Skip to main content

Army imposters: diversification of army ant-mimicking beetles with their Eciton hosts

Insectes Sociaux volume 65, pages 59–75 (2018)Cite this article

Abstract

Colonies of neotropical army ants of the genus Eciton Latreille offer some of the most captivating examples of intricate interactions between species, with hundreds of associated species already described in colonies of Eciton burchellii Westwood. Among this plethora of species found with Eciton colonies, two genera of staphylinid beetles, Ecitomorpha Wasmann, and Ecitophya Wasmann, have evolved to mimic the appearance and parallel the colouration of the most abundant ant worker cast. Here, we study for the first time the association of these ant-mimicking beetles with their ant host in an evolutionary and population genetics framework. The central emphasis is on colonies of E. burchellii, the only Eciton species that harbours both genera of ant-mimicking beetles. Phylogenetic and population structure analyses using the same mtDNA COI region (802 bp) for ants and beetles indicated that speciation patterns of the myrmecophiles were congruent with specialization to a particular Eciton (sub)species. Therefore, current taxonomic treatments of Eciton and its Ecitomorpha and Ecitophya associates need revision. Molecular clock analyses suggested that diversification of the Eciton hosts pre-date that of their guests, with a possible earlier association of Ecitophya (found with a large number of Eciton species) than with Ecitomorpha (found only with E. burchellii colonies). Population-level analyses revealed that patterns of diversification for the myrmecophiles are also consistent with specialisation to a particular host across broad geographical areas but not at small geographical scales, with gene flow within each species found between host colonies, even across landscape features that are strong barriers for Eciton female-mediated gene flow.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  • Akre RD, Rettenmeyer CW (1968) Trail-following by guests of army ants (Hymenoptera: Formicidae: Ecitonini). J Kansas Entomol Soc 41:165–174

    Google Scholar 

  • Akre RD, Rettenmeyer CW (1966) Behavior of Staphylinidae associated with army ants (Formicidae: Ecitonini). J Kansas Entomol Soc 39(4):745–782

    Google Scholar 

  • Akre RD, Torgerson RL (1969) Behavior of Vatesus beetles associated with army ants (Coleoptera: Staphylinidae). Pan-Pac Entomol 45:269–281

    Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge

    Google Scholar 

  • Berghoff SM, Kronauer DJC, Edwards KJ, Franks NR (2008) Dispersal and population structure of a new world predator, the army ant Eciton burchellii. J Evol Biol 21(4):1125–1132. doi:10.1111/j.1420-9101.2008.01531.x

    Article  CAS  PubMed  Google Scholar 

  • Berghoff SM, Wurst E, Ebermann E, Sendova-Franks AB, Rettenmeyer CW, Franks NR (2009) Symbionts of societies that fission: mites as guests or parasites of army ants. Ecol Entomol 34:684–695. doi:10.1111/j.1365-2311.2009.01125.x

    Article  Google Scholar 

  • Borgmeier T (1955) Die Wanderameisen der neotropischen region (Hym. Formicidae). Stud Entomol 3:1–716

    Google Scholar 

  • Brady SG (2003) Evolution of the army ant syndrome: the origin and long-term evolutionary stasis of a complex of behavioral and reproductive adaptations. Proc Natl Acad Sci USA 100:6575–6579. doi:10.1073/pnas.1137809100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brady SG, Ward PS (2005) Morphological phylogeny of army ants and other dorylomorphs (Hymenoptera: Formicidae). Syst Entomol 30:593–618. doi:10.1111/j.1365-3113.2005.00290.x

    Article  Google Scholar 

  • Chatzimanolis S, Ashe JS, Hanley RS (2004) Diurnal/nocturnal activity of rove beetles (Coleoptera: Staphylinidae) on Barro Colorado Island, Panama assayed by flight intercept trap. Coleopt Bull 58:569–577. doi:10.1649/689.1

    Article  Google Scholar 

  • Darwin C (1859) On the origin of the species by means of natural selection, or the preservation of favoured races in the struggle for life. John Murray, London. doi:10.1016/S0262-4079(09)60380-8

    Book  Google Scholar 

  • Elven H, Bachmann L, Gusarov VI (2012) Molecular phylogeny of the Athetini–Lomechusini–Ecitocharini clade of aleocharine rove beetles (Insecta). Zool Scr 41:617–636. doi:10.1111/j.1463-6409.2012.00553.x

    Article  PubMed  PubMed Central  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinf Online 1:47–50. doi:10.1111/j.1755-0998.2010.02847.x

    Article  CAS  Google Scholar 

  • Franks NR (1985) Reproduction, foraging efficiency and worker polymorphism in army ants. In: Hölldobler B, Lindauer M, Franks NR (eds) Experimental behavioral ecology and sociobiology: in memoriam Karl von Frisch, 1886–1982. Sinauer Associates, Inc., Sunderland, MA, p 488

  • Franks NR (1982) A new method for censusing animal populations: the number of Eciton burchelli army ant colonies on Barro Colorado Island, Panama. Oecologia 52:266–268. doi:10.1007/BF00363847

    Article  PubMed  Google Scholar 

  • Franks NR, Hölldobler B (1987) Sexual competition during colony reproduction in army ants. Biol J Linn Soc 30:229–243. doi:10.1111/j.1095-8312.1987.tb00298.x

    Article  Google Scholar 

  • Gotwald WH Jr (1995) Army ants: the biology of social predation. Cornell University Press, Ithaca

  • Hasegawa E, Tinaut A, Ruano F (2002) Molecular phylogeny of two slave-making ants: Rossomyrmex and Polyergus (Hymenoptera: Formicidae). Ann Zool Fennici 39:267–271

    Google Scholar 

  • Ho JWK, Adams CE, Lew JB, Matthews TJ, Ng CC, Shahabi-Sirjani A, Tan LH, Zhao Y, Easteal S, Wilson SR, Jermiin LS (2006) SeqVis: visualization of compositional heterogeneity in large alignments of nucleotides. Bioinformatics 22:2162–2163. doi:10.1093/bioinformatics/btl283

    Article  CAS  PubMed  Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, Cambridge

    Book  Google Scholar 

  • Hughes DP, Pierce NE, Boomsma JJ (2008) Social insect symbionts: evolution in homeostatic fortresses. Trends Ecol Evol 23:672–677. doi:10.1016/j.tree.2008.07.011

    Article  PubMed  Google Scholar 

  • Ivens ABF, von Beeren C, Blüthgen N, Kronauer DJC (2016) Studying the complex communities of ants and their symbionts using ecological network analysis. Annu Rev Entomol 61:353–371. doi:10.1146/annurev-ento-010715-023719

    Article  CAS  PubMed  Google Scholar 

  • Jaffé R, Moritz R.F.A., Kraus FB (2009) Gene flow is maintained by polyandry and male dispersal in the army ant Eciton burchellii. Popul Ecol 51:227–236. doi:10.1007/s10144-008-0133-1

    Article  Google Scholar 

  • Kistner DH (1979) Social and evolutionary significance of social insect symbionts. In: Hermann HR (ed) Social insects, p. 1. Academic Press, New York, pp 339–413

    Chapter  Google Scholar 

  • Kistner DH, Jacobson HR (1990) Cladistic analysis and taxonomic revision of the ecitophilous tribe Ecitocharini with studies of their behavior and evolution (Coleoptera, Staphylinidae, Aleocharinae). Sociobiology 17:333–480

    Google Scholar 

  • Kronauer DJC, Schöning C, D’Ettorre P, Boomsma JJ (2010) Colony fusion and worker reproduction after queen loss in army ants. Proc R Soc B Biol Sci 277:755–763. doi:10.1098/rspb.2009.1591

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451–1452. doi:10.1093/bioinformatics/btp187

    Article  CAS  PubMed  Google Scholar 

  • Lin C-P, Danforth BN (2004) How do insect nuclear and mitochondrial gene substitution patterns differ? Insights from Bayesian analyses of combined datasets. Mol Phylogenet Evol 30:686–702

    Article  CAS  PubMed  Google Scholar 

  • Mann WM (1926) New neotropical myrmecophiles. J Wash Acad Sci 16:448–455

    Google Scholar 

  • Mann WM (1921) Three new myrmecophilous beetles. Proc US Natl Mus 59:547–552

    Article  Google Scholar 

  • Maruyama M, Parker J (2017) Deep-time convergence in rove beetle symbionts of army ants. Curr Biol 27:920–926

    Article  CAS  PubMed  Google Scholar 

  • Maus C, Peschke K, Dobler S (2001) Phylogeny of the genus Aleochara inferred from mitochondrial cytochrome oxidase sequences (Coleoptera: Staphylinidae). Mol Phylogenet Evol 18:202–216. doi:10.1006/mpev.2000.0874

    Article  CAS  PubMed  Google Scholar 

  • Moore W, Robertson JA (2014) Report explosive adaptive radiation and extreme phenotypic diversity within ant-nest beetles. Curr Biol 24:2435–2439. doi:10.1016/j.cub.2014.09.022

    Article  CAS  PubMed  Google Scholar 

  • Moriyama EN, Powell JR (1997) Synonymous substitutions rates in Drosophila mitochondrial versus nuclear genes. J Mol Evol 45:378–391

    Article  CAS  PubMed  Google Scholar 

  • Moser JC (1967) Mating activities of Atta texana. (Hymenoptera, Formicidae). Insectes Soc 14:295–312. doi:10.1007/BF02252831

    Article  Google Scholar 

  • Parker J (2016) Myrmecophily in beetles (Coleoptera): evolutionary patterns and biological mechanisms. Myrmecol News 22:65–108

    Google Scholar 

  • Parker J, Grimaldi DA (2014) Specialized myrmecophily at the ecological dawn of modern ants. Curr Biol 24:2428–2434. doi:10.1016/j.cub.2014.08.068

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Espona S, McLeod JE, Franks NR (2012) Landscape genetics of a top neotropical predator. Mol Ecol 21:5969–5985. doi:10.1111/mec.12088

    Article  PubMed  Google Scholar 

  • Reichensperger A (1935) Beitrag zur Kenntnis der Myrmecophilenfauna Brasiliens und Costa Ricas III. (Col. Staphyl. Hist.). Arb iiber Morphol Taxon Entomol Aus Berlin Dahlem 2:188–218

    Google Scholar 

  • Reichensperger A (1933) Ecitophilen aus Costa Rica (II), Brasilien und Peru (Staph. Hist. Clavig.). Rev. Entomol 3:179–194

    Google Scholar 

  • Rettenmeyer CW, Rettenmeyer ME, Joseph J, Berghoff SM (2011) The largest animal association centered on one species: The army ant Eciton burchellii and its more than 300 associates. Insectes Soc 58:281–292. doi:10.1007/s00040-010-0128-8

    Article  Google Scholar 

  • Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542. doi:10.1093/sysbio/sys029

    Article  PubMed  PubMed Central  Google Scholar 

  • Santschi F (1925) Nouveaux Formicides brésiliens et autres. Extr des Ann Bull la Soc Entomol Belg 65:221–247

    Google Scholar 

  • Schneirla T (1971) Army ants: a study in social organization. Freeman, WH, San Francisco

    Google Scholar 

  • Schneirla T (1940) Further studies on the army-ant behavior patterns: mass organization in the swarm-raiders. J Comp Psychol 29:401–460

    Article  Google Scholar 

  • Schneirla T, Brown RZ (1950) Army ant life and behavior under dry season conditions. 4. Further investigation of cyclic processes in behavioral and reproductive functions. Bull Am Mus Nat Hist 95:263–354

    Google Scholar 

  • Schonrogge K, Barr B, Wardlaw JC, Naf E, Gardner MG, Breen J, Elmes GW, Thomas JA, Olg PH, Bassett S, East C (2002) When rare species become endangered: cryptic speciation in myrmecophilous hoverflies. Biol J Linn Soc 75:291–300

    Article  Google Scholar 

  • Seevers CH (1965) The systematics, evolution and zoogeography of staphylinid beetles associated with army ants (Coleoptera, Staphylinidae). Fieldiana Zool 47:137–351

    Google Scholar 

  • Simon C, Buckley TR, Frati F, Stewart JB, Beckenbach AT (2006) Incorporating molecular evolution into phylogenetic analysis, and a new compilation of conserved polymerase chain reaction primers for animal mitochondrial DNA. Annu Rev Ecol Evol Syst 37:545–579

    Article  Google Scholar 

  • Simon C, Frati F, Beckenbach A, Crespi B, Liu H, Flook P (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann Entomol Soc Am 87:651–701. doi:10.1093/aesa/87.6.651

    Article  CAS  Google Scholar 

  • Soare TW, Kumar A, Naish KA, O’Donnell S (2014) Genetic evidence for landscape effects on dispersal in the army ant Eciton burchellii. Mol Ecol 23:96–109. doi:10.1111/mec.12573

    Article  PubMed  Google Scholar 

  • Sunnucks P (2000) Efficient genetic markers for population biology. Trends Ecol Evol 15:199–203. doi:10.1016/S0169-5347(00)01825-5

    Article  CAS  PubMed  Google Scholar 

  • Swofford DL (2002) PAUP*. phylogenetic analysis using parsimony (* and other methods). Version 4b10. Sinauer Assoc. Sunderland

    Google Scholar 

  • Tack AJM, Roslin T (2010) Overrun by the neighbors: landscape context affects strength and sign of local adaptation. Ecology 91:2253–2260. doi:10.1890/09-0080.1

    Article  PubMed  Google Scholar 

  • Thomas F, Verneau O, De Meeûs T, Renaud F (1996) Parasites as to host evolutionary prints: insights into host evolution from parasitological data. Int J Parasitol 26:677–686. doi:10.1016/0020-7519(96)00023-9

    Article  CAS  PubMed  Google Scholar 

  • Thompson JN (1994) The coevolutionary process. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Thompson JN (2013) Relentless evolution. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Von Beeren C, Maruyama M, Kronauer DJC (2016a) Cryptic diversity, high host specificity and reproductive synchronization in army ant-associated Vatesus beetles. Mol Ecol 25:990–1005. doi:10.1111/mec.13500

    Article  Google Scholar 

  • Von Beeren C, Maruyama M, Kronauer D.J.C. (2016b) Community sampling and integrative taxonomy reveal new species and host specificity in the army ant-associated beetle genus Tetradonia (Coleoptera, Staphylinidae, Aleocharinae). PLoS One 11:e0165056

    Article  Google Scholar 

  • Watkins JF (1976) The identification and distribution of new world army ants. Baylor University Press, Waco

    Google Scholar 

  • Whitfield JB, Lockhart PJ (2007) Deciphering ancient rapid radiations. Trends Ecol Evol 22:258–265. doi:10.1016/j.tree.2007.01.012

    Article  PubMed  Google Scholar 

  • Winston ME, Kronauer D.J.C., Moreau C (2017) Early and dynamic colonization of Central America drives speciation in neotropical army ants. Mol Ecol 26:859–870

    Article  PubMed  Google Scholar 

  • Zhang D-X, Hewitt GM (2003) Nuclear DNA analyses in genetic studies of populations: practice, problems and prospects. Mol Ecol 12:563–584

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Autoridad Nacional del Ambiente (ANAM), Smithsonian Tropical Research Institute (STRI) and Centro de Estudios de Acción Social Panameña (CEASPA) are thanked for arranging permits and fieldwork activities. We thank J. Domínguez and F. García for assistance in the field, Carles Molina Rubio for laboratory assistance, John N. Thompson for discussion of results, and two anonymous referees for comments on a previous version of the manuscript. Cambridge Conservation Forum and Cambridge Conservation Initiative are thanked for allowing Sílvia Pérez-Espona to use their office space in the David Attenborough Building while writing this manuscript. Samples for this study were collected and exported under the permits SEX/A-8-08 and SEX/A-24-08, respectively. This study was funded by The Leverhulme Trust (Project Grant F/00 182/AI).

Author information

Authors and Affiliations

  1. School of Biological Sciences, The University of Bristol, 24 Tyndall Avenue, Bristol, BS8 1TH, UK

    S. Pérez-Espona, S. M. Berghoff, K. J. Edwards & N. R. Franks

  2. Estación Biológica de Doñana, CSIC, Isla de La Cartuja, Américo Vespucio s/n, Sevilla, E41092, Spain

    S. Pérez-Espona

  3. British Antarctic Survey, High Cross, Madingley Road, Cambridge, CB3 0ET, UK

    W. P. Goodall-Copestake

  4. Max Planck Institute of Neurobiology, Am Kopferspitz 18, 82152, Martinsried, Germany

    S. M. Berghoff

Authors
  1. S. Pérez-Espona
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. W. P. Goodall-Copestake
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. M. Berghoff
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. K. J. Edwards
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. N. R. Franks
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to S. Pérez-Espona.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Pérez-Espona, S., Goodall-Copestake, W.P., Berghoff, S.M. et al. Army imposters: diversification of army ant-mimicking beetles with their Eciton hosts. Insect. Soc. 65, 59–75 (2018). https://doi.org/10.1007/s00040-017-0588-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00040-017-0588-1

Keywords

  • Gene flow
  • Mimicry
  • Mitochondrial DNA
  • Myrmecophily
  • Myrmecophory
  • Population structure
  • Speciation
  • Taxonomy