Herbivorous insects: model systems for the comparative study of speciation ecology

  • Daniel J. Funk
  • Kenneth E. Filchak
  • Jeffrey L. Feder
Part of the Contemporary Issues in Genetics and Evolution book series (CIGE, volume 9)


Does ecological divergence drive species-level evolutionary diversification? How so and to what degree? These questions were central to the thinking of the evolutionary synthesis. Only recently, however, has the ecology of speciation become an important focus of empirical study. Here, we argue that ecologically specialized, phylo- genetically diverse, and experimentally tractable herbivorous insect taxa offer great opportunities to study the myriad mechanisms by which ecology may cause reproductive isolation and promote speciation. We call for the development and integrated experimental study of a taxonomic diversity of herbivore model systems and discuss the availability and recent evaluation of suitable taxa. Most importantly, we describe a general comparative framework that can be used to rigorously test a variety of hypotheses about the relative contributions and the macroevolutionary generality of particular mechanisms. Finally, we illustrate important issues for the experimental analysis of speciation ecology by demonstrating the consequences of specialized host associations for ecological divergence and premating isolation in Neochlamisus bebbianae leaf beetles.

Key words

ecological specialization ecology of speciation host fidelity host preference host race Neochlamisus phytophagous insects pleiotropy premating isolation reproductive isolation 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Abe, Y., 1991. Host race formation in the gall wasp Andricus mukigawae. Ent. Exp. Appl. 58: 15–20.CrossRefGoogle Scholar
  2. Adams, D. & D.J. Funk, 1997. Morphometric inferences on sibling species and sexual dimorphism in Neochlamisus bebbianae leaf beetles: multivariate applications of the thin-plate spline. Syst. Biol. 46: 178–192.CrossRefGoogle Scholar
  3. Allmon, W.D., 1992. A causal analysis of stages in allopatric speciation. Oxford Surv. Evol. Biol. 9: 219–257.Google Scholar
  4. Berlocher, S.H., 1998. Can sympatric speciation through host or habitat shift be proven from phylogenetic and biogeographic evidence? pp. 99–113 in Endless Forms: Species and Speciation, edited by D.J. Howard & S.H. Berlocher. Oxford University Press, New York.Google Scholar
  5. Berlocher, S.H. & J.L. Feder, 2002. Sympatric speciation in phytophagous insects: moving beyond controversy? Ann. Rev. Entomol. 47: 773–815.CrossRefGoogle Scholar
  6. Bernays, E.A., 1998. Evolution of feeding behavior in insect herbivores. Bioscience 48: 35–44.CrossRefGoogle Scholar
  7. Bernays, E.A. & R.F. Chapman, 1994. Host-Plant Selection by Phytophagous Insects. Chapman and Hall, London.Google Scholar
  8. Bovey, P. & J.K. Maksymov, 1959. Le problème des races biologiques chez la tordeuse grise du mélèze Zeiraphera griseana (Hb.). Note préliminaire. Vierteljahrsschrift Naturforsch. Ges. Zürich. 104: 264–274.Google Scholar
  9. Brazner, J.C. & W.J. Etges, 1993. Pre-mating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. 2. effects of larval substrates on time to copulation, mate choice and mating propensity. Evol. Ecol. 7: 605–624.CrossRefGoogle Scholar
  10. Brown, W.J., 1943. The Canadian species of Exema and Arthroch-lamys (Coleoptera, Chrysomelidae). Can. Entomol. 75: 119–131.CrossRefGoogle Scholar
  11. Brown, W.J., 1946. Some new Chrysomelidae, with notes on other species (Coleoptera). Can. Entomol. 78: 47–54.CrossRefGoogle Scholar
  12. Brown, W.J., 1952. Some species of Phytophaga (Coleoptera). Can. Entomol. 84: 335–342.CrossRefGoogle Scholar
  13. Brown, W.J., 1961. Notes on North American Chrysomelidae (Coleoptera). Can. Entomol. 93: 966–977.Google Scholar
  14. Bush, G.L., 1969. Sympatric host race formation and speciation in frugivorous flies of genus Rhagoletis (Diptera, Tephritidae). Evolution 23: 237–251.CrossRefGoogle Scholar
  15. Bush, G.L. & R. Butlin. Sympatric speciation in insects: an overview, in Adaptive Speciation, edited by U. Dieckmann, H. Metz, M. Doebeli & D. Tautz. Cambridge University Press, Cambridge (in press).Google Scholar
  16. Butlin, R.K., 1993. The variability of mating signals and preferences in the brown planthopper, Nilaparvata lugens (Homoptera, Delphacidae). J. Ins. Behav. 6: 125–140.CrossRefGoogle Scholar
  17. Butlin, R.K., 1996. Co-ordination of the sexual signaling system and the genetic basis of differentiation between populations in the brown planthopper, Nilaparvata lugens. Heredity 77: 369–377.CrossRefGoogle Scholar
  18. Carroll, S.P. & C. Boyd, 1992. Host race radiation in the soapberry bug: natural history with the history. Evolution 46: 1052–1069.CrossRefGoogle Scholar
  19. Carroll, S.P. & H. Dingle, 1996. The biology of post-invasion events. Biol. Conserv. 78: 207–214.CrossRefGoogle Scholar
  20. Carroll, S.P., H. Dingle & S.P. Klassen, 1998. Rapidly evolving adaptations to host ecology and nutrition in the soapberry bug. Evol. Ecol. 12: 955–968.CrossRefGoogle Scholar
  21. Caillaud, M.C. & S. Via, 2000. Specialized feeding behavior influences both ecological specialization and assortative mating in sympatric host races of pea aphids. Am. Nat. 156: 606–621.CrossRefGoogle Scholar
  22. Coyne, J.A. & H.A. Orr, 1989. Patterns of speciation in Drosophila. Evolution 43: 362–381.CrossRefGoogle Scholar
  23. Coyne, J.A. & H.A. Orr, 1997. Patterns of speciation in Drosophila revisited. Evolution 51: 295–303.CrossRefGoogle Scholar
  24. Coyne, J.A. & H.A. Orr, 1998. The evolutionary genetics of speciation. Phil. Trans. R. Soc. Lond. B 353: 287–305.CrossRefGoogle Scholar
  25. Craig, T.P., J.K. Itami, W.G. Abrahamson & J.D. Horner. 1993. Behavioral evidence for host-race formation in Eurosta solidaginis. Evolution 47: 1696–1710.CrossRefGoogle Scholar
  26. Craig, T.P., J.D. Horner & J.K. Itami, 1997. Hybridization studies on the host races of Eurosta solidaginis: implications for sympatric speciation. Evolution 51: 1552–1560.CrossRefGoogle Scholar
  27. Craig, T.P., J.D. Horner & J.K. Itami, 2001. Genetics, experience, and host-plant preference in Eurosta solidaginis: implications for sympatric speciation. Evolution 51: 1552–1560.CrossRefGoogle Scholar
  28. Day, K., 1984. Phenology, polymorphism and insect-plant relationships of the larch budmoth, Zeiraphera diniana (Guenée) (Lepidoptera: Tortricidae), on alternative conifer hosts in Britain. Bull. Entomol. Res. 74: 47–64.CrossRefGoogle Scholar
  29. Denno, R.F., M.S. McClure & J.R. Ott, 1995. Interspecific interactions in phytophagous insects: competition reexamined and resurrected. Ann. Rev. Entomol. 40: 297–331.CrossRefGoogle Scholar
  30. Diehl, S.R. & G.L. Bush, 1984. An evolutionary and applied perspective of insect biotypes. Ann. Rev. Entomol. 29: 471–504.CrossRefGoogle Scholar
  31. Dobzhansky, T., 1936. Studies on hybrid sterility. II. Localization of sterility factors in Drosophila pseudoobscura hybrids. Genetics 21: 113–135.PubMedGoogle Scholar
  32. Dopman, E.B., G.A. Sword & D.M. Hillis, 2002. The importance of the ontogenetic niche in resource-associated divergence: evidence from a generalist grasshopper. Evolution 56: 731–740.PubMedGoogle Scholar
  33. Ehrlich, P.R. & P.H. Raven, 1964. Butterflies and plants: a study in coevolution. Evolution 18: 586–608.CrossRefGoogle Scholar
  34. Ehrman, L. & C. Petit, 1968. Genotype frequency and mating success in the willistoni species group of Drosophila. Evolution 22: 649–658.CrossRefGoogle Scholar
  35. Emelianov, I., M. Drès, W. Baltensweiler & J. Mallet, 2002. Host-induced assortative mating in host races of the larch budmoth. Evolution 55: 2002–2010.Google Scholar
  36. Etges, W.J., 1998. Premating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. IV. Correlated responses in behavioral isolation to artificial selection on a life-history trait. Am. Nat. 152: 129–144.PubMedCrossRefGoogle Scholar
  37. Etges, W.J. & M.A. Ahrens, 2001. Premating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. V. Deep geographic variation in epicuticular hydrocarbons among isolated populations. Am. Nat. 158: 585–598.PubMedCrossRefGoogle Scholar
  38. Farrell, B.D., 1998. ‘Inordinate fondness’ explained: Why are there so many beetles? Science 281: 555–559.PubMedCrossRefGoogle Scholar
  39. Feder, J.L., 1998. The apple maggot fly, Rhagoletis pomonella: flies in the face of conventional wisdom about speciation? pp. 130–144 in Endless Forms: Species and Speciation, edited by D.J. Howard & S.H. Berlocher. Oxford University Press, Oxford.Google Scholar
  40. Feder, J.L. & G.L. Bush, 1989. A field test of differential host plant usage between two sibling species of Rhagoletis pomonella fruit flies (Diptera, Tephritidae) and its consequences for sympatric models of speciation. Evolution 43: 1813–1819.CrossRefGoogle Scholar
  41. Feder, J.L. & K.E. Filchak, 1999. It’s about time: the evidence for host plant-mediated selection in the apple maggot fly, Rhagoletis pomonella, and its implications for fitness trade-offs in phytophagous insects. Ent. Exp. Appl. 91: 211–225.CrossRefGoogle Scholar
  42. Feder, J.L., S. Opp, B. Wazlo, K. Reynolds, W. Go & S. Spizak, 1994. Host fidelity as an effective premating barrier between sympatric races of the apple maggot fly. Proc. Natl. Acad. Sci. USA 91: 7990–79994.PubMedCrossRefGoogle Scholar
  43. Feder, J.L., J.B. Roethele, B. Wlazlo & S.H. Berlocher, 1997. Selective maintenance of allozyme differences among sympatric host races of the apple maggot fly. Proc. Natl. Acad. Sci. USA 94: 11417–11421.PubMedCrossRefGoogle Scholar
  44. Filchak, K.E., J.B. Roethele & J.L. Feder, 2000. Natural selection and sympatric divergence in the apple maggot Rhagoletis pomonella. Nature 407: 739–742.PubMedCrossRefGoogle Scholar
  45. Funk, D.J., 1996. The evolution of reproductive isolation in Neoch-lamisus leaf beetles: a role for selection. PhD Dissertation, State University of New York, Stony Brook, NY.Google Scholar
  46. Funk, D.J., 1998. Isolating a role for selection in speciation: host adaptation and sexual isolation in Neochlamisus hebbianae leaf beetles. Evolution 52: 1744–1759.CrossRefGoogle Scholar
  47. Funk, D.J., 1999. Molecular systematics of cytochrome oxidase I and 16S from Neochlamisus leaf beetles and the importance of sampling. Mol. Biol. Evol. 16: 67–82.PubMedCrossRefGoogle Scholar
  48. Futuyma, D.J. 1983. Selective factors in the evolution of host choice by phytophagous insects, pp. 227–244 in Herbivorous Insects, edited by S. Ahmad (ed.). Academic Press, San Diego, CA.Google Scholar
  49. Groman, J.D. & O. Pellmyr, 2000. Rapid evolution and specialization following host colonization in a yucca moth. J. Evol. Biol. 13: 223–226.CrossRefGoogle Scholar
  50. Guldemond, J.A., 1990. Choice of host plant as a factor in reproductive isolation of the aphid genus Cryptomyzus (Homoptera, Aphididae). Ecol. Entomol. 15: 43–51.CrossRefGoogle Scholar
  51. Hawthorne, D.J. & S. Via, 2001. Genetic linkage of ecological specialization and reproductive isolation in pea aphids. Nature 412: 904–907.PubMedCrossRefGoogle Scholar
  52. Henry, C.S., 1994. Singing and cryptic speciation in insects. Trends Ecol. Evol. 9: 388–392.PubMedCrossRefGoogle Scholar
  53. Horner, J.D., T.P. Craig & J.K. Itami, 1999. The influence of oviposition phenology on survival in the host races of Eurosta solidaginis. Entomol. Exp. Appl. 93: 121–129.CrossRefGoogle Scholar
  54. Hunt, R.E., 1993. Role of vibrational signals in mating behavior of Spissistilus festinus (Homoptera, Membracidae). Ann. Entomol. Soc. Am. 86:356–361.Google Scholar
  55. Itami, J.K., T.P. Craig & J.D. Horner, 1998. Factors affecting gene flow between the host races of Eurosta solidaginis, pp. 375–407 in Genetic Structure and Local Adaptation in Natural Insect Populations: Effects of Ecology, Life History, and Behavior, edited by S. Mopper & S.Y. Strauss. Chapman and Hall, New York.Google Scholar
  56. Jaenike, J., 1981. Criteria for ascertaining the existence of host races. Am. Nat. 117: 830–834.CrossRefGoogle Scholar
  57. Jaenike, J., 1990. Host specialization in phytophagous insects. Ann. Rev. Ecol. Syst. 21:243–273.CrossRefGoogle Scholar
  58. Jiggins, C.D. & J. Mallet, 2000. Bimodal hybrid zones and speciation. Trends Ecol. Evol. 15: 250–255.PubMedCrossRefGoogle Scholar
  59. Karren, J.B., 1972. A revision of the subfamily Chlamisinae of America north of Mexico (Coleoptera: Chrysomelidae). Univ Kansas Sci. Bull. 49: 875–988.Google Scholar
  60. Katakura, H., 1997. Species of Epilachna ladybird beetles. Zool. Sci. 14: 869–881.CrossRefGoogle Scholar
  61. Katakura, H., M. Shioi & Y. Kira, 1989. Reproductive isolation by host specificity in a pair of phytophagous ladybird beetles. Evolution 43: 1045–1053.CrossRefGoogle Scholar
  62. Landolt, P.J. & T.W. Phillips, 1997. Host plant influences on sex pheromone behavior of phytophagous insects. Ann. Rev. Entomol. 42:371–391.CrossRefGoogle Scholar
  63. LeSage, L., 1984. Immature stages of Canadian Neochlamisus Karren (Coleoptera: Chrysomelidae). Can. Entomol. 116: 383–409.CrossRefGoogle Scholar
  64. Lu, G.Q. & L. Bernatchez, 1999. Correlated trophic specialization and genetic divergence in sympatric whitefish ecotypes (Coregonus clupeaformis): support for the ecological speciation hypothesis. Evolution 53: 1491–1505.CrossRefGoogle Scholar
  65. Maksymov, J.K., 1959. Beitrag zur Biologie und Ökologie des Grauen Lärchenwicklers, Zeiraphera griseana (Hb.) (Lepid-optera: Tortricidae) im Engadin. Mitt. Schweitz. Anst. forstl. Versuchw. 35:277–315.Google Scholar
  66. Mayr, E., 1942. Systematics and the Origin of Species. Columbia University Press, New York.Google Scholar
  67. Mayr, E., 1963. Animal Species and Evolution. Harvard University Press, Cambridge, MA.Google Scholar
  68. Mitter, C. & B. Farrell, 1991. Macroevolutionary aspects of insect-plant relationships, pp. 35–78 in Insect-Plant Interactions, Vol. 3, edited by E.A. Bernays. CRC Press, Boca Raton, FL.Google Scholar
  69. Mitter, C., B. Farrell & B. Wiegmann, 1988. The phylogenetic study of adaptive zones: has herbivory promoted insect diversification? Am. Nat. 132: 107–128.CrossRefGoogle Scholar
  70. Mopper, S. & S.Y. Strauss (eds), 1998. Genetic Structure and Local Adaptation in Natural Insect Populations: Effects of Ecology, Life History, and Behavior. Chapman and Hall, London.Google Scholar
  71. Morrell, V., 1999. Ecology returns to speciation studies. Science 284: 2106–2108.CrossRefGoogle Scholar
  72. Muller, H.J., 1939. Reversibility in evolution considered from the standpoint of genetics. Biol. Rev. 14: 261–280.CrossRefGoogle Scholar
  73. Muller, H.J., 1942. Isolating mechanisms, evolution and temperature. Biol. Symp. 6:71–125.Google Scholar
  74. Nagel, L. & D. Schluter, 1998. Body size, natural selection, and speciation in sticklebacks. Evolution 52: 209–218.CrossRefGoogle Scholar
  75. Newby, B.D. & W.J. Etges, 1998. Host preference among populations of Drosophila mojavensis (Diptera: Drosophilidae) that use different host cacti. J. Ins. Behav. 11: 691–712.CrossRefGoogle Scholar
  76. Nishida, T., L.E. Pudjiastuti, S. Nakano, I. Abbas, S. Kahono, K. Nakamura & H. Katakura, 1997. The eggplant beetle on a leguminous weed: host race formation in progress? Tropics 7: 115–121.CrossRefGoogle Scholar
  77. Nosil, P., B.J. Crespi & C.P. Sandoval, 2002. Host-plant adaptation drives the parallel evolution of reproductive isolation. Nature 417: 440–443.PubMedCrossRefGoogle Scholar
  78. Orr, M.R. & T.B. Smith, 1998. Ecology and speciation. Trends Ecol. Evol. 13: 502–506.PubMedCrossRefGoogle Scholar
  79. Pashley, D.P., 1986. Host associated genetic differentiation in fall armyworm: a sibling species complex? Ann. Entomol. Soc. Am. 79: 898–904.Google Scholar
  80. Pashley, D.P., 1988. Quantitative genetics, development and physiological adaptation in sympatric host strains of fall army-worm. Evolution 42: 93–102.CrossRefGoogle Scholar
  81. Pashley, D.P., 1993. Causes of host-associated variation in insect herbivores: an example from fall armyworm. pp. 351–359 in Evolution of Insect Pests: the Pattern of Variation, edited by K.C. Kim. Wiley, New York.Google Scholar
  82. Pashley, D.P., A.M. Hammond & T.N. Hardy, 1992. Reproductive isolating mechanisms in fall armyworm host strains (Lepidop-tera, Noctuidae). Ann. Entomol. Soc. Am. 85: 400–405.Google Scholar
  83. Pashley, D.P. & J.A. Martin, 1987. Reproductive incompatibility between host strains of fall armyworm (Lepidoptera: Noctuidae). Ann. Entomol. Soc. Am. 80: 731–733.Google Scholar
  84. Price, P.W., 1975. Introduction, pp. 1–19 in Evolutionary Strategies of Parasitic Insects, edited by P.W. Price. Plenum Press, London.CrossRefGoogle Scholar
  85. Priesner, E., 1979. Specificity studies on pheromone receptors of noctuid and tortricid Lepidoptera, pp. 57–71 in Chemical Ecology: Odour Communication in Animals, edited by F.J. Ritter. North-Holland Biomedical Press, Amsterdam.Google Scholar
  86. Priesner, E. & W. Baltensweiler, 1987a. A study of pheromone polymorphism in Zeiraphera diniana Gn (Lep, Tortricidae). 1. Male pheromonal response types in European wild populations, 1978-1985. J. Appl. Entomol. 104: 234–256.CrossRefGoogle Scholar
  87. Priesner, E. & W. Baltensweiler, 1987b. A study of pheromone polymorphism in Zeiraphera diniana Gn (Lep. Tortricidae). 2. Pheromonal response types in F1 hybrids between three host races. J. Appl. Entomol. 104: 433–448.CrossRefGoogle Scholar
  88. Prokopy, R.J., A.L. Averill, S.S. Cooley & C.A. Roitberg, 1982. Associative learning in egglaying site selection by apple maggot flies. Science 218: 76–77.PubMedCrossRefGoogle Scholar
  89. Prokopy, R.J., S.R. Diehl & S.S. Cooley, 1988. Behavioral evidence for host races in Rhagoletis pomonella flies. Oecologia 76: 138–147.Google Scholar
  90. Prowell, D.P., 1998. Sex linkage and speciation in Lepidoptera, pp. 309–319 in Endless Forms: Species and Speciation, edited by D.J. Howard & S.H. Berlocher. Oxford University Press, New York.Google Scholar
  91. Reissig, H. & D.C. Smith, 1978. Bioeconomics of Rhagoletis pomonella in Crataegus. Ann. Entomol. Soc. Am. 71: 155–159.Google Scholar
  92. Rundle, H.D., L. Nagel, J.W. Boughman & D. Schluter, 2000. Natural selection and parallel speciation in sympatric sticklebacks. Science 287: 306–308.PubMedCrossRefGoogle Scholar
  93. Sandoval, C.P., 1993. Geographic, ecological, and behavioral factors affecting spatial variation in color morph frequency in the walking stick Timema cristinae. PhD Dissertation. University of California, Santa Barbara.Google Scholar
  94. Schluter, D., 1996a. Ecological causes of adaptive radiation. Am. Nat. 148: S40–S64.CrossRefGoogle Scholar
  95. Schluter, D., 1996b. Ecological speciation in postglacial lakes. Phil. Trans. Roy. Soc. Lond. B 351: 807–814.CrossRefGoogle Scholar
  96. Schluter, D., 2000. The Ecology of Adaptive Radiation. Oxford University Press, Oxford.Google Scholar
  97. Schluter, D., 2001. Ecology and the origin of species. Trends Ecol. Evol. 16:372–381.PubMedCrossRefGoogle Scholar
  98. Sezer, M. & R.K. Butlin, 1998. The genetic basis of oviposition preference differences between sympatric host races of the brown planthopper (Nilaparvata lugens). Proc. Roy. Soc. Lond. B 265: 2399–2405.CrossRefGoogle Scholar
  99. Simpson, G.G., 1944. Tempo and Mode in Evolution. Columbia University Press, New York.Google Scholar
  100. Smith, D.C., 1986. Genetic and reproductive isolation of Rhagoletis flies. PhD Thesis, University of Illinois, Urbana-Champaign, 189 pp.Google Scholar
  101. Spieth, H.T. & J.M. Ringo, 1983. Mating behavior and sexual isolation in Drosophila, pp. 223–284 in The Genetics and Biology of Drosophila, Vol. 3c, edited by M. Ashburner, H.L. Carson & J.N. Thompson Jr. Academic Press, New York.Google Scholar
  102. Stennett, M.D. & W.J. Etges, 1997. Premating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. III. Epicuticular hydrocarbon variation is determined by use of different host plants in Drosophila mojavensis and Drosophila arizonae. J. Chem. Ecol. 23: 2803–2824.CrossRefGoogle Scholar
  103. Strong, D.R., J.H. Lawton & R. Southwood, 1984. Insects on Plants. Harvard University Press, Cambridge.Google Scholar
  104. Sword, G.A. & E.B. Dopman, 1999. Developmental specialization and geographic structure of host plant use in a polyphagous grasshopper, Schistocerca emarginata (=lineata) (Orthoptera: Acrididae). Oecologia 120: 437–445.CrossRefGoogle Scholar
  105. Szentesi, A. & T. Jermy, 1990. The role of experience in host plant choice by phytophagous insects, pp. 39–74 in Insect-Plant Interactions, Vol. 2, edited by E.A. Bernays. CRC Press, Boca Raton, FL.Google Scholar
  106. Tilmon, K.J., T.K. Wood & J.D. Pesek, 1998. Genetic variation in performance traits and the potential for host shifts in Enchenopa treehoppers (Homoptera: Membracidae). Ann. Entomol. Soc. Am. 91:397–403.Google Scholar
  107. Via, S., 1999. Reproductive isolation between sympatric races of pea aphids. I. Gene flow restriction and habitat choice. Evolution 53: 1446–1457.CrossRefGoogle Scholar
  108. Via, S., 2001. Sympatric speciation in animals: the ugly duckling grows up. Trends Ecol. Evol. 16: 381–390.PubMedCrossRefGoogle Scholar
  109. Via, S., Bouck, A.C. & S. Skillman, 2000. Reproductive isolation between divergent races of pea aphids on two hosts. II. Selection against migrants and hybrids in the parental environment. Evolution 54: 1626–1637.PubMedGoogle Scholar
  110. Walsh, B.D., 1864. On phytophagic varieties and phytophagic species. Proc. Entomol. Soc. Philadelphia 3: 403–430.Google Scholar
  111. Ward, L. & D.F. Spalding, 1993. Phytophagous British insects and mites and their food plant families: total numbers and polyphagy. Biol. J. Linn. Soc. 49: 257–276.CrossRefGoogle Scholar
  112. Wiegmann, B.M., C. Mitter & B. Farrell, 1993. Diversification of carnivorous parasitic insects: extraordinary radiation or specialized dead end? Am. Nat. 142: 737–754.CrossRefGoogle Scholar
  113. Wood, T.K., 1980. Intraspecific divergence in Enchenopa binotata Say (Homoptera: Membracidae) effected by host plant adaptation. Evolution 34: 147–160.CrossRefGoogle Scholar
  114. Wood, T.K. & S.I. Guttman, 1982. Ecological and behavioral basis for reproductive isolation in the sympatric Enchenopa binotata complex (Homoptera: Membracidae). Evolution 36: 233–242.CrossRefGoogle Scholar
  115. Wood, T.K. & M.C. Keese, 1990. Host plant induced assortative mating in Enchenopa treehoppers. Evolution 44: 619–628.CrossRefGoogle Scholar
  116. Wood, T.K., H.J. Tilmon, A.B. Shantz, C.K. Harris & J. Pesek. 1999. The role of host-plant fidelity in initiating insect race formation. Evol. Ecol. Res. 1: 317–332.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2002

Authors and Affiliations

  • Daniel J. Funk
    • 1
  • Kenneth E. Filchak
    • 2
  • Jeffrey L. Feder
    • 2
  1. 1.Department of Biological SciencesVanderbilt UniversityNashvilleUSA
  2. 2.Department of Biological SciencesUniversity of Notre DameSouth BendUSA

Personalised recommendations