Chemical mimicry or crypsis—the evolutionary game played by parasitic ants invading other colonies

Abstract

Some ant species are specialised parasites that invade the nests of other ants and steal their food, larvae, and eggs. To be successful, they must evade detection by patrolling hosts who attack invaders. Ants distinguish invaders from individuals of their own nest through the cuticular hydrocarbon profile, as their nestmates have a similar mixture of coating chemicals. To circumvent this, some parasites adopt mimicry, using a mixture of chemicals that has a similar composition to that of their hosts, whilst others adopt crypsis, with a reduced amount of chemicals. Here, we develop a mathematical model to describe the conditions under which each of these strategies evolves, assuming that the parasites and hosts are ants with their own colonies. Host ants distinguish their nestmates from parasites through differences in their chemical traits, which are represented in multi-dimensional space. Parasitic ants engage in competition with other conspecific colonies, which is more intense between colonies with similar chemical traits, jeopardising the advantage of cryptic parasites. We then define parasites’ fitness with respect to chemical profiles and discuss the evolution of their chemical strategies. Cryptic parasites evolve when competition among colonies is weak, when many types of host colonies exist, and when host recognition accuracy is high. Mimetic parasites evolve under the opposite conditions.

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References

  1. Akino T (2008) Chemical strategies to deal with ants: a review of mimicry, camouflage, propaganda, and phytomimesis by ants (Hymenoptera: Formicidae) and other arthropods. Myrmecological News 11:173–181

    Google Scholar 

  2. Akino T, Terayama M, Wakamura S, Yamaoka R (2002) Intraspecific variation of cuticular hydrocarbon composition in Formica japonica Motschoulsky (Hymenoptera: Formicidae). Zool Sci 19(10):1155–1165

    CAS  Article  Google Scholar 

  3. 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(3):381–387

    CAS  Article  Google Scholar 

  4. Bowers MD, Larin Z (1989) Acquired chemical defense in the lycaenid butterfly, Eumaeus atala. J Chem Ecol 15(4):1133–1146

    CAS  Article  Google Scholar 

  5. Brandt M, Heinze J, Schmitt T, Foitzik S (2005) A chemical level in the coevolutionary arms race between an ant social parasite and its hosts. J Evol Biol 18(3):576–586. https://doi.org/10.1111/j.1420-9101.2004.00867.x

    CAS  Article  PubMed  Google Scholar 

  6. Breed MD, Cook C, Krasnec MO (2012) Cleptobiosis in social insects. Psyche, 488765. https://doi.org/10.1155/2012/484765

    Article  Google Scholar 

  7. Cappa F, Bruschini C, Cipollini M, Pieraccini G, Cervo R (2014) Sensing the intruder: a quantitative threshold for recognition cues perception in honeybees. Naturwissenschaften 101(2):149–152. https://doi.org/10.1007/s00114-013-1135-1

    CAS  Article  PubMed  Google Scholar 

  8. Cronin AL, Fédérici P, Doums C, Monnin T (2012) The influence of intraspecific competition on resource allocation during dependent colony foundation in a social insect. Oecologia 168(2):361–369

    Article  Google Scholar 

  9. Cheney KL (2012) Cleaner wrasse mimics inflict higher costs on their models when they are more aggressive towards signal receivers. Biol Lett 8(1):10–12

    Article  Google Scholar 

  10. Cini A, Gioli L, Cervo R (2009) A quantitative threshold for nest-mate recognition in a paper social wasp. Biol Lett 5(4):459–461

    Article  Google Scholar 

  11. Dettner K, Liepert C (1994) Chemical mimicry and camouflage. Annu Rev Entomol 39:129–154

    CAS  Article  Google Scholar 

  12. Elgar MA, Allan RA (2004) Predatory spider mimics acquire colony-specific cuticular hydrocarbons from their ant model prey. Naturwissenschaften 91(3):143–147

    CAS  Article  Google Scholar 

  13. Ettershank G, Ettershank J (1982) Ritualised fighting in the meat ant Iridomyrmex purpureus (Smith)(Hymenoptera: Formicidae). Aust J Entomol 21(2):97–102

    Article  Google Scholar 

  14. Fielde AM (1905) The progressive odor of ants. Biol Bull 10(1):1–16

    Article  Google Scholar 

  15. Fürst MA, Durey M, Nash DR (2012) Testing the adjustable threshold model for intruder recognition on Myrmica ants in the context of a social parasite. Proc Biol Sci 279(1728):516–522

    Article  Google Scholar 

  16. Gavrilets S (1997) Coevolutionary chase in exploiter–victim systems with polygenic characters. J Theor Biol 186(4):527–534

    CAS  Article  Google Scholar 

  17. Gordon DM (1991) Behavioral flexibility and the foraging ecology of seed-eating ants. Am Nat 138:379–411

    Article  Google Scholar 

  18. Hölldobler B (1976) Recruitment behavior, home range orientation and territoriality in harvester ants, Pogonomyrmex. Behav Ecol Sociobiol 1(1):3–44

    Article  Google Scholar 

  19. Hölldobler B (1983) Territorial behavior in the green tree ant (Oecophylla smaragdina). Biotropica 15:241–250

    Article  Google Scholar 

  20. Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371–393

    CAS  Article  Google Scholar 

  21. Huang J-N, Cheng R-C, Li D, Tso I-M (2010) Salticid predation as one potential driving force of ant mimicry in jumping spiders. Proc R Soc Lond B Biol Sci 278:1356–1364

    Article  Google Scholar 

  22. Jandt JM, Hunt EM, McGlynn TP (2015) Intraspecific food-robbing and neighborhood competition: consequences for anti-robber vigilance and colony productivity. Biotropica 47(4):491–496

    Article  Google Scholar 

  23. Kilner RM, Langmore NE (2011) Cuckoos versus hosts in insects and birds: adaptations, counter-adaptations and outcomes. Biol Rev Camb Philos Soc 86(4):836–852. https://doi.org/10.1111/j.1469-185X.2010.00173.x

    Article  PubMed  Google Scholar 

  24. Lenoir A, D'Ettorre P, Errard C, Hefetz A (2001) Chemical ecology and social parasitism in ants. Annu Rev Entomol 46:573–599. https://doi.org/10.1146/annurev.ento.46.1.573

    CAS  Article  PubMed  Google Scholar 

  25. Lenoir A, Fresneau D, Errard C, Hefetz A (1999) Individuality and colonial identity in ants: the emergence of the social representation concept. In: Dertain C, Deneubourg JL, Pasteels JM (eds) Information processing in social insects. Birkhauser Verlag, Basel, pp 219–237

    Google Scholar 

  26. Lhomme P, Ayasse M, Valterova I, Lecocq T, Rasmont P (2012) Born in an alien nest : how do social parasite male offspring escape from host aggression? PLoS One 7(9):e43053. https://doi.org/10.1371/journal.pone.0043053

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. Martin S, Drijfhout F (2009) A review of ant cuticular hydrocarbons. J Chem Ecol 35(10):1151–1161

    CAS  Article  Google Scholar 

  28. Maschwitz U, Dorow W, Buschinger A, Kalytta G (2000) Social parasitism involving ants of different subfamilies: Polyrhachis lama (Formicinae) an obligatory inquiline of Diacamma sp.(Ponerinae) in Java. Insect Soc 47(1):27–35

    Article  Google Scholar 

  29. Maschwitz U, Go C, Kaufmann E, Buschinger A (2004) A unique strategy of host colony exploitation in a parasitic ant: workers of Polyrhachis lama rear their brood in neighbouring host nests. Naturwissenschaften 91(1):40–43

    CAS  Article  Google Scholar 

  30. Morel L, Vander Meer RK, Lavine BK (1988) Ontogeny of nestmate recognition cues in the red carpenter ant (Camponotus floridanus). Behav Ecol Sociobiol 22(3):175–183

    Article  Google Scholar 

  31. Mori n A, D'Ettorre P, Le Moli F (1995) Host nest usurpation and colony foundation in the European amazon ant, Polyergus rufescens Latr.(Hymenoptera: Formicidae). Insect Soc 42(3):279–286

    Article  Google Scholar 

  32. 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

    CAS  Article  Google Scholar 

  33. Nehring V, Dani FR, Turillazzi S, Boomsma JJ, D'Ettorre P (2015) Integration strategies of a leaf-cutting ant social parasite. Anim Behav 108:55–65

    Article  Google Scholar 

  34. Ozaki, M., & Wada-Katsumata, A. (2010). Perception and olfaction of cuticular compounds. Insect hydrocarbons: biology, biochemistry and chemical ecology (Ed. by Blomquist G.J. and Bagneres A-G.), 10, pp. 207–221, Cambridge University Press, Cambridge.

  35. Pasteur G (1982) A classification review of mimicry systems. Annu Rev Ecol Syst 13:169–199

    Article  Google Scholar 

  36. Perfecto I, Vandermeer J (1993) Cleptobiosis in the antEctatomma ruidum in Nicaragua. Insect Soc 40(3):295–299

    Article  Google Scholar 

  37. Rodríguez-Gironés MA, Lotem A (1999) How to detect a cuckoo egg: a signal-detection theory model for recognition and learning. Am Nat 153(6):633–648

    Article  Google Scholar 

  38. Ryti RT, Case TJ (1988) Field experiments on desert ants: testing for competition between colonies. Ecology 69(6):1993–2003

    Article  Google Scholar 

  39. Saul-Gershenz LS, Millar JG (2006) Phoretic nest parasites use sexual deception to obtain transport to their host’s nest. Proc Natl Acad Sci U S A 103(38):14039–14044. https://doi.org/10.1073/pnas.0603901103

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. Singer TL (1998) Roles of hydrocarbons in the recognition systems of insects. Am Zool 38(2):394–405

    CAS  Article  Google Scholar 

  41. Sledge MF, Dani FR, Cervo R, Dapporto L, Turillazzi S (2001) Recognition of social parasites as nest-mates: adoption of colony-specific host cuticular odours by the paper wasp parasite Polistes sulcifer. Proc R Soc Lond B Biol Sci 268(1482):2253–2260

    CAS  Article  Google Scholar 

  42. Stevens M (2013) Sensory ecology, behaviour, and evolution. Oxford University Press

  43. Sumner S, Nash DR, Boomsma JJ (2003) The adaptive significance of inquiline parasite workers. Proc R Soc Lond B Biol Sci 270(1521):1315–1322

    Article  Google Scholar 

  44. 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(3):479–486

    Article  Google Scholar 

  45. van Zweden, J. S., & d’Ettorre, P. (2010). Nestmate recognition in social insects and the role of hydrocarbons. Insect hydrocarbons: biology, biochemistry and chemical ecology (Ed. by Blomquist G.J. and Bagneres A-G.), 11, pp. 222–243, Cambridge University Press, Cambridge

  46. Vander Meer RK, Morel L (1998) Nestmate recognition in ants. Pheromone Communication in Social Insects:79–103

  47. von Beeren CV, Schulz S, Hashim R, Witte V (2011) Acquisition of chemical recognition cues facilitates integration into ant societies. BMC Ecology 11:30. https://doi.org/10.1186/1472-6785-11-30

    Article  PubMed  Google Scholar 

  48. Ward S (1996) A new workerless social parasite in the ant genus Pseudomyrmex (Hymenoptera: Formicidae), with a discussion of the origin of social parasitism in ants. Syst Entomol 21(3):253–263

    Article  Google Scholar 

  49. Witte V, Lehmann L, Lustig A, Maschwitz U (2009) Polyrhachis lama, a parasitic ant with an exceptional mode of social integration. Insect Soc 56(3):301–307

    Article  Google Scholar 

  50. Yamaguchi T (1995) Intraspecific competition through food robbing in the harvester ant, Messor aciculatus (Fr. Smith), and its consequences on colony survival. Insect Soc 42(1):89–101

    Article  Google Scholar 

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Acknowledgements

We thank T. Akino, M. Hojo, M. Maruyama, K. Tsuji, and J. Wang for their very helpful comments.

Funding

This work has been supported by a research fellowship for Young Scientists (DC1) from the Japan Society for the Promotion of Science to S.S., a Grant-in-Aid for Encouragement of Young Scientists No. JP16J01030 to S.S., a Grant-in-Aid for Basic Scientific Research (B) No. JP15H004423 to Y.I., and The Natio Foundation.

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Correspondence to Shinsuke Satoi.

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Satoi, S., Iwasa, Y. Chemical mimicry or crypsis—the evolutionary game played by parasitic ants invading other colonies. Theor Ecol 12, 391–399 (2019). https://doi.org/10.1007/s12080-018-0406-z

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Keywords

  • Ant nest parasites
  • Chemical strategy
  • Mimicry
  • Crypsis