Behavioral Ecology and Sociobiology

, Volume 64, Issue 1, pp 45–56 | Cite as

Fight or flight? A geographic mosaic in host reaction and potency of a chemical weapon in the social parasite Harpagoxenus sublaevis

  • Sabine Bauer
  • Volker Witte
  • Melanie Böhm
  • Susanne Foitzik
Original Paper


Ant social parasites use chemical warfare to facilitate host colony takeover, which is a critical but recurring step in their life cycle. Many slave-making ants use the secretion of the Dufour gland to manipulate host behaviour during parasitic nest foundation and slave raids. Harpagoxenus sublaevis applies this chemical weapon onto defending Leptothorax host workers, which elicits deadly fights amongst them. Host species are expected to evolve counter-adaptations against this behavioural manipulation and in this study we investigated the geographic structure of this co-evolving trait. We compared the effectiveness of the parasitic gland secretion from different H. sublaevis populations in host colonies from various sites and analysed the occurrence of local adaptation. The two host species L. muscorum and L. acervorum generally showed different responses to the parasites’ chemical weapon: L. acervorum attacked nestmates treated with Dufour gland secretion, while L. muscorum workers fled. Flight, instead of intraspecific fights, is an adaptive host reaction as it results in fewer host fatalities during raids. Beside interspecific host differences, we found a geographic mosaic of host resistance: parasites from a German population strongly manipulated the behaviour of both sympatric Leptothorax populations. Russian or Italian hosts instead did not react with intracolonial aggression, but fled when confronted with the gland secretion of their sympatric parasite. Not only variation in host resistance explains differences in the effectiveness of the parasitic gland secretion but also interpopulational differences in its chemical composition, which were revealed by gas chromatography and mass spectrometry.


Local adaptation Co-evolution Arms race Dufour gland Slave-making ants 


  1. Ali MF, Morgan ED, Attygalle AB, Billen JPJ (1987) Comparison of Dufour gland secretions of two species of Lepthothorax ants (Hymenoptera: Formicidae). Z Naturforsch C J Biosci 42:955–960Google Scholar
  2. Ali MF, Billen JPJ, Jackson BD, Morgan ED (1989) The Dufour gland contents of three species of Euro-African Messor ants and a comparison with those of North American Pogonomyrmex (Hymenoptera: Formicidae). Biochem Syst Ecol 17:469–477CrossRefGoogle Scholar
  3. Allies AB, Bourke AFG, Franks NR (1986) Propaganda substances in the cuckoo ant Leptothorax kutteri and the slave-maker Harpagoxenus sublaevis. J Chem Ecol 12:1285–1293CrossRefGoogle Scholar
  4. Bagnères A-G, Morgan ED, Clement JL (1991) Species-specific secretions of the Dufour glands of three species of formicine ants (Hymenoptera, Formicidae). Biochem Syst Ecol 19:25–33CrossRefGoogle Scholar
  5. Beibl J, Stuart R, Heinze J, Foitzik S (2005) Six origins of slavery in formicoxenine ants. Insect Soc 52:291–297CrossRefGoogle Scholar
  6. Bestmann HJ, Janssen E, Kern F, Liepold B (1995) All-trans geranylgeranyl acetate and geranylgeraniol, recruitment pheromone components in the dufour gland of the ponerine ant Ectatomma ruidum. Naturwissenschaften 82:334–336Google Scholar
  7. Billen J, Morgan ED (1998) Pheromone communication in social insects—sources and secretions. In: Vander Meer RK, Breed MD, Winston ML, Espelie KE (eds) Pheromone communication in social insects: ants, wasps, bees, and termites. Westview Press, Boulder, pp 3–33Google Scholar
  8. Blatrix R, Schulz C, Jaisson P, Francke W, Hefetz A (2002) Trail pheromone of ponerine ant Gnamptogenys striatula: 4-methylgeranyl esters from Dufour’s gland. J Chem Ecol 28:2557–2567CrossRefPubMedGoogle Scholar
  9. Brandt M, Foitzik S, Fischer-Blass B, Heinze J (2005a) The coevolutionary dynamics of obligate ant social parasite systems—between prudence and antagonism. Biol Rev Cam Phil Soc 80:251–267CrossRefGoogle Scholar
  10. Brandt M, Heinze J, Schmitt T, Foitzik S (2005b) A chemical level in the coevolutionary arms race between an ant social parasite and its hosts. J Evol Biol 18:576–586CrossRefPubMedGoogle Scholar
  11. Brandt M, Heinze J, Schmitt T, Foitzik S (2006) Convergent evolution of the Dufour's gland secretion as a propaganda substance in the slave-making ant genera Protomognathus and Harpagoxenus. Insectes Soc 53:291–299CrossRefGoogle Scholar
  12. Brandt M, Fischer-Blass B, Heinze J, Foitzik S (2007) Population structure and the co-evolution between social parasites and their hosts. Mol Ecol 16:2063–2078CrossRefPubMedGoogle Scholar
  13. Buschinger A (1974) Experimente und Beobachtungen zur Grundung und Entwicklung neuer Sozietaten der sklavenhaltenden Ameise Harpagoxenus sublaevis (Nyl.). Insectes Soc 21:381–406CrossRefGoogle Scholar
  14. Clarke KR (1999) Nonmetric multivariate analysis in community level ecotoxicology. Environ Toxicol Chem 18:118–127CrossRefGoogle Scholar
  15. Coll M, Hefetz A, Lloyd HA (1987) Adnexal glands chemistry of Messor ebenius Forel (Formicidae, Myrmicinae). Z Naturforsch 42C:1027–1029Google Scholar
  16. D'Ettorre P, Errard C, Ibarra F, Francke W, Hefetz A (2000) Sneak in or repel your enemy: Dufour's gland repellent as a strategy for successful usurpation in the slave-maker Polyergus rufescens. Chemoecology 10:135–142CrossRefGoogle Scholar
  17. 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 Biol Sci 269:1911–1918CrossRefGoogle Scholar
  18. Fischer B, Foitzik S (2004) Local co-adaptation leading to a geographical mosaic of coevolution in a social parasite system. J Evol Biol 17(5):1026–1034CrossRefPubMedGoogle Scholar
  19. Fischer-Blass B, Heinze J, Foitzik S (2006) Microsatellite analysis revealed strong, but differential impact of a social parasite on its two host species. Mol Ecol 15:863–872CrossRefPubMedGoogle Scholar
  20. Foitzik S, Herbers JM (2001) Colony structure of a slavemaking ant: II. Frequency of slave raids and impact on host population. Evolution 55:316–323PubMedGoogle Scholar
  21. Foitzik S, Fischer B, Heinze J (2003) Arms-races between social parasites and their hosts: geographic patterns of manipulation and resistance. Behav Ecol 14:80–88CrossRefGoogle Scholar
  22. Heinze J, Ortius D (1991) Social organization of Leptothorax acervorum from Alaska (Hymenoptera: Formicidae). Psyche 98:227–240CrossRefGoogle Scholar
  23. Heinze J, Oberstadt B, Tentschert J, Hölldobler B, Bestmann HJ (1998) Colony specificity of Dufour gland secretions in a functionally monogynous ant. Chemoecology 8:169–174CrossRefGoogle Scholar
  24. Hölldobler B, Carlin NF (1987) Anonymity and specificity in the chemical communication signals of social insects. J Comp Physiol A Sens Neural Behav Physiol 161:567–581CrossRefGoogle Scholar
  25. Johansson BG, Jones TM (2007) The role of chemical communication in mate choice. Biological Reviews 82:265–289CrossRefPubMedGoogle Scholar
  26. 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 27:1787–1804CrossRefPubMedGoogle Scholar
  27. Kaltz O, Shykoff J (1998) Local adaptation in host–parasite systems. Heredity 81:361–370CrossRefGoogle Scholar
  28. Martin SJ (2001) The role of Varroa and viral pathogens in the collapse of honeybee colonies: a modelling approach. J Appl Ecol 38:1082–1093CrossRefGoogle Scholar
  29. Martin SJ, Jenner EA, Drijfhout FP (2007) Chemical deterrent enables a socially parasitic ant to invade multiple hosts. Proc Roy Soc B 274:2717–2722CrossRefGoogle Scholar
  30. Morgan ED, Jungnickel H, Keegans SJ, Do Nascimento RR, Billen J, Gobin B, Ito F (2003) Comparative survey of abdominal gland secretions of the ant subfamily Ponerinae. J Chem Ecol 29:95–114CrossRefPubMedGoogle Scholar
  31. Mori A, Grasso DA, Visicchio R, Le Moli F (2000a) Colony founding in Polyergus rufescens: the role of the Dufour's gland. Insectes Soc 47:7–10CrossRefGoogle Scholar
  32. Mori A, Visicchio R, Sledge MF, Grasso DA, Le Moli F, Turillazzi S, Spencer S, Jones GR (2000b) Behavioural assays testing the appeasement allomone of Polyergus rufescens queens during host-colony usurpation. Ethol Ecol & Evol 12:315–322Google Scholar
  33. Oldham NJ, Boland W (1996) Chemical ecology: multifunctional compounds and multitrophic interactions. Naturwissenschaften 83:248–254CrossRefGoogle Scholar
  34. Ollett DG, Morgan ED, Attygalle AB, Billen JPJ (1987) The contents of the Dufour gland of the ant Harpaxogenus sublaevis Nyl. (Hymenoptera: Formicidae). Z Naturforsch 42:141–146Google Scholar
  35. Radchenko AG, Czechowski W, Czechowska W (1999) The tribe Formicoxenini (Hymenoptera, Formicidae) in Poland—a taxonomic review and keys for identification. Ann Zool Warszawa 49:129–150Google Scholar
  36. Regnier FE, Wilson EO (1971) Chemical communication and “propaganda” in slave-maker ants. Science (Wash D C) 172:267–269CrossRefGoogle Scholar
  37. Rieder JP, Newbold TAS, Sato S, Yasuda H, Evans EW (2008) Intra-gild predation and variation in egg defence between sympatric and allopatric populations of two species of ladybird beetles. Ecological Entomology 33:53–58Google Scholar
  38. Springer YP (2007) Clinal resistance structure and pathogen local adaptation in a serpentine flax–flax rust interaction. Evolution 61:1812–1822CrossRefPubMedGoogle Scholar
  39. Thompson JN (1999) Specific hypotheses on the geographic mosaic of coevolution. Am Nat 153:1–14CrossRefGoogle Scholar
  40. Topoff H, Zimmerli E (1993) Colony takeover by a socially parasitic ant, Polyergus breviceps: the role of chemicals obtained during host-queen killing. Anim Behav 46:479–486CrossRefGoogle Scholar
  41. Topoff H, Cover S, Greenberg L, Goodloe L, Sherman P (1988) Colony founding by queens of the obligatory slave-making ant, Polyergus breviceps: the role of the Dufour'sgland. Ethology 78:209–218CrossRefGoogle Scholar
  42. Visicchio R, Sledge MF, Mori A, Grasso DA, Le Moli F, Turillazzi S, Moneti G, Spencer S, Jones GR (2000) Dufour's gland contents of queens of the slave-making ant Polyergus rufescens and its host species Formica cunicularia. Ethol Ecol & Evol 12:67–73Google Scholar
  43. Witte V, Abrell L, Attygalle AB, Wu X, Meinwald J (2007) Structure and function of Dufour gland pheromones from the crazy ant Paratrechina longicornis. Chemoecology 17:63–69CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Sabine Bauer
    • 1
  • Volker Witte
    • 1
  • Melanie Böhm
    • 1
  • Susanne Foitzik
    • 1
  1. 1.Department Biologie IILudwig Maximilians Universität MünchenPlanegg-MartinsriedGermany

Personalised recommendations