Advertisement

Insectes Sociaux

, Volume 65, Issue 4, pp 639–648 | Cite as

Do mutualistic associations have broader host ranges than neutral or antagonistic associations? A test using myrmecophiles as model organisms

  • J. R. N. Glasier
  • A. G. B. Poore
  • D. J. Eldridge
Research Article

Abstract

Symbiotic associations are found across all kingdoms of life and are integral to ecosystem structure and function. Central to understanding the ecology and evolution of symbiotic relationships is an understanding of what influences host range; the number of host species that a symbiont can utilize. Despite the importance of host breadth among symbionts, relatively little is known about how the relationship that a symbiont has with its host influences its host range. Additionally, contrasts among interaction types often involve diverse groups of unrelated host species. To test how host range varied with interaction type, we used a global synthesis of over 1600 species of myrmecophiles, those organisms that have symbiotic associations with ants. We used an indexed literature search to collate known myrmecophile species and their hosts, and to determine how two degrees of dependence (facultative, obligate) and four types of relationships (mutualism, commensalism, kleptoparasitism, and parasitism) among myrmecophiles and their hosts influence host range. Our synthesis showed that, overall, myrmecophiles exhibited a high degree of host specialization, and facultatively dependent myrmecophiles had broader host ranges than those with obligate interactions. Myrmecophiles with mutualistic relationships had broader host ranges than neutral or antagonistic relationships. Additionally, lepidopteran myrmecophiles exhibited broader host range patterns than other taxa. Our results have important implications for how symbiotic associations are understood, with positive relationships (mutualisms) associated with broader host range, and antagonistic relationships (parasitism) associated with narrow host range.

Keywords

Symbiotic associations Myrmecophiles Host range Symbionts 

Notes

Acknowledgements

We thank Gerry Cassis, Stephen Bonser, and Angela Moles for comments on an earlier version of this manuscript. We thank Mitchell Lyons and Andrew Letten for advice on statistical analyses.

Supplementary material

40_2018_655_MOESM1_ESM.docx (46 kb)
Supplementary material 1 (DOCX 46 KB)

References

  1. Akino T, Knapp JJ, Thomas JA, Elmes GW (1999) Chemical mimicry and host specificity in the butterfly Maculinea rebeli, a social parasite of Myrmica ant colonies. Proc Biol Sci 266:1419–1426CrossRefGoogle Scholar
  2. Baker AC (2003) Flexibility and specificity in coral–algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689CrossRefGoogle Scholar
  3. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-7. http://CRAN.R-project.org/package=lme4. Accessed Dec 2016
  4. Blüthgen N, Mezger D, Linsenmair KE (2006) Ant–hemipteran trophobioses in a Bornean rainforest diversity, specificity and monopolisation. Insectes Soc 53:194–203CrossRefGoogle Scholar
  5. Boucher DH, James S, Keeler KH (1982) The ecology of mutualism. Annu Rev Ecol Syst 13:315–317CrossRefGoogle Scholar
  6. Brockmann HJ, Barnard CJ (1979) Kleptoparasitism in birds. Anim Behav 27:487–514CrossRefGoogle Scholar
  7. Campbell KU, Klompen H, Crist TO (2013) The diversity and host specificity of mites associated with ants: the roles of ecological and life history traits of ant hosts. Insectes Soc 60:31–41CrossRefGoogle Scholar
  8. Chamberlain SA, Holland JN (2009) Quantitative synthesis of context dependency in ant-plant protection mutualisms. Ecology 90:2384–2392CrossRefGoogle Scholar
  9. Davies NB, Brooker MDL (1989) An experimental study of co-evolution between the Cuckoo, Cuculus canorus, and its hosts. I. Host egg discrimination. J Anim Ecol 58:207–224CrossRefGoogle Scholar
  10. Delabie JHC (2001) Trophiobiosis between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): an overview. Neotropical Entomol 30:501–516CrossRefGoogle Scholar
  11. Eastwood R, Pierce NE, Kitching RL, Huges JM (2006) Do ants enhance diversification in Lycaenid butterflies? Phylogeographic evidence from a model myrmecophile, Jalmenus evagoras. Evolution 60:315–327CrossRefGoogle Scholar
  12. Edgar MA, Allan RA (2006) Chemical mimicry of the ant Oecophylla smaragdina, by the myrmecophilous spider Cosmophasis bitaeniata: is it colony-specific? J Ethol 24:239–246CrossRefGoogle Scholar
  13. Fleming TH, Holland JN (1998) The evolution of obligate pollination mutualisms: senita cactus and senita moth. Oecologia 114:368–375CrossRefGoogle Scholar
  14. Fielder K (1996) Host-plant relationships of lycaenid butterflies: large-scale patterns, interactions with plant chemistry, and mutualism with ants. Entomol Exp Appl 80:259–267CrossRefGoogle Scholar
  15. Glasier JRN, Acorn JH (2013) First record of the myrmecophilous sap beetle Amphotis ulkei Leconte (Coleoptera: Nitidulidae) in Canada. Coleopterists Bull 67:188–189CrossRefGoogle Scholar
  16. Gray B (1971) Note on the biology of the ant species Myrmecia dispar (Clark) (Hymenoptera: Formicidae). Insectes Soc 2:71–80CrossRefGoogle Scholar
  17. Hoeksema JD, Bruna EM (2000) Pursuing the big questions about interspecific mutualism: a review of theoretical approaches. Oecologia 125:321–330CrossRefGoogle Scholar
  18. Hölldobler B (1971) Communications between ants and their guests. Sci Am 224:86–93CrossRefGoogle Scholar
  19. Hölldobler B, Wilson EO (1990) The ants. The Belknap Press of Harvard University Press, CambridgeCrossRefGoogle Scholar
  20. Hughes DP, Pierce NE, Boomsma JJ (2008) Social insect symbionts: evolution in homeostatic fortresses. Trends Ecol Evol 23:672–677CrossRefGoogle Scholar
  21. Ivens ABF (2015) Cooperation and conflict in ant (Hymenoptera: Formicidae) farming mutualisms—a review. Myrmecol News 21:19–36Google Scholar
  22. Jackson DE, Ratnieks FLW (2006) Communication in ants. Curr Biol 16:570–574CrossRefGoogle Scholar
  23. Kaminski LA, Freiras AVL, Oliveira PS (2010) Interactions between mutualisms: ant-tended butterflies exploit enemy-free space provided by ant-treehopper associations. Am Nat 176:322–334CrossRefGoogle Scholar
  24. Kaminski LA, Rodrigues DA (2011) Species-specific levels of ant attendance mediate performance costs in a facultative myrmecophilous butterfly. Physiol Entomol 36:208–214CrossRefGoogle Scholar
  25. Kamiya T, O’Dwyer K, Nakagawa S, Poulin R (2014) Host diversity drives parasite diversity: meta-analytical insights into patterns and causal mechanisms. Ecography 37:689–697CrossRefGoogle Scholar
  26. Kawakita A, Okamoto T, Goto R, Kato M (2010) Mutualism favours higher host specificity than does antagonism in plant-herbivore interaction. Proc R Soc B 277:2756–2774CrossRefGoogle Scholar
  27. Kindlmann P, Hulle M, Stadler B (2007) Timing of dispersal: effect of ants on aphids. Oecologia 152:625–631CrossRefGoogle Scholar
  28. Kistner DH (1982) The social insects’ bestiary. In: Hermann HR (ed) Social insects, pp 1–244. Academic Press, New YorkGoogle Scholar
  29. Komatsu T, Maruyama M, Itino T (2009) Behavioral differences between two ant cricket species in Nansei Islands: host-specialist versus host-generalist. Insectes Soc 56:389–396CrossRefGoogle Scholar
  30. Krasnov BR, Mouillot D, Shenbrot GI, Khokhlova IS, Poulin R (2001) Beta-specificity: the turnover of host species in space and another way to measure host specificity. Int J Parasitol 41:33–41CrossRefGoogle Scholar
  31. Kronauer DJC, Pierce NE (2011) Myrmecophiles. Curr Biol 21:208–209CrossRefGoogle Scholar
  32. Lapeva-Gjonova A, Rücker WH (2011) Latridiidae and Endomychidae beetles (Coleoptera) from ant nests in Bulgaria. Latridiidae 8:1–8Google Scholar
  33. Lencina JL, Torres JL, Baena M, Andújar C, Gallego D, González E, Zuzarte AJ (2011) Notas sobre Amphotis Erichson, 1843. Ibéros (Coleoptera: Nitidulidae). Bol Soc Entomol Aragon 49:149–152Google Scholar
  34. Loiacono MS, Margaria CB, Aquino DA (2013) Diapriinae wasps (Hymenoptera: Diaprioidea: Diapriidae) associated with ants (Hymenoptera: Formicidae) in Argentina. Psyche 2013:1–11CrossRefGoogle Scholar
  35. Machado CA, Robbins N, Thomas M, Gilbert P, Herre EA (2005) Critical review of host specificity and its coevolutionary implications in the fig/fig-wasp mutualism. Proc Natl Acad Sci 102:6558–6565CrossRefGoogle Scholar
  36. Maruyama M, Parker J (2017) Deep-time convergence in rove beetle symbionts of army ants. Curr Biol 27:920–926.  https://doi.org/10.1016/j.cub.2017.02.030 CrossRefPubMedGoogle Scholar
  37. Maschwitz U, Hänel H (1985) The migrating herdsman Dolichoderus (Diabolus) cuspidatus: an ant with a novel life mode. Behav Ecol Sociobiol 17:171–184Google Scholar
  38. Mynhardt G (2013) Declassifying myrmecophily in the Coleoptera to promote the study of ant-beetle symbioses. Psyche 2013:1–8CrossRefGoogle Scholar
  39. Nunn CL, Altizer S, Sechrest W, Jones KE, Barton R, Gittleman JL (2004) Parasites and the evolutionary diversification of primate clades. Am Nat 164:90–103.  https://doi.org/10.1086/424608 CrossRefGoogle Scholar
  40. Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19:207–233CrossRefGoogle Scholar
  41. Oliver TH, Leather SR, Cook JM (2008) Macroevolutionary patterns in the origin of mutualisms involving ants. J Evol Biol 21:1597–1608CrossRefGoogle Scholar
  42. Ollerton J, McCollin D, Fautin DG, Allen GR (2007) Finding NEMO: nestedness engendered by mutualistic organization in anemonefish and their hosts. Proc R Soc B 274:591–598CrossRefGoogle Scholar
  43. Parker J, Grimaldi DA (2014) Specialized myrmecophily at the ecological dawn of modern ants. Curr Biol 24:2428–2434.  https://doi.org/10.1016/j.cub.2014.08.068 CrossRefPubMedGoogle Scholar
  44. Parker J (2016) Myrmecophily in beetles (Coleoptera): evolutionary patterns and biological mechanisms. Myrmecol News 22:65–108Google Scholar
  45. Papstamatiou TP, Wetherbee BM, O’Sullivan J, Goodmanlowe GD, Lowe CG (2010) Foraging ecology of Cookiecutter Sharks (Isistius brasiliensis) on pelagic fishes in Hawaii, inferred from prey bite wounds. Environ Biol Fishes 88:361–368CrossRefGoogle Scholar
  46. Pellissier L, Kostikova A, Litsios G, Salamin N, Alvarez N (2017) High rate of protein coding sequence evolution and species diversification in the Lycaenids. Front Ecol Evol 5:1–7CrossRefGoogle Scholar
  47. Poore AGB, Hill NA, Sotka EE (2008) Phylogenetic and geographic variation in host breadth and composition by herbivorous amphipods in the family Ampithoidae. Evolution 62:21–38PubMedGoogle Scholar
  48. Porter SD (1998) Biology and behaviour of Pseudacteon decapitating flies (Diptera: Phoridae) that parasitize Solenopsis fire ants (Hymenoptera: Formicidae). Fla Entomol 81:292–309CrossRefGoogle Scholar
  49. Poulin R (1999) The functional importance of parasites in animal communities: many roles at many levels? Int J Parasitol 29:903–914CrossRefGoogle Scholar
  50. Poulin R (2004) Macroecological patterns of species richness in parasite assemblages. Basic Appl Ecol 5:423–434CrossRefGoogle Scholar
  51. Poulin R, Krasnov BR, Mouillot D (2011) Host specificity in phylogenetic and geographic space. Trends Parasitol 27:355–361CrossRefGoogle Scholar
  52. Price PW (1980) Evolutionary biology of parasites. Princeton University Press, New JerseyGoogle Scholar
  53. Proctor H, Owens I (2000) Mites and birds: diversity. Parasit Coevol TREE 15:358–364Google Scholar
  54. Ramirez W (1970) Host specificity of fig wasps (Agaonidae). Evolution 24:680–691CrossRefGoogle Scholar
  55. 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 58:281–292CrossRefGoogle Scholar
  56. Rodrigues D, Kaminski LA, Freitas AVL, Oliveira PS (2010) Trade-offs underlying polyphagy in a facultative ant-tended florivorous butterfly: the role of host plant quality and enemy-free space. Oecologia 163:719–728CrossRefGoogle Scholar
  57. Rubin BER, Moreau CS (2016) Comparative genomics reveals convergent rates of evolution in ant–plant mutualisms. Nature Commun 7:1–11CrossRefGoogle Scholar
  58. Sakagami SF, Inoue T, Yamane S, Salmah S (1989) Nest of the myrmecophilous stingless bee Trigona moorei: how do bees initiate their nest within an arboreal ant nest? Biotropica 21:265–274CrossRefGoogle Scholar
  59. Sala M, Casacci LP, Balletto E, Bonelli S, Barbero F (2014) Variation in butterfly larval acoustics as a strategy to infiltrate and exploit host ant colony resources, PLoS One.  https://doi.org/10.1371/journal.pone.0094341 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Sanchez-Pena S, Davis DR, Mueller UG (2003) A gregarious, mycophagous, myrmecophilous moth, Amydria anceps Walsingham (Lepidoptera: Acrophidae), living in Atta mexicana (Smith F) (Hymenoptera: Formicidae) spent fungal culture accumulations. Proc Entomol Soc Wash 105:186–194Google Scholar
  61. Sanders CJ (1964) The biology of carpenter ants in New Brunswick. Can Entomol 96:894–909CrossRefGoogle Scholar
  62. Schär S, Vorburger C (2013) Host specialization of parasitoids and their hyperparasitoids on a pair of syntopic aphid species. Bull Entomol Res 103:530–537CrossRefGoogle Scholar
  63. Schneider SA, LaPolla JS (2011) Systematics of the mealybug tribe Xenococcini (Hemiptera: Coccoidea: Pseudococcidae), with a discussion of trophobiotic associations with Acropyga Roger ants. Syst Entomol 36:57–82CrossRefGoogle Scholar
  64. Schönrogge K, Wardlaw JC, Thomas JA, Thomas GW (2000) Polymorphic growth rates in myrmecophilous insects. Proc R Soc Lond B Biol Sci 267:771–777CrossRefGoogle Scholar
  65. Smith CR, Oettler J, Kay A, Deans C (2007) First recorded mating flight of the hypogeic ant, Acropyga epedana, with its obligate mutualist mealybug, Rhizoecus colombiensis. J Insect Sci 7:1–5CrossRefGoogle Scholar
  66. Stadler B, Dixon AFG (1999) Ant attendance in aphids: why different degrees of myrmecophily? Ecol Entomol 24:363–369CrossRefGoogle Scholar
  67. Tegelaar K, Hagman M, Glinwood R, Pattersson J, Leimar O (2012) Ant–aphid mutualism: the influence of ants on the aphid summer cycle. Oikos 121:61–66CrossRefGoogle Scholar
  68. Thomas JA, Elmes GW (2004) Higher productivity at the cost of increased host–specificity when Maculinea butterfly larvae exploit ant colonies through trophollaxis rather than by predation. Ecological Entomology 23:457–464CrossRefGoogle Scholar
  69. Thompson JN (1994) The coevolutionary process. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  70. Van Klinken RD (2000) Host specificity testing: why do we do it and how we can do it better. In: Van Driesche R, Heard TA, McClay AS, Reardon R (eds), Proceedings of session: host specificity testing of exotic arthropod biological control agents—the biological basis for improvement in safety. USDA Forest Service, Publication #FHTET-99-1, Morgantown, pp 54–68Google Scholar
  71. Voigt CC, Kelm DH (2006) Host preference of the common vampire bat (Desmodus rotundus; Chiroptera) assessed by stable isotopes. J Mammal 87:1–6CrossRefGoogle Scholar
  72. von Beeren C, Maruyama M, Hashim R, Witte V (2011) Differential host defense against multiple parasites in ants. Evol Ecol 25:259–276CrossRefGoogle Scholar
  73. Werner G, Guven S (2007) GLM basic modeling: avoiding common pitfalls. Casualty Actuarial Society Forum. United Book Press, Baltimore, MD, pp 257–272Google Scholar
  74. Witek M, Śliwińska EB, Skórka P, Nowicki P, Wantuch M, Vrabec V, Settele J, Woyciechowski M (2008) Host ant specificity of large blue butterflies Phengaris (Maculinea) (Lepidoptera: Lycaenidae) inhabiting humid grasslands in east–central Europe. Eur J Entomol 105:871–877CrossRefGoogle Scholar
  75. Witte V, Foitzik S, Hashim R, Maschwitz U, Schulz S (2009) Fine tuning of social integration by two myrmecophiles of the ponerine army ant, Leptogenys distinguenda. J Chem Ecol 35:355–367CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Evolution and Ecology Research Centre, School of Biological, Earth and Environmental SciencesUniversity of New South WalesSydneyAustralia
  2. 2.Centre for Ecosystem Studies, School of Biological, Earth and Environmental SciencesUniversity of New South WalesSydneyAustralia

Personalised recommendations