Eur. J. Entomol. 113: 150-157, 2016 | 10.14411/eje.2016.019

Co-occurrence of host plants associated with plant quality determines performance patterns of the specialist butterfly, Battus polydamas archidamas (Lepidoptera: Papilionidae: Troidini)

Rodrigo S. RIOS1, Cristian SALGADO-LUARTE1, Gisela C. STOTZ2, Ernesto GIANOLI1,3
1 Departamento de Biología, Universidad de La Serena, Raúl Bitrán #1305, La Serena, IV Region de Coquimbo 1720170, Chile; e-mails: srrios@userena.cl, crisalga@gmail.com
2 Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada; e-mail: stotzgisela@gmail.com
3 Departamento de Botánica, Universidad de Concepción, Concepción, Chile; e-mail: gianoli@gmail.com

In herbivorous insects, differences in the degree of specialization to host plants emerge when the distribution of an herbivore differs from that of its host plants, which results in a mosaic of populations differing in performance on the different host plants. Using a specialized butterfly, Battus polydamas archidamas Boisduval, 1936, which feeds exclusively on the genus Aristolochia, we test whether host plant co-occurrence and associated differences in host quality modify local adaptation in terms of larval preference and performance. We compared individuals from a monospecific host stand of Aristolochia chilensis with those from a mixed host stand of A. chilensis and A. bridgesii. Individuals were reared in a reciprocal transfer experiment in which source population and the host species fed to larvae were fully crossed in a two-by-two factorial experiment in order to quantify their preference, performance (development time, size and growth rate) and survival. Individuals from both populations preferred the species they ate during their larval development over the other host, which indicates host plant-induced preference with non-adaptive implications. Larvae from mixed and monospecific stands grew faster and survived better when reared on A. bridgesii than A. chilensis. Larvae from a monospecific host stand grew slower and fewer individuals survived under the same local conditions, which is contrary to expectations. Therefore, rearing the butterfly on A. bridgesii consistently resulted in better performance, which indicates that the monospecific population is less well adapted to its host than the mixed population. Variation in the occurrence of the two host plants in the two populations can result in divergent selection due to the variation in plant quality, which in this case could result in opposing adaptive processes.

Keywords: Lepidoptera, Papilionidae, Troidini, Battus polydamas archidamas, Aristolochia, polydamas swallowtail, larval performance on host plants, host plant-induced preference, performance mosaic, plant quality

Received: March 2, 2015; Accepted: December 8, 2015; Published online: February 5, 2016

Download citation

References

  1. Agrawal A.A. 2000a: Specificity of induced resistance in wild radish: causes and consequences for two specialist and two generalist caterpillars. - Oikos 89: 493-500. Go to original source...
  2. Agrawal A.A. 2000b: Host-range evolution: adaptation and trade-offs in fitness of mites on alternative hosts. - Ecology 81: 500-508. Go to original source...
  3. Agresti A. 1996: An Introduction to Categorical Data Analysis. Wiley, New York, 400 pp.
  4. Awmack C.S. & Leather S.R. 2002: Host plant quality and fecundity in herbivorous insects. - Annu. Rev. Entomol. 47: 817-844. Go to original source...
  5. Bolnick D.I., Yang L.H., Fordyce J.A., Davis J.M. & Svanbäck R. 2002: Measuring individual-level resource specialization. Ecology 83: 2936-2941. Go to original source...
  6. Bowers M.D. 1983: The role of iridoid glycosides in host plant specificity of checkerspot butterflies. - J. Chem. Ecol. 9: 475-494. Go to original source...
  7. Bowers M.D. & Puttick G.M. 1988: Response of generalist and specialist insects to qualitative allelochemical variation. - J. Chem. Ecol. 14: 319-334. Go to original source...
  8. Crespi B.J. 2000: The evolution of maladaptation. - Heredity 84: 623-629. Go to original source...
  9. Devictor V., Clavel J., Julliard R., Lavergne S., Mouillot D., Thuiller W., Venail P., Villéger S. & Mouquet N. 2010: Defining and measuring ecological specialization. - J. Appl. Ecol. 47: 15-25. Go to original source...
  10. Ehrlich P.R. & Raven P.H. 1964: Butterflies and plants: a study in coevolution. - Evolution 18: 586-608. Go to original source...
  11. Endler J.A. 1977: Geographic Variation, Speciation and Clines. Princeton University Press, Princeton, NJ, 262 pp.
  12. Fordyce J.A., Marion Z.H. & Shapiro A.M. 2005: Phenological variation in chemical defense of the pipevine swallowtail. - J. Chem. Ecol. 31: 3835-2846. Go to original source...
  13. Fox L.R. & Morrow P.A. 1981: Specialization: Species property or local phenomenon. - Science 211: 887-893. Go to original source...
  14. Futuyma D.J. & Moreno G. 1988: The evolution of ecological specialization. - Annu. Rev. Ecol. Syst. 19: 207-233. Go to original source...
  15. Hanks L.M. & Denno R.F. 1994: Local adaptation in the armored scale insect Pseudaulacaspis pentagona (Homoptera: Diaspididae). - Ecology 75: 2301-2310. Go to original source...
  16. Hereford J. 2009: A quantitative survey of local adaptation and fitness trade-offs. - Am. Nat. 173: 579-588. Go to original source...
  17. Hougen-Eitzman D. & Rausher M.D. 1994: Interactions between herbivorous insects and plant-insect coevolution. - Am. Nat. 143: 677-697. Go to original source...
  18. How S.T., Abrahamson W.G. & Craig T.P. 1993: Role of host plant phenology in host use by Eurosta solidaginis (Diptera: Tephritidae) on Solidago (Compositae). - Environ. Entomol. 22: 388-396. Go to original source...
  19. Jaenike J. 1978: On optimal oviposition behaviour in phytophagous insects. - Theor. Popul. Biol. 14: 350-356. Go to original source...
  20. Jaenike J. 1990: Host specialization in phytophagous insects. - Annu. Rev. Ecol. Syst. 21: 243-273. Go to original source...
  21. Jaenike J. & Papaj D.R. 1992: Learning and patterns of host use by insects. In Isman M.B. & Roitberg B.D. (eds): Chemical Ecology: An Evolutionary Perspective. Chapman and Hall, New York, pp. 245-264.
  22. Karban R. & Agrawal A.A. 2002: Herbivore offense. - Annu. Rev. Ecol. Syst. 33: 641-664. Go to original source...
  23. Kassen R. 2002: The experimental evolution of specialists, generalists, and the maintenance of diversity. - J. Evol. Biol. 15: 173-190. Go to original source...
  24. Kawecki T.J. 1994: Accumulation of deleterious mutations and the evolutionary cost of being a generalist. - Am. Nat. 144: 833-838. Go to original source...
  25. Kawecki T.J. & Ebert D. 2004: Conceptual issues in local adaptation. - Ecol. Lett. 7: 1225-1241. Go to original source...
  26. Kraft S.A. & Denno R.F. 1982: Feeding responses of adapted and non-adapted insects of the defensive properties of Baccharis halimifolia L. (Compositae). - Oecologia 52: 156-163. Go to original source...
  27. Laukkanen L., Leimu R., Muola A., Lilley M., Salminen J.-P. & Mutikainen P. 2012: Plant chemistry and local adaptation of a specialized folivore. - PLoS ONE 7: e38225, 8 pp. Go to original source...
  28. Mayhew P.J. 2001: Herbivore host choice and optimal bad motherhood. - Trends Ecol. Evol. 16: 165-167. Go to original source...
  29. Miller J.J. & Feeny P.P. 1989: Interspecific differences among swallowtail larvae (Lepidoptera: Papilionidae) in susceptibility to aristolochic acids and berberine. - Ecol. Entomol. 14: 287-296. Go to original source...
  30. Mopper S., Beck M., Simberloff D. & Stiling P. 1995: Local adaptation and agents of selection in a mobile insect. - Evolution 49: 810-815. Go to original source...
  31. Ortegón-Campos I., Parra-Tabla V., Abdala-Roberts L. & Herrera C.M. 2009: Local adaptation of Ruellia nudiflora (Acanthaceae) to counterparts: complex scenarios revealed when two herbivore guilds are considered. - J. Evol. Biol. 22: 2288-2297. Go to original source...
  32. Peña L.E. & Ugarte A.J. 1996: Mariposas de Chile. Editorial Universitaria, Santiago, Chile, 359 pp.
  33. Pinto C.F., Troncoso A.J., Urzúa A. & Niemeyer H.M. 2009a: Use of volatiles of Aristolochia chilensis (Aristolochiaceae) in host searching by fourth-instar larvae and adults of Battus polydamas archidamas (Lepidoptera: Papilionidae: Troidini). - Eur. J. Entomol. 106: 63-68. Go to original source...
  34. Pinto C.F., Troncoso A.J., Urzúa A. & Niemeyer H.M. 2009b: Aristolochic acids affect the feeding behaviour and development of Battus polydamas archidamas larvae (Lepidoptera: Papilionidae: Troidini). - Eur. J. Entomol. 106: 357-361. Go to original source...
  35. Pinto C.F., Urzúa A. & Niemeyer H.M. 2011: Sequestration of aristolochic acids from meridic diets by larvae of Battus polydamas archidamas (Papilionidae: Troidini). - Eur. J. Entomol. 108: 41-45. Go to original source...
  36. Poisot T., Bever J.D., Nemri A., Thrall P.H. & Hochberg M.E. 2011: A conceptual framework for the evolution of ecological specialisation. - Ecol. Lett. 14: 841-851. Go to original source...
  37. Poonam V.K., Prasad A.K. & Parmar V.S. 2003: Naturally occurring aristolactams, aristolochic acids and dioxoaporphines and their biological activities. - Prod. Rep. 20: 565-583. Go to original source...
  38. R Core Team 2013: R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria, URL: http://www.Rproject.org/.
  39. Rausher M.D. 1981: Host plant selection by Battus philenor butterflies: the roles of predation, nutrition, and plant chemistry. - Ecol. Monogr. 51: 1-20. Go to original source...
  40. Reznick D.N. & Ghalambor C.K. 2001: The population ecology of contemporary adaptations: what empirical studies reveal about the conditions that promote adaptive evolution. - Genetica 112-113: 183-198. Go to original source...
  41. Riedemann P., Aldunate G. & Teillier S. 2006: Flora Nativa de Valor Ornamental: Identificación y Propagación Chile Zona Norte. Productora Gráfica Andros, Chile, 404 pp.
  42. Sachdev-Gupta K., Feeny P.P. & Carter M. 1993: Oviposition stimulants for the pipevine swallowtail butterfly, Battus philenor (Papilionidae), from an Aristolochia host plant: synergism between inositols, aristolochic acids and monogalactosyl diglyceride. - Chemoecology 4: 19-28. Go to original source...
  43. Scheirs J., De Bruyn L. & Verhagen R. 2000: Optimization of adult performance determines host choice in a grass miner. - Proc. R. Soc. Lond. (B) 267: 2065-2069. Go to original source...
  44. Scriber J.M. & Slansky F. 1981: The nutritional ecology of immature insects. - Annu. Rev. Entomol. 26: 183-211. Go to original source...
  45. Spitzer B. 2006: Local maladaptation in the soft scale insect Saissetia coffeae (Hemiptera: Coccidae). - Evolution 60: 1859-1867. Go to original source...
  46. Stotz G.C. & Gianoli E. 2013: Pollination biology and floral longevity of Aristolochia chilensis in an arid ecosystem. - Plant Ecol. Divers. 6: 181-186. Go to original source...
  47. Stotz G.C., Suárez L.H., Gonzáles W.L. & Gianoli E. 2013: Local host adaptation and use of a novel host in the seed beetle Megacerus eulophus. - PLoS ONE 8: e53892, 5 pp. Go to original source...
  48. Strauss S.Y. 1997: Lack of evidence for local adaptation to individual plant clones or site by a mobile specialist herbivore. - Oecologia 110: 77-85. Go to original source...
  49. Thompson J.N. 1999: Specific hypotheses on the geographic mosaic of coevolution. - Am. Nat. 153: 1-4. Go to original source...
  50. Thompson J.N. 2005: The Geographic Mosaic of Coevolution. University Chicago Press, Chicago, 400 pp.
  51. Thompson J.N. & Cunningham B.M. 2002: Geographic structure and dynamics of coevolutionary selection. - Nature 417: 735-738. Go to original source...
  52. Toju H. & Sota T. 2006: Imbalance of predator and prey armament: geographic clines in phenotypic interface and natural selection. - Am. Nat. 167: 105-117. Go to original source...
  53. Urzúa A., Rodríguez R. & Cassels B.K. 1987: Fate of ingested aristolochic acids in Battus polydamas archidamas. - Biochem. Syst. Ecol. 15: 687-689. Go to original source...
  54. Urzúa A., Santander R. & Sotes G. 2009: Aristoloic acids from Aristolochia bridgesii, a host-plant of Battus polydamas archidamas. - J. Chil. Chem. Soc. 54: 437-438. Go to original source...
  55. Van Zandt P.A. & Mopper S. 1998: A meta-analysis of adaptive deme formation in phytophagous insect populations. - Am. Nat. 152: 595-604. Go to original source...
  56. Via S. 1990: Ecological genetics and host adaptation in herbivorous insects: the experimental study of evolution in natural and agricultural systems. - Annu. Rev. Entomol. 35: 421-446. Go to original source...
  57. Via S. & Lande R. 1985: Genotype-environment interaction and the evolution of phenotypic plasticity. - Evolution 39: 505-522. Go to original source...
  58. Whitlock M.C. 1996: The red queen beats the jack-of-all-trades: the limitations on the evolution of phenotypic plasticity and niche breadth. - Am. Nat. 148: S65-S77. Go to original source...
  59. Zangerl A.R. & Berenbaum M.R. 2003: Phenotype matching in wild parsnips and parsnip webworms: causes and consequences. - Evolution 57: 806-815. Go to original source...