar 

  • Isingrini M, Lenoir A, Jaisson P (1985) Preimaginal learning as a basis of colony brood recognition in the ant Cataglyphis cursor. Proc Nat Acad Sci, USA 82:8545–8547

    CAS  Google Scholar 

  • Ito K, Hotta Y (1992) Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster. Dev Biol 149:134–148

    CAS  PubMed  Google Scholar 

  • Jaisson P (1972) Mise en évidence d’une phéromone d’attractivité produite la jeune ouvrière Formica (Hymenoptera : Formicidae). C R Acad Sci Paris Ser D 274:429–432

    Google Scholar 

  • Jaisson P (1980) Environmental preference induced experimentally in ants (Hymenoptera: Formicidae). Nature 286:388–389

    Google Scholar 

  • Jaisson P (1987) The construction of fellowship between nestmates in social hymenoptera. In: Pasteels JM, Deneubourg JL (eds) Experientia supplementum 54. From individual to collective behaviour in social insects. Birkhauser Verlag, Basel, pp 313–331

    Google Scholar 

  • Jaisson P (1991) Kinship and fellowship in ants and social wasps. In. Hepper PG (ed) Kin recognition. Cambridge University Press, Cambridge, pp 60–93

    Google Scholar 

  • Jeanson R, Weidenmüller A (2013) Interindividual variability in social insects–proximate causes and ultimate consequences. Biol Rev, pp 671–687

    Google Scholar 

  • Johnson CA, Vander Meer RK, Lavine B (2001) Changes in the cuticular hydrocarbon profile of the slave-maker ant queen, Polyergus breviceps Emery, after killing a Formica host queen (Hymenoptera: Formicidae). J Chem Ecol 27(9):1787–1804

    CAS  PubMed  Google Scholar 

  • Johnson BR, van Wilgenburg E, Tsutsui ND (2011) Nestmate recognition in social insects: overcoming physiological constraints with collective decision making. Behav Ecol Sociobiol 65(5):935–944

    PubMed Central  PubMed  Google Scholar 

  • Jutsum AR, Saunders TS, Cherrett JM (1979) Intraspecific aggression in the leaf-cutting ant Acromyrmex octospinosus. Anim Behav 27:839–844

    Google Scholar 

  • Kaib M, Heinze J, Ortius D (1993) Cuticular hydrocarbons profiles in the slave-making ant Harpogoxenus sublaevis and its hosts. Naturwissenschaften 80:281–285

    CAS  Google Scholar 

  • Keegans SJ, Morgan ED, Turillazzi S, Jackson BD, Billen J (1993) The dufour gland and the secretion placed on eggs of two species of social wasps, Liostenogaster flavolineata and Parischnogaster jacobsoni (Vespidae: Stenogastrinae). J Chem Ecol 19:279–290

    CAS  PubMed  Google Scholar 

  • Lahav S, Soroker V, VanderMeer RK, Hefetz A (2001) Segregation of colony odor in the desert ant Cataglyphis niger. J Chem Ecol 27:927–943

    CAS  PubMed  Google Scholar 

  • Lambardi D, Dani FR, Turillazzi S, Boomsma JJ (2007) Chemical mimicry in an incipient leaf-cutting ant social parasite. Behav Ecol Sociobiol 61(6):843–851

    Google Scholar 

  • Lee T, Lee A, Luo L (1999) Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 126:4065–4076

    CAS  PubMed  Google Scholar 

  • Lenoir A, Errard C, Francoeur A, Loiselle R (1992) Relations entre la fourmi parasite Formicoxenus provancheri et sur hôte Myrmica incompleta. Données biologiques et éthologiques (Hym. Formicidae). Insect Soc 39:81–97

    Google Scholar 

  • Lenoir A, Fresneau D, Errard C, Hefetz A (1999) Individuality and colonial identity in ants: the emergence of the social representation concept. In: Detrain C, Deneubourg J-L, Pasteels JM (eds) Information processing in social insects. Birkhäuser Verlag, Basel, pp 219–237

    Google Scholar 

  • Lenoir A, d’Ettorre P, Errard C, Hefetz A (2001) Chemical ecology and social parasitism in ants. Annu Rev Entomol 46:573–599

    CAS  PubMed  Google Scholar 

  • Lenoir A, Depickere S, Devers S, Christides JP, Detrain C (2009) Hydrocarbons in the ant Lasius niger: from the cuticle to the nest and home range marking. J Chem Ecol 35:913–921

    CAS  PubMed  Google Scholar 

  • Leonhardt SD, Brandstaetter AS, Kleineidam CJ (2007) Reformation process of the neuronal template for nestmate-recognition cues in the carpenter ant Camponotus floridanus. J Comp Physiol 193:993–1000

    Google Scholar 

  • Liebig J (2010) Hydrocarbon profiles indicate fertility and dominance status in ant, bee, and wasp colonies. Insect hydrocarbons: biology, biochemistry, and chemical ecology. Cambridge University Press, Cambridge, pp 254–281

    Google Scholar 

  • Liebig J, Peeters C, Oldham NJ, Markstädter C, Hölldobler B (2000) Are variations in cuticular hydrocarbons of queens and workers a reliable signal of fertility in the ant Harpegnathos saltator? Proc Natl Acad Sci USA 97:4124–4131

    PubMed Central  CAS  PubMed  Google Scholar 

  • Liu Z, Yamane S, Wang Q, Yamamoto H (1998) Nestmate recognition and temporal modulation in the patterns of cuticular hydrocarbons in natural colonies of Japanese carpenter ant Camponotus japonicus Mayr (Hymenoptera: Formicidae). J Ethol 16:57–65

    CAS  Google Scholar 

  • Lockey KH (1988) Lipids of the insect cuticle: origin composition and function. Comp Biochem Physiol 89B:595–645

    Google Scholar 

  • Lorenzi MC (1992) Epicuticular hydrocarbons of Polistes biglumis bimaculatus (Hymenoptera, Vespidae): preliminary results. Ethol Ecol Evol 3: 61–63, (Special Issue)

    Google Scholar 

  • Lorenzi MC, Bagnères AG (1996) Hydrocarbon pattern variations in the paper of Polistes biglumis bimaculatus nests usurped or not by the social parasite Polistes atrimandibularis (Hymenoptera Vespidae). Proc XX Int Congr Entomol Firenze 416:13–107

    Google Scholar 

  • Lorenzi MC, Bagnères AG, Clément JL (1996) The role of cuticular hydrocarbons in insect societies: is it the same in paper wasps? In: Turillazzi S, West Eberhard MJ (eds) Natural history and the evolution of paper wasps. Oxford University Press, Oxford, pp 178–189

    Google Scholar 

  • Lorenzi MC, Cometto I, Marchisio G (1999) Species and colony components in the recognition odor of young social wasps: their expression and learning (Polistes biglumis and P. atrimandibularis; Hymenoptera: Vespidae). J Insect Behav 12(2):147–158

    Google Scholar 

  • Lorenzi MC, Sledge MF, Laiolo P, Sturlini E, Turillazzi S (2004) Cuticular hydrocarbon dynamics in young adult Polistes dominulus (Hymenoptera: Vespidae) and the role of linear hydrocarbons in nestmate recognition systems. J Insect Physiol 50:935–941

    CAS  PubMed  Google Scholar 

  • Lorenzi MC, Caldi M, Cervo R (2007) The chemical strategies used by Polistes nimphus social wasp usurpers (Hymenoptera Vespidae). Biol J Linn Soc 91:505–512

    Google Scholar 

  • Lorenzi MC, Cervo R, Bagneres A-G (2011) Facultative social parasite mark host nests with branched hydrocarbons. Anim Behav 42(5):1143–1149

    Google Scholar 

  • Martin SJ, Vitikainen E, Helanterä H, Drijfhout FP (2008) Chemical basis of nest-mate discrimination in the ant Formica exsecta. Proc R Soc B 275(1640):1271–1278

    PubMed Central  CAS  PubMed  Google Scholar 

  • Masson C, Pham-Delègue MH, Fonta C, Gascuel J, Arnold G, Nicolas G, Kerszberg M (1993) Recent advances in the concepts of adaptation to natural odour signals in the honeybee, Apis mellifera L. Apidologie 24:169–194

    Google Scholar 

  • Mateo JM (2004) Recognition systems and biological organization: the perception component of recognition. Ann Zool Fennici 41:729–745

    Google Scholar 

  • Menzel R (1993) Associative learning in honey bees. Apidologie 24:157–168

    Google Scholar 

  • Meskali M, Bonavita-Cougourdan A, Provost E, Bagnères AG, Dusticier G, Clément JL (1995) Mechanism underlying cuticular hydrocarbon homogeneity in the ant Camponotus vagus (SCOP.)(Hymenoptera: Formicidae): role of postpharyngeal glands. J Chem Ecol 21(8):1127–1148

    CAS  PubMed  Google Scholar 

  • Michener CD, Smith BH (1987) Kin recognition in primitively social insects. In: Fletcher DJC, Michener CD (eds) Kin recognition in animals. John Wiley and Sons Press, Chichester, pp 209–242

    Google Scholar 

  • Mintzer A, Vinson SB (1985) Kinship and incompatibility between colonies of the acacia-ant Pseudomyrmex ferruginea. Behav Ecol Sociobiol 17:75–78

    Google Scholar 

  • Mitra A, Ramachandran A, Gadagkar R (2014) Nestmate discrimination in the social wasp Ropalidia marginata: chemical cues and chemosensory mechanism. Anim Behav 88:113–124

    Google Scholar 

  • Monnin T (2006) Chemical recognition of reproductive status in social insects. Ann Zool Fenn 43:515–530

    Google Scholar 

  • Morel L (1983) Relation entre comportement agressif et privation sociale précoce chez les jeunes fourmis immatures de la fourmi Camponotus vagus Scop. (Hymenoptera: Formicidae). C R Hebd Séances. Acad Sci Série D 296:449–452

    Google Scholar 

  • Morel L (1988) Ontogènese de la reconnaissance des membres de la société chez Camponotus floridanus (Hymenoptera: Formicidae). Role de l’expérience sociale précoce. Biologie du Comportement 13:59–72

    Google Scholar 

  • Newey PS, Robson SKA, Crozier RH (2009) Temporal variation in recognition cues: implications for the social life of weaver ants Oecophylla smaragdina. Anim Behav 77:481–488

    Google Scholar 

  • Nielsen J, Boomsma JJ, Oldham NJ, Petersen HC, Morgan ED (1999) Colony level and season-specific variation in cuticular hydrocarbon profiles of individual workers in the ant Formica truncorum. Insect Soc 46:58–65

    Google Scholar 

  • Nowbahari E, Lenoir A (1989) Age related changes in aggression in ant Cataglyphis cursor (Hymenoptera, Formicidae). Behav Process 18:173–181

    CAS  Google Scholar 

  • Ozaki M, Hefetz A (2014) Neural mechanisms and information processing in recognition systems. Insects 5:722–741  

    Google Scholar 

  • Ozaki M, Wada-Katsumata A (2010) Perception and olfaction of cuticular compounds. In: Blomquist GJ, Bagnères AG (eds) Insect hydrocarbons: biology, biochemistry and chemical ecology. Cambridge University Press, Cambridge, pp 207–221

    Google Scholar 

  • Ozaki M, Wada-Katsumata A, Fujikawa K, Iwasaki M, Yokohari F, Satoji Y, Nisimura T, Yamaoka R (2005) Ant nestmate and non-nestmate discrimination by a chemosensory sensillum. Science 309:311–314

    CAS  PubMed  Google Scholar 

  • Page RE, Breed ME (1987) Kin recognition in social bees. Trends Ecol Evol 2:272–275

    PubMed  Google Scholar 

  • Panek LM, Gamboa GJ, Espelie KE (2001) The effect of a wasp’s age on its cuticular hydrocarbon profile and its tolerance by nestmate and non-nestmate conspecifics (Polistes fuscatus, Hymenoptera: Vespidae). Ethology 107:55–63

    Google Scholar 

  • Pauls D, Selcho M, Gendre N, Stocker RF, Thum AS (2010) Drosophila larvae establish appetitive olfactory memories via mushroom body neurons of embryonic origin. J Neurosci 30:10655–10666

    CAS  PubMed  Google Scholar 

  • Peeters C, Monnin T, Malosse C (1999) Cuticular hydrocarbons correlated with reproductive status in a queenless ant. Proc R Soc Lond B 266:1323–1327

    CAS  Google Scholar 

  • Pfenning DW, Reeve HK, Shellmann JS (1983a) Learned component of nestmate discrimination in workers of a social wasp, Polistes fuscatus (Hymenoptera, Vespidae). Anim Behav 31:412–416

    Google Scholar 

  • Pfenning DW, Gamboa GJ, Reeve HK, Shellmann JS, Reeve JS, Ferguson ID (1983b) The mechanism of nestmate discrimination in social wasps (Hymenoptera: Vespidae). Behav Ecol Sociobiol 13:299–305

    Google Scholar 

  • Provost E, Blight O, Tirard A, Renucci M (2008) Hydrocarbons and insects’ social physiology. In: Maes RP (ed) Insect physiology: new research. Nova Science Publishers, New York, pp 19–72

    Google Scholar 

  • Python F, Stocker RF (2002) Adult-like complexity of the larval antennal lobe of D. melanogaster despite markedly low numbers of odorant receptor neurons. J Comp Neurol 445:374–387

    PubMed  Google Scholar 

  • Ramaekers A, Magnenat E, Marin EC, Gendre N, Jefferis GSXE, Luo L, Stocker RF (2005) Glomerular maps without cellular redundancy at successive levels of the Drosophila larval olfactory circuit. Curr Biol 15:982–992

    CAS  PubMed  Google Scholar 

  • Ratnieks FL (1991) The evolution of genetic odor-cue diversity in social Hymenoptera. Am Nat pp 202–226

    Google Scholar 

  • Ray S (1999) Survival of olfactory memory through metamorphosis in the fly Musca domestica. Neurosci Lett 259:37–40

    CAS  PubMed  Google Scholar 

  • Reeve HK (1989) The evolution of conspecific acceptance thresholds. Am Nat 133:407–435

    Google Scholar 

  • Robinson SR, Smotherman WP (1991) Fetal learning: implications for the development of kin recognition. In: Hepper PG (ed) kin recognition. Cambridge University Press, Cambridge, England, pp 308–334

    Google Scholar 

  • Ross NM, Gamboa GJ (1981) Nestmate discrimination in social wasps (Polistes metricus, Hymenoptera: Vespidae). Behav Ecol Sociobiol 9:163–165

    Google Scholar 

  • Schaal B, Marlier L, Soussignan R (2000) Human fetuses learn odours from their pregnant mother’s diet. Chem Sens 25:729–737

    CAS  Google Scholar 

  • Shellman JS, Gamboa GJ (1982) Nestmate discrimination in social wasps: the role of exposure to nest and nestmates. Behav Ecol Sociobiol 11:51–53

    Google Scholar 

  • Signorotti L, Cappa F, d’Ettorre P, Cervo R (2014a) Novel insights into the ontogeny of nestmate recognition in Polistes social wasps. PLoS ONE 9(5):e97024

    PubMed Central  PubMed  Google Scholar 

  • Signorotti L, Jaisson P, d’Ettorre P (2014b) Larval memory affects adult nestmate recognition in the ant Aphaenogaster senilis. Proc R Soc B 281:20132579

    PubMed Central  PubMed  Google Scholar 

  • Singer TL (1998) Roles of hydrocarbons in the recognition systems of insects. Am Zool 38(2):394–405

    CAS  Google Scholar 

  • Singer TL, Espelie KE (1992) Social wasps use nest paper hydrocarbons for nestmate recognition. Anim Behav 44(1):63–68

    Google Scholar 

  • Singer TL, Camann MA, Espelie KE (1992) Discriminant analysis of cuticular hydrocarbons of social wasp Polistes exclamans Viereck and surface hydrocarbons of its nest paper and pedicel. J Chem Ecol 18:785–797

    CAS  PubMed  Google Scholar 

  • Singh RN, Singh K (1984) Fine structure of the sensory organs of Drosophila melanogaster Meigen larva (Diptera: Drosophilidae). Int J Insect Morphol Embryol 13:255–273

    Google Scholar 

  • Sledge MF, Trinca I, Massolo A, Boscaro F, Turillazzi S (2004) Variation in cuticular hydrocarbon signatures, hormonal correlates and establishment of reproductive dominance in a polistine wasp. J Insect Physiol 50:73–83

    CAS  PubMed  Google Scholar 

  • Soroker V, Vienne C, Hefetz A, Nowbahari E (1994) The postpharyngeal gland as a “gestalt” organ for nestmate recognition in the ant Cataglyphis niger. Naturwissenschaften 81:510–513

    CAS  Google Scholar 

  • Soroker V, Vienne C, Hefetz A (1995) Hydrocarbon dynamics within and between nestmates in Cataglyphis niger (Hymenoptera: Formicidae). J Chem Ecol 21(3):365–378

    CAS  PubMed  Google Scholar 

  • Soroker V, Fresneau D, Hefetz A (1998) Formation of colony odor in ponerine ant Pachycondyla apicalis. J Chem Ecol 24(6):1077–1090

    CAS  Google Scholar 

  • Soroker V, Lucas C, Simon T, Fresneau D, Durand JL, Hefetz A (2003) Hydrocarbon distribution and colony odour homogenization in Pachycondyla Apicalis. Insect Soc 50:212–217

    Google Scholar 

  • Starks PT (2004) Recognition systems: from components to conservation. In: Annales Zoologici Fennici, vol 41(6). Suomen Biologian Seura Vanamo, Helsinki, pp 689–690 (1964-)

    Google Scholar 

  • Stroeymeyt N, Guerrieri FJ, van Zweden JS, d’Ettorre P (2010) Rapid decision-making with side-specific perceptual discrimination in ants. PLoS ONE 5(8):e12377

    PubMed Central  PubMed  Google Scholar 

  • Stuart RJ (1987a) Nestmate recognition in leptothoracine ants: testing Fielde’s progressive odor hypothesis. Ethology 76(2):116–123

    Google Scholar 

  • Stuart RJ (1987b) Individual workers produce colony-specific nestmate recognition cues in the ant, Leptothorax curvispinosus. Anim Behav 35:1062–1069

    Google Scholar 

  • Stuart RJ (1988) Collective cues as a basis for nestmate recognition in polygynous leptothoracine ants. Proc R Soc B 85(12):4572–4575

    CAS  Google Scholar 

  • Stuart RJ (1992) Nestmate recognition and the ontogeny of acceptability in the ant, Leptothorax curvispinosus. Behav Ecol Sociobiol 30:403–408

    Google Scholar 

  • Sturgis S, Gordon DM (2012) Nestmate recognition in ants (Hymenoptera, Formicidae): a review. Myrmecological News 16:101–110

    Google Scholar 

  • Tibbetts EA (2002) Visual signals of individual identity in the wasp Polistes fuscatus. Proc R Soc B 269(1469):1423–1428

    PubMed Central  PubMed  Google Scholar 

  • Tissot M, Stocker RF (2000) Metamorphosis in Drosophila and other insects: the fate of neurons throughout the stages. Prog Neurobiol 62(1):89–111

    CAS  PubMed  Google Scholar 

  • Turillazzi S (1985) Function and characteristics of the abdominal substance secreted by wasps of the genus Parischnogaster (Hymenoptera Stenogastrinae). Monit Zool Ital 19:91–99

    Google Scholar 

  • Turillazzi S, Cervo R, Cavallari I (1990) Invasion of the nest of Polistes dominulus by the social parasite Sulcopolistes sulcifer (Hymenoptera, Vespidae). Ethology 84:47–59

    Google Scholar 

  • Turillazzi S, Sledge MF, Dani FR, Cervo R, Massolo A, Fondelli L (2000) Social hackers: integration in the host chemical recognition system by a paper wasp social parasite. Naturwissenschaften 87(4):172–176

    CAS  PubMed  Google Scholar 

  • Turillazzi S, Fanelli D, Theodora P, Lambardi D, Ortolani I, Hashim R, Baracchi D (2008) Determinants of immature brood and nest recognition in a stenogastrine wasp (Hymenoptera Vespidae). Ethol Ecol Evol 20(1):17–33

    Google Scholar 

  • Tully T, Cambiazo V, Kruse L (1994) Memory through metamorphosis in normal and mutant Drosophila. J Neurosci 14:68–74

    CAS  PubMed  Google Scholar 

  • Vander Meer RK, Morel L (1998) Nestmate recognition in ants. In: Vander Meer RK, Breed MD, Winston M, Espelie C (eds) Pheromone communication in social insects: ants, wasps, bees and termites, pp 79–103

    Google Scholar 

  • Van Hooser CA, Gamboa GJ, Fishwild TG (2002) The function of abdominal stroking in the paper wasp, Polistes fuscatus (Hymenoptera Vespidae). Ethol Ecol Evol 14(2):141–148

    Google Scholar 

  • Van Oystaeyen A, Oliveira RC, Holman L, van Zweden JS, Romero C, Oi CA, d’Ettorre P, Khalesi M, Billen J, Wäckers F, Millar JG, Wenseleers T (2014) Conserved class of queen pheromones stops social insect workers from reproducing. Science 343(6168):287–290

    PubMed  Google Scholar 

  • van Zweden JS, d’Ettorre P (2010) Nestmate recognition in social insects and the role of hydrocarbons. In: Blomquist GJ, Bagnères AG (eds) Insect hydrocarbons: biology, biochemistry and chemical ecology. Cambridge University Press, Cambridge, pp 222–243

    Google Scholar 

  • van Zweden JS, Dreier S, d’Ettorre P (2009) Disentangling environmental and heritable nestmate recognition cues in a carpenter ant. J Insect Physiol 55:158–163

    PubMed  Google Scholar 

  • van Zweden JS, Brask JB, Christensen JH, Boomsma JJ, Linksvayer TA, d’Ettorre P (2010) Blending of heritable recognition cues among ant nestmates creates distinct colony gestalt odours but prevents within-colony nepotism. J Evol Biol 23(7):1498–1508

    PubMed  Google Scholar 

  • Vienne C, Bagnères AG, Lange C, Errard C (1990) Etude chimique de la reconnaissance interindividuelle chez Myrmica rubra et Manica rubida (Formicidae, Myrmicinae) élevées en colonies mixtes artificielles. Actes Colloq Insectes Soc 6:261–265

    Google Scholar 

  • Vienne NC, Soroker V, Hefetz A (1995) Congruency of hydrocarbon patterns in heterospecific groups of ants: transfer and/or biosynthesis? Insect Soc 42(3):267–277

    Google Scholar 

  • Wagner D, Brown MJF, Broun P, Cuevas W, Moses LE, Chao DL, Gordon DM (1998) Task related differences in the cuticular hydrocarbon composition of harvester ants, Pogonomyrmex barbatus. J Chem Ecol 24:2021–2037

    CAS  Google Scholar 

  • Waldman B (1988) The ecology of kin recognition. Ann Rev Ecol Syst 19:543–571

    Google Scholar 

  • Wilson EO (1971) The insect societies. Belknap Press of Harvard University Press, Cambridge

    Google Scholar 

  • Zacchi F, Cervo R, Turillazzi S (1996) How Polistes semenowi, obligate social parasite, invades the nest of its host, Polistes dominulus (Hymenoptera, Vespidae). Insect Soc Life 1:125–130

    Google Scholar 

  • Zahavi A (1977) Reliability in communication system and the evolution of altruism. In: Stonehous B, Perrins C (eds) Evolutionary ecology. University Park Press, Baltimore

    Google Scholar 

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Authors and Affiliations

  1. Laboratory of Experimental and Comparative Ethology (LEEC), University of Paris 13, Sorbonne Paris Cité, Villetaneuse, France

    Lisa Signorotti & Patrizia d’Ettorre

  2. Department of Biology, University of Firenze, Sesto Fiorentino, Italy

    Rita Cervo

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    Laura Aquiloni

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    Elena Tricarico

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Signorotti, L., Cervo, R., d’Ettorre, P. (2015). Ontogeny of Nestmate Recognition in Social Hymenoptera. In: Aquiloni, L., Tricarico, E. (eds) Social Recognition in Invertebrates. Springer, Cham. https://doi.org/10.1007/978-3-319-17599-7_10

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