Evolutionary Ecology

, Volume 28, Issue 6, pp 1075–1093 | Cite as

Host plant specialization in the generalist moth Heliothis virescens and the role of egg imprinting

  • Anne Karpinski
  • Sabine Haenniger
  • Gerhard Schöfl
  • David G. Heckel
  • Astrid T. Groot
Original Paper


Even though generalist insects are able to feed on many different host plants, local specialization may occur, which could lead to genetic differentiation. In this paper we assessed the level and extent of host plant specialization in the generalist herbivore Heliothis virescens Fabricius (Lepidoptera, Noctuidae). This generalist can grow and survive on many different plant species, belonging to more than 37 families. Previously, two laboratory strains were described that differ in their performance on cotton and chickpea. In this study we explored this phenomenon further. Specifically, we asked the following questions: (1) Do the two strains still differ in their performance on cotton and chickpea? Since we found that the most pronounced difference between the two strains was in their growth on fresh chickpea leaves, we then asked: (2) Does this variation in performance have a genetic basis? In our genetic analysis, we found that growth rates changed over time and that two linkage groups significantly affected the ability to grow on chickpea. One QTL was homologous to Bombyx mori chromosome 15, onto which genes for insecticide resistance and detoxicative enzymes have previously been mapped. (3) Is there a difference in oviposition preference between the two strains? Oviposition experiments revealed no preference in either strain when females were reared on the same artificial diet. However, we did find a maternal inheritance of oviposition preference: daughters collected as eggs from cotton oviposited significantly more eggs on cotton, and daughters collected as eggs from chickpea likewise laid more eggs on chickpea. Thus, Hopkins’ host selection principle seems to holds in this species, although imprinting seems to happen not at the larval but at the egg stage, which is a new finding. This study shows how genetic and nongenetic factors can interact to shape the patterns of local specialization in a generalist herbivore.


Tobacco budworm Gossypium hirsutum Cicer arietinum Herbivore Oviposition Quantitative trait locus analysis Preference Performance Maternal imprinting 



We thank Dr. Carlos Blanco from the USDA for providing us with individuals from the MON and ARS strains, Susanne Donnerhacke and Antje Schmaltz for their help with the creation of the AFLP markers and the chromosome mapping, and Regina Seibt for the rearing of the two strains. We also thank Domenica Schnabelrauch for sequencing the selected AFLP markers. This research was partly funded by the National Science Foundation (award IOS-1052238), the W. M. Keck Center for Behavioral Biology, and the Max-Planck-Gesellschaft.

Supplementary material

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  1. Akhtar Y, Isman MB (2003) Binary mixtures of feeding deterrents mitigate the decrease in feeding deterrent response to antifeedants following prolonged exposure in the cabbage looper, Trichoplusia ni (Lepidoptera : Noctuidae). Chemoecology 13:177–182CrossRefGoogle Scholar
  2. Anderson P, Sadek MM, Larsson M, Hansson BS, Thoming G (2013) Larval host plant experience modulates both mate finding and oviposition choice in a moth. Anim Behav 85:1169–1175CrossRefGoogle Scholar
  3. Barron AB (2001) The life and death of Hopkins’ host-selection principle. J Insect Behav 14:725–737CrossRefGoogle Scholar
  4. Belknap JK, Mitchell SR, Otoole LA, Helms ML, Crabbe JC (1996) Type I and Type II error rates for quantitative trait loci (QTL) mapping studies using recombinant inbred mouse strains. Behav Genet 26:149–160PubMedCrossRefGoogle Scholar
  5. Bernays EA (1999) Plasticity and the problem of choice in food selection. Ann Entomol Soc Am 92:944–951Google Scholar
  6. Bernays EA (2001) Neural limitations in phytophagous insects: implications for diet breadth and evolution of host affiliation. Annu Rev Entomol 46:703–727PubMedCrossRefGoogle Scholar
  7. Bernays EA, Minkenberg O (1997) Insect herbivores: different reasons for being a generalist. Ecology 78:1157–1169CrossRefGoogle Scholar
  8. Blanco CA, Teran-Vargas AP, Lopez JD, Kauffman JV, Wei XK (2007) Densities of Heliothis virescens and Helicoverpa zea (Lepidoptera : Noctuidae) in three plant hosts. Fla Entomol 90:742–750CrossRefGoogle Scholar
  9. Blanco CA, Teran-Vargas AP, Abel CA, Portilla M, Rojas MG, Morales-Ramos JA, Snodgrass GL (2008) Plant host effect on the development of Heliothis virescens F. (Lepidoptera: Noctuidae). Environ Entomol 37:1538–1547PubMedCrossRefGoogle Scholar
  10. Blanco CA, Teran-Vargas AP, Lopez JD, Abel CA (2009) Incidence of Heliothis virescens on garbanzo varieties in Northwestern Mississippi. Southwest Entomol 34:61–67CrossRefGoogle Scholar
  11. Broman KW, Sen S (2009) A guide to QTL mapping with R/qtl, Vol. II. Springer, New YorkCrossRefGoogle Scholar
  12. Broman KW, Wu H, Sen S, Churchill GA (2003) R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889–890PubMedCrossRefGoogle Scholar
  13. Cahenzli F, Erhardt A (2013) Transgenerational acclimatization in an herbivore—host plant relationship. Proc R Soc B Biol Sci 280(1756):20122856CrossRefGoogle Scholar
  14. Caillaud MC, Via S (2012) Quantitative genetics of feeding behavior in two ecological races of the pea aphid, Acyrthosiphon pisum. Heredity 108:211–218PubMedCrossRefPubMedCentralGoogle Scholar
  15. Chow JK, Akhtar Y, Isman MB (2005) The effects of larval experience with a complex plant latex on subsequent feeding and oviposition by the cabbage looper moth: Trichoplusia ni (Lepidoptera: Noctuidae). Chemoecology 15:129–133CrossRefGoogle Scholar
  16. Crispo E (2008) Modifying effects of phenotypic plasticity on interactions among natural selection, adaptation and gene flow. J Evol Biol 21:1460–1469PubMedCrossRefGoogle Scholar
  17. de Jong PW, Frandsen HO, Rasmussen L, Nielsen JK (2000) Genetics of resistance against defences of the host plant Barbarea vulgaris in a Danish flea beetle population. Proc R Soc B-Biol Sci 267:1663–1670CrossRefGoogle Scholar
  18. Dres M, Mallet J (2002) Host races in plant-feeding insects and their importance in sympatric speciation. Philos Trans R Soc Lond B Biol Sci 357:471–492PubMedCrossRefPubMedCentralGoogle Scholar
  19. Dukas R (2008) Evolutionary biology of insect learning. Annu Rev Entomol 53:145–160PubMedCrossRefGoogle Scholar
  20. Emelianov I, Mallet J, Baltensweiler W (1995) Genetic differentiation in Zeiraphera diniana (Lepidoptera, Tortricidae, the larch budmoth)—polymorphism, host races or sibling species. Heredity 75:416–424CrossRefGoogle Scholar
  21. Emelianov I, Simpson F, Narang P, Mallet J (2003) Host choice promotes reproductive isolation between host races of the larch budmoth Zeiraphera diniana. J Evol Biol 16:208–218PubMedCrossRefGoogle Scholar
  22. Etges WJ, de Oliveira CC, Noor MAF, Ritchie MG (2010) Genetics of incipient speciation in Drosophila mojavensis. III. Life-history divergence in allopatry and reproductive isolation. Evolution 64:3549–3569PubMedCrossRefGoogle Scholar
  23. Fitt GP (1989) The ecology of Heliothis species in relation to agroecosystems. Annu Rev Entomol 34:17–52CrossRefGoogle Scholar
  24. Fox CW, Waddell KJ, Mousseau TA (1995) Parental host plant affects offspring life histories in a seed beetle. Ecology 76:402–411CrossRefGoogle Scholar
  25. Funk WC, Murphy MA (2010) Testing evolutionary hypotheses for phenotypic divergence using landscape genetics. Mol Ecol 19:427–430PubMedCrossRefGoogle Scholar
  26. Futuyma DJ, Moreno G (1988) The evolution of ecological specialization. Annu Rev Ecol Syst 19:207–233CrossRefGoogle Scholar
  27. Groot AT, Estock ML, Horovitz JL, Hamilton J, Santangelo RG, Schal C, Gould F (2009) QTL analysis of sex pheromone blend differences between two closely related moths: insights into divergence in biosynthetic pathways. Insect Biochem Mol Biol 39:568–577PubMedCrossRefGoogle Scholar
  28. Groot AT, Classen A, Staudacher H, Schal C, Heckel DG (2010) Phenotypic plasticity in sexual communication signal of a noctuid moth. J Evol Biol 23:2731–2738PubMedCrossRefGoogle Scholar
  29. Groot AT, Classen A, Inglis O, Blanco CA, Lopez J, Vargas AT, Schal C, Heckel DG, Schofl G (2011) Genetic differentiation across North America in the generalist moth Heliothis virescens and the specialist H. subflexa. Mol Ecol 20:2676–2692PubMedCrossRefGoogle Scholar
  30. Hawthorne DJ, Via S (2001) Genetic linkage of ecological specialization and reproductive isolation in pea aphids. Nature 412:904–907PubMedCrossRefGoogle Scholar
  31. Heckel DG (1993) Comparative genetic linkage mapping in insects. Annu Rev Entomol 38:381–408CrossRefGoogle Scholar
  32. Heidel-Fischer HM, Vogel H, Heckel DG, Wheat CW (2010) Microevolutionary dynamics of a macroevolutionary key innovation in a Lepidopteran herbivore. BMC Evol Biol 10(1):60PubMedCrossRefPubMedCentralGoogle Scholar
  33. Hendricks DE, Graham HM, Raulston JR (1973) Dispersal of sterile tobacco budworms from release points in Northeastern Mexico and Southern Texas. Environ Entomol 2:1085–1088Google Scholar
  34. Henniges-Janssen K, Reineke A, Heckel DG, Groot AT (2011a) Complex inheritance of larval adaptation in Plutella xylostella to a novel host plant. Heredity 107:421–432PubMedCrossRefPubMedCentralGoogle Scholar
  35. Henniges-Janssen K, Schofl G, Reineke A, Heckel DG, Groot AT (2011b) Oviposition of diamondback moth in the presence and absence of a novel host plant. Bull Entomol Res 101:99–105PubMedCrossRefGoogle Scholar
  36. Hilker M, Meiners T (2011) Plants and insect eggs: how do they affect each other? Phytochemistry 72:1612–1623PubMedCrossRefGoogle Scholar
  37. Hilker M, Rohfritsch O, Meiners T (2002) The plant’s response towards insect egg deposition. In: Hilker M, Meiners T (eds) Chemoecology of insect eggs and egg deposition. Blackwell Publishing Ltd., Berlin, pp 205–233Google Scholar
  38. Hora KH, Roessingh P, Menken SBJ (2005) Inheritance and plasticity of adult host acceptance in Yponomeuta species: implications for host shifts in specialist herbivores. Entomol Exp Appl 115:271–281CrossRefGoogle Scholar
  39. Jaenike J (1983) Induction of host preference in Drosophila melanogaster. Oecologia 58:320–325CrossRefGoogle Scholar
  40. Jaenike J (1990) Host specialization in phytophagous insects. Annu Rev Ecol Syst 21:243–274CrossRefGoogle Scholar
  41. Janz N, Nylin S (1997) The role of female search behaviour in determining host plant range in plant feeding insects: a test of the information processing hypothesis. Proc R Soc Lond B Biol Sci 264:701–707CrossRefGoogle Scholar
  42. Janz N, Nylin S, Wahlberg N (2006) Diversity begets diversity: host expansions and the diversification of plant-feeding insects. BMC Evol Biol 6(1):4PubMedCrossRefPubMedCentralGoogle Scholar
  43. Janz N, Soderlind L, Nylin S (2009) No effect of larval experience on adult host preferences in Polygonia c-album (Lepidoptera: Nymphalidae): on the persistence of Hopkins’ host selection principle. Ecol Entomol 34:50–57CrossRefGoogle Scholar
  44. Jones CD (2005) The genetics of adaptation in Drosophila sechellia. Genetica 123:137–145PubMedCrossRefGoogle Scholar
  45. Joyner K, Gould F (1985) Developmental consequences of cannibalism in Heliothis zea (Lepidoptera, Noctuidae). Ann Entomol Soc Am 78:24–28Google Scholar
  46. Liu SM, Zhou S, Tian L, Guo EN, Luan YX, Zhang JZ, Li S (2011) Genome-wide identification and characterization of ATP-binding cassette transporters in the silkworm, Bombyx mori. BMC Genomics 12(1):491PubMedCrossRefPubMedCentralGoogle Scholar
  47. Matsubayashi KW, Ohshima I, Nosil P (2010) Ecological speciation in phytophagous insects. Entomol Exp Appl 134:1–27CrossRefGoogle Scholar
  48. Maurya S, Singh UP, Singh DP, Singh KP, Srivastava JS (2005) Secondary metabolites of chickpea (Cicer arietinum) and their role in pathogenesis after infection by Sclerotium rolfsii. Z Pflanzenkr Pflanzenschutz 112:118–123Google Scholar
  49. Moreau J, Rahme J, Benrey B, Thiery D (2008) Larval host plant origin modifies the adult oviposition preference of the female European grapevine moth Lobesia botrana. Naturwissenschaften 95:317–324PubMedCrossRefGoogle Scholar
  50. Oppenheim SJ, Gould F, Hopper KR (2012) The genetic architecture of a complex ecological trait: host plant use in the specialist moth, Heliothis subflexa. Evolution 66:3336–3351PubMedCrossRefPubMedCentralGoogle Scholar
  51. Pashley DP (1986) Host-associated genetic differentiation in fall armyworm (Lepidoptera, Noctuidae)—a sibling species complex. Ann Entomol Soc Am 79:898–904Google Scholar
  52. Price TD, Qvarnstrom A, Irwin DE (2003) The role of phenotypic plasticity in driving genetic evolution. Proc R Soc Lond Ser B Biol Sci 270:1433–1440CrossRefGoogle Scholar
  53. Raulston JR, Wolf WW, Lingren PD, Sparks AN (1982) Migration as a factor in Heliothis management. International Proceedings workshop on Heliothis management. Patancheru, India, pp 61–73Google Scholar
  54. Raulston JR, Pair SD, Pedraza Martinez FA, Westbrook J, Sparks AN, Sanchez Valdez VM (1986) Ecological studies indicating the migration of Heliothis zea, Spodoptera frugiperda, and Heliothis virescens from Northeastern Mexico and Texas. Insect flight: dispersal and migration. Springer, Berlin, pp 204–220CrossRefGoogle Scholar
  55. Reese JC (1978) Chronic effects of plant allelochemicals on insect nutritional physiology. Entomol Exp Appl 24:625–631CrossRefGoogle Scholar
  56. Scriber JM, Larsen ML, Allen GR, Walker PW, Zalucki MP (2008) Interactions between Papilionidae and ancient Australian angiosperms: evolutionary specialization or ecological monophagy? Entomol Exp Appl 128:230–239CrossRefGoogle Scholar
  57. Sezer M, Butlin RK (1998) The genetic basis of oviposition preference differences between sympatric host races of the brown planthopper (Nilaparvata lugens). Proc R Soc B-Biol Sci 265:2399–2405CrossRefGoogle Scholar
  58. Sheck AL, Gould F (1993) The genetic basis of host range in Heliothis virescens—larval survival and growth. Entomol Exp Appl 69:157–172CrossRefGoogle Scholar
  59. Sheck AL, Gould F (1995) Genetic analysis of differences in oviposition preferences of Heliothis virescens and Heliothis subflexa (Lepidoptera, Noctuidae). Environ Entomol 24:341–347Google Scholar
  60. Sheck AL, Gould F (1996) The genetic basis of differences in growth and behavior of specialist and generalist herbivore species: selection on hybrids of Heliothis virescens and Heliothis subflexa (Lepidoptera). Evolution 50:831–841CrossRefGoogle Scholar
  61. Sheck AL, Groot AT, Ward CM, Gemeno C, Wang J, Brownie C, Schal C, Gould F (2006) Genetics of sex pheromone blend differences between Heliothis virescens and Heliothis subflexa: a chromosome mapping approach. J Evol Biol 19:600–617PubMedCrossRefGoogle Scholar
  62. Simmonds MSJ, Stevenson PC (2001) Effects of isoflavonoids from Cicer on larvae of Heliocoverpa armigera. J Chem Ecol 27:965–977PubMedCrossRefGoogle Scholar
  63. Thomas Y, Bethenod MT, Pelozuelo L, Frerot B, Bourguet D (2003) Genetic isolation between two sympatric host-plant races of the European corn borer, Ostrinia nubilalis Hubner. I. sex pheromone, moth emergence timing, and parasitism. Evolution 57:261–273PubMedGoogle Scholar
  64. Thoming G, Larsson MC, Hansson BS, Anderson P (2013) Comparison of plant preference hierarchies of male and female moths and the impact of larval rearing hosts. Ecology 94:1744–1752PubMedCrossRefGoogle Scholar
  65. Thompson JN (1988) Evolutionary genetics of oviposition preference in swallowtail butterflies. Evolution 42:1223–1234CrossRefGoogle Scholar
  66. Thompson JN, Pellmyr O (1991) Evolution of oviposition behavior and host preference in Lepidoptera. Annu Rev Entomol 36:65–89CrossRefGoogle Scholar
  67. Waldvogel M, Gould F (1990) Variation in oviposition preference of Heliothis virescens. Evolution 44:1326–1337CrossRefGoogle Scholar
  68. Wheat CW, Vogel H, Wittstock U, Braby MF, Underwood D, Mitchell-Olds T (2007) The genetic basis of a plant-insect coevolutionary key innovation. Proc Natl Acad Sci U S A 104:20427–20431PubMedCrossRefPubMedCentralGoogle Scholar
  69. Wittstock U, Agerbirk N, Stauber EJ, Olsen CE, Hippler M, Mitchell-Olds T, Gershenson J, Vogel H (2004) Successful herbivore attack due to metabolic diversion of a plant chemical defense. Proc Natl Acad Sci U S A 101:4859–4864PubMedCrossRefPubMedCentralGoogle Scholar
  70. Yu QY, Lu C, Li WL, Xiang ZH, Zhang Z (2009) Annotation and expression of carboxylesterases in the silkworm, Bombyx mori. BMC Genomics 10:553PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Anne Karpinski
    • 1
  • Sabine Haenniger
    • 1
  • Gerhard Schöfl
    • 2
  • David G. Heckel
    • 1
  • Astrid T. Groot
    • 1
    • 3
  1. 1.Department of EntomologyMax Planck Institute for Chemical EcologyJenaGermany
  2. 2.Leibniz Institute for Natural Product Research and Infection BiologyJenaGermany
  3. 3.Institute for Biodiversity and Ecosystem DynamicsUniversity of AmsterdamAmsterdamThe Netherlands

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