Skip to main content
SpringerLink
Log in

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

  • Research Article
  • Published:
Insectes Sociaux Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • 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 30:161–172

    Article  Google Scholar 

  • 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 19:25–33

    Article  Google Scholar 

  • 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 31:829–843

    Article  CAS  PubMed  Google Scholar 

  • Buschinger A (1986) Evolution of social parasitism in ants. Trends Ecol Evol 1(6):155–160

    Article  CAS  PubMed  Google Scholar 

  • Buschinger A (2009) Social parasitism among ants: a review (Hymenoptera: Formicidae). Myrmecol News 12:219–235

    Google Scholar 

  • Chernenko A, Helanterä H, Sundström L (2011) Egg recognition and social parasitism in Formica ants. Ethology 117:1081–1092

    Article  Google Scholar 

  • 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):467–475

    Article  Google Scholar 

  • Collingwood CA (1979) The Formicidae (Hymenoptera) of Fennoscandia and Denmark. Fauna Entomol Scand 8:1–174

    Google Scholar 

  • Czechowski W, Godzińska EJ (2015) Enslaved ants: not as helpless as they were thought to be. Insectes Sociaux 62(1):9–22

    Article  CAS  PubMed  Google Scholar 

  • Emery C (1909) Über den Ursprung der dulotischen, parasitischen und myrmekophilen Ameisen. Biol Cent 29:352–362

    Google Scholar 

  • 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 26:1–452

    Google Scholar 

  • Forel A (1886) Études Myrmécologiques en 1886. Ann Soc Entomol Belg 30:131–215

    Google Scholar 

  • Forel A (1900) Fourmis du Japon. Nids en toile. Strongylognathus Huberi et voisins. Fourmiliére triple. Cyphomyrmex Wheeleri. Fourmis importées. Mitteilungen Der Schweizerischen Entomologischen Gesellschaft 10:267–287

    Article  Google Scholar 

  • Forel A (1913) Notes sur quelques Formica. Ann Soc Entomol Belg 57:360–361

    Google Scholar 

  • Gökcen OA, Morgan ED, Dani FR, Agosti D, Wehner R (2002) Dufour gland contents of ants of the Cataglyphis bicolor group. J Chem Ecol 28:71–87

    Article  PubMed  Google Scholar 

  • 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 7:1–7

    Article  CAS  Google Scholar 

  • Higashi S (1983) Mechanism underlaying the appearance of secondary polygyny in subgenus Formica ants. Environ Sci Hokkaido 6:1–13

    Google Scholar 

  • Holldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge, p 732

    Book  Google Scholar 

  • 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 33:589–596

    Article  Google Scholar 

  • 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 8:33–35

    Article  Google Scholar 

  • Kather R, Martin SJ (2012) Cuticular hydrocarbon profiles as a taxonomic tool: advantages, limitations and technical aspects. Physiol Entomol 37:25–32

    Article  CAS  Google Scholar 

  • Kilner RM, Langmore NE (2011) Cuckoos versus hosts in insects and birds: adaptations, counter-adaptations and outcomes. Biol Rev 86:836–852

    Article  PubMed  Google Scholar 

  • 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 673–675

    Google Scholar 

  • Lenoir A, D’Ettorre P, Errard C, Hefetz A (2001) Chemical ecology and social parasitism in ants. Annu Rev Entomol 46:573–599

    Article  CAS  PubMed  Google Scholar 

  • Liang D, Silverman J (2000) “You are what you eat”: diet modifies cuticular hydrocarbons and nestmate recognition in the Argentine ant, Linepithema humile. Naturwissenschaften 87:412–416

    Article  CAS  PubMed  Google Scholar 

  • 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 2:150159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin SJ, Helanterä H, Drijfhout FP (2008) Evolution of species-specific cuticular hydrocarbon patterns in Formica ants. Biol J Lin Soc 95:131–140

    Article  Google Scholar 

  • 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):496–503

    Article  Google Scholar 

  • 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):323–331

    Article  PubMed  Google Scholar 

  • 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 48:302–314

    Article  Google Scholar 

  • 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):30–37

    Article  Google Scholar 

  • 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):2443–2456

    Article  CAS  PubMed  Google Scholar 

  • Pherobase (2017) http://www.pherobase.com/. Accessed 26 May 2017

  • Pisarski B, Czechowski W (1994) Ways to reproductive success of wood ant queens. Memorab Zool 48(48):181–186

    Google Scholar 

  • Regnier FE, Wilson EO (1971) Chemical communication and ‘‘propaganda’’ in slave-maker ants. Science 172:267–269

    Article  CAS  PubMed  Google Scholar 

  • 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):40

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 57:47–58

    Article  Google Scholar 

  • 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 1–35

    Google Scholar 

  • Svensson EI, Råberg L (2010) Resistance and tolerance in animal enemy–victim coevolution. Trends Ecol Evol 25:267–274

    Article  PubMed  Google Scholar 

  • Tinaut A (1990) Descripción del macho de Formica subrufa Roger, 1859 y creación de un nuevo subgénero (Hymenoptera, Formicidae). Eos 65:281–291

    Google Scholar 

  • Tinaut A, Martínez Ibáñez MD (1998) Taxonomy and distribution of Formica dusmeti Emery, 1909 and of F. frontalis Santschi, 1919 (Hymenoptera, Formicidae). Graellsia 54:31–41

    Article  Google Scholar 

  • 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 48:121–131

    Google Scholar 

  • 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):115–133

    Google Scholar 

  • van Zweden JS, Dreier S, d’Ettorre P (2009) Disentangling environmental and heritable nestmate recognition cues in a carpenter ant. J Insect Physiol 55:159–164

    Article  CAS  Google Scholar 

  • Wilson EO (1971) The insect societies. Harvard University Press, Cambridge

    Google Scholar 

  • Włodarczyk T (2011) Recognition of individuals from mixed colony by Formica sanguinea and Formica polyctena ants. J Insect Behav 25(2):105–113

    Article  Google Scholar 

  • 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):214

    Article  Google Scholar 

  • Zamora-Muñoz C, Ruano F, Errard C, Lenoir A, Hefetz A, Tinaut A (2003) Coevolution in the slave-parasite system Proformica longiseta–Rossomyrmex minuchae (Hymenoptera:Formicidae). Sociobiology 42:299–317

    Google Scholar 

Download references

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).

Author information

Authors and Affiliations

  1. Departamento de Zoologia, Universidad de Granada, Granada, Spain

    F. Ruano, M. Silvestre & A. Tinaut

  2. IRBI, Institut de Recherche sur la Biologie de l’Insecte, UMR CNRS, Faculté des Sciences, Parc de Grandmont, Université de Tours, Tours, France

    A. Lenoir & A. Khalil

  3. Departamento de Ecología, Universidad Autónoma de Madrid, Madrid, Spain

    M. Silvestre

Authors
  1. F. Ruano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Lenoir
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Silvestre
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Khalil
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. Tinaut
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to F. Ruano.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 391 KB)

Supplementary material 2 (PDF 480 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ruano, F., Lenoir, A., Silvestre, M. et al. Chemical profiles in Iberoformica subrufa and Formica frontalis, a new example of temporary host–parasite interaction. Insect. Soc. 66, 223–233 (2019). https://doi.org/10.1007/s00040-018-00677-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00040-018-00677-6

Keywords

Search

Navigation