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


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.

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  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 266:1419–1426

  2. Baker AC (2003) Flexibility and specificity in coral–algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst 34:661–689

  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. Accessed Dec 2016

  4. Blüthgen N, Mezger D, Linsenmair KE (2006) Ant–hemipteran trophobioses in a Bornean rainforest diversity, specificity and monopolisation. Insectes Soc 53:194–203

  5. Boucher DH, James S, Keeler KH (1982) The ecology of mutualism. Annu Rev Ecol Syst 13:315–317

  6. Brockmann HJ, Barnard CJ (1979) Kleptoparasitism in birds. Anim Behav 27:487–514

  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 60:31–41

  8. Chamberlain SA, Holland JN (2009) Quantitative synthesis of context dependency in ant-plant protection mutualisms. Ecology 90:2384–2392

  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 58:207–224

  10. Delabie JHC (2001) Trophiobiosis between Formicidae and Hemiptera (Sternorrhyncha and Auchenorrhyncha): an overview. Neotropical Entomol 30:501–516

  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 60:315–327

  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 24:239–246

  13. Fleming TH, Holland JN (1998) The evolution of obligate pollination mutualisms: senita cactus and senita moth. Oecologia 114:368–375

  14. Fielder K (1996) Host-plant relationships of lycaenid butterflies: large-scale patterns, interactions with plant chemistry, and mutualism with ants. Entomol Exp Appl 80:259–267

  15. Glasier JRN, Acorn JH (2013) First record of the myrmecophilous sap beetle Amphotis ulkei Leconte (Coleoptera: Nitidulidae) in Canada. Coleopterists Bull 67:188–189

  16. Gray B (1971) Note on the biology of the ant species Myrmecia dispar (Clark) (Hymenoptera: Formicidae). Insectes Soc 2:71–80

  17. Hoeksema JD, Bruna EM (2000) Pursuing the big questions about interspecific mutualism: a review of theoretical approaches. Oecologia 125:321–330

  18. Hölldobler B (1971) Communications between ants and their guests. Sci Am 224:86–93

  19. Hölldobler B, Wilson EO (1990) The ants. The Belknap Press of Harvard University Press, Cambridge

  20. Hughes DP, Pierce NE, Boomsma JJ (2008) Social insect symbionts: evolution in homeostatic fortresses. Trends Ecol Evol 23:672–677

  21. Ivens ABF (2015) Cooperation and conflict in ant (Hymenoptera: Formicidae) farming mutualisms—a review. Myrmecol News 21:19–36

  22. Jackson DE, Ratnieks FLW (2006) Communication in ants. Curr Biol 16:570–574

  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 176:322–334

  24. Kaminski LA, Rodrigues DA (2011) Species-specific levels of ant attendance mediate performance costs in a facultative myrmecophilous butterfly. Physiol Entomol 36:208–214

  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 37:689–697

  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 277:2756–2774

  27. Kindlmann P, Hulle M, Stadler B (2007) Timing of dispersal: effect of ants on aphids. Oecologia 152:625–631

  28. Kistner DH (1982) The social insects’ bestiary. In: Hermann HR (ed) Social insects, pp 1–244. Academic Press, New York

  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 56:389–396

  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 41:33–41

  31. Kronauer DJC, Pierce NE (2011) Myrmecophiles. Curr Biol 21:208–209

  32. Lapeva-Gjonova A, Rücker WH (2011) Latridiidae and Endomychidae beetles (Coleoptera) from ant nests in Bulgaria. Latridiidae 8:1–8

  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 49:149–152

  34. Loiacono MS, Margaria CB, Aquino DA (2013) Diapriinae wasps (Hymenoptera: Diaprioidea: Diapriidae) associated with ants (Hymenoptera: Formicidae) in Argentina. Psyche 2013:1–11

  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 102:6558–6565

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

  37. Maschwitz U, Hänel H (1985) The migrating herdsman Dolichoderus (Diabolus) cuspidatus: an ant with a novel life mode. Behav Ecol Sociobiol 17:171–184

  38. Mynhardt G (2013) Declassifying myrmecophily in the Coleoptera to promote the study of ant-beetle symbioses. Psyche 2013:1–8

  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.

  40. Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19:207–233

  41. Oliver TH, Leather SR, Cook JM (2008) Macroevolutionary patterns in the origin of mutualisms involving ants. J Evol Biol 21:1597–1608

  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 274:591–598

  43. Parker J, Grimaldi DA (2014) Specialized myrmecophily at the ecological dawn of modern ants. Curr Biol 24:2428–2434.

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

  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 88:361–368

  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 5:1–7

  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 62:21–38

  48. Porter SD (1998) Biology and behaviour of Pseudacteon decapitating flies (Diptera: Phoridae) that parasitize Solenopsis fire ants (Hymenoptera: Formicidae). Fla Entomol 81:292–309

  49. Poulin R (1999) The functional importance of parasites in animal communities: many roles at many levels? Int J Parasitol 29:903–914

  50. Poulin R (2004) Macroecological patterns of species richness in parasite assemblages. Basic Appl Ecol 5:423–434

  51. Poulin R, Krasnov BR, Mouillot D (2011) Host specificity in phylogenetic and geographic space. Trends Parasitol 27:355–361

  52. Price PW (1980) Evolutionary biology of parasites. Princeton University Press, New Jersey

  53. Proctor H, Owens I (2000) Mites and birds: diversity. Parasit Coevol TREE 15:358–364

  54. Ramirez W (1970) Host specificity of fig wasps (Agaonidae). Evolution 24:680–691

  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 58:281–292

  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 163:719–728

  57. Rubin BER, Moreau CS (2016) Comparative genomics reveals convergent rates of evolution in ant–plant mutualisms. Nature Commun 7:1–11

  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 21:265–274

  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.

  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 105:186–194

  61. Sanders CJ (1964) The biology of carpenter ants in New Brunswick. Can Entomol 96:894–909

  62. Schär S, Vorburger C (2013) Host specialization of parasitoids and their hyperparasitoids on a pair of syntopic aphid species. Bull Entomol Res 103:530–537

  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 36:57–82

  64. Schönrogge K, Wardlaw JC, Thomas JA, Thomas GW (2000) Polymorphic growth rates in myrmecophilous insects. Proc R Soc Lond B Biol Sci 267:771–777

  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 7:1–5

  66. Stadler B, Dixon AFG (1999) Ant attendance in aphids: why different degrees of myrmecophily? Ecol Entomol 24:363–369

  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 121:61–66

  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 23:457–464

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

  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 54–68

  71. Voigt CC, Kelm DH (2006) Host preference of the common vampire bat (Desmodus rotundus; Chiroptera) assessed by stable isotopes. J Mammal 87:1–6

  72. von Beeren C, Maruyama M, Hashim R, Witte V (2011) Differential host defense against multiple parasites in ants. Evol Ecol 25:259–276

  73. Werner G, Guven S (2007) GLM basic modeling: avoiding common pitfalls. Casualty Actuarial Society Forum. United Book Press, Baltimore, MD, pp 257–272

  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 105:871–877

  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 35:355–367

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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.

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Correspondence to J. R. N. Glasier.

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Glasier, J.R.N., Poore, A.G.B. & Eldridge, D.J. Do mutualistic associations have broader host ranges than neutral or antagonistic associations? A test using myrmecophiles as model organisms. Insect. Soc. 65, 639–648 (2018).

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  • Symbiotic associations
  • Myrmecophiles
  • Host range
  • Symbionts