1932

Abstract

This review was solicited as an autobiography. The “problems” in my title have two meanings. First, they were professional difficulties caused by my decision to study oviposition preferences of butterflies that were not susceptible to traditional preference-testing designs. Until I provided video, my claim that the butterflies duplicate natural post-alighting host-assessment behavior when placed on hosts by hand was not credible, and the preference-testing technique that I had developed elicited skepticism, anger, and derision. The second meaning of “problems” is scientific. Insect preference comes with complex dimensionality that interacts with host acceptability. Part Two of this review describes how my group's work in this area has revealed unexpected axes of variation in plant–insect interactions—axes capable of frustrating attempts to derive unequivocal conclusions from apparently sensible experimental designs. The possibility that these complexities are lurking should be kept in mind as preference and performance experiments are devised.

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2021-01-07
2024-04-24
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Literature Cited

  1. 1. 
    Agnew K, Singer MC. 2000. Does fecundity drive the evolution of insect diet. Oikos 88:533–38
    [Google Scholar]
  2. 2. 
    Barron AB. 2001. The life and death of Hopkins’ host-selection principle. J. Insect Behav. 14:725–37
    [Google Scholar]
  3. 3. 
    Bennett NL, Severns PM, Parmesan C, Singer MC 2015. Geographic mosaics of host preference, phenology, adult size and microhabitat choice predict butterfly resilience to climate warming. Oikos 124:41–53
    [Google Scholar]
  4. 4. 
    Bernays EA. 1998. The value of being a resource specialist: behavioral support for a neural hypothesis. Am. Nat. 151:451–64
    [Google Scholar]
  5. 5. 
    Bernays EA. 2019. An unlikely beginning: a fortunate life. Annu. Rev. Entomol. 64:1–13
    [Google Scholar]
  6. 6. 
    Bernays EA, Bright KL, Howard JJ, Raubenheimer D, Champagne D 1992. Variety is the spice of life: frequent switching between foods in the polyphagous grasshopper, Taeniopoda eques. Anim. Behav. 44:721–31
    [Google Scholar]
  7. 7. 
    Bernays EA, Funk D. 1999. Specialists make faster decisions than generalists: experiments with aphids. Proc. R. Soc. B 266:151–56
    [Google Scholar]
  8. 8. 
    Bernays EA, Graham M. 1988. On the evolution of host specificity in phytophagous arthropods. Ecology 69:886–92
    [Google Scholar]
  9. 9. 
    Bernays EA, Wcislo W. 1994. Sensory capabilities, information processing and resource specialization. Q. Rev. Biol. 69:187–204
    [Google Scholar]
  10. 10. 
    Boughton DA. 1999. Empirical evidence for complex source-sink dynamics with alternative states in a butterfly metapopulation. Ecology 80:2727–39
    [Google Scholar]
  11. 11. 
    Brady SP, Bolnick DI, Angert AL, Gonzalez A, Barrett RDH et al. 2019. Causes of maladaptation. Evol. Appl. 12:S11229–42
    [Google Scholar]
  12. 12. 
    Cahenzli F, Wenk BA, Erhardt A 2015. Female butterflies adapt and allocate their progeny to the host-plant quality of their own larval experience. Ecology 96:1966–73
    [Google Scholar]
  13. 13. 
    Chew FS, Robbins RK. 1984. Egg laying in butterflies. The Biology of Butterflies RI Vane-Wright, P Ackery 65–79 Cambridge, MA: Academic
    [Google Scholar]
  14. 14. 
    Dethier VG. 1954. Evolution of feeding preferences in phytophagous insects. Evolution 8:33–54
    [Google Scholar]
  15. 15. 
    Dethier VG. 1959. Egg-laying habits of Lepidoptera in relation to available food. Can. Entomol. 91:554–61
    [Google Scholar]
  16. 16. 
    Dethier VG, MacArthur RH. 1964. A field's capacity to support a butterfly population. Nature 201:728–29
    [Google Scholar]
  17. 17. 
    Dukas R, Bernays EA. 2000. Learning improves growth in the grasshopper, Schistocerca americana. PNAS 97:2637–40
    [Google Scholar]
  18. 18. 
    Dyer LA, Forister ML 2015. The Lives of Lepidopterists Berlin: Springer
  19. 19. 
    Ehrlich PR. 1961. Intrinsic barriers to dispersal in checkerspot butterfly. Science 134:108–9
    [Google Scholar]
  20. 20. 
    Ehrlich PR. 1965. The population biology of the butterfly Euphydryas editha. II. The structure of the Jasper Ridge colony. Evolution 19:327–36
    [Google Scholar]
  21. 21. 
    Ehrlich PR. 1968. The Population Bomb San Francisco/New York: Sierra Club Books/Ballantine Books
  22. 22. 
    Ford HD, Ford EB. 1930. Fluctuation in numbers and its influence on variation in Melitaea aurinia Rott. (Lepidoptera). Trans. Entomol. Soc. Lond. 78:345–51
    [Google Scholar]
  23. 23. 
    Fordyce JA, Gompert Z, Forister ML, Nice C 2011. A hierarchical Bayesian approach to ecological count data: a flexible tool for ecologists. PLOS ONE 6:11e26785
    [Google Scholar]
  24. 24. 
    Friberg M, Olofsson M, Berger D, Karlsson B, Wiklund C 2008. Habitat choice precedes host plant choice—niche separation in a pair of a generalist and a specialist butterfly. Oikos 117:1337–44
    [Google Scholar]
  25. 25. 
    Futuyma DJ. 1983. Evolutionary interactions among herbivorous insects and plants. Coevolution DJ Futuyma, M Slatkin 207–31 Sunderland, MA: Sinauer
    [Google Scholar]
  26. 26. 
    Hanski I, Singer MC. 2001. Extinction-colonization dynamics and host plant choice in butterfly metapopulations. Am. Nat. 158:341–53
    [Google Scholar]
  27. 27. 
    Hilker M, Fatouros NE. 2015. Plant responses to insect egg deposition. Annu. Rev. Entomol. 60:493–515
    [Google Scholar]
  28. 28. 
    Hopkins AD. 1917. A discussion of C.G. Hewitt's paper on insect behaviour. J. Econ. Entomol. 10:92–93
    [Google Scholar]
  29. 29. 
    Jaenike J. 1983. Induction of host preference in Drosophila melanogaster. Oecologia 58:320–25
    [Google Scholar]
  30. 30. 
    Jaenike J. 1990. Host specialization in phytophagous insects. Annu. Rev. Ecol. Syst. 21:243–73
    [Google Scholar]
  31. 31. 
    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. Biol. Sci. 264:7017
    [Google Scholar]
  32. 32. 
    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. 34:50–57
    [Google Scholar]
  33. 33. 
    Kuussaari M, Singer MC, Hanski I 2000. Local specialization and landscape-level influence on host use in a herbivorous insect. Ecology 81:2177–87
    [Google Scholar]
  34. 34. 
    Mackay DA, Singer MC. 1982. The basis of an apparent preference for isolated plants by ovipositing Euptychia libye butterflies. Ecol. Entomol. 7:299–303
    [Google Scholar]
  35. 35. 
    McBride CS, Singer MC. 2010. Field studies reveal strong postmating isolation between ecologically divergent butterfly populations. PLOS Biol 8:10e1000529
    [Google Scholar]
  36. 36. 
    McNeely C, Singer MC. 2001. Contrasting the roles of learning in butterflies foraging for nectar and oviposition sites. Anim. Behav. 61:847–52
    [Google Scholar]
  37. 37. 
    Mikheyev AS, McBride CS, Mueller UG, Parmesan C, Smee MR et al. 2013. Host-associated genomic differentiation in congeneric butterflies: Now you see it, now you don't. Mol. Ecol. 22:4753–66
    [Google Scholar]
  38. 38. 
    Ng D. 1988. A novel level of interaction in plant-insect systems. Nature 334:611–12
    [Google Scholar]
  39. 39. 
    Parmesan C. 1991. Evidence against plant “apparency” as a constraint on evolution of insect search efficiency (Lepidoptera: Nymphalidae). J. Insect Behav. 4:417–30
    [Google Scholar]
  40. 40. 
    Parmesan C, Singer MC, Harris I 1995. Absence of adaptive learning from the oviposition behavior of a checkerspot butterfly. Anim. Behav. 50:161–75
    [Google Scholar]
  41. 41. 
    Parmesan C, Duarte C, Poloczanska E, Richardson AJ, Singer MC 2011. Overstretching attribution. Nat. Clim. Chang. 1:2–4
    [Google Scholar]
  42. 42. 
    Parmesan C, Burrows MT, Duarte C, Poloczanska E, Richardson AJ, Singer MC 2013. Beyond climate change attribution in conservation and ecological research. Ecol. Lett. 16:58–71
    [Google Scholar]
  43. 43. 
    Parmesan C, Williams-Anderson A, Moskwik M, Mikheyev AS, Singer MC 2015. Endangered Quino checkerspot butterfly and climate change: short-term success but long-term vulnerability. J. Insect Conserv. 9:185–204
    [Google Scholar]
  44. 44. 
    Rausher MD, Mackay DA, Singer MC 1981. Pre- and post-alighting host discrimination by Euphydryas editha butterflies: the behavioral mechanisms causing clumped distributions of egg clusters. Anim. Behav. 29:1220–28
    [Google Scholar]
  45. 45. 
    Singer MC. 1971. Evolution of food-plant preferences in the butterfly Euphydryas editha. Evolution 25:383–89
    [Google Scholar]
  46. 46. 
    Singer MC. 1982. Quantification of host preference by manipulation of oviposition behavior in the butterfly Euphydryas editha. Oecologia 52:224–29
    [Google Scholar]
  47. 47. 
    Singer MC. 1983. Determinants of multiple host use by a phytophagous insect population. Evolution 37:389–403
    [Google Scholar]
  48. 48. 
    Singer MC. 1986. The definition and measurement of oviposition preference. Plant-Insect Interactions J Miller, TA Miller 65–94 Berlin: Springer
    [Google Scholar]
  49. 49. 
    Singer MC. 2000. Reducing ambiguity in describing plant-insect interaction: “preference,” “acceptability” and “electivity.. Ecol. Lett. 3:159–62
    [Google Scholar]
  50. 50. 
    Singer MC. 2015. Adaptive and maladaptive consequences of “matching habitat choice”: lessons from a rapidly-evolving insect metapopulation. Evol. Ecol. 29:905–25
    [Google Scholar]
  51. 51. 
    Singer MC, Ehrlich PR, Gilbert LE 1971. Butterfly feeding on Lycopsid. Science 172:1341–42
    [Google Scholar]
  52. 52. 
    Singer MC, Kuussaari M, van Nouhuys S 2017. Attraction of Melitaea cinxia butterflies to previously-attacked hosts: a likely complement to known Allee effects. Ann. Zool. Fenn. 54:205–11
    [Google Scholar]
  53. 53. 
    Singer MC, Lee JR. 2000. Discrimination within and between host species by a butterfly: implications for design of preference experiments. Ecol. Lett. 3:101–5
    [Google Scholar]
  54. 54. 
    Singer MC, Mandracchia J. 1982. On the failure of two butterfly species to respond to the presence of conspecific eggs prior to oviposition. Ecol. Entomol. 7:327–30
    [Google Scholar]
  55. 55. 
    Singer MC, McBride CS. 2010. Multitrait, host-associated divergence among sets of butterfly populations: implications for reproductive isolation and ecological speciation. Evolution 64:921–33
    [Google Scholar]
  56. 56. 
    Singer MC, McBride CS. 2012. Geographic mosaics of species’ association: a definition and an example driven by plant-insect phenological synchrony. Ecology 93:2658–73
    [Google Scholar]
  57. 57. 
    Singer MC, Ng D, Thomas CD 1988. Heritability of oviposition preference and its relationship to offspring performance within a single insect population. Evolution 42:977–85
    [Google Scholar]
  58. 58. 
    Singer MC, Ng D, Vasco DA, Thomas CD 1992. Rapidly evolving associations among oviposition preferences fail to constrain evolution of insect diet breadth. Am. Nat. 139:9–20
    [Google Scholar]
  59. 59. 
    Singer MC, Parmesan C. 1993. Sources of variation in patterns of plant-insect association. Nature 361:251–53
    [Google Scholar]
  60. 60. 
    Singer MC, Parmesan C. 2010. Phenological asynchrony between herbivorous insects and their hosts: signal of climate change or pre-existing adaptive strategy. Phil. Trans. R. Soc. Lond. B 365:3161–76
    [Google Scholar]
  61. 61. 
    Singer MC, Parmesan C. 2018. Lethal trap created by adaptive evolutionary response to an exotic resource. Nature 557:238–41
    [Google Scholar]
  62. 62. 
    Singer MC, Parmesan C. 2018. A poison'd chalice tale: butterfly extinction in eco-evolutionary trap. Nature Research Ecology & Evolution Community May 10. https://natureecoevocommunity.nature.com/channels/521-behind-the-paper/posts/32973-a-poison-d-chalice-tale-butterfly-extinction-in-eco-evolutionary-trap
    [Google Scholar]
  63. 63. 
    Singer MC, Parmesan C. 2019. Butterflies embrace maladaptation and raise fitness in colonizing novel host. Evol. Appl. 12:1417–33
    [Google Scholar]
  64. 64. 
    Singer MC, Stefanescu C, Pen I 2002. When random sampling doesn't work: Standard design falsely indicates maladaptive host preferences in a butterfly. Ecol. Lett. 5:1–6
    [Google Scholar]
  65. 65. 
    Singer MC, Thomas CD. 1996. Evolutionary responses of a butterfly metapopulation to human and climate-caused environmental variation. Am. Nat. 148:S9–39
    [Google Scholar]
  66. 66. 
    Singer MC, Thomas CD, Billington HL, Parmesan C 1989. Variation among conspecific insect populations in the mechanistic basis of diet breadth. Anim. Behav. 37:751–59
    [Google Scholar]
  67. 67. 
    Singer MC, Thomas CD, Billington HL, Parmesan C 1994. Correlates of speed of evolution of host preference in a set of twelve populations of the butterfly Euphydryas editha. Ecoscience 1:107–14
    [Google Scholar]
  68. 68. 
    Singer MC, Thomas CD, Parmesan C 1993. Rapid human-induced evolution of insect diet. Nature 366:681–83
    [Google Scholar]
  69. 69. 
    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. 44:463–71
    [Google Scholar]
  70. 70. 
    Singer MC, Wee B, Hawkins S, Butcher M 2008. Rapid natural and anthropogenic diet evolution: three examples from checkerspot butterflies. The Evolutionary Ecology of Herbivorous Insects: Speciation, Specialization and Radiation KJ Tilmon 311–24 Berkeley, CA: Univ. Calif. Press
    [Google Scholar]
  71. 71. 
    Singer MS, Mace KC, Bernays EA 2009. Self-medication as adaptive plasticity: increased ingestion of plant toxins by parasitized caterpillars. PLOS ONE 4:389–97
    [Google Scholar]
  72. 72. 
    Steward RA, Boggs CL. 2020. Experience may outweigh cue similarity in maintaining a persistent host plant-based evolutionary trap. Ecol. Monogr. 90:e01412
    [Google Scholar]
  73. 73. 
    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
    [Google Scholar]
  74. 74. 
    Thomas CD, Singer MC. 1987. Variation in host preference affects movement patterns in a butterfly population. Ecology 68:1262–67
    [Google Scholar]
  75. 75. 
    Thompson JN. 1988. Evolutionary genetics of oviposition preference in swallowtail butterflies. Evolution 42:1223–34
    [Google Scholar]
  76. 76. 
    Thompson JN. 1988. Variation in preference and specificity in monophagous and oligophagous swallowtail butterflies. Evolution 42:118–28
    [Google Scholar]
  77. 77. 
    Thorpe WH. 1930. Biological races in insects and allied groups. Biol. Rev. 5:177–212
    [Google Scholar]
  78. 78. 
    Van Nouhuys S, Singer MC, Nieminen M 2003. Spatial and temporal patterns of caterpillar performance and the suitability of two host plant species. Ecol. Entomol. 28:193–202
    [Google Scholar]
  79. 79. 
    Wee B, Singer MC. 2007. Variation among individual butterflies along a generalist-specialist axis: no support for the “neural constraint” hypothesis. Ecol. Entomol. 32:257–61
    [Google Scholar]
  80. 80. 
    Wiklund C. 1975. The evolutionary relationship between adult oviposition preferences and larval host plant range in Papilio machaon. Oecologia 18:185–97
    [Google Scholar]
  81. 81. 
    Wiklund C. 1981. Generalist versus specialist oviposition behaviour in Papilio machaon (Lepidoptera) and functional aspects on the hierarchy of oviposition preferences. Oikos 36:163–70
    [Google Scholar]
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