Evolutionary Ecology

, 25:1205 | Cite as

Evolution of influence: signaling in a lycaenid-ant interaction

Original Paper

Abstract

Some phytophagous insects gain defense from natural enemies by associating with otherwise potentially harmful top predators. Many lycaenid butterfly caterpillars are involved in such interactions with ants: larvae provide carbohydrate rewards from the dorsal nectary organ (DNO) to associated ants in return for protection from natural enemies. The stability of these interactions involves signals that identify the lycaenid caterpillar as a mutualist. However, larvae of some lycaenid species, such as Lycaena xanthoides, are found in close association with ants but do not possess the reward producing DNO. Evaluating the relationship in a phylogenetic framework, we show that the association between L. xanthoides and ants likely evolved from a non-ant-associated ancestor. Behavioral trials also show that L. xanthoides larvae are capable of influencing ant behavior to increase ant tending when faced with a simulated predator attack, without providing DNO-derived rewards to ant associates. These results demonstrate that the DNO is not necessary to maintain associations between lycaenid larvae and ants. Third-party interactions may affect the evolution of mutualisms and consideration of underlying evolutionary history is necessary to understand contemporary species associations.

Keywords

Mutualism Myrmecophily Myrmecoxeny Character evolution Lycaena 

Supplementary material

10682_2011_9478_MOESM1_ESM.pdf (2.1 mb)
Supplementary material 1 (PDF 2084 kb)

References

  1. Agarwal AA, Fordyce JA (2000) Induced indirect defense in a lycaenid-ant association: the regulation of a resource in a mutualism. Proc R Soc Lond B 267:1857–1861CrossRefGoogle Scholar
  2. 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 R Soc Lond B 266:1419–1426CrossRefGoogle Scholar
  3. Allen TJ, Brock JP, Glassberg J (2005) Caterpillars in the field and garden: a field guide to the butterfly caterpillars of North America. Oxford University Press, OxfordGoogle Scholar
  4. Atsatt PR (1981) Lycaenid butterflies and ants: selection for enemy-free space. Am Nat 118:638–654CrossRefGoogle Scholar
  5. Ballmer GR, Pratt GF (1988) A survey of the last instar larvae of the Lycaenidae (Lepidoptera) of California. J Res Lepid 27:1–81CrossRefGoogle Scholar
  6. Ballmer GR, Pratt GF (1991) Quantification of ant attendance (myrmecophily) of lycaenid larvae. J Res Lepid 30:95–112Google Scholar
  7. Bozano GC, Weidenhoffer Z (2001) Lycaenidae part I: subfamily Lycaeninae. In: Bozano GC (ed) Guide to the butterflies of the Palearctic region. Omnes Artes, Milan, pp 1–62Google Scholar
  8. Bronstein JL (2001) The exploitation of mutualisms. Ecol Lett 4:277–287CrossRefGoogle Scholar
  9. Caterino MS, Sperling FAH (1999) Papilio phylogeny based on mitochondrial cytochrome oxidase I and II genes. Mol Phylogenet Evol 11:122–137PubMedCrossRefGoogle Scholar
  10. Cushman JH, Rashbrook VK, Beattie AJ (1994) Assessing benefits to both participants in a lycaenid-ant association. Ecology 75:1031–1041CrossRefGoogle Scholar
  11. Daniels, H. 2004. Facultative butterfly-ant interactions—the role of variation in composition of nectar secretions. Ph.D. dissertation, University of Bayreuth, BayreuthGoogle Scholar
  12. Dettner K, Liepert C (1994) Chemical mimicry and camouflage. Annu Rev Entomol 39:129–154CrossRefGoogle Scholar
  13. DeVries PJ (1984) Of crazy-ants and Curetinae: are Curetis butterflies tended by ants? Zool J Linnean Soc 80:59–66CrossRefGoogle Scholar
  14. Eliot JN (1973) The higher classification of the Lycaenidae (Lepidoptera): a tentative arrangement. Bull Brit Mus (Nat Hist), Entomol 28:1–505Google Scholar
  15. Fiedler K, Maschwitz U (1989) Functional analysis of the myrmecophilous relationships between ants (Hymenoptera: Formicidae) and Lycaenids (Lepidoptera: Lycaenidae). Ethology 80:71–80CrossRefGoogle Scholar
  16. Fiedler K, Saam C (1995) Ants benefit from attending facultatively myrmecophilous Lycaenidae caterpillars: evidence from a survival study. Oecologia 104:316–322CrossRefGoogle Scholar
  17. Fiedler K, Seufert P, Pierce NE, Pearson JG, Baumgarten H-T (1992) Exploitation of lycaenid-ant mutualisms by braconid parasitoids. J Res Lepid 31:153–168Google Scholar
  18. Fiedler K, Hölldobler B, Seufert P (1996) Butterflies and ants: the communicative domain. Experientia 52:14–24CrossRefGoogle Scholar
  19. Francoeur A (1973) Revision taxonomique des especes nearctiques du group fusca, genre Formica (Hymenoptera: Formicidae). Mem Soc Entomol Québec 3:1–316Google Scholar
  20. Fraser AM, Axén AH, Pierce NE (2001) Assessing the quality of different ant species as partners of a myrmecophilous butterfly. Oecologia 129:452–460Google Scholar
  21. Green P (1999) Phrap. http://phrap.org
  22. Green P, Ewing B (2002) Phred. http://phrap.org
  23. Gross P (1993) Insect behavioral and morphological defenses against parasitoids. Ann Rev Entomol 38:251–273CrossRefGoogle Scholar
  24. Henning FF (1983) Chemical communication between lycaenid larvae (Lepidoptera: Lycaenidae) and ants (Hymenoptera: Formicidae). J Entomol Soc S Afr 46:341–366Google Scholar
  25. Hinton HE (1951) Myrmecophilous Lycaenidae and other Lepidoptera—a summary. Proc Trans S London Entomol Nat Hist Soc 1949–50:111–175Google Scholar
  26. Hodges RW, Dominick T, Davis DR, Ferguson DC, Franclemont JG, Munroe EG, Powell JA (eds) (1983) Check list of the lepidoptera of America North of Mexico (Including Greenland). E. W. Classey Ltd. and The Wedge Entomological Research Foundation, LondonGoogle Scholar
  27. Kitching RL, Luke B (1985) The myrmecophilous organs of the larvae of some British Lycaenidae (Lepidoptera): a comparative study. J Nat Hist 19:259–276CrossRefGoogle Scholar
  28. Leimar O, Axén AH (1993) Strategic behaviour in an interspecific mutualism: interactions between lycaenid larvae and ants. Anim Behav 46:1177–1182CrossRefGoogle Scholar
  29. Maddison WP (1997) Gene trees in species trees. Syst Biol 46:523–536CrossRefGoogle Scholar
  30. Maddison WP, Knowles LL (2006) Inferring phylogeny despite incomplete lineage sorting. Syst Biol 55:21–30PubMedCrossRefGoogle Scholar
  31. Maddison DR, Maddison WP (2007a) Chromaseq: a Mesquite module for analyzing sequence chromatograms. Version 0.91. http://mesquiteproject.org/packages/chromaseq
  32. Maddison WP, Maddison DR (2007b) Mesquite: a modular system for evolutionary analysis. Version 2.0bi44. http://mesquiteproject.org
  33. Maschwitz U, Wüst M, Schurian K (1975) Bläulingsraupen als Zuckerlieferanten für Ameisen. Oecologia 18:17–21Google Scholar
  34. Megens H-J, de Jong R, Fiedler K (2005) Phylogenetic patterns in larval host plant and ant association of Indo-Australian Arhopalini butterflies (Lycaenidae: Theclinae). Biol J Linn Soc 84:225–241CrossRefGoogle Scholar
  35. Monteiro A, Pierce NE (2001) Phylogeny of Bicyclus (Lepidoptera: Nymphalidae) inferred from COI, COII and EF-1alpha gene sequences. Mol Phylogenet Evol 18:264–281PubMedCrossRefGoogle Scholar
  36. Nault LR, Montgomery ME, Bowers WS (1976) Ant-aphid association: role of aphid alarm pheromone. Science 192:1349–1351PubMedCrossRefGoogle Scholar
  37. Newcomer EJ (1912) Some observations on the relation of ants and lycaenid caterpillars, and a description of the relational organs of the latter. J NY Entomol Soc 20:31–36Google Scholar
  38. Oliver JC (2008) AUGIST: Inferring species trees while accommodating gene tree uncertainty. Bioinformatics 24:2932–2933PubMedCrossRefGoogle Scholar
  39. Oliver JC, Shapiro AM (2007) Genetic isolation and cryptic variation within the Lycaena xanthoides species group (Lepidoptera: Lycaenidae). Mol Ecol 16:4308–4320PubMedCrossRefGoogle Scholar
  40. Oliver JC, Prudic KL, Pauly GB (2007) Parasitism rates in larval Lycaena xanthoides (Godart) (Lepidoptera: Lycaenidae) and a new host record for Cotesia theclae (Riley) (Hymenoptera: Braconidae). Pan-Pac Entomol 83:262–264CrossRefGoogle Scholar
  41. Osborn F, Jaffé K (1997) Cooperation vs. exploitation: interactions between Lycaenid (Lepidoptera: Lycaenidae) larvae and ants. J Res Lepid 34:69–82Google Scholar
  42. Pasteels JM, Grégoire J-C, Rowell-Rahier M (1983) The chemical ecology of defense in arthropods. Ann Rev Entomol 28:263–289CrossRefGoogle Scholar
  43. Pierce NE (1983) Ecology and evolution of symbioses between lycaenid butterflies and ants. Ph.D. thesis, Harvard University, Cambridge, MassachusettsGoogle Scholar
  44. Pierce NE, Mead PS (1981) Parasitoids as selective agents in the symbiosis between lycaenid butterfly larvae and ants. Science 211:1185–1187PubMedCrossRefGoogle Scholar
  45. Pierce NE, Braby MF, Heath A, Lohman DJ, Mathew J, Rand DB, Travassos MA (2002) The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). Ann Rev Entomol 47:733–771CrossRefGoogle Scholar
  46. Pratt GF, Wright DM (2002) Allozyme phylogeny of North American coppers (Lycaeninae: Lycaenidae). Pan-Pac Entomol 78:219–229Google Scholar
  47. R Development Core Team (2007) R: a language and environment for statistical computing (R Foundation for Statistical Computing, Vienna, Austria) ISBN 3-900051-07-0, URL http://www.R-project.org
  48. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  49. Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack: the evolutionary ecology of crypsis, Warning Signals and Mimicry. Oxford University Press, OxfordGoogle Scholar
  50. Saarinen EV (2006) Differences in worker caste behaviour of Oecophylla smaragdina (Hymenoptera: Formicidae) in response to larvae of Anthene emolus (Lepidoptera: Lycaenidae). Biol J Linnean Soc 88:391–395CrossRefGoogle Scholar
  51. Scott JA (1986) The Butterflies of North America: a natural history and field guide. Stanford University Press, StanfordGoogle Scholar
  52. Stadler B, Dixon AFG (2005) Ecology and evolution of aphid-ant interactions. Ann Rev Ecol Evol Syst 36:345–372CrossRefGoogle Scholar
  53. Stadler B, Dixon AFG (2008) Mutualism: ants and their insect partners. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  54. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690PubMedCrossRefGoogle Scholar
  55. Stanton ML (2003) Interacting guilds: moving beyond the pairwise perspective on mutualisms. Am Nat 162:S10–S23PubMedCrossRefGoogle Scholar
  56. Travassos MA, Pierce NE (2000) Acoustics, context and function of vibrational signalling in a lycaenid butterfly–ant mutualism. Anim Behav 60:13–26PubMedCrossRefGoogle Scholar
  57. van Dorp K (2004) Molecular systematics of Lycaena F., 1807 (Lepidoptera: Lycaenidae)—Some preliminary results. Proc Neth Entomol Soc 15:65–70Google Scholar
  58. Vane-Wright RI (1976) A unified classification of mimetic resemblances. Biol J Linnean Soc 8:25–56CrossRefGoogle Scholar
  59. Wahlberg N, Braby MF, Brower AVZ, de Jong R, Lee M-M, Nylin S, Pierce NE, Sperling FAH, Vila R, Warren AD, Zakharov E (2005) Synergistic effects of combining morphological and molecular data in resolving the phylogeny of butterflies and skippers. Proc R Soc B 272:1577–1586PubMedCrossRefGoogle Scholar
  60. Weeks JA (2003) Parasitism and ant protection alter the survival of the lycaenid Hemiargus isola. Ecol Entomol 28:228–232CrossRefGoogle Scholar
  61. Wickler W (1968) Mimicry in plants and animals. McGraw-Hill Book Company, New YorkGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyYale UniversityNew HavenUSA
  2. 2.Interdisciplinary Program in Insect ScienceUniversity of ArizonaTucsonUSA
  3. 3.Department of Ecology and Evolutionary BiologyUniversity of ArizonaTucsonUSA
  4. 4.Department of Animal BiologyUniversity of IllinoisUrbanaUSA

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