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Evolutionary Ecology

, Volume 24, Issue 2, pp 317–332 | Cite as

An ant social parasite in-between two chemical disparate host species

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

Abstract

Host-parasite coevolution shapes the structure of communities and simultaneously the traits of the interacting species. Social parasites developed sophisticated chemical integration strategies to circumvent host defences. Here, we show that the two Leptothorax host species of the obligate social parasite Harpagoxenus sublaevis exhibit extremely divergent chemical profiles, making it nearly impossible for this parasite to closely adapt to both hosts at once. Our cuticular hydrocarbon analyses demonstrate that H. sublaevis acquires some host chemicals passively, but additionally, actively biosyntheses some host hydrocarbons. The parasite adjusts thereby more closely to its smaller host, L. muscorum, because it actively produces two of its cuticular substances and also more easily acquires the short-chained hydrocarbons of this host. Community composition analyses indicate that the social parasite overexploits this chemical closer host species and, albeit costly for the parasite, frequently enslaves workers of the second host concurrently.

Keywords

Coevolution Specialization Cuticular hydrocarbons Nestmate recognition Slavemaking ants 

Notes

Acknowledgments

We thank Alexandra Achenbach, Juliane Pätzold, Matthias Rohde and several students for helping in ant collecting and to the whole working group for helpful comments on this manuscript. This work was funded by the DFG (Fo 298/7).

References

  1. Akino T, Knapp JJ, Thomas JA, Elmes GW (1999) Chemical mimicry and host specificity in the butterfly Maculinea rebeli, a social parasite of Myrmica ant colonies. Proc R Soc Lond B Biol Sci 266:1419–1426. doi: 10.1098/rspb.1999.0796 CrossRefGoogle Scholar
  2. Alloway TM (1990) Slave-species ant colonies recognize slavemakers as enemies. Anim Behav 39:1218–1220. doi: 10.1016/S0003-3472(05)80797-3 CrossRefGoogle Scholar
  3. Beibl J, Stuart R, Heinze J, Foitzik S (2005) Six origins of slavery in formicoxenine ants. Insectes Soc 52:291–297. doi: 10.1007/s00040-005-0808-y CrossRefGoogle Scholar
  4. Beibl J, D’Ettorre P, Heinze J (2007) Cuticular profiles and mating preference in a slave-making ant. Insectes Soc 54:174–182. doi: 10.1007/s00040-007-0929-6 CrossRefGoogle Scholar
  5. Bonavita-Cougourdan A, Bagnères AG, Provost E, Dusticier G, Clément JL (1997) Plasticity of the cuticular hydrocarbon profile of the slave-making ant Polyergus rufescens depending on the social environment. Comp Biochem Physiol B Biochem Mol Biol 116:287–302. doi: 10.1016/S0305-0491(96)00250-7 CrossRefGoogle Scholar
  6. Bono J, Antolin M, Herbers J (2006) Parasite virulence and host resistance in a slave-making ant community. Evol Ecol Res 8:1117–1128Google Scholar
  7. Brandt M, Foitzik S (2004) Community context and specialization influence the coevolutionary interactions in a slavemaking ant. Ecology 85:2997–3009. doi: 10.1890/03-0778 CrossRefGoogle Scholar
  8. 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 Camb Philos Soc 80:251–267. doi: 10.1017/S1464793104006669 CrossRefPubMedGoogle Scholar
  9. 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 18:576–586. doi: 10.1111/j.1420-9101.2004.00867.x CrossRefPubMedGoogle Scholar
  10. Brandt M, Fischer-Blass B, Heinze J, Foitzik S (2007) Population structure and the co-evolution between social parasites and their hosts. Mol Ecol 16:2063–2078. doi: 10.1111/j.1365-294X.2007.03300.x CrossRefPubMedGoogle Scholar
  11. Brown MJF, Schmid-Hempel P (2003) The evolution of female multiple mating in social hymenoptera. Evol Int J Org Evol 57:2067–2081Google Scholar
  12. Buschinger A (1974) Experimente und Beobachtungen zur Gründung und Entwicklung neuer Sozietäten der sklavenhaltenden Ameise Harpagoxenus sublaevis (Nyl.). Insectes Soc 21:381–406. doi: 10.1007/BF02331567 CrossRefGoogle Scholar
  13. Buschinger A (1989) Evolution, speciation, and inbreeding in the parasitic ant genus Epimyrma (Hymenoptera, Formicidae). J Evol Biol 2:265–283. doi: 10.1046/j.1420-9101.1989.2040265.x CrossRefGoogle Scholar
  14. Buschinger A, Ehrhardt W, Fischer K, Ofer J (1988) The slave-making ant genus Chalepoxenus (Hymenoptera, Formicidae). I Review of literature, range, slave species. Zool Jahrb Abt Syst Okol Geogr Tiere 115:383–401Google Scholar
  15. Carlson DA, Bernier UR, Sutton BD (1998) Elution patterns from capillary GC for Methyl-branched alkanes. Chem Ecol 24:1845–1865. doi: 10.1023/A:1022311701355 CrossRefGoogle Scholar
  16. Collingwood CA (1971) A synopsis of the Formicidae of north Europe. Entomologist 104:150–176Google Scholar
  17. Couvillon MJ, Ratnieks FLW (2008) Odour transfer in stingless bee marmelada (Frieseomelitta varia) demonstrates that entrance guards use an “undesirable–absent” recognition system. Behav Ecol Sociobiol 62:1099–1105. doi: 10.1007/s00265-007-0537-5 CrossRefGoogle Scholar
  18. D’Ettorre P, Errard C (1998) Chemical disguise during colony founding in the dulotic ant Polyergus rufescens Latr. (Hymenoptera, Formicidae). Insect Soc Life 2:71–77Google Scholar
  19. 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 269:1911–1918. doi: 10.1098/rspb.2002.2110 CrossRefGoogle Scholar
  20. Dani FR, Jones GR, Corsi S et al (2005) Nestmate recognition cues in the honey bee: differential importance of cuticular alkanes and alkenes. Chem Senses 30:477–489. doi: 10.1093/chemse/bji040 CrossRefPubMedGoogle Scholar
  21. Davies NB (2000) Cuckoos, cowbirds and other cheats. T and AD Poyser, LondonGoogle Scholar
  22. Dettner K, Liepert C (1994) Chemical mimicry and camouflage. Annu Rev Entomol 39:129–154. doi: 10.1146/annurev.en.39.010194.001021 CrossRefGoogle Scholar
  23. Errard C, Ruano F, Richard F-J, Lenoir A, Tinaut A, Hefetz A (2006) Co-evolution-driven cuticular hydrocarbon variation between the slave-making ant Rossomyrmex minuchae and its host Proformica longiseta (Hymenoptera: Formicidae). Chemoecology 16:235–240. doi: 10.1007/s00049-006-0358-4 CrossRefGoogle Scholar
  24. Finzi B (1922) Note alla fauna mirmecologica della Venezia Giulia. Rend Unione Zool Ital 1921:29–32Google Scholar
  25. Fischer B, Foitzik S (2004) Local co-adaptation leading to a geographic mosaic of coevolution in a social parasite system. J Evol Biol 17:1026–1034. doi: 10.1111/j.1420-9101.2004.00749.x CrossRefPubMedGoogle Scholar
  26. Fischer-Blass B, Heinze J, Foitzik S (2006) Microsatellite analysis reveals strong, but differential impact of a social parasite on its two host species. Mol Ecol 15:863–872. doi: 10.1111/j.1365-294X.2005.02798.x CrossRefPubMedGoogle Scholar
  27. Foitzik S, Heinze J (1999) Non-random size differences between sympatric species of the ant genus Leptothorax (Hymenoptera: Formicidae). Entomol Gen 24:65–74Google Scholar
  28. 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 Biol Sci 268:1139–1146. doi: 10.1098/rspb.2001.1627 CrossRefGoogle Scholar
  29. Foitzik S, Fischer B, Heinze J (2003) Arms-races between social parasites and their hosts: geographic patterns of manipulation and resistance. Behav Ecol 14:80–88. doi: 10.1093/beheco/14.1.80 CrossRefGoogle Scholar
  30. Foitzik S, Sturm H, Pusch K, D’Ettorre P, Heinze J (2007) Variation in nestmate recognition abilities, chemical cues and genetic diversity in Temnothorax ants. Anim Behav 73:999–1007. doi: 10.1016/j.anbehav.2006.07.017 CrossRefGoogle Scholar
  31. Fournier D, Battaille G, Timmermans I, Aron S (2008) Genetic diversity, worker size polymorphism and division of labour in the polyandrous ant Cataglyphis cursor. Anim Behav 75:151–158. doi: 10.1016/j.anbehav.2007.04.023 CrossRefGoogle Scholar
  32. Franks N, Blum M, Smith RK, Allies AB (1990) Behavior and chemical disguise of cuckoo ant Leptothorax kutteri in relation to its host Leptothorax acervorum. J Chem Ecol 16:1431–1444CrossRefGoogle Scholar
  33. Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19:207–233. doi: 10.1146/annurev.es.19.110188.001231 CrossRefGoogle Scholar
  34. Heinze J, Ortius D, Kaib M, Hölldobler B (1994) Interspecific aggression in colonies of the slave-making ant Harpagoxenus sublaevis. Behav Ecol Sociobiol 35:75–83. doi: 10.1007/BF00171496 CrossRefGoogle Scholar
  35. Herbers JM, Foitzik S (2002) The ecology of slavemaking ants and their hosts in north temperate forests. Ecology 83:148–163CrossRefGoogle Scholar
  36. Hojo M, Wada-Katsumata A, Akino T, Yamaguchi S, Ozaki M, Yamaoka R (2009) Chemical disguise as particular caste of host ants in the ant inquiline parasite Niphanda fusca (Lepidoptera: Lycaenidae). Proc R Soc Lond B Biol Sci 276:551–558. doi: 10.1098/rspb.2008.1064 CrossRefGoogle Scholar
  37. Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393. doi: 10.1146/annurev.ento.50.071803.130359 CrossRefPubMedGoogle Scholar
  38. Howard RW, Akre RD, Garnett WB (1990a) Chemical mimicry in an obligate predator of carpenter ants (Hymenoptera: Formicidae). Ann Entomol Soc Am 83:607–616Google Scholar
  39. Howard RW, Stanley-Samuelson DW, Akre RD (1990b) Biosynthesis and chemical mimicry of cuticular hydrocarbons from the obligate predator, Microdon albicomatus Novak (Diptera: Syrphidae) and its ant prey, Myrmica incompleta Provancher (Hymenoptera: Formicidae). J Kans Entomol Soc 63:437–443Google Scholar
  40. 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 27:1787–1804. doi: 10.1023/A:1010456608626 CrossRefPubMedGoogle Scholar
  41. Kaib M (1993) Cuticular hydrocarbon profiles in the slave—making ant Harpagoxenus sublaevis and its hosts. Naturwissenschaften 80:281–285. doi: 10.1007/BF01135915 CrossRefGoogle Scholar
  42. Kaib M, Eisermann B, Schoeters E, Billen J, Franke S, Francke W (2000) Task-related variation of postpharyngeal and cuticular hydrocarhon compositions in the ant Myrmicaria eumenoides. J Comp Physiol [A] 186:939–948. doi: 10.1007/s003590000146 CrossRefGoogle Scholar
  43. Lahav S, Soroker V, Hefetz A, Vander Meer RK (1999) Direct behavioral evidence for hydrocarbons as ant recognition discriminators. Naturwissenschaften 86:246–249. doi: 10.1007/s001140050609 CrossRefGoogle Scholar
  44. Lambardi D, Dani F, Turillazzi S, Boomsma J (2007) Chemical mimicry in an incipient leaf-cutting ant social parasite. Behav Ecol Sociobiol 61:843–851. doi: 10.1007/s00265-006-0313-y CrossRefGoogle Scholar
  45. Lenoir A, Malosse C, Yamaoka R (1997) Chemical mimicry between parasitic ants of the genus Formicoxenus and their host Myrmica (Hymenoptera, Formicidae). Biochem Syst Ecol 25:379–389. doi: 10.1016/S0305-1978(97)00025-2 CrossRefGoogle Scholar
  46. Lenoir A, D’Ettorre P, Errard C, Hefetz A (2001) Chemical ecology and social parasitism in ants. Annu Rev Entomol 46:573–599. doi: 10.1146/annurev.ento.46.1.573 CrossRefPubMedGoogle Scholar
  47. Mac Arthur RH, Pianka ER (1966) Optimal use of a patchy environment. Am Nat 100:603–609. doi: 10.1086/282454 CrossRefGoogle Scholar
  48. Martin SJ, Vitikainen E, Helantera H, Drijfhout FP (2008) Chemical basis of nest-mate discrimination in the ant Formica exsecta. Proc R Soc Lond B Biol Sci 275:1271–1278. doi: 10.1098/rspb.2007.1708 CrossRefGoogle Scholar
  49. Mattila HR, Seeley TD (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317:362–364. doi: 10.1126/science.1143046 CrossRefPubMedGoogle Scholar
  50. Monnin T (2006) Chemical recognition of reproductive status in social insects. Ann Zool Fenn 43:515–530Google Scholar
  51. Nash DR, Als TD, Maile R, Jones GR, Boomsma JJ (2008) A mosaic of chemical coevolution in a large blue butterfly. Science 319:88–90. doi: 10.1126/science.1149180 CrossRefPubMedGoogle Scholar
  52. 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
  53. Ratschenko AG, Czechowski W, Czechowska W (1999) The tribe Formicoxenini (Hymenoptera, Formicidae) in Poland—a taxonomic review and keys for identification. Ann Zool 49:129–150Google Scholar
  54. Vander Meer RK, Morel L (1998) Nestmate recognition in ants. In: Vander Meer RK, Breed M, Winston M, Espelie KE (eds) Pheromone communication in social insects. Westview Press, Boulder, pp 79–103Google Scholar
  55. Ward SA (1992) Assessing functional explanations of host specificity. Am Nat 139:883–891. doi: 10.1086/285363 CrossRefGoogle Scholar
  56. Wilson EO (1971) The insect societies. Harvard University Press, Cambridge, MassGoogle Scholar
  57. Yamaoka R (1990) Chemical approach to understanding interactions among organisms. Physiol Ecol Jpn 27:31–52Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

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

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