Oecologia

, Volume 160, Issue 3, pp 551–561 | Cite as

Host range evolution is not driven by the optimization of larval performance: the case of Lycaeides melissa (Lepidoptera: Lycaenidae) and the colonization of alfalfa

  • Matthew L. Forister
  • Chris C. Nice
  • James A. Fordyce
  • Zachariah Gompert
Plant-Animal Interactions - Original Paper

Abstract

Herbivorous insects that have recently incorporated novel hosts into their diet provide unique opportunities for understanding factors that promote or constrain the evolution of niche breadth. Lycaeides melissa has colonized both cultivated and feral alfalfa (Medicago sativa) throughout much of North America within the past 200 years. We investigated the quality of the novel host as a resource for juvenile development, and asked if the novel host is a preferred host for oviposition relative to a native host (Astragalus canadensis). Larval-performance and oviposition-preference were examined using L. melissa individuals from a population associated with both M. sativa and A. canadensis, and oviposition-preference was also examined in another population associated exclusively with M. sativa. In addition, we investigated the effects of M. sativa and A. canadensis flowers on both preference and performance. Only one of the hosts, M. sativa, has flowers that are accessible to nectaring butterflies, and we hypothesized that the presence of flowers could affect female behavior. We find that the novel host is a relatively poor larval resource: adults that were reared as larvae on M. sativa were roughly one-third the size of adults that were reared on the native host, A. canadensis. The native host, Astragalus canadensis, is the preferred host in choice experiments involving only foliage. However, when flowers were included in preference assays, the native and novel hosts received similar numbers of eggs. Thus, the presence of flowers on hosts in the field might influence the utilization of a novel and inferior larval resource. These results are consistent with a model in which host shifts are driven by adult behavior that does not directly optimize larval performance.

Keywords

Niche breadth Niche shift Preference Performance Specialization 

References

  1. Adler LS, Bronstein JL (2004) Attracting antagonists: does floral nectar increase leaf herbivory? Ecology 85:1519–1526CrossRefGoogle Scholar
  2. Atsatt PR (1981) Ant-dependent food plant-selection by the mistletoe butterfly Ogyris amaryllis (Lycaenidae). Oecologia 48:60–63CrossRefGoogle Scholar
  3. Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844PubMedCrossRefGoogle Scholar
  4. Axen AH, Pierce NE (1998) Aggregation as a cost-reducing strategy for lycaenid larvae. Behav Ecol 9:109–115CrossRefGoogle Scholar
  5. Barron AB (2001) The life and death of Hopkins’ host-selection principle. J Insect Behav 14:725–737CrossRefGoogle Scholar
  6. Berenbaum M, Feeny P (2008) Chemical mediation of host-plant specialization: the Papilionid paradigm. In: Tilmon KJ (ed) Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects. University of California Press, BerkeleyGoogle Scholar
  7. Bernays EA, Graham M (1988) On the evolution of host specificity in phytophagous arthropods. Ecology 69:886–892CrossRefGoogle Scholar
  8. Brommer JE, Fred MS (1999) Movement of the Apollo butterfly Parnassius apollo related to host plant and nectar plant patches. Ecol Entomol 24:125–131CrossRefGoogle Scholar
  9. Brues CT (1924) The specificity of food-plants in the evolution of phytophagous insects. Am Nat 58:127–144CrossRefGoogle Scholar
  10. Carroll SP, Dingle H, Klassen SP (1997) Genetic differentiation of fitness-associated traits among rapidly evolving populations of the soapberry bug. Evolution 51:1182–1188CrossRefGoogle Scholar
  11. Castillo-Chavez C, Levin SA, Gould F (1988) Physiological and behavioral adaptation to varying environments: a mathematical model. Evolution 42:986–994CrossRefGoogle Scholar
  12. Chew FS (1977) Coevolution of pierid butterflies and their cruciferous foodplants. II. Evolution 31:568–579CrossRefGoogle Scholar
  13. Conover WJ (1999) Practical nonparametric statistics. Wiley, New YorkGoogle Scholar
  14. Courtney SP, Kibota TT (1990) Mother doesn’t know best: selection of hosts by ovipositing insects. In: Bernays EA (ed) Insect-plant interactions. CRC Press, Boca Raton, pp 161–188Google Scholar
  15. Dethier VG (1954) Evolution of feeding preferences in phytophagous insects. Evolution 8:33–54CrossRefGoogle Scholar
  16. Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608CrossRefGoogle Scholar
  17. Feder JL (1998) The apple maggot fly, Rhagoletis pomonella: flies in the face of conventional wisdom about speciation? In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, New York, pp 130–144Google Scholar
  18. Fox LR, Eisenbach J (1992) Contrary choices: possible exploitation of enemy-free space by herbivorous insects in cultivated vs. wild crucifers. Oecologia 89:574–579Google Scholar
  19. Fraenkel G (1959) The raison d’etre of secondary plant substances. Science 129:1466–1470PubMedCrossRefGoogle Scholar
  20. Fraser AM, Tregenza T, Wedell N, Elgar MA, Pierce NE (2002) Oviposition tests of ant preference in a myrmecophilous butterfly. J Evol Biol 15:861–870CrossRefGoogle Scholar
  21. Fry JD (1993) The general vigor problem—can antagonistic pleiotropy be detected when genetic covariances are positive. Evolution 47:327–333CrossRefGoogle Scholar
  22. Futuyma DJ, Mitter C (1996) Insect-plant interactions: the evolution of component communities. Philos Trans R Soc Lond B 351:1361–1366CrossRefGoogle Scholar
  23. Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19:207–233CrossRefGoogle Scholar
  24. Gompert Z, Fordyce JA, Forister ML, Shapiro AM, Nice CC (2006) Homoploid hybrid speciation in an extreme habitat. Science 314:1923–1925PubMedCrossRefGoogle Scholar
  25. Gratton C, Welter SC (1999) Does “enemy-free space” exist? Experimental host shifts of an herbivorous fly. Ecology 80:773–785Google Scholar
  26. Graves SD, Shapiro AM (2003) Exotics as host plants of the California butterfly fauna. Biol Conserv 110:413–433CrossRefGoogle Scholar
  27. Groman JD, Pellmyr O (2000) Rapid evolution and specialization following host colonization in a yucca moth. J Evol Biol 13:223–236CrossRefGoogle Scholar
  28. Grossmueller DW, Lederhouse RC (1987) The role of nectar source distribution in habitat use and oviposition by the tiger swallowtail butterfly. J Lepid Soc 41:159–165Google Scholar
  29. Hsiao TH (1978) Host plant adaptations among geographic populations of the Colorado potato beetle. Entomol Exp Appl 24:237–247CrossRefGoogle Scholar
  30. Jaenike J (1990) Host specialization in phytophagous insects. Annu Rev Ecol Syst 21:243–273CrossRefGoogle Scholar
  31. Jaenike J, Holt RD (1991) Genetic variation for habitat preference: evidence and explanations. Am Nat 137:S67–S90Google Scholar
  32. Janz N (2005) The relationship between habitat selection and preference for adult and larval food resources in the polyphagous butterfly Vanessa cardui (Lepidoptera: Nympalidae). J Insect Behav 18:767–780CrossRefGoogle Scholar
  33. Jeffries MJ, Lawton JH (1984) Enemy free space and the structure of ecological communities. Biol J Linn Soc 23:269–286CrossRefGoogle Scholar
  34. Jermy T (1984) Evolution of insect host plant relationships. Am Nat 124:609–630CrossRefGoogle Scholar
  35. Joshi A, Thompson JN (1995) Trade-offs and the evolution of host specialization. Evol Ecol 9:82–92CrossRefGoogle Scholar
  36. Karban R (1997) Neighborhood affects a plant’s risk of herbivory and subsequent success. Ecol Entomol 22:433–439CrossRefGoogle Scholar
  37. Karowe DN (1990) Predicting host range evolution: colonization of Coronilla varia by Colias philodice (Lepidoptera, Pieridae). Evolution 44:1637–1647CrossRefGoogle Scholar
  38. Labandeira CC, Dilcher DL, Davis DR, Wagner DL (1994) 97-million years of angiosperm-insect association: paleobiological insights into the meaning of coevolution. Proc Natl Acad Sci USA 91:12278–12282PubMedCrossRefGoogle Scholar
  39. Levins R, MacArthur RH (1969) An hypothesis to explain the incidence of monophagy. Ecology 50:910–911CrossRefGoogle Scholar
  40. Littell RC, Milliken WW, Wolfinger RD (1996) SAS system for mixed models. SAS Institute, CaryGoogle Scholar
  41. Mayhew PJ (1997) Adaptive patterns of host-plant selection by phytophagous insects. Oikos 79:417–428CrossRefGoogle Scholar
  42. Mayhew PJ (2001) Herbivore host choice and optimal bad motherhood. Trends Ecol Evol 16:165–167PubMedCrossRefGoogle Scholar
  43. Michaud R, Lehman WF, Rumbaugh MD (1988) World distribution and historical developments. In: Hanson AA, Barnes DK, Hill RR (eds) Alfalfa and alfalfa improvement, vol 29. ASA-CSSA-SSSA, Madison, pp 25–56Google Scholar
  44. Moon DC, Stiling P (2006) Trade-off in oviposition strategy: choosing poor quality host plants reduces mortality from natural enemies for a salt marsh plant hopper. Ecol Entomol 31:236–241CrossRefGoogle Scholar
  45. Murphy SM (2004) Enemy-free space maintains swallowtail butterfly host shift. Proc Natl Acad Sci USA 101:18048–18052PubMedCrossRefGoogle Scholar
  46. Murphy SM, Feeny P (2006) Chemical facilitation of a naturally occurring host shift by Papilio machaon butterflies (Papilionidae). Ecol Monogr 76:399–414CrossRefGoogle Scholar
  47. Nice CC, Shapiro AM (1999) Molecular and morphological divergence in the butterfly genus Lycaeides (Lepidoptera: Lycaenidae) in North America: evidence of recent speciation. J Evol Biol 12:936–950CrossRefGoogle Scholar
  48. Nice CC, Fordyce JA, Shapiro AM, Ffrench-Constant R (2002) Lack of evidence for reproductive isolation among ecologically specialised lycaenid butterflies. Ecol Entomol 27:702–712CrossRefGoogle Scholar
  49. Rosenheim JA, Jepsen SJ, Matthews CE, Smith DS, Rosenheim MR (2008) Time limitation, egg limitation, the cost of oviposition, and lifetime reproduction by an insect in nature. Am Nat 172:486–496PubMedCrossRefGoogle Scholar
  50. SAS Institute (2007) JMP version 7.0. SAS Institute, CaryGoogle Scholar
  51. Scheirs J, De Bruyn L (2002) Integrating optimal foraging and optimal oviposition theory in plant-insect research. Oikos 96:187–191CrossRefGoogle Scholar
  52. Scheirs J, De Bruyn L, Verhagen R (2000) Optimization of adult performance determines host choice in a grass miner. Proc R Soc Lond B 267:2065–2069CrossRefGoogle Scholar
  53. Shapiro AM (1980) The opportunistic origin of a new citrus pest. Calif Agric 34:4–5Google Scholar
  54. Singer MS, Stireman JO (2005) The tri-trophic niche concept and adaptive radiation of phytophagous insects. Ecol Lett 8:1247–1255CrossRefGoogle Scholar
  55. Singer MC, Vasco D, Parmesan C, Thomas CD, Ng D (1992) Distinguishing between preference and motivation in food choice: an example from insect oviposition. Anim Behav 44:463–471CrossRefGoogle Scholar
  56. Singer MC, Thomas CD, Parmesan C (1993) Rapid human-induced evolution of insect host associations. Nature 366:681–683CrossRefGoogle Scholar
  57. Singer MC, Wee B, Hawkins S, Butcher M (2008) Rapid natural and anthropogenic diet evolution: three examples from checkerspot butterflies. In: Tilmon KJ (ed) Specialization, speciation, and radiation: the evolutionary biology of herbivorous insects. The University of California Press, BerkeleyGoogle Scholar
  58. Tabashnik BE (1983) Host range evolution—the shift from native legume hosts to alfalfa by the butterfly, Colias philodice eriphyle. Evolution 37:150–162CrossRefGoogle Scholar
  59. Thomas JA, Elmes GW (2001) Food-plant niche selection rather than the presence of ant nests explains oviposition patterns in the myrmecophilous butterfly genus Maculinea. Proc R Soc Lond B 268:471–477CrossRefGoogle Scholar
  60. Thomas CD, Ng D, Singer MC, Mallet JLB, Parmesan C, Billington HL (1987) Incorporation of a European weed into the diet of a North-American herbivore. Evolution 41:892–901CrossRefGoogle Scholar
  61. Thompson JN (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol Exp Appl 47:3–14CrossRefGoogle Scholar
  62. Thompson JN, Pellmyr O (1991) Evolution of oviposition behavior and host preference in Lepidoptera. Annu Rev Entomol 36:65–89CrossRefGoogle Scholar
  63. Wackers FL, Romeis J, van Rijn P (2007) Nectar and pollen feeding by insect herbivores and implications for multitrophic interactions. Annu Rev Entomol 52:301–323PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Matthew L. Forister
    • 1
  • Chris C. Nice
    • 2
  • James A. Fordyce
    • 3
  • Zachariah Gompert
    • 4
  1. 1.Department of Biology/MS 314University of NevadaRenoUSA
  2. 2.Department of Biology, Population and Conservation Biology ProgramTexas State UniversitySan MarcosUSA
  3. 3.Department of Ecology and Evolutionary BiologyUniversity of TennesseeKnoxvilleUSA
  4. 4.Department of Botany, Program in EcologyUniversity of WyomingLaramieUSA

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