Abstract
Reproductive division of labor in social insects is accompanied by the reliable communication of individual fertility status. A central question is whether there exists a general mechanism underlying this communication system across species. The best way to produce reliable information is through physiological markers tightly associated with reproductive status. Cuticular hydrocarbons exhibit this link to individual fertility in several species of ants, bees, and wasps, and we present the first evidence for such a system in a non-Hymenopteran eusocial species. In the termite Zootermopsis nevadensis, we identified four polyunsaturated alkenes, which only occur in significant amounts on reproductives that are actively producing gametes. These compounds are either absent or only occur in small amounts in soldiers, worker-like larvae, and secondary reproductives with inactive gonads. In contrast to Hymenopteran social insects, both sexes express the reproductive peaks. The reproductive-specific hydrocarbons may promote tending behavior by worker-like larvae or act as a primer pheromone, inhibiting the reproductive development of immature conspecifics.
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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
Ayasse M, Marlovits T, Tengö J, Taghizadeh T, Francke W (1995) Are there pheromonal dominance signals in the bumblebee Bombus hypnorum L (Hymenoptera, Apidae)? Apidologie 26:163–180
Bonavita-Cougourdan A, Theraulaz G, Bagnères AG, Roux M, Pratte M, Provost E, Clement JL (1991) Cuticular hydrocarbons, social organization and ovarian development in a polistine wasp: Polistes dominulus Christ. Comp Biochem Physiol B 100:667–680
Brent CS, Traniello JFA (2001a) Social regulation of testicular development in primary and secondary males of the dampwood termite Zootermopsis angusticollis Hagen. Insect Soc 48:384–391
Brent CS, Traniello JFA (2001b) Influence of sex-specific stimuli on ovarian maturation in both primary and secondary reproductives of the dampwood termite Zootermopsis angusticollis. Physiol Entomol 26:239–247
Brent CS, Schal C, Vargo EL (2005) Endocrine changes in maturing primary queens of Zootermopsis angusticollis. J Ins Physiol 51:1200–1209
Brent CS, Peeters C, Dietemann V, Crewe R, Vargo EL (2006) Hormonal correlates of reproductive status in the queenless ponerine ant, Streblognathus peetersi. J Comp Physiol A 192:315–320
Castle GB (1934) The dampwood termites of the western United State, genus Zootermopsis (formerly Termopsis). In: Kofoid J (ed) Termites and termite control. University of California Press, Berkeley, pp 273–310
Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E, Plymouth
Clément JL, Bagnères AG (1998) Nestmate recognition in termites. In: Vander Meer RK, Breed MD, Espelie KE, Winston ML (eds) Pheromone communication in social insects ants, wasps, bees, and termites. Westview, Boulder, pp 126–155
Cuvillier-Hot V, Cobb M, Malosse C, Peeters C (2001) Sex, age and ovarian activity affect cuticular hydrocarbons in Diacamma ceylonense, a queenless ant. J Ins Physiol 47:485–493
Cuvillier-Hot V, Lenoir A, Crewe R, Malosse C, Peeters C (2004) Fertility signalling and reproductive skew in queenless ants. Anim Behav 68:1209–1219
Danforth BN (2002) Evolution of sociality in a primitively eusocial lineage of bees. Proc Natl Acad Sci USA 99:286–290
Dani FR (2006) Cuticular lipids as semiochemicals in paper wasps and other social insects. Ann Zool Fennici 43:500–514
de Biseau JC, Passera L, Daloze D, Aron S (2004) Ovarian activity correlates with extreme changes in cuticular hydrocarbon profile in the highly polygynous ant, Linepithema humile. J Ins Physiol 50:585–593
Denis D, Blatrix R, Fresneau D (2006) How an ant manages to display individual and colonial signals by using the same channel. J Chem Ecol 32:1647–1661
Dietemann V, Peeters C, Liebig J, Thivet V, Hölldobler B (2003) Cuticular hydrocarbons mediate recognition of queens and reproductive workers in the ant Myrmecia gulosa. Proc Natl Acad Sci USA 100:10341–10346
Dietemann V, Liebig J, Hölldobler B, Peeters C (2005) Changes in the cuticular hydrocarbons of incipient reproductives correlate with triggering of worker policing in the bulldog ant Myrmecia gulosa. Behav Ecol Sociobiol 58:486–496
Dillwith JW, Adams TS, Blomquist GJ (1983) Correlation of housefly sex pheromone production with ovarian development. J Insect Physiol 29:377–386
D'Ettorre P, Heinze J, Ratnieks FLW (2004) Worker policing by egg-eating in the ponerine ant, Pachycondyla inversa. Proc R Soc Lond B Biol Sci 271:1427–1434
Endler A, Liebig J, Schmitt T, Parker JE, Jones GR, Schreier P, Hölldobler B (2004) Surface hydrocarbons of queen eggs regulate worker reproduction in a social insect. Proc Natl Acad Sci USA 101:2945–2950
Endler A, Liebig J, Hölldobler B (2006) Queen fertility, egg marking and colony size in the ant Camponotus floridanus. Behav Ecol Sociobiol 59:490–499
Fan Y, Chase J, Sevala VL, Schal C (2002) Lipophorin-facilitated hydrocarbon uptake by oocytes in the German cockroach Blattella germanica (L.) J Exp Biol 205:781–790
Gadagkar R (1994) Why the definition of eusociality is not helpful to understand its evolution and what should we do about it. Oikos 70:485–488
Gibbs AG (1998) Water-proofing properties of cuticular lipids. Am Zool 38:471–482
Greenberg SLW, Stuart AM (1979) The influence of group size on ovarian development in adult and neotenic reproductives of the termite Zootermopsis angusticollis Hagen (Hodotermitidae). Internatl J Invert Repro 1:99–108
Greenberg SLW, Tobe SS (1985) Adaptation of a radiochemical assay for juvenile hormone biosynthesis to study caste differentiation in a primitive termite. J Ins Physiol 31:347–352
Grozinger CM, Robinson GE (2007) Endocrine modulation of a pheromone-responsive gene in the honey bee brain. J Comp Physiol A 193:461–470
Hannonen M, Sledge MF, Turillazzi S, Sundström L (2002) Queen reproduction, chemical signalling and worker behaviour in polygyne colonies of the ant Formica fusca. Anim Behav 64:477–485
Hartfelder K, Emlen DJ (2005) Endocrine control of insect polyphenism. In: Gilbert LI, Iatrou K, Gill SS (eds) Comprehensive molecular insect science, vol. 3. Elsevier, Boston, pp 651–703
Haverty MI, Thorne BL (1989) Agonistic behavior correlated with hydrocarbon phenotypes in dampwood termites, Zootermopsis (Isoptera, Termopsidae). J Ins Behav 2:523–543
Haverty MI, Page M, Nelson LJ, Blomquist GJ (1988) Cuticular hydrocarbons of dampwood termites, Zootermopsis: intracolony and intercolony variation and potential as taxonomic characters. J Chem Ecol 14:1035–1058
Heath H (1903) The habits of California termites. Biol Bull 4:7–63
Heinze J (2004) Reproductive conflict in insect societies. Adv Stud Behav 34:1–57
Heinze J, Stengl B, Sledge MF (2002) Worker rank, reproductive status and cuticular hydrocarbon signature in the ant. Pachycondyla cf. inversa. Behav Ecol Sociobiol 52:59–65
Hewitt PH, Watson JAL, Nel JJC, Schoeman I (1972) Control of the change from group to pair behaviour by Hodotermes mossambicus reproductives. J Ins Physiol 18:143–150
Holbrook GL, Bachmann JAS, Schal C (2000) Effects of ovariectomy and mating on the activity of the corpora allata in adult female Blattella germanica (L.) (Dictyoptera: Blattellidae). Physiol Entomol 25:27–34
Hoover SER, Keeling CI, Winston ML, Slessor KN (2003) The effect of queen pheromones on worker honey bee ovary development. Naturwissenschaften 90:477–480
Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Ann Rev Entomol 50:371–393
Kambhampati S (1995) A phylogeny of cockroaches and related insects based on DNA sequence of mitochondrial ribosomal RNA genes. Proc Natl Acad Sci USA 92:2017–2020
Keller L, Nonacs P (1993) The role of queen pheromones in social insects: queen control or queen signal? Anim Behav 45:787–794
Korb J (2005) Regulation of sexual development in the basal termite Cryptotermes secundus: mutilation, pheromonal manipulation or honest signal? Naturwissenschaften 92:45–49
Lahav S, Soroker V, Hefetz A (1999) Direct behavioral evidence for hydrocarbons as ant recognition discriminators. Naturwissenschaften 86:246–249
Le Conte Y, Hefetz A (2008) Primer pheromones in social hymenoptera. Ann Rev Entomol 53:523–542
Lefeuve P, Bordereau C (1984) Soldier formation regulated by a primer pheromone from the soldier frontal gland in a higher termite, Nasutitermes lujae. Proc Natl Acad Sci USA 81:7665–7668
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
Light SF, Weesner FM (1951) Further studies in the production of supplementary reproductives in Zootermopsis (Isoptera). J Exp Zool 117:397–414
Lüscher M (1972) Environmental control of juvenile hormone (JH) secretion and caste differentiation in termites. Gen Comp Endo Supp 3:509–514
Martin SJ, Vitikainen E, Helanterä H, Drijfhout FP (2008) Chemical basis of nest-mate discrimination in the ant Formica exsecta. Proc Roy Soc Lond B 275:1271–1278
Monnin T (2006) Chemical recognition of reproductive status in social insects. Ann Zool Fennici 43:515–530
Monnin T, Peeters C (1997) Cannibalism of subordinates’ eggs in the monogynous queenless ant Dinoponera quadriceps. Naturwissenschaften 84:499–502
Monnin T, Malosse C, Peeters C (1998) Solid-phase microextraction and cuticular hydrocarbon differences related to reproductive activity in the queenless ant Dinoponera quadriceps. J Chem Ecol 24:473–490
Okot-Kotber BM, Prestwich GD (1991a) Identification of a juvenile hormone binding protein in the castes of the termite, Reticulitermes flavipes, by photoaffinity labeling. Ins Biochem 21:775–784
Okot-Kotber BM, Prestwich GD (1991b) Juvenile hormone binding proteins of termites detected by photoaffinity labeling: comparison of Zootermopsis nevadensis with two Rhinotermitids. Arch Ins Biochem Physiol 17:119–128
Ortius D, Heinze J (1999) Fertility signaling in queens of a North American ant. Behav Ecol Sociobiol 45:151–159
Pasteels JM (1972) Sex-specific pheromones in a termite. Experientia 28:105–106
Pasteels JM, Bordereau C (1998) Releaser pheromones in termites. In: Vander Meer RK, Breed MD, Winston ML, Espelie KE (eds) Pheromone communication in social insects. Westview, Boulder, pp 193–215
Peeters C, Liebig J (2009) Fertility signaling as a general mechanism of regulating reproductive division of labor in ants. In: Gadau J, Fewell J (eds) Organization of insect societies: from genome to socio-complexity. Harvard University Press, Cambridge, pp 220–242
Peeters C, Monnin T, Malosse C (1999) Cuticular hydrocarbons correlated with reproductive status in a queenless ant. Proc Roy Soc Lond B 266:1323–1327
Pickens AL (1932) Distribution and life histories of the species of Reticulitermes Holmgren in California; a study of the subterranean termites with reference to (l) zoogeography, and (2) life histories. Ph.D. Thesis. Univ. Calif
Prouvost O, Trabalon M, Papke M, Schulz S (1999) Contact sex signals on web and cuticle of Tegenaria atrica (Araneae, Agelenidae). Arch Ins Biochem Physiol 40:194–202
Roisin Y (1994) Intragroup conflicts and the evolution of sterile castes in termites. Am Nat 143:751–765
Rosengaus RB, Traniello JF (1993) Temporal polyethism in incipient colonies of the primitive termite Zootermopsis angusticollis: a single multistage caste. J Insect Behav 6:237–252
Schal C, Chiang A-S, Burns EL, Gadot M (1993) Role of the brain in juvenile hormone synthesis and oöcyte development: effects of dietary protein on the cockroach Blattella germanica. J Ins Physiol 39:303–313
Schal C, Gu X, Burns EL, Blomquist GJ (1994) Patterns of biosynthesis and accumulation of hydrocarbons and contact sex pheromone in the female German cockroach, Blattella germanica. Arch Ins Biochem Physiol 25:375–391
Schal C, Holbrook GL, Bachmann JAS, Veeresh LS (1997) Reproductive biology of the German cockroach, Blattella germanica: juvenile hormone as a pleiotropic master regulator. Arch Ins Biochem Physiol 35:405–426
Schal C, Sevala V, Cardé RT (1998) Novel and highly specific transport of a volatile sex pheromone by hemolymph lipophorin in moths. Naturwissenschaften 85:339–342
Sevala V, Shu SQ, Ramaswamy SB, Schal C (1999) Lipophorin of female Blattella germanica (L.): characterization and relation to hemolymph titers of juvenile hormone and hydrocarbons. J Ins Physiol 45:431–441
Sevala VL, Bagnères AG, Kuenzli M, Blomquist GJ, Schal C (2000) Cuticular hydrocarbons of the dampwood termite, Zootermopsis nevadensis: caste differences and role of lipophorin in transport of hydrocarbons and hydrocarbon metabolites. J Chem Ecol 26:765–789
Sherman PW, Lacey EA, Reeve HK, Keller L (1995) The eusociality continuum. Behav Ecol 6:102–108
Sledge MF, Boscaro F, Turillazzi S (2001) Cuticular hydrocarbons and reproductive status in the social wasp Polistes dominulus. Behav Ecol Sociobiol 49:401–409
Slessor KN, Kaminski LA, King GGS, Borden JH, Winston ML (1988) Semiochemical basis of the retinue response to queen honey bees. Nature 332:354–356
Smith A, Hölldobler B, Liebig J (2008) Hydrocarbon signals explain the pattern of worker and egg policing in the ant Aphaenogaster cockerelli. J Chem Ecol 34:1275–1282
Smith A, Hölldobler B, Liebig J (2009) Cuticular hydrocarbons reliably identify cheaters and allow enforcement of altruism in a social insect. Curr Biol 19:78–81
Steiger S, Peschke K, Francke W, Müller JK (2007) The smell of parents: breeding status influences cuticular hydrocarbon pattern in the burying beetle Nicrophorus vespilloides. Proc Roy Soc Lond B 274:2211–2220
Tentschert J, Bestmann HJ, Heinze J (2002) Cuticular compounds of workers and queens in two Leptothorax ant species—a comparison of results obtained by solvent extraction, solid sampling, and SPME. Chemoecology 12:15–21
Thomas ML, Parry LJ, Allan RA, Elgar MA (1999) Geographic affinity, cuticular hydrocarbons and colony recognition in the Australian meat ant Iridomyrmex purpureus. Naturwissenschaften 86:87–92
Trabalon M, Campan M, Hartmann N, Baehr P, Porcheron P, Clément JL (1994) Effects of allatectomy and ovariectomy on cuticular hydrocarbons in Calliphora vomitoria (Diptera). Arch Ins Biochem Physiol 25:363–373
Uva P, Clement J, Austin JW, Zaffagnini V, Quintana A, Bagnères AG (2004) Origin of a new Reticulitermes termite (Isoptera, Rhinotermitidae) inferred from mitochondrial DNA data. Mol Phylogen Evol 30:344–353
Vargo EL (1997) Poison gland of queen fire ants (Solenopsis invicta) is the source of a primer pheromone. Naturwissenschaften 84:507–510
Vieau F (1990) The male effect upon the female reproductive potency in the incipient laboratory colonies of Kalotermes flavicollis Fabr. Insect Soc 37:169–180
Wagner D, Tissot M, Cuevas W, Gordon DM (2000) Harvester ants utilize cuticular hydrocarbons in nestmate recognition. J Chem Ecol 26:2245–2257
Watson JAL, Abbey HM (1985) Development of neotenics in Mastotermes darwinensis Froggatt: an alternative strategy. In: Watson JAL, Okot-Kotber BM, Noirot CH (eds) Caste differentiation in social insects. Pergamon, New York, pp 107–124
Weil T, Hoffmann K, Kroiss J, Strohm E, Korb J (2009) Scent of a queen-cuticular hydrocarbons specific for female reproductives in lower termites. Naturwissenschaften 96:315–319
Wilson EO (1971) The insect societies. Harvard University Press, Cambridge
Zimmerman RB (1983) Sibling manipulation and indirect fitness in termites. Beh Ecol Sociobiol 12:143–145
Acknowledgements
We thank the administrators of the Pebble Beach Company for permission to collect termites. We would also like to thank Kevin Haight for assisting with colony collection and maintenance, Thomas Schmitt for supplying a sample of 6,9-nonacosadiene, and Steven Pratt, Thomas Schmitt, and two referees for helpful comments on the manuscript. All experiments were conducted in accordance with American statutes governing research. The project was supported by the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service, grant ARZR-2007-02202.
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Liebig, J., Eliyahu, D. & Brent, C.S. Cuticular hydrocarbon profiles indicate reproductive status in the termite Zootermopsis nevadensis . Behav Ecol Sociobiol 63, 1799–1807 (2009). https://doi.org/10.1007/s00265-009-0807-5
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DOI: https://doi.org/10.1007/s00265-009-0807-5