Advertisement

Journal of Chemical Ecology

, Volume 44, Issue 9, pp 818–826 | Cite as

Chemical Fertility Signaling in Termites: Idiosyncrasies and Commonalities in Comparison with Ants

  • Judith Korb
Review Article

Abstract

Termites evolved eusociality independently from social Hymenoptera. As a common trait, reproductive monopoly is maintained through chemical communication. The queen (and in termites also a king) prevents workers from reproduction by conveying their reproductive status. In termites all soldiers are sterile, but workers’ potential to reproduce differs between species. It ranges from totipotency in wood-dwelling lower termites where workers are a transient stage from which all other castes develop, to sterile workers in some higher termites. Intermediate are species in which workers can develop into replacement sexuals within the nest but not into winged sexuals. I summarize the patchy picture about fertility signaling that we currently have for termites, pointing also to potential conflicts over reproduction that differ from those in social Hymenoptera. Recent findings imply that, similar to many social Hymenoptera, wood-dwelling termites that live in confined nests use long-chain cuticular hydrocarbons (CHCs) as fertility signals. Yet other compounds are important as well, comprising proteinaceous secretions and especially volatiles. For a subterranean termite, two volatiles have been identified as primer pheromones that prevent reproductive differentiation of workers. It requires more data to test whether wood-dwelling termites use CHCs, while species with larger colonies and less confined nests use volatiles, or whether all species rely on multicomponent signals. Ultimately, we need more effort to model and test potential conflicts over reproduction between queens, kings and workers. Here results from social Hymenoptera cannot be transferred to termites as the latter are diploid and commonly inbred. This review illustrates promising future research avenues.

Keywords

CHC Chemical communication Conflict Fertility signaling Manipulation Termites 

Notes

Acknowledgements

I hope that this review will inspire young researchers to step into termite research. I thank Volker Nehring for comments on the manuscript and English editing, two anonymous reviewers for helpful comments, and Abraham Hefetz and Etya Amsalem for inviting me to contribute to this special issue and for their efforts in organizing it. This work was supported by a DFG grant (KO1895/23-1).

References

  1. Bagnères AG, Hanus R (2015) Communication and social regulation in termites. In: Aquiloni L, Tricarico E (eds) Social recognition in invertebrates. Springer International Publishing, Heidelberg, pp 193–248CrossRefGoogle Scholar
  2. Blomquist CJ, Bagnères AG (2010) Insect hydrocarbons. Biology, biochemistry, and chemical ecology. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  3. Blomquist CJ, Dwyer LA, Chu AJ, Ryan RO, Renobales MD (1982) Biosynthesis of linoleic acid in a termite, cockroach and cricket. Insect Biochem 12:349–353CrossRefGoogle Scholar
  4. Bourguignon T, Lo N, Cameron SL et al (2015) The evolutionary history of termites as inferred from 66 mitochondrial genomes. Mol Biol Evol 32:406–421CrossRefPubMedGoogle Scholar
  5. Brent CS, Schal C, Vargo EL (2005) Endocrine changes in maturing primary queens of Zootermopsis angusticollis. J Insect Physiol 51:1200–1209CrossRefPubMedGoogle Scholar
  6. Brent CS, Penick CA, Trobaugh B, Moore D, Liebig J (2016) Induction of a reproductive-specific cuticular hydrocarbon profile by a juvenile hormone analog in the termite Zootermopsis nevadensis. Chemoecology 26:195–203.  https://doi.org/10.1017/s00049-016-0219-8 CrossRefGoogle Scholar
  7. Brune A, Ohkuma M (2011) Role of the termite gut microbiota in symbiotic digestion. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, Heidelberg, London, New York, pp 439–476Google Scholar
  8. Cornette R, Farine JP, Abed-Viellard D, Quennedey B, Brossut R (2003) Molecular characterization of a male-specific glycosyl hydrolase, Lma-p72, secreted on to the abdominal surface of the Madeira cockroach Leucophaea maderae (Blaberidae, Oxyhaloinae). Biochem J 372:535–541CrossRefPubMedPubMedCentralGoogle Scholar
  9. Cuvillier-Hot V, Gadagkar R, Peeters C, Cobb M (2002) Regulation of reproduction in a queenless ant: aggression, pheromones and reduction in conflict. Proc R Soc B 269:1295–1300CrossRefPubMedGoogle Scholar
  10. 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
  11. Dillwith JW, Adams TS, Blomquist GJ (1983) Correlation of housefly sex pheromone production with ovarian development. J Insect Physiol 29:77–386CrossRefGoogle Scholar
  12. Engel MS, Grimaldi DA, Krishna K (2009) Termites (Isoptera): their phylogeny, classification, and rise to ecological dominance. Am Mus Novitates 3650:1–27CrossRefGoogle Scholar
  13. 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
  14. Fan Y, Schal C, Vargo EL, Bagnères AG (2004) Characterization of termite lipophorin and its involvement in hydrocarbon transport. J Insect Physiol 50:609–620CrossRefPubMedGoogle Scholar
  15. Feyereisen R (2005) Insect cytochrome P450. In: Gilbert LI, Iatrou K, Gill SS (eds) Comprehensive molecular insect science, vol 4. Elsevier, Oxford, pp 1–77Google Scholar
  16. Greenberg SLW, Stuart AM (1982) Precocious reproductive development (neoteny) by larvae of a primitive termite Zootermopsis angusticollis (Hagen). Insect Soc 29:535–547CrossRefGoogle Scholar
  17. Hanus R, Vrkoslav V, Hrdy I, Cvacka J, Sobotnik J (2010) Beyond cuticular hydrocarbons: evidence of proteinaceous secretion specific to termite kings and queens. Proc R Soc B 277:995–1002CrossRefPubMedGoogle Scholar
  18. Harrison MC, Jongepier E, Robertson HM, Arning N, Bitard-Feildel T, Chao H, Childers CP, Dinh H, Doddapaneni H, Dugan S, Gowin J, Greiner C, Han Y, Hu H, Hughes DST, Huylmans AK, Kemena C, Kremer LPM, Lee SL, Lopez-Ezquerra A, Mallet L, Monroy-Kuhn JM, Moser A, Murali SC, Muzny DM, Otani S, Piulachs MD, Poelchau M, Qu J, Schaub F, Wada-Katsumata A, Worley KC, Xie Q, Ylla G, Poulsen M, Gibbs RA, Schal C, Richards S, Belles X, Korb J, Bornberg-Bauer E (2018) Hemimetabolous genomes reveal molecular basis of termite eusociality. Nature Ecol Evol 2:557–566CrossRefGoogle Scholar
  19. Higashi M, Abe T, Burns TP (1992) Carbo-nitrogen balance and termite ecology. Proc R Soc B 249:303–308CrossRefGoogle Scholar
  20. Himuro C, Yokoi T, Matsuura K (2011) Queen-specific volatile in a higher termite Nasutitermes takasagoensis (Isoptera: Termitidae). J Isect Physiol 57:962–965CrossRefGoogle Scholar
  21. Hoffmann K, Korb J (2011) Is there conflict over direct reproduction in lower termite colonies? Anim Behav 81:265–274CrossRefGoogle Scholar
  22. Hoffmann K, Gowin J, Hartfelder K, Korb J (2014) The scent of royalty: a P450 gene signals reproductive status in a social insect. Mol Biol Evol 31:2689–2696CrossRefPubMedGoogle Scholar
  23. Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393CrossRefPubMedGoogle Scholar
  24. Howard KJ, Thorne BL (2011) Eusocial evolution in termites and hymenoptera. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, Heidelberg, London, New York, pp 97–132Google Scholar
  25. Howard RW, McDaniel CA, Blomquist GJ (1978) Cuticular hydrocarbons of eastern subterranean termite, Reticulitermes flavipes (Kollar) (Isoptera Rhinotermitidae). J Chem Ecol 4:233–245CrossRefGoogle Scholar
  26. Howard RW, McDaniel CA, Nelson DR, Blomquist CJ, Gelbaum LT, Zalkow LH (1982) Cuticular hydrocarbons of Reticulitermes virginicus (Banks) (Isoptera, Rhinotermitidae) and their role as potential species recognition and caste recognition cues. J Chem Ecol 8:1227–1239CrossRefPubMedGoogle Scholar
  27. Johns PM, Howard KJ, Breisch NL, Rivera A, Thorne BL (2009) Non-relatives inherit colony resources in a primitive termite. Proc Natl Acad Sci U S A 106:17452–17456CrossRefPubMedPubMedCentralGoogle Scholar
  28. Korb J (2015) Juvenile hormone, a central regulator of termite caste polyphenism. In: Zayed A, Kent CF (eds) Advances in insect physiology, vol 48. Academic Press, Oxford, pp 131–161Google Scholar
  29. Korb J, Hartfelder K (2008) Life history and development - a framework for understanding the ample developmental plasticity in lower termites. Biol Rev 83:295–313CrossRefPubMedGoogle Scholar
  30. Korb J, Roux EA (2012) Why join a neighbour: fitness consequences of colony fusions in termites. J Evol Biol 25:2161–2170CrossRefPubMedGoogle Scholar
  31. Korb J, Schmidinger S (2004) Help or disperse? Cooperation in termites influenced by food conditions. Behav Ecol Sociobiol 56:89–95CrossRefGoogle Scholar
  32. Korb J, Schneider K (2007) Does kin structure explain the occurrence of workers in a lower termite? Evol Ecol 21:817–828CrossRefGoogle Scholar
  33. Korb J, Thorne BL (2017) Sociality in termites. In: Rubenstein DR, Abbot P (eds) Comparative social evolution. Cambridge University Press, Cambridge, pp 124–153CrossRefGoogle Scholar
  34. Korb J, Hoffmann K, Hartfelder K (2009a) Endocrine signatures underlying plasticity in postembryonic development of a lower termite, Cryptotermes secundus (Kalotermitidae). Evol Dev 11:269–277CrossRefPubMedGoogle Scholar
  35. Korb J, Weil T, Hoffmann K, Foster KR, Rehli M (2009b) A gene necessary for reproductive suppression in termites. Science 324:758–758CrossRefPubMedGoogle Scholar
  36. Korb J, Poulsen M, Hu H, Li C, Boomsma JJ, Zhang G, Liebig J (2015) A genomic comparison of two termites with different social complexity. Front Genet 6:e9CrossRefGoogle Scholar
  37. Le Conte Y, Hefetz A (2008) Primer pheromones in social Hymenoptera. Annu Rev Entomol 53:1–20CrossRefGoogle Scholar
  38. Liebig J (2010) Hydrocarbon profiles indicate fertility and dominance status in ant, bee, and wasp colonies. In: Blomquist GJ, Bagnères AG (eds) Insect hydrocarbons. Biology, biochemistry, and chemical ecology. Cambridge University Press, Cambridge, pp 254–281CrossRefGoogle Scholar
  39. Liebig J, Eliyahu D, Brent CS (2009) Cuticular hydrocarbon profiles indicate reproductive status in the termite Zootermopsis nevadensis. Behav Ecol Sociobiol 63:1799–1807CrossRefGoogle Scholar
  40. Lu KH, Bradfield JY, Keeley LL (1999) Juvenile hormone inhibition of gene expression for cytochrome P4504C1 in adult females of the cockroach, Blaberus discoidalis. Insect Biochem Mol Biol 29:667–673CrossRefPubMedGoogle Scholar
  41. Luchetti A, Dedeine F, Velona A, Mantovani B (2013) Extreme genetic mixing within colonies of the wood-dwelling termite Kalotermes flavicollis (Isoptera, Kalotermitidae). Mol Ecol 22:3391–3402CrossRefPubMedGoogle Scholar
  42. Lüscher M (1955) Zur Frage der Übertragung sozialer Wirkstoffe bei Termiten. Naturwissenschaften 7:186–187CrossRefGoogle Scholar
  43. Lüscher M (1974) Kasten und Kastendifferenzierung bei niederen Termiten. In: Schmidt GH (ed) Sozialpolymorphismus bei Insekten. Wissenschaftliche Verlagsgesellschaft, Stuttgart, pp 694–739Google Scholar
  44. Maekawa K, Ishitani K, Gotoh H, Cornette R, Miura T (2010) Juvenile hormone titre and vitellogenin gene expression related to ovarian development in primary reproductives compared with nymphs and nymphoid reproductives of the termite Reticulitermes speratus. Physiol Entomol 35:52–58CrossRefGoogle Scholar
  45. Matsuura K (2011) Sexual and asexual reproduction in termites. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, Dordrecht, Heidelberg, London, New York, pp 255–278Google Scholar
  46. Matsuura K (2012) Multifunctional queen pheromone and maintenance of reproductive harmony in termite colonies. J Chem Ecol 38:746–754CrossRefPubMedGoogle Scholar
  47. Matsuura K, Himuro C, Yokoi T, Yamamoto Y, Vargo EL, Keller L (2010) Identification of a pheromone regulating caste differentiation in termites. Proc Natl Acad Sci U S A 107:12963–12968CrossRefPubMedPubMedCentralGoogle Scholar
  48. Maynard Smith J, Harper DGC (1995) Animal signals: models and terminology. J Theoret Biol 177:305–311CrossRefGoogle Scholar
  49. Mitaka Y, Kobayashi K, Mikheyev AS, Tin MMY, Watanabe Y, Matsuura K (2016) Caste-specific and sex-specific expression of chemoreceptor genes in a termite. PLoS One 11:e0146125CrossRefPubMedPubMedCentralGoogle Scholar
  50. Monnin T, Ratnieks FLW (2001) Policing in queenless ponerine ants. Behav Ecol Sociobiol 50:97–108CrossRefGoogle Scholar
  51. Myles TG (1999) Review of secondary reproduction in termites (Insecta: Isoptera) with comments on its role in termite ecology and social evolution. Sociobiology 33:1–91Google Scholar
  52. Noirot C (1990) Sexual castes and reproductive strategies in termites. In: Engels W (ed) An evolutionary approach to castes and reproduction. Springer, Berlin, pp 5–35Google Scholar
  53. Nunes TM, Turatti ICC, Lopez NP, Zucchi R (2009) Chemical signals in the stingless bee, Friseomelitta varia, indicate caste, gender, age, and reproductive status. J Chem Ecol 35:1172–1180CrossRefPubMedGoogle Scholar
  54. Okot-Kotber BM, Prestwich GD (1991a) Identification of a juvenile-hormone binding protein in the castes of the termite, Reticulitermes flavipes, by photoaffinity labeling. Insect Biochem 21:775–784CrossRefGoogle Scholar
  55. Okot-Kotber BM, Prestwich GD (1991b) Juvenile hormone binding proteins of termites detected by photoaffinity labeling: comparison of Zootermopsis nevadensis with two rhinotermitids Coptotermes formosanus and Reticulitermes flavipes. Arch Insect Biochem Physiol 17:119–128CrossRefGoogle Scholar
  56. Pask GM et al (2017) Specialized odorant receptors in social insects that detect cuticular hydrocarbon cues and candidate pheromones. Nature Comm 8:e297CrossRefGoogle Scholar
  57. Peeters C, Monnin T, Malosse C (1999) Cuticular hydrocarbons correlated with reproductive status in a queenless ant. Proc R Soc B 266:0782Google Scholar
  58. Penick CA, Trobaugh B, Brent CS, Liebig J (2013) Head-butting as ane early indicator of reproductive disinhibition in the termite Zootermopsis nevadensis. J Insect Behav 26:23–34CrossRefGoogle Scholar
  59. Prouvost O, Trabalon M, Papke M, Schulz S (1999) Contact sex signals on web and cuticle of Tegenaria atrica (Araneae, Agelenidae). Arch Insect Biochem Physiol 40:194–202CrossRefGoogle Scholar
  60. Ratnieks FLW (1988) Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am Nat 132:217–236CrossRefGoogle Scholar
  61. Ratnieks FLW, Foster KR, Wenseleers T (2006) Conflict resolution in insect societies. Annu Rev Entomol 51:581–608CrossRefPubMedGoogle Scholar
  62. Saiki R, Gotoh H, Toga K, Miura T, Maekawa K (2015) High juvenile hormone titre and abdominal activation of JH signalling may induce reproduction of termite neotenics. Insect Mol Biol 24:432–441CrossRefPubMedGoogle Scholar
  63. 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 Insect Biochem Physiol 25:375–391CrossRefPubMedGoogle Scholar
  64. Sevala VL, Bachmann JAS, Schal C (1997) Lipophorin: a hemolymph juvenile hormone binding protein in the German cockroach, Blattella germanica. Insect Biochem Mol Biol 27:663–670CrossRefGoogle Scholar
  65. Sevala VL, 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 Insect Physiol 45:431–441CrossRefPubMedGoogle Scholar
  66. Sevala VL, Bagnères AG, Kuenzli M, Blomquist GJ, Schal C (2000) Cuticular hydrocarbons of the dampwood termite, Zootermopsis nevadensis: caste differences and the role of lipophorin in transport of hydrocarbons and hydrocarbon metabolites. J Chem Ecol 26:765–789CrossRefGoogle Scholar
  67. Shimoji H, Oguchi K, Hayashi Y, Hojo MK, Miura T (2017) Regulation of neotenic differentaition through direct physical contact in the damp-wood termite Hodotermopsis sjostedti. Insect Soc 64:393–401CrossRefGoogle Scholar
  68. 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 R Soc B 274:2211–2220CrossRefPubMedGoogle Scholar
  69. Stuart AM (1979) The determination and regulation of the neotenic reproductive caste in the lower termites (Isoptera): with special reference to the genus Zootermopsis (Hagen). Sociobiology 4:223–237Google Scholar
  70. Suehiro W, Matsuura K (2015) Queen pheromone promotes production of salivary lysozyme by workers in a termite. Insect Soc 62:193–198CrossRefGoogle Scholar
  71. Sun Q, Haynes KF, Hampton JD, Zhou X (2017) Sex-specific inhibition and stimulation of worker-reproductive transition in a termite. Sci Nat 104:e79CrossRefGoogle Scholar
  72. Terrapon N et al (2014) Molecular traces of alternative social organization in a termite genome. Nature Comm 5:e3636CrossRefGoogle Scholar
  73. Trabalon M, Campan M, Hartmann N, Baehr P, Porcheron P, Clement JL (1994) Effects of allatectomy and ovariectomy on cuticular hydrocarbons in Calliphora vomitoria (Diptera). Arch Insect Biochem Physiol 25:363–373CrossRefGoogle Scholar
  74. Trible W, Olivos-Cisneros L, McKenzie SK, sragosti J, Chang N-C, Matthews BJ, Oxley PR, Kronauer D (2017) Orco mutagenesis causes loss of antennal lobe glomeruli and impaired social behavior in ants. Cell 170:727–735CrossRefPubMedGoogle Scholar
  75. Van Oystaeyen A et al (2014) Conserved class of queen pheromones stops social insect workers from reproducing. Science 343:287–290CrossRefPubMedGoogle Scholar
  76. Vargo EL, Laurel M (1994) Studies on the mode of action of a primer pheromone of the fire nat Solenopsis invicta. J Insect Physiol 40:601–610CrossRefGoogle Scholar
  77. Weil T, Rehli M, Korb J (2007) Molecular basis for the reproductive division of labour in a lower termite. BMC Genomics 8:198CrossRefPubMedPubMedCentralGoogle Scholar
  78. 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 96:315–319CrossRefPubMedGoogle Scholar
  79. Yan H, Opachaloemphan C, Mancini G, Yang H, Gallitto M, Mlejnek J et al (2017) An engineered orco mutation produces aberrant social behavior and defective neural development in ants. Cell 170:736–747CrossRefPubMedGoogle Scholar
  80. Zhou X, Rokas A, Berger SL, Liebig J, Ray A, Zwiebel LJ (2015) Chemoreceptor evolution in Hymenoptera and its implications for the evolution of eusociality. Genome Biol Evol 7:2407–24116CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Evolutionary Biology & EcologyUniversity of FreiburgFreiburgGermany

Personalised recommendations