Advertisement

Chemical profiles in Iberoformica subrufa and Formica frontalis, a new example of temporary host–parasite interaction

  • F. Ruano
  • A. Lenoir
  • M. Silvestre
  • A. Khalil
  • A. Tinaut
Research Article

Abstract

The aim of this paper is to describe the relationship between two ant species, Formica frontalis and Iberoformica subrufa, found together in shared nests. Therefore, we obtained data from dug nests and outdoor activity in two sympatric populations and investigated the cuticular hydrocarbons (CHCs) in both sympatric populations and in 10 I. subrufa allopatric populations to unravel whether the relationship becomes tuned between both species. We also determined the CHCs of two sympatric Serviformica species (F. cunicularia and F. lemani). Our results showed that the ant F. frontalis is a temporary parasite of I. subrufa which facultatively forms mixed colonies complying with a loose form of the Emery’s rule. Alkanes and methylalkanes are the most abundant compounds found in F. frontalis and I. subrufa CHCs, respectively, but esters were only abundant in I. subrufa. As far as the CHC similarity is concerned, the sympatric free-living hosts were chemically closer to the parasite, albeit not identical, whereas the allopatric I. subrufa populations always maintained a separate CHC composition. We provide different potential hypotheses to explain this similarity of cuticular profiles only in the two geographically distant sympatric populations.

Keywords

Emery’s rule Esters Environmental hypothesis Different species hypothesis Host-tolerance hypothesis F. lemani F. cunicularia 

Notes

Acknowledgements

We are grateful to Abraham Hefetz for his collaboration with identifying the esters, editing the manuscript, and discussing the resistance-tolerance hypothesis, which has significantly improved the manuscript. Raphaël Boulay and David Tinaut collected samples of Iberoformica subrufa at different sites in Spain. We are also grateful to the authorities of the Environmental Agency of the Andalusian Government and especially the National Parks of Sierra Nevada, Sierra de Baza and Doñana, who gave permission and facilities to collect samples. Fran Oi and Hugo Álvarez helped us to manage some graphs and tables and Angela Tate edited the English language as a professional scientific editor. This work was supported by the PRES Centre Val de Loire Université (APR-IA 2012).

Supplementary material

40_2018_677_MOESM1_ESM.pdf (392 kb)
Supplementary material 1 (PDF 391 KB)
40_2018_677_MOESM2_ESM.pdf (480 kb)
Supplementary material 2 (PDF 480 KB)

References

  1. Arnan X, Rodrigo A, Retana J (2007) Uncoupling the effects of shade and food resources of vegetation on Mediterranean ants: an experimental approach at the community level. Ecography 30:161–172CrossRefGoogle Scholar
  2. Bagnères AG, Morgan ED, Clément JL (1991) Species-specific secretions of the Dufour gland of three species of Formicinae ants (Hymenoptera:Formicidae). Biochem Syst Ecol 19:25–33CrossRefGoogle Scholar
  3. Buczkowski G, Kumar R, Suib SL, Silverman J (2005) Diet-related modification of cuticular hydrocarbon profiles of the Argentine ant, Linepithema humile, diminishes intercolony aggression. J Chem Ecol 31:829–843CrossRefPubMedGoogle Scholar
  4. Buschinger A (1986) Evolution of social parasitism in ants. Trends Ecol Evol 1(6):155–160CrossRefPubMedGoogle Scholar
  5. Buschinger A (2009) Social parasitism among ants: a review (Hymenoptera: Formicidae). Myrmecol News 12:219–235Google Scholar
  6. Chernenko A, Helanterä H, Sundström L (2011) Egg recognition and social parasitism in Formica ants. Ethology 117:1081–1092CrossRefGoogle Scholar
  7. Cini A, Nieri R, Dapporto L, Monnin T, Cervo R (2014) Almost royal: incomplete suppression of host worker ovarian development by a social parasite wasp. Behav Ecol Sociobiol 68(3):467–475CrossRefGoogle Scholar
  8. Collingwood CA (1979) The Formicidae (Hymenoptera) of Fennoscandia and Denmark. Fauna Entomol Scand 8:1–174Google Scholar
  9. Czechowski W, Godzińska EJ (2015) Enslaved ants: not as helpless as they were thought to be. Insectes Sociaux 62(1):9–22CrossRefPubMedGoogle Scholar
  10. Emery C (1909) Über den Ursprung der dulotischen, parasitischen und myrmekophilen Ameisen. Biol Cent 29:352–362Google Scholar
  11. Forel A (1874) Les fourmis de la Suisse. Systématique, notices anatomique et physiologiques, architecture, distribution géographique, nouvelles expériences et observations de moeurs. Neue Denkschr. Allg. Scweiz. Ges Gesammten Naruwiss 26:1–452Google Scholar
  12. Forel A (1886) Études Myrmécologiques en 1886. Ann Soc Entomol Belg 30:131–215Google Scholar
  13. Forel A (1900) Fourmis du Japon. Nids en toile. Strongylognathus Huberi et voisins. Fourmiliére triple. Cyphomyrmex Wheeleri. Fourmis importées. Mitteilungen Der Schweizerischen Entomologischen Gesellschaft 10:267–287CrossRefGoogle Scholar
  14. Forel A (1913) Notes sur quelques Formica. Ann Soc Entomol Belg 57:360–361Google Scholar
  15. Gökcen OA, Morgan ED, Dani FR, Agosti D, Wehner R (2002) Dufour gland contents of ants of the Cataglyphis bicolor group. J Chem Ecol 28:71–87CrossRefPubMedGoogle Scholar
  16. Goropashnaya AV, Fedorov VB, Seifert B, Pamilo P (2012) Phylogenetic relationships of palaearctic Formica species (Hymenoptera, Formicidae) based on mitochondrial cytochrome b sequences. PLoS One 7:1–7CrossRefGoogle Scholar
  17. Higashi S (1983) Mechanism underlaying the appearance of secondary polygyny in subgenus Formica ants. Environ Sci Hokkaido 6:1–13Google Scholar
  18. Holldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge, p 732CrossRefGoogle Scholar
  19. Huang MH, Dornhaus A (2008) A meta-analysis of ant social parasitism: host characteristics of different parasitism types and a test of Emery’s rule. Ecol Entomol 33:589–596CrossRefGoogle Scholar
  20. Ito F, Higashi S (1990) Temporary social parasitism in the enslaving ant species Formica sanguinea Latreille: an important discovery related to the evolution of Dulosis in Formica ants. J Ethol 8:33–35CrossRefGoogle Scholar
  21. Kather R, Martin SJ (2012) Cuticular hydrocarbon profiles as a taxonomic tool: advantages, limitations and technical aspects. Physiol Entomol 37:25–32CrossRefGoogle Scholar
  22. Kilner RM, Langmore NE (2011) Cuckoos versus hosts in insects and birds: adaptations, counter-adaptations and outcomes. Biol Rev 86:836–852CrossRefPubMedGoogle Scholar
  23. Le Masne G (1956) Recherches sur les fourmis parasites: Plagiolepis grassei et l’évolution des Plagiolepis parasites, 243. Comptes Rendus de l’Académie des Sciences, Paris, pp 673–675Google Scholar
  24. Lenoir A, D’Ettorre P, Errard C, Hefetz A (2001) Chemical ecology and social parasitism in ants. Annu Rev Entomol 46:573–599CrossRefPubMedGoogle Scholar
  25. Liang D, Silverman J (2000) “You are what you eat”: diet modifies cuticular hydrocarbons and nestmate recognition in the Argentine ant, Linepithema humile. Naturwissenschaften 87:412–416CrossRefPubMedGoogle Scholar
  26. Lopez-Osorio F, Perrard A, Pickett KM, Carpenter JM, Agnarsson I (2015) Phylogenetic tests reject Emery’s rule in the evolution of social parasitism in yellowjackets and hornets (Hymenoptera:Vespidae, Vespinae). R Soc Open Sci 2:150159CrossRefPubMedPubMedCentralGoogle Scholar
  27. Martin SJ, Helanterä H, Drijfhout FP (2008) Evolution of species-specific cuticular hydrocarbon patterns in Formica ants. Biol J Lin Soc 95:131–140CrossRefGoogle Scholar
  28. Martin SJ, Helanterä H, Drijfhout FP (2011) Is parasite pressure a driver of chemical cue diversity in ants? Proc R Soc Lond B Biol Sci 278(1705):496–503CrossRefGoogle Scholar
  29. Martin SJ, Vitikainen E, Drijfhout FP, Jackson D (2012) Conspecific ant aggression is correlated with chemical distance, but not with genetic or spatial distance. Behav Genet 42(2):323–331CrossRefPubMedGoogle Scholar
  30. Mori A, Grasso DA, Visicchio R, Le Moli F (2001) Comparison of reproductive strategies and raiding behaviour in facultative and obligatory slave-making ants: the case of Formica sanguinea and Polyergus rufescens. Insectes Soc 48:302–314CrossRefGoogle Scholar
  31. Muñoz-López M, Palomeque T, Carrillo JA, Pons J, Tinaut A, Lorite P (2012) A new taxonomic status for Iberoformica (Hymenoptera, Formicidae) based on the use of molecular markers. J Zool Syst Evol Res 50(1):30–37CrossRefGoogle Scholar
  32. Pamminger T, Foitzik S, Metzler D, Pennings PS (2014) Oh sister, where art thou? Spatial population structure and the evolution of an altruistic defence trait. J Evol Biol 27(11):2443–2456CrossRefPubMedGoogle Scholar
  33. Pherobase (2017) http://www.pherobase.com/. Accessed 26 May 2017
  34. Pisarski B, Czechowski W (1994) Ways to reproductive success of wood ant queens. Memorab Zool 48(48):181–186Google Scholar
  35. Regnier FE, Wilson EO (1971) Chemical communication and ‘‘propaganda’’ in slave-maker ants. Science 172:267–269CrossRefPubMedGoogle Scholar
  36. Romiguier J, Rolland J, Morandin C, Keller L (2018) Phylogenomics of palearctic Formica species suggests a single origin of temporary parasitism and gives insights to the evolutionary pathway toward slave-making behaviour. BMC Evol Biol 18(1):40CrossRefPubMedPubMedCentralGoogle Scholar
  37. Savolainen R, Deslippe JR (1996) Facultative and obligate slavery in Formicine ants: frequency of slavery, and proportion and size of slaves. Biol J Lin Soc 57:47–58CrossRefGoogle Scholar
  38. Stockan JA, Robinson EJ, Trager JC, Yao I, Seifert B (2016) Introducing wood ants: evolution, phylogeny, identification and distribution. In: Stockan J, Robinson EJ (eds) Wood ant ecology and conservation. Cambridge University Press, Cambridge, pp 1–35Google Scholar
  39. Svensson EI, Råberg L (2010) Resistance and tolerance in animal enemy–victim coevolution. Trends Ecol Evol 25:267–274CrossRefPubMedGoogle Scholar
  40. Tinaut A (1990) Descripción del macho de Formica subrufa Roger, 1859 y creación de un nuevo subgénero (Hymenoptera, Formicidae). Eos 65:281–291Google Scholar
  41. Tinaut A, Martínez Ibáñez MD (1998) Taxonomy and distribution of Formica dusmeti Emery, 1909 and of F. frontalis Santschi, 1919 (Hymenoptera, Formicidae). Graellsia 54:31–41CrossRefGoogle Scholar
  42. Tinaut A, Ruano F (1992) Braquipterismo y apterismo en formicidos. Morfología y biometría en las hembras de especies ibéricas de vida libre (Hymenoptera: Formicidae). Graellsia 48:121–131Google Scholar
  43. Tinaut A, Ruano F, Silvestre M, Martínez Ibañez MD (2015) Distribución de Formica frontalis Santschi, 1919 en la península ibérica (Hymenoptera: Formicidae). Boletín Asociación española de Entomología 39(1–2):115–133Google Scholar
  44. van Zweden JS, Dreier S, d’Ettorre P (2009) Disentangling environmental and heritable nestmate recognition cues in a carpenter ant. J Insect Physiol 55:159–164CrossRefGoogle Scholar
  45. Wilson EO (1971) The insect societies. Harvard University Press, CambridgeGoogle Scholar
  46. Włodarczyk T (2011) Recognition of individuals from mixed colony by Formica sanguinea and Formica polyctena ants. J Insect Behav 25(2):105–113CrossRefGoogle Scholar
  47. Włodarczyk T, Szczepaniak L (2014) Incomplete homogenization of chemical recognition labels between Formica sanguinea and Formica rufa ants (Hymenoptera:Formicidae) living in a mixed colony. J Insect Sci 14(1):214PubMedPubMedCentralGoogle Scholar
  48. Zamora-Muñoz C, Ruano F, Errard C, Lenoir A, Hefetz A, Tinaut A (2003) Coevolution in the slave-parasite system Proformica longisetaRossomyrmex minuchae (Hymenoptera:Formicidae). Sociobiology 42:299–317Google Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2018

Authors and Affiliations

  1. 1.Departamento de ZoologiaUniversidad de GranadaGranadaSpain
  2. 2.IRBI, Institut de Recherche sur la Biologie de l’Insecte, UMR CNRS, Faculté des Sciences, Parc de Grandmont, Université de ToursToursFrance
  3. 3.Departamento de EcologíaUniversidad Autónoma de MadridMadridSpain

Personalised recommendations