Behavioral Ecology and Sociobiology

, Volume 63, Issue 12, pp 1799–1807 | Cite as

Cuticular hydrocarbon profiles indicate reproductive status in the termite Zootermopsis nevadensis

Original Paper

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.

Keywords

Fertility signal Queen pheromone Reproductive inhibition Social insects Isoptera Dampwood termite 

Notes

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.

References

  1. 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 39:381–387CrossRefGoogle Scholar
  2. 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 26:163–180CrossRefGoogle Scholar
  3. 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 100:667–680CrossRefGoogle Scholar
  4. Brent CS, Traniello JFA (2001a) Social regulation of testicular development in primary and secondary males of the dampwood termite Zootermopsis angusticollis Hagen. Insect Soc 48:384–391Google Scholar
  5. 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 26:239–247CrossRefGoogle Scholar
  6. Brent CS, Schal C, Vargo EL (2005) Endocrine changes in maturing primary queens of Zootermopsis angusticollis. J Ins Physiol 51:1200–1209CrossRefGoogle Scholar
  7. 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 192:315–320CrossRefGoogle Scholar
  8. 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 273–310Google Scholar
  9. Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E, PlymouthGoogle Scholar
  10. 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 126–155Google Scholar
  11. 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 47:485–493CrossRefGoogle Scholar
  12. Cuvillier-Hot V, Lenoir A, Crewe R, Malosse C, Peeters C (2004) Fertility signalling and reproductive skew in queenless ants. Anim Behav 68:1209–1219CrossRefGoogle Scholar
  13. Danforth BN (2002) Evolution of sociality in a primitively eusocial lineage of bees. Proc Natl Acad Sci USA 99:286–290PubMedCrossRefGoogle Scholar
  14. Dani FR (2006) Cuticular lipids as semiochemicals in paper wasps and other social insects. Ann Zool Fennici 43:500–514Google Scholar
  15. 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 50:585–593CrossRefGoogle Scholar
  16. 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 32:1647–1661PubMedCrossRefGoogle Scholar
  17. 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 100:10341–10346PubMedCrossRefGoogle Scholar
  18. 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 58:486–496CrossRefGoogle Scholar
  19. Dillwith JW, Adams TS, Blomquist GJ (1983) Correlation of housefly sex pheromone production with ovarian development. J Insect Physiol 29:377–386CrossRefGoogle Scholar
  20. 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 271:1427–1434CrossRefGoogle Scholar
  21. 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 101:2945–2950PubMedCrossRefGoogle Scholar
  22. Endler A, Liebig J, Hölldobler B (2006) Queen fertility, egg marking and colony size in the ant Camponotus floridanus. Behav Ecol Sociobiol 59:490–499CrossRefGoogle Scholar
  23. 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 205:781–790PubMedGoogle Scholar
  24. Gadagkar R (1994) Why the definition of eusociality is not helpful to understand its evolution and what should we do about it. Oikos 70:485–488CrossRefGoogle Scholar
  25. Gibbs AG (1998) Water-proofing properties of cuticular lipids. Am Zool 38:471–482Google Scholar
  26. 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 1:99–108Google Scholar
  27. 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 31:347–352CrossRefGoogle Scholar
  28. Grozinger CM, Robinson GE (2007) Endocrine modulation of a pheromone-responsive gene in the honey bee brain. J Comp Physiol A 193:461–470CrossRefGoogle Scholar
  29. 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 64:477–485CrossRefGoogle Scholar
  30. 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 651–703CrossRefGoogle Scholar
  31. Haverty MI, Thorne BL (1989) Agonistic behavior correlated with hydrocarbon phenotypes in dampwood termites, Zootermopsis (Isoptera, Termopsidae). J Ins Behav 2:523–543CrossRefGoogle Scholar
  32. 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 14:1035–1058CrossRefGoogle Scholar
  33. Heath H (1903) The habits of California termites. Biol Bull 4:7–63CrossRefGoogle Scholar
  34. Heinze J (2004) Reproductive conflict in insect societies. Adv Stud Behav 34:1–57CrossRefGoogle Scholar
  35. Heinze J, Stengl B, Sledge MF (2002) Worker rank, reproductive status and cuticular hydrocarbon signature in the ant. Pachycondyla cf. inversa. Behav Ecol Sociobiol 52:59–65CrossRefGoogle Scholar
  36. 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 18:143–150CrossRefGoogle Scholar
  37. 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 25:27–34CrossRefGoogle Scholar
  38. Hoover SER, Keeling CI, Winston ML, Slessor KN (2003) The effect of queen pheromones on worker honey bee ovary development. Naturwissenschaften 90:477–480PubMedCrossRefGoogle Scholar
  39. Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Ann Rev Entomol 50:371–393CrossRefGoogle Scholar
  40. Kambhampati S (1995) A phylogeny of cockroaches and related insects based on DNA sequence of mitochondrial ribosomal RNA genes. Proc Natl Acad Sci USA 92:2017–2020PubMedCrossRefGoogle Scholar
  41. Keller L, Nonacs P (1993) The role of queen pheromones in social insects: queen control or queen signal? Anim Behav 45:787–794CrossRefGoogle Scholar
  42. Korb J (2005) Regulation of sexual development in the basal termite Cryptotermes secundus: mutilation, pheromonal manipulation or honest signal? Naturwissenschaften 92:45–49PubMedCrossRefGoogle Scholar
  43. Lahav S, Soroker V, Hefetz A (1999) Direct behavioral evidence for hydrocarbons as ant recognition discriminators. Naturwissenschaften 86:246–249CrossRefGoogle Scholar
  44. Le Conte Y, Hefetz A (2008) Primer pheromones in social hymenoptera. Ann Rev Entomol 53:523–542CrossRefGoogle Scholar
  45. 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 81:7665–7668PubMedCrossRefGoogle Scholar
  46. 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 97:4124–4131PubMedCrossRefGoogle Scholar
  47. Light SF, Weesner FM (1951) Further studies in the production of supplementary reproductives in Zootermopsis (Isoptera). J Exp Zool 117:397–414CrossRefGoogle Scholar
  48. Lüscher M (1972) Environmental control of juvenile hormone (JH) secretion and caste differentiation in termites. Gen Comp Endo Supp 3:509–514CrossRefGoogle Scholar
  49. 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 275:1271–1278CrossRefGoogle Scholar
  50. Monnin T (2006) Chemical recognition of reproductive status in social insects. Ann Zool Fennici 43:515–530Google Scholar
  51. Monnin T, Peeters C (1997) Cannibalism of subordinates’ eggs in the monogynous queenless ant Dinoponera quadriceps. Naturwissenschaften 84:499–502CrossRefGoogle Scholar
  52. 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 24:473–490CrossRefGoogle Scholar
  53. 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 21:775–784CrossRefGoogle Scholar
  54. 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 17:119–128CrossRefGoogle Scholar
  55. Ortius D, Heinze J (1999) Fertility signaling in queens of a North American ant. Behav Ecol Sociobiol 45:151–159CrossRefGoogle Scholar
  56. Pasteels JM (1972) Sex-specific pheromones in a termite. Experientia 28:105–106CrossRefGoogle Scholar
  57. 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 193–215Google Scholar
  58. 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 220–242Google Scholar
  59. Peeters C, Monnin T, Malosse C (1999) Cuticular hydrocarbons correlated with reproductive status in a queenless ant. Proc Roy Soc Lond B 266:1323–1327CrossRefGoogle Scholar
  60. 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. CalifGoogle Scholar
  61. 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 40:194–202CrossRefGoogle Scholar
  62. Roisin Y (1994) Intragroup conflicts and the evolution of sterile castes in termites. Am Nat 143:751–765CrossRefGoogle Scholar
  63. Rosengaus RB, Traniello JF (1993) Temporal polyethism in incipient colonies of the primitive termite Zootermopsis angusticollis: a single multistage caste. J Insect Behav 6:237–252CrossRefGoogle Scholar
  64. 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 39:303–313CrossRefGoogle Scholar
  65. 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 25:375–391CrossRefGoogle Scholar
  66. 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 35:405–426CrossRefGoogle Scholar
  67. Schal C, Sevala V, Cardé RT (1998) Novel and highly specific transport of a volatile sex pheromone by hemolymph lipophorin in moths. Naturwissenschaften 85:339–342CrossRefGoogle Scholar
  68. 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 45:431–441CrossRefGoogle Scholar
  69. 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 26:765–789CrossRefGoogle Scholar
  70. Sherman PW, Lacey EA, Reeve HK, Keller L (1995) The eusociality continuum. Behav Ecol 6:102–108CrossRefGoogle Scholar
  71. Sledge MF, Boscaro F, Turillazzi S (2001) Cuticular hydrocarbons and reproductive status in the social wasp Polistes dominulus. Behav Ecol Sociobiol 49:401–409CrossRefGoogle Scholar
  72. Slessor KN, Kaminski LA, King GGS, Borden JH, Winston ML (1988) Semiochemical basis of the retinue response to queen honey bees. Nature 332:354–356CrossRefGoogle Scholar
  73. 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 34:1275–1282PubMedCrossRefGoogle Scholar
  74. Smith A, Hölldobler B, Liebig J (2009) Cuticular hydrocarbons reliably identify cheaters and allow enforcement of altruism in a social insect. Curr Biol 19:78–81PubMedCrossRefGoogle Scholar
  75. 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 274:2211–2220CrossRefGoogle Scholar
  76. 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 12:15–21CrossRefGoogle Scholar
  77. Thomas ML, Parry LJ, Allan RA, Elgar MA (1999) Geographic affinity, cuticular hydrocarbons and colony recognition in the Australian meat ant Iridomyrmex purpureus. Naturwissenschaften 86:87–92CrossRefGoogle Scholar
  78. 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 25:363–373CrossRefGoogle Scholar
  79. 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 30:344–353CrossRefGoogle Scholar
  80. Vargo EL (1997) Poison gland of queen fire ants (Solenopsis invicta) is the source of a primer pheromone. Naturwissenschaften 84:507–510CrossRefGoogle Scholar
  81. Vieau F (1990) The male effect upon the female reproductive potency in the incipient laboratory colonies of Kalotermes flavicollis Fabr. Insect Soc 37:169–180CrossRefGoogle Scholar
  82. Wagner D, Tissot M, Cuevas W, Gordon DM (2000) Harvester ants utilize cuticular hydrocarbons in nestmate recognition. J Chem Ecol 26:2245–2257CrossRefGoogle Scholar
  83. 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 107–124Google Scholar
  84. 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 96:315–319PubMedCrossRefGoogle Scholar
  85. Wilson EO (1971) The insect societies. Harvard University Press, CambridgeGoogle Scholar
  86. Zimmerman RB (1983) Sibling manipulation and indirect fitness in termites. Beh Ecol Sociobiol 12:143–145CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Jürgen Liebig
    • 1
    • 3
  • Dorit Eliyahu
    • 1
  • Colin S. Brent
    • 1
    • 2
  1. 1.School of Life SciencesArizona State UniversityTempeUSA
  2. 2.US Arid-Land Agricultural Research CenterMaricopaUSA
  3. 3.Center for Social Dynamics and ComplexityArizona State UniversityTempeUSA

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