Skip to main content
SpringerLink
Log in

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

  • Plant-Animal Interactions - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adler LS, Bronstein JL (2004) Attracting antagonists: does floral nectar increase leaf herbivory? Ecology 85:1519–1526

    Article  Google Scholar 

  • Atsatt PR (1981) Ant-dependent food plant-selection by the mistletoe butterfly Ogyris amaryllis (Lycaenidae). Oecologia 48:60–63

    Article  Google Scholar 

  • Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844

    Article  PubMed  CAS  Google Scholar 

  • Axen AH, Pierce NE (1998) Aggregation as a cost-reducing strategy for lycaenid larvae. Behav Ecol 9:109–115

    Article  Google Scholar 

  • Barron AB (2001) The life and death of Hopkins’ host-selection principle. J Insect Behav 14:725–737

    Article  Google Scholar 

  • 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, Berkeley

    Google Scholar 

  • Bernays EA, Graham M (1988) On the evolution of host specificity in phytophagous arthropods. Ecology 69:886–892

    Article  Google Scholar 

  • Brommer JE, Fred MS (1999) Movement of the Apollo butterfly Parnassius apollo related to host plant and nectar plant patches. Ecol Entomol 24:125–131

    Article  Google Scholar 

  • Brues CT (1924) The specificity of food-plants in the evolution of phytophagous insects. Am Nat 58:127–144

    Article  Google Scholar 

  • Carroll SP, Dingle H, Klassen SP (1997) Genetic differentiation of fitness-associated traits among rapidly evolving populations of the soapberry bug. Evolution 51:1182–1188

    Article  Google Scholar 

  • Castillo-Chavez C, Levin SA, Gould F (1988) Physiological and behavioral adaptation to varying environments: a mathematical model. Evolution 42:986–994

    Article  Google Scholar 

  • Chew FS (1977) Coevolution of pierid butterflies and their cruciferous foodplants. II. Evolution 31:568–579

    Article  Google Scholar 

  • Conover WJ (1999) Practical nonparametric statistics. Wiley, New York

    Google Scholar 

  • 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 161–188

    Google Scholar 

  • Dethier VG (1954) Evolution of feeding preferences in phytophagous insects. Evolution 8:33–54

    Article  Google Scholar 

  • Ehrlich PR, Raven PH (1964) Butterflies and plants: a study in coevolution. Evolution 18:586–608

    Article  Google Scholar 

  • 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 130–144

    Google Scholar 

  • Fox LR, Eisenbach J (1992) Contrary choices: possible exploitation of enemy-free space by herbivorous insects in cultivated vs. wild crucifers. Oecologia 89:574–579

    Google Scholar 

  • Fraenkel G (1959) The raison d’etre of secondary plant substances. Science 129:1466–1470

    Article  PubMed  CAS  Google Scholar 

  • Fraser AM, Tregenza T, Wedell N, Elgar MA, Pierce NE (2002) Oviposition tests of ant preference in a myrmecophilous butterfly. J Evol Biol 15:861–870

    Article  Google Scholar 

  • Fry JD (1993) The general vigor problem—can antagonistic pleiotropy be detected when genetic covariances are positive. Evolution 47:327–333

    Article  Google Scholar 

  • Futuyma DJ, Mitter C (1996) Insect-plant interactions: the evolution of component communities. Philos Trans R Soc Lond B 351:1361–1366

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Gompert Z, Fordyce JA, Forister ML, Shapiro AM, Nice CC (2006) Homoploid hybrid speciation in an extreme habitat. Science 314:1923–1925

    Article  PubMed  CAS  Google Scholar 

  • Gratton C, Welter SC (1999) Does “enemy-free space” exist? Experimental host shifts of an herbivorous fly. Ecology 80:773–785

    Google Scholar 

  • Graves SD, Shapiro AM (2003) Exotics as host plants of the California butterfly fauna. Biol Conserv 110:413–433

    Article  Google Scholar 

  • Groman JD, Pellmyr O (2000) Rapid evolution and specialization following host colonization in a yucca moth. J Evol Biol 13:223–236

    Article  CAS  Google Scholar 

  • Grossmueller DW, Lederhouse RC (1987) The role of nectar source distribution in habitat use and oviposition by the tiger swallowtail butterfly. J Lepid Soc 41:159–165

    Google Scholar 

  • Hsiao TH (1978) Host plant adaptations among geographic populations of the Colorado potato beetle. Entomol Exp Appl 24:237–247

    Article  Google Scholar 

  • Jaenike J (1990) Host specialization in phytophagous insects. Annu Rev Ecol Syst 21:243–273

    Article  Google Scholar 

  • Jaenike J, Holt RD (1991) Genetic variation for habitat preference: evidence and explanations. Am Nat 137:S67–S90

    Google Scholar 

  • 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 18:767–780

    Article  Google Scholar 

  • Jeffries MJ, Lawton JH (1984) Enemy free space and the structure of ecological communities. Biol J Linn Soc 23:269–286

    Article  Google Scholar 

  • Jermy T (1984) Evolution of insect host plant relationships. Am Nat 124:609–630

    Article  Google Scholar 

  • Joshi A, Thompson JN (1995) Trade-offs and the evolution of host specialization. Evol Ecol 9:82–92

    Article  Google Scholar 

  • Karban R (1997) Neighborhood affects a plant’s risk of herbivory and subsequent success. Ecol Entomol 22:433–439

    Article  Google Scholar 

  • Karowe DN (1990) Predicting host range evolution: colonization of Coronilla varia by Colias philodice (Lepidoptera, Pieridae). Evolution 44:1637–1647

    Article  Google Scholar 

  • 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 91:12278–12282

    Article  PubMed  CAS  Google Scholar 

  • Levins R, MacArthur RH (1969) An hypothesis to explain the incidence of monophagy. Ecology 50:910–911

    Article  Google Scholar 

  • Littell RC, Milliken WW, Wolfinger RD (1996) SAS system for mixed models. SAS Institute, Cary

    Google Scholar 

  • Mayhew PJ (1997) Adaptive patterns of host-plant selection by phytophagous insects. Oikos 79:417–428

    Article  Google Scholar 

  • Mayhew PJ (2001) Herbivore host choice and optimal bad motherhood. Trends Ecol Evol 16:165–167

    Article  PubMed  Google Scholar 

  • 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 25–56

    Google Scholar 

  • 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 31:236–241

    Article  Google Scholar 

  • Murphy SM (2004) Enemy-free space maintains swallowtail butterfly host shift. Proc Natl Acad Sci USA 101:18048–18052

    Article  PubMed  CAS  Google Scholar 

  • Murphy SM, Feeny P (2006) Chemical facilitation of a naturally occurring host shift by Papilio machaon butterflies (Papilionidae). Ecol Monogr 76:399–414

    Article  Google Scholar 

  • 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 12:936–950

    Article  CAS  Google Scholar 

  • Nice CC, Fordyce JA, Shapiro AM, Ffrench-Constant R (2002) Lack of evidence for reproductive isolation among ecologically specialised lycaenid butterflies. Ecol Entomol 27:702–712

    Article  Google Scholar 

  • 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 172:486–496

    Article  PubMed  Google Scholar 

  • SAS Institute (2007) JMP version 7.0. SAS Institute, Cary

  • Scheirs J, De Bruyn L (2002) Integrating optimal foraging and optimal oviposition theory in plant-insect research. Oikos 96:187–191

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Shapiro AM (1980) The opportunistic origin of a new citrus pest. Calif Agric 34:4–5

    Google Scholar 

  • Singer MS, Stireman JO (2005) The tri-trophic niche concept and adaptive radiation of phytophagous insects. Ecol Lett 8:1247–1255

    Article  Google Scholar 

  • 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 44:463–471

    Article  Google Scholar 

  • Singer MC, Thomas CD, Parmesan C (1993) Rapid human-induced evolution of insect host associations. Nature 366:681–683

    Article  Google Scholar 

  • 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, Berkeley

    Google Scholar 

  • Tabashnik BE (1983) Host range evolution—the shift from native legume hosts to alfalfa by the butterfly, Colias philodice eriphyle. Evolution 37:150–162

    Article  Google Scholar 

  • 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 268:471–477

    Article  CAS  Google Scholar 

  • 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 41:892–901

    Article  Google Scholar 

  • Thompson JN (1988) Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol Exp Appl 47:3–14

    Article  Google Scholar 

  • Thompson JN, Pellmyr O (1991) Evolution of oviposition behavior and host preference in Lepidoptera. Annu Rev Entomol 36:65–89

    Article  Google Scholar 

  • Wackers FL, Romeis J, van Rijn P (2007) Nectar and pollen feeding by insect herbivores and implications for multitrophic interactions. Annu Rev Entomol 52:301–323

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank Akiko Endo and Hiroaki Zama for their assistance in rearing larvae. Thanks to Arthur Shapiro for pointing us towards the study location. We also thank two anonymous reviewers for their useful comments and suggestions. This work was supported by the University of Nevada, Reno. This study complied with the laws and regulations of the United States of America.

Author information

Authors and Affiliations

  1. Department of Biology/MS 314, University of Nevada, Reno, NV, 89557, USA

    Matthew L. Forister

  2. Department of Biology, Population and Conservation Biology Program, Texas State University, San Marcos, TX, 78666, USA

    Chris C. Nice

  3. Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN, 37996, USA

    James A. Fordyce

  4. Department of Botany, Program in Ecology, University of Wyoming, Laramie, WY, 82071, USA

    Zachariah Gompert

Authors
  1. Matthew L. Forister
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chris C. Nice
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. James A. Fordyce
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zachariah Gompert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matthew L. Forister.

Additional information

Communicated by Konrad Fiedler.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Forister, M.L., Nice, C.C., Fordyce, J.A. et al. Host range evolution is not driven by the optimization of larval performance: the case of Lycaeides melissa (Lepidoptera: Lycaenidae) and the colonization of alfalfa. Oecologia 160, 551–561 (2009). https://doi.org/10.1007/s00442-009-1310-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-009-1310-4

Keywords

Search

Navigation