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

  • S. Pérez-Espona
  • W. P. Goodall-Copestake
  • S. M. Berghoff
  • K. J. Edwards
  • N. R. Franks
Research 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.

Keywords

Gene flow Mimicry Mitochondrial DNA Myrmecophily Myrmecophory Population structure Speciation Taxonomy 

References

  1. Akre RD, Rettenmeyer CW (1968) Trail-following by guests of army ants (Hymenoptera: Formicidae: Ecitonini). J Kansas Entomol Soc 41:165–174Google Scholar
  2. Akre RD, Rettenmeyer CW (1966) Behavior of Staphylinidae associated with army ants (Formicidae: Ecitonini). J Kansas Entomol Soc 39(4):745–782Google Scholar
  3. Akre RD, Torgerson RL (1969) Behavior of Vatesus beetles associated with army ants (Coleoptera: Staphylinidae). Pan-Pac Entomol 45:269–281Google Scholar
  4. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  5. 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 CrossRefPubMedGoogle Scholar
  6. 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 CrossRefGoogle Scholar
  7. Borgmeier T (1955) Die Wanderameisen der neotropischen region (Hym. Formicidae). Stud Entomol 3:1–716Google Scholar
  8. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 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 CrossRefGoogle Scholar
  10. 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 CrossRefGoogle Scholar
  11. 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 CrossRefGoogle Scholar
  12. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 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 Google Scholar
  14. 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 488Google Scholar
  15. 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 CrossRefPubMedGoogle Scholar
  16. 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 CrossRefGoogle Scholar
  17. Gotwald WH Jr (1995) Army ants: the biology of social predation. Cornell University Press, IthacaGoogle Scholar
  18. Hasegawa E, Tinaut A, Ruano F (2002) Molecular phylogeny of two slave-making ants: Rossomyrmex and Polyergus (Hymenoptera: Formicidae). Ann Zool Fennici 39:267–271Google Scholar
  19. 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 CrossRefPubMedGoogle Scholar
  20. Hölldobler B, Wilson EO (1990) The ants. Harvard University Press, CambridgeCrossRefGoogle Scholar
  21. 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 CrossRefPubMedGoogle Scholar
  22. 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 CrossRefPubMedGoogle Scholar
  23. 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 CrossRefGoogle Scholar
  24. Kistner DH (1979) Social and evolutionary significance of social insect symbionts. In: Hermann HR (ed) Social insects, p. 1. Academic Press, New York, pp 339–413Google Scholar
  25. 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 17:333–480Google Scholar
  26. 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 CrossRefGoogle Scholar
  27. Lenoir A, Ettorre PD, Errard C (2001) Chemical ecology and social parasitism in ants. Annu Rev Entomol 46:573–599CrossRefPubMedGoogle Scholar
  28. 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 CrossRefPubMedGoogle Scholar
  29. 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 30:686–702CrossRefPubMedGoogle Scholar
  30. Mann WM (1926) New neotropical myrmecophiles. J Wash Acad Sci 16:448–455Google Scholar
  31. Mann WM (1921) Three new myrmecophilous beetles. Proc US Natl Mus 59:547–552CrossRefGoogle Scholar
  32. Maruyama M, Parker J (2017) Deep-time convergence in rove beetle symbionts of army ants. Curr Biol 27:920–926CrossRefPubMedGoogle Scholar
  33. 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 CrossRefPubMedGoogle Scholar
  34. 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 CrossRefPubMedGoogle Scholar
  35. Moriyama EN, Powell JR (1997) Synonymous substitutions rates in Drosophila mitochondrial versus nuclear genes. J Mol Evol 45:378–391CrossRefPubMedGoogle Scholar
  36. Moser JC (1967) Mating activities of Atta texana. (Hymenoptera, Formicidae). Insectes Soc 14:295–312. doi:10.1007/BF02252831 CrossRefGoogle Scholar
  37. Parker J (2016) Myrmecophily in beetles (Coleoptera): evolutionary patterns and biological mechanisms. Myrmecol News 22:65–108Google Scholar
  38. 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 CrossRefPubMedGoogle Scholar
  39. 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 CrossRefPubMedGoogle Scholar
  40. Reichensperger A (1935) Beitrag zur Kenntnis der Myrmecophilenfauna Brasiliens und Costa Ricas III. (Col. Staphyl. Hist.). Arb iiber Morphol Taxon Entomol Aus Berlin Dahlem 2:188–218Google Scholar
  41. Reichensperger A (1933) Ecitophilen aus Costa Rica (II), Brasilien und Peru (Staph. Hist. Clavig.). Rev. Entomol 3:179–194Google Scholar
  42. 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 CrossRefGoogle Scholar
  43. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Santschi F (1925) Nouveaux Formicides brésiliens et autres. Extr des Ann Bull la Soc Entomol Belg 65:221–247Google Scholar
  45. Schneirla T (1971) Army ants: a study in social organization. Freeman, WH, San FranciscoGoogle Scholar
  46. Schneirla T (1940) Further studies on the army-ant behavior patterns: mass organization in the swarm-raiders. J Comp Psychol 29:401–460CrossRefGoogle Scholar
  47. 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 95:263–354Google Scholar
  48. 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 75:291–300CrossRefGoogle Scholar
  49. Seevers CH (1965) The systematics, evolution and zoogeography of staphylinid beetles associated with army ants (Coleoptera, Staphylinidae). Fieldiana Zool 47:137–351Google Scholar
  50. 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 37:545–579CrossRefGoogle Scholar
  51. 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 CrossRefGoogle Scholar
  52. 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 CrossRefPubMedGoogle Scholar
  53. Sunnucks P (2000) Efficient genetic markers for population biology. Trends Ecol Evol 15:199–203. doi:10.1016/S0169-5347(00)01825-5 CrossRefPubMedGoogle Scholar
  54. Swofford DL (2002) PAUP*. phylogenetic analysis using parsimony (* and other methods). Version 4b10. Sinauer Assoc. SunderlandGoogle Scholar
  55. 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 CrossRefPubMedGoogle Scholar
  56. 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 CrossRefPubMedGoogle Scholar
  57. Thompson JN (1994) The coevolutionary process. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  58. Thompson JN (2013) Relentless evolution. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  59. Thompson JN (2005) The geographic mosaic of coevolution. University of Chicago Press, ChicagoGoogle Scholar
  60. 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 CrossRefGoogle Scholar
  61. 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:e0165056CrossRefGoogle Scholar
  62. Watkins JF (1976) The identification and distribution of new world army ants. Baylor University Press, WacoGoogle Scholar
  63. Whitfield JB, Lockhart PJ (2007) Deciphering ancient rapid radiations. Trends Ecol Evol 22:258–265. doi:10.1016/j.tree.2007.01.012 CrossRefPubMedGoogle Scholar
  64. Winston ME, Kronauer D.J.C., Moreau C (2017) Early and dynamic colonization of Central America drives speciation in neotropical army ants. Mol Ecol 26:859–870CrossRefPubMedGoogle Scholar
  65. Zhang D-X, Hewitt GM (2003) Nuclear DNA analyses in genetic studies of populations: practice, problems and prospects. Mol Ecol 12:563–584CrossRefPubMedGoogle Scholar

Copyright information

© International Union for the Study of Social Insects (IUSSI) 2017

Authors and Affiliations

  1. 1.School of Biological SciencesThe University of BristolBristolUK
  2. 2.Estación Biológica de Doñana, CSIC, Isla de La CartujaSevillaSpain
  3. 3.British Antarctic SurveyCambridgeUK
  4. 4.Max Planck Institute of NeurobiologyMartinsriedGermany

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