Multitrait, host-associated divergence among sets of butterfly populations: implications for reproductive isolation and ecological speciation

Evolution

Volumn 64, Issue 4, 2010, Pages 921-933

  Singer, Michael C ^a   McBride, Carolyn S ^b,c  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Adaptive suites; Clutch size; Euphydryas; Host adaptation; Performance; Preference

Indexed keywords

BUTTERFLY; CLUTCH SIZE; DIVERGENCE; GENE FLOW; HOST PREFERENCE; ISOLATED POPULATION; REPRODUCTIVE EFFORT; REPRODUCTIVE ISOLATION; SYMPATRY;

COLLINSIA; COLLINSIA TORREYI; EUPHYDRYAS; EUPHYDRYAS EDITHA; PAPILIONOIDEA; PEDICULARIS; PEDICULARIS SEMIBARBATA;

ADAPTATION; ANIMAL; ARTICLE; BUTTERFLY; CLUTCH SIZE; DECISION MAKING; ECOSYSTEM; EGG LAYING; GENETICS; LARVA; PEDICULARIS; PHYSIOLOGY; REPRODUCTION; SPECIES DIFFERENCE; SPECIES DIFFERENTIATION;

ADAPTATION, BIOLOGICAL; ANIMALS; BUTTERFLIES; CHOICE BEHAVIOR; CLUTCH SIZE; ECOSYSTEM; GENETIC SPECIATION; LARVA; OVIPOSITION; PEDICULARIS; REPRODUCTION; SPECIES SPECIFICITY;

EID: 77955007182     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2009.00866.x     Document Type: Article

References (87)

1. Anthes N, Fartmann T, Hermann G. Wie lasst sich der Ruckgang des Goldenen Scheckfalters (Euphydryas aurinia) in Mitteleuropa stoppen?. Naturschutz und Landschaftsplanung 2003, 32:279-287.
2. Berlocher S H, Feder J L. Sympatric speciation in phytophagous insects: moving beyond controversy?. Ann. Rev. Entomol. 2002, 47:773-815.
3. Bernard G D, Remington C L. Color vision in Lycaena butterflies: spectral tuning of receptor arrays in relation to behavioral ecology. Proc. Natl. Acad. Sci. USA 1991, 88:2783-2787.
4. Boughton D A. Empirical evidence for complex source-sink dynamics with alternative states in a butterfly metapopulation. Ecology 1999, 80:2727-2739.
5. Bush G L. Sympatric speciation in phytophagous parasitic insects. Evolutionary strategies of parasitic insects and mites 1975, 187-207. Price P W. ed, Plenum, New York, NY
6. Caillaud M C, Via S. Specialized feeding behavior influences both ecological specialization and assortative mating in sympatric host races of pea aphids. Am. Nat. 2000, 156:606-621.
7. Carroll S P. Facing change: forms and foundations of contemporary adaptation to biotic invasions. Mol. Ecol. 2008, 17:361-372.
8. Carroll S P, Dingle H, Klassen S P. Genetic differentiation of fitness-associated traits among rapidly evolving populations of the soapberry bug. Evolution 1997, 51:1182-1188.
9. Carroll S P, Klassen S T P, Dingle H. Rapidly evolving adaptations to host ecology and nutrition in the soapberry bug. Evol. Ecol. 1998, 12:955-968.
10. Carroll S P, Marler M, Winchell R, Dingle H. Evolution of cryptic flight morph and life history differences during host race radiation in the soapberry bug, Jadera haematoloma Herrich-Schaeffer (Hemiptera: Rhopalidae). Ann. Entomol. Soc. Am. 2003, 96:135-143.
11. Chew F S, Robbins R K. Egg-laying in butterflies. The biology of butterflies 1984, 65-79. Vane-Wright R I, Ackery P R.eds, Academic Press, London, U.K
12. Clausen J, Keck D D, Hiesey W M. Experimental studies on the nature of species. IV. Genetic structure of ecological races 1941, Carnegie Institution of Washington Publication No. 242, Washington, DC
13. Coyne J A, Orr H A. Speciation 2004, Sinauer & Associates, Sunderland, MA
14. Craig T P, Itami J K, Abrahamson W G, Horner J D. Behavioral evidence for host-race formation in Eurosta solidaginis. Evolution 1993, 47:1696-1710.
15. Dambroski H R, Feder J L. Host plant and latitude-related diapause variation in Rhagoletis pomonella: a test for multifaceted life history adaptation on different stages of diapause development. J. Evol. Biol. 2007, 20:2101-2112.
16. Darwin C. On the origin of species by means of natural selection, or the preservation of favored races in the struggle for life 1859, John Murray, London, U.K
17. Diehl S R, Bush G L. The role of habitat preference in adaptation and speciation. Speciation and its consequences 1989, 345-365. Otte D, Endler J A. eds, Sinauer & Associates, Sunderland, MA
18. Dorchin N, Scott E R, Clarkin C E, Luongo M P, Jordan S, Abrahamson W G. Behavioral, ecological and genetic evidence confirm the occurrence of host-associated differentiation in goldenrod gall-midges. J. Evol. Biol. 2009, 22:729-739.
19. Dres M, Mallet J. Host races in plant-feeding insects and their importance in sympatric speciation. Philos. Trans. R. Soc. Lond. B 2002, 357:471-492.
20. Ehrlich P R. Intrinsic barriers to dispersal in the checkerspot butterfly Euphydryas editha. Science 1961, 134:108-109.
21. Ehrlich P R, Hanski I. On the wings of checkerspots: a model system for population biology 2004, Oxford Univ. Press, Oxford
22. Emelianov I, Mallet J, Baltensweiler W. Genetic differentiation in Zeiraphera diniana (Lepidoptera, Tortricidae, the Larch Budmoth): polymorphism, host races or sibling species. Heredity 1995, 75:416-424.
23. Emelianov I, Dres M, Baltensweiler W, Mallet J. Host-induced assortative mating in host races of the larch budmoth. Evolution 2001, 55:2002-2010.
24. Filchak K E, Roethele J B, Feder J L. Natural selection and sympatric divergence in the apple maggot Rhagoletis pomonella. Nature 2000, 407:739-742.
25. Forbes A A, Feder J L. Divergent preferences of Rhagoletis pomonella host races for olfactory and visual fruit cues. Entomol. Exp. Appl. 2006, 119:121-127.
26. Fordyce J A, Nice C C. Geographic variation in clutch size and a realized benefit of aggregative feeding. Evolution 2004, 58:447-450.
27. Forister M L. Independent inheritance of preference and performance in hybrids between host races of Mitoura butterflies (Lepidoptera: Lycaenidae). Evolution 2005, 59:1149-1155.
28. Frantz A, Calcagno V, Mieuzet L, Plantegenest M, Simon J C. Complex trait differentiation between host-populations of the pea aphid Acyrthosiphon pisum (Harris): implications for the evolution of ecological specialisation. Biol. J. Linn. Soc. 2009, 97:718-727.
29. Funk D J. Isolating a role for natural selection in speciation: host adaptation and sexual isolation in Neochlamisus bebbianae leaf beetles. Evolution 1998, 52:1744-1759.
30. Funk D J, Filchak K E, Feder J L. Herbivorous insects: model systems for the comparative study of speciation ecology. Genetica 2002, 116:251-267.
31. Hanski I. Metapopulation ecology 1999, Oxford Univ. Press, Oxford, U.K
32. Hanski I, Singer M C. Extinction-colonization dynamics and host-plant choice in butterfly metapopulations. Am. Nat. 2001, 158:341-353.
33. Harrison S, Murphy D D, Ehrlich P R. Distribution of the Bay Checkerspot Butterfly, Euphydryas editha bayensis: evidence for a metapopulations model. Am. Nat. 1988, 132:360-382.
34. Kuussaari M, Singer M C, Hanski I. Local specialization and landscape-level influence on host use in an herbivorous insect. Ecology 2000, 81:2177-2187.
35. Lafranchis T. Les papillons de jour de France, Belgique et Luxembourg, et leurs chenilles 2000, Collection Parthenope, Meze, France
36. Langerhans R B, Layman C A, Shokrollahi A M, DeWitt T J. Predator-driven phenotypic diversification in Gambusia affinis. Evolution 2004, 58:2305-2318.
37. Linn C, Feder J L, Nojima S, Dambroski H R, Berlocher S H, Roelofs W. Fruit odor discrimination and sympatric host race formation in Rhagoletis. Proc. Natl. Acad. Sci. USA 2003, 100:11490-11493.
38. Mackay D A. Prealighting search behavior and host plant selection by ovipositing Euphydryas editha butterflies. Ecology 1985, 66:142-151.
39. Mallet J. Hybridization, ecological races and the nature of species: empirical evidence for the ease of speciation. Philos. Trans. R. Soc. Lond. B 2008, 363:2971-2986.
40. Mayr E. Ecological factors in speciation. Evolution 1947, 1:263-288.
41. Mazel R. Structure et evolution du peuplement d'Euphydryas aurinia (Lepidoptera) dans le sud-ouest europeen. Vie Milieu 1986, 36:205-225.
42. McBride C S. Ecological genomics and incipient speciation in insects that have invaded novel host plants. 2008, Ph.D. thesis, Population Biology, Univ. of California at Davis, Davis, CA
43. McNeely C, Singer M C. Contrasting the roles of learning in butterflies foraging for nectar and oviposition sites. Anim. Behav. 2001, 61:847-852.
44. McPhail J D. Ecology and evolution of sympatric sticklebacks (Gasterosteus): morphological and genetic evidence for a species pair in Enos Lake, British Columbia. Can. J. Zool. 1984, 62:1402-1408.
45. Mercader R J, Aardema M L, Scriber J M. Hybridization leads to host-use divergence in a polyphagous butterfly sibling species pair. Oecologia 2009, 158:651-662.
46. Moore S D. Patterns of juvenile mortality within an oligophagous insect population. Ecology 1989, 70:1726-1737.
47. Ng D. A novel level of interactions in plant-insect systems. Nature 1988, 334:611-613.
48. Nosil P. Divergent host plant adaptation and reproductive isolation between ecotypes of Timema cristinae walking sticks. Am. Nat. 2007, 169:151-162.
49. Nosil P, Vines T H, Funk D J. Perspective: reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 2005, 59:705-719.
50. Nosil P, Harmon L J, Seehausen O. Ecological explanations for (incomplete) speciation. Trends Ecol. Evol. 2009, 24:145-156.
51. Opler P A, Wright A B. Peterson field guides: western butterflies 1999, Houghton Mifflin, Boston & New York
52. Papaj D R. Conditioning of leaf-shape discrimination by chemical cues in the butterfly, Battus philenor. Anim. Behav. 1986, 34:1281-1288.
53. Parmesan C. Climate and species' range. Nature 1996a, 382:765-766.
54. Parmesan C. Ecological and behavioral aspects of the interaction between host-plants and the checkerspot butterfly, Euphydryas editha. Integrative Biology 1996b, Ph.D. thesis, Univ. of Texas at Austin, Austin, TX
55. Parmesan C, Singer M C, Harris I. Absence of adaptive learning from the oviposition behavior of a checkerspot butterfly. Anim. Behav. 1995, 50:161-175.
56. Pratt G F, Hein E W, Krofta D M. Newly discovered populations and food plants extend the range of the endangered quino checkerspot butterfly, Euphydryas editha quino (Nymphalidae) in Southern California. J. Lepid. Soc. 2001, 55:176-178.
57. Radtkey R R, Singer M C. Repeated reversals of host-preference evolution in a specialist insect herbivore. Evolution 1995, 49:351-359.
58. Rausher M D. Search image for leaf shape in a butterfly. Science 1978, 200:1071-1073.
59. Rausher M D, Mackay D A, Singer M C. Pre-alighting and post-alighting host discrimination by Euphydryas editha butterflies: the behavioral mechanisms causing clumped distributions of egg clusters. Anim. Behav. 1981, 29:1220-1228.
60. Rice W R, Hostert E E. Laboratory experiments on speciation: what have we learned in 40 years?. Evolution 1993, 47:1637-1653.
61. Sandoval C P. Differential visual predation on morphs of Timema cristinae (Phasmatodeae, Timemidae) and its consequences for host-range. Biol. J. Linn. Soc. 1994, 52:341-356.
62. Sandoval C P, Nosil P. Counteracting selective regimes and host preference evolution in ecotypes of two species of walking-sticks. Evolution 2005, 59:2405-2413.
63. Schluter D. The ecology of adaptive radiations 2000, Oxford Univ. Press, Oxford, U.K
64. Singer M C. Evolution of food-plant preference in the butterfly Euphydryas editha. Evolution 1971, 25:383-389.
65. Singer M C. Complex components of habitat suitability within a butterfly colony. Science 1972, 176:75-77.
66. Singer M C. Determinants of multiple host use by a phytophagous insect population. Evolution 1983, 37:389-403.
67. Singer M C. The definition and measurement of oviposition preference in plant-feeding insects. Insect-plant interactions 1986, 65-94. Miller J RMiller T A. eds, Springer, New York, NY
68. Singer M C, Parmesan C. Sources of variations in patterns of plant insect association. Nature 1993, 361:251-253.
69. Singer M C, Thomas C D. Evolutionary responses of a butterfly metapopulation to human- and climate-caused environmental variation. Am. Nat. 1996, 148:S9-S39.
70. Singer M C, Wee B. Spatial pattern in checkerspot butterfly-host plant association at local, metapopulation and regional scales. Ann. Zool. Fenn. 2005, 42:347-361.
71. Singer M C, Ng D, Thomas C D. Heritability of oviposition preference and its relationship to offspring performance within a single insect population. Evolution 1988, 42:977-985.
72. Singer M C, Vasco D, Parmesan C, Thomas C D, Ng D. Distinguishing between preference and motivation in food choice - an example from insect oviposition. Anim. Behav. 1992, 44:463-471.
73. Singer M C, Thomas C D, Parmesan C. Rapid human-induced evolution of insect host associations. Nature 1993, 366:681-683.
74. Singer M C, Stefanescu C, Pen I. When random sampling does not work: standard design falsely indicates maladaptive host preferences in a butterfly. Ecol. Lett. 2002, 5:1-6.
75. Singer M C, Wee B, Hawkins S, Butcher M. Rapid natural and anthropogenic diet evolution: three examples from checkerspot butterflies. The evolutionary ecology of herbivorous insects: speciation, specialization and radiation 2008, 311-324. Tilmon K J, ed, Univ. of California Press, Berkeley, CA
76. Smith D C. Heritable divergence of Rhagoletis pomonella host races by seasonal asynchrony. Nature 1988, 336:66-67.
77. Thomas C D. Butterfly larvae reduce host plant survival in vicinity of alternative host species. Oecologia 1986, 70:113-117.
78. Thomas C D, Singer M C. Variation in host preference affects movement patterns within a butterfly population. Ecology 1987, 68:1262-1267.
79. Thomas C D, Vasco D, Singer M C, Ng D, White R R, Hinkley D. Diet divergence in two sympatric congeneric butterflies: community or species level phenomenon?. Evol. Ecol. 1990, 4:62-74.
80. Thomas C D, Singer M C, Boughton D A. Catastrophic extinction of population sources in a butterfly metapopulation. Am. Nat. 1996, 148:957-975.
81. Thompson J N. Evolutionary ecology of the relationship between oviposition preference and performance of offspring in phytophagous insects. Entomol. Exp. Appl. 1988, 47:1570-7458.
82. Thompson J N, Pellmyr O. Evolution of oviposition behavior and host preference in Lepidoptera. Ann. Rev. Entomol. 1991, 36:65-89.
83. Tilmon K J. The evolutionary biology of herbivorous insects: specialization, speciation, and radiation 2008, Univ. of California Press, Berkeley, CA
84. Turesson G. The genotypical response of the plant species to the habitat. Hereditas 1922, 3:211-350.
85. Via S. Reproductive isolation between sympatric races of pea aphids. I. Gene flow restriction and habitat choice. Evolution 1999, 53:1446-1457.
86. Wee B. Effects of geographic distance, landscape features and host association on genetic differentiation of checkerspot butterflies. Integrative biology 2004, Ph.D. thesis, Univ. of Texas at Austin, Austin, TX
87. Weiss S B, Murphy D D, White R R. Sun, slope, and butterflies - topographic determinants of habitat quality for Euphydryas editha. Ecology 1988, 69:1486-1496.