Divergent host plant specialization as the critical driving force in speciation between populations of a phytophagous ladybird beetle

Journal of Evolutionary Biology

Volumn 24, Issue 7, 2011, Pages 1421-1432

  Matsubayashi, K W ^a   Kahono, S ^b   Katakura, H ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b INDONESIAN INSTITUTE OF SCIENCES   (Indonesia)

Author keywords

Ecological speciation; Extreme host shift; Host fidelity; Host race; Immigrant inviability

Indexed keywords

MITOCHONDRIAL DNA; SPACER DNA;

BEETLE; DIVERGENCE; FIELD SURVEY; GENE FLOW; HOST PLANT; HOST PREFERENCE; IMMIGRANT POPULATION; SPECIALIZATION; SPECIATION (BIOLOGY); SYMPATRY;

ANGIOSPERM; ANIMAL; ARTICLE; BEETLE; DEMOGRAPHY; FEEDING BEHAVIOR; GENETIC VARIABILITY; GENETICS; INDONESIA; INTRODUCED SPECIES; LARVA; MIKANIA; PHYSIOLOGY; SPECIES DIFFERENCE; SPECIES DIFFERENTIATION;

ANIMALS; BEETLES; DEMOGRAPHY; DNA, INTERGENIC; DNA, MITOCHONDRIAL; FEEDING BEHAVIOR; GENETIC SPECIATION; GENETIC VARIATION; INDONESIA; INTRODUCED SPECIES; LAMIACEAE; LARVA; MIKANIA; SPECIES SPECIFICITY;

COCCINELLIDAE; COLEOPTERA; HENOSEPILACHNA;

EID: 79959341438     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2011.02274.x     Document Type: Article

References (72)

1. Ballkau, B.J. & Feldman, M.W. 1973. Selection for migration modification. Genetics 74: 171-174.
2. Bandelt, H.J., Forster, P. & Röhl, A. 1999. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16: 37-48.
3. Berlocher, S.H. & Feder, J.L. 2002. Sympatric speciation in phytophagous insects: moving beyond controversy? Annu. Rev. Entomol. 47: 773-815.
4. Bush, G.L. 1969. Sympatric host race formation and speciation in frugivorous flies of the genus Rhagoletis (Diptera, Tephritidae). Evolution 23: 237-251.
5. Carvajal-Rodriguez, A. & Rolan-Alvarez, E. 2005. JMATING: a software for the analysis of sexual selection and sexual isolation effects from mating frequency data. BMC Evol. Biol. 6: 40.
6. Coyne, J.A. & Orr, H.A. 1989. Patterns of speciation in Drosophila. Evolution 43: 362-381.
7. Coyne, J.A. & Orr, H.A. 1997. "Patterns of speciation in Drosophila" revisited. Evolution 51: 295-303.
8. Coyne, J.A. & Orr, H.A. 2004. Speciation. Sinauer Associates, Sunderland, MA.
9. Craig, T.P., Itami, J.K. & Abrahamson, W.G. 1993. Behavioral evidence for host-race formation in Eurosta solidaginis. Evolution 47: 1696-1710.
10. Dieckmann, U., Doebeli, M., Metz, J.A.J. & Tautz, D. 2004. Adaptive Speciation. Cambridge Univ. Press, Cambridge, UK.
11. Diehl, S.R. & Bush, G.L. 1984. An evolutionary and applied perspective of insects biotypes. Annu. Rev. Entomol. 29: 471-504.
12. Diehl, S.R. & Bush, G.L. 1989. The role of habitat preference in adaptation and speciation. In: Speciation and Its Consequences (D. Otte & J.A. Endler, eds), pp. 345-365. Sinauer Associates, Sunderland, MA.
13. Dobzhansky, T. 1937. Genetics and the Origin of Species. Columbia Univ Press, New York.
14. Drés, 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: 471-492.
15. Excoffier, L., Smouse, P.E. & Quattro, J.M. 1992. Analysis of molecular variance inferred from metric distance among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479-491.
16. Excoffier, L., Laval, G. & Schneider, S. 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol. Bioinform. Online 1: 47-50.
17. Feder, J.L., Opp, S., Wlazlo, B., Reynolds, K., Go, W. & Spisak, S. 1994. Host fidelity is an effective pre-mating barrier between sympatric races of the apple maggot fly. Proc. Natl Acad. Sci. USA 91: 7990-7994.
18. Feder, J.L., Roethle, J.B., Wlazlo, B. & Berlocher, S.H. 1997. The selective maintenance of allozyme differences between sympatric host races of the apple maggot fly. Proc. Natl Acad. Sci. USA 94: 11417-11421.
19. Filchak, K.E., Roethele, J.B. & Feder, J.L. 2000. Natural selection and sympatric divergence in the apple maggot Rhagoletis pomonella. Nature 407: 739-742.
20. Fry, J.D. 1996. The evolution of host specialization: are trade-offs overrated? Am. Nat. 148: S84-S107.
21. Fujiyama, N., Ueno, H., Kahono, S. & Katakura, H. 2001. Preliminary experiments on adult food preference of the Indonesian phytophagous ladybird beetle, Epilachna sp. aff. emarginata (Coleoptera: Coccinellidae). Entomol. Sci. 4: 35-37.
22. Funk, D.J. 1998. Isolating a role for natural selection in speciation: host adaptation and sexual isolation in Neochlamisus bebbianae leaf beetles. Evolution 52: 1744-1759.
23. Funk, D.J. 2009. Investigating ecological speciation. In: Speciation and Patterns of Diversity (R.B. Butlin, J.R. Bridle & D. Schluter, eds), pp. 195-218. Cambridge Univ. Press, Cambridge, UK.
24. Funk, D.J. & Nosil, P. 2008. Comparative analyses of ecological speciation. In: Specialization, Speciation and Radiation: The Evolutionary Biology of Herbivorous Insects (K. Tilmon, ed), pp. 117-135. University of California Press, Berkeley, London, UK.
25. Funk, D.J., Filchak, K.E. & Feder, J.L. 2002. Herbivorous insects: model systems for the comparative study of speciation ecology. Genetica 116: 251-267.
26. Funk, D.J., Nosil, P. & Etges, W.J. 2006. Ecological divergence exhibits consistently positive associations with reproductive isolation across disparate taxa. Proc. Natl Acad. Sci. USA 103: 3209-3213.
27. Futuyma, D.J. & Moreno, G. 1988. The evolution of ecological specialization. Ann. Rev. Ecol. Syst. 19: 207-233.
28. Gavrilets, S. 2004. Fitness Landscapes and the Origin of Species. Princeton Univ Press, Princeton, NJ, USA.
29. Gavrilets, S. & Vose, A. 2005. Dynamic patterns of adaptive radiation. Proc. Natl Acad. Sci. USA 102: 18040-18045.
30. Gleason, J.M. & Ritchie, M.G. 1998. Evolution of courtship song and reproductive isolation in the Drosophila willistoni complex: do sexual signals diverge the most quickly? Evolution 52: 1492-1500.
31. Hawthorne, D.J. & Via, S. 2001. Genetic linkage of ecological specialization and reproductive isolation in pea aphids. Nature 412: 904-907.
32. Hendry, A.P., Nosil, P. & Rieseberg, L.H. 2007. The speed of ecological speciation. Funct. Ecol. 21: 455-464.
33. Hirai, Y., Kobayashi, H., Koizumi, T. & Katakura, H. 2006. Field-cage experiments on host fidelity in a pair of sympatric phytophagous ladybird beetles. Entomol. Exp. Appl. 118: 129-135.
34. Joshi, A. & Thompson, J.N. 1995. Trade-offs and the evolution of host specialization. Evol. Ecol. 9: 82-92.
35. Kahono, S., Pujiastuti, L.E., Fujiyama, N., Nakano, S. & Katakura, H. 2002. Food preference of some populations of a ladybird beetle Epilachna sp. aff. emarginata (Coleoptera; Coccinellidae; Epilachninae). Berita Biologi. 6: 481-485.
36. Katakura, H. 1985. Sperm displacement in Henosepilachna pustulosa (Coleoptera, Coccinellidae). Kontyu (Tokyo) 53: 516-519.
37. Katakura, H. & Hosogai, T. 1994. Performance of hybrid ladybird beetles (Epilachna spp.) on the host plants of parental species. Entomol. Exp. Appl. 71: 81-85.
38. Katakura, H., Shioi, M. & Kira, Y. 1989. Reproductive isolation by host specificity in a pair of phytophagous ladybird beetles. Evolution 43: 1045-1053.
39. Katakura, H., Nakano, S., Kahono, S., Abbas, I. & Nakamura, K. 2001. Epilachnine ladybird beetles (Coleoptera, Coccinellidae) of Sumatra and Java. Tropics 10: 325-352.
40. Kirkpatrick, M. & Ravigné, V. 2002. Speciation by natural and sexual selection: models and experiments. Am. Nat. 159(Suppl): S22-S35.
41. Kobayashi, N., Ohta, Y., Katoh, T., Kahono, S., Hartini, S. & Katakura, H. 2009. Molecular phylogenetic analysis of three groups of Asian epilachnine ladybird beetles recognized by the female internal reproductive organs and modes of sperm transfer. J. Nat. Hist. 431: 637-1649.
42. Kostermans, A.J.G., Wirjahardja, S. & Dekker, R.J. 1987. The weeds: description, ecology and control. In: Weeds of rice in Indonesia (M. Soerjani, A.J.G. Kostermans & G. Tjitrosoepomo, eds), pp. 24-565. Balai Pustaka, Jakarta.
43. Lowry, B.D., Modliszewski, J.L., Wright, K.M., Wu, C.A. & Willis, J.H. 2008. The strength and genetic basis of reproductive isolating barriers in flowering plants. Philos. Trans. R. Soc. Lond. B Biol. Sci. 363: 3009-3021.
44. Malausa, T., Bethenod, M.-T., Bontemps, A., Bourguet, D., Crnuet, J.-M. & Ponsard, S. 2005. Assortative mating in sympatric host-races of the European corn borer. Science 308: 258-260.
45. Matsubayashi, K.W. & Katakura, H. 2009. Contribution of multiple isolating barriers to reproductive isolation between a pair of phytophagous ladybird beetles. Evolution 63: 2563-2580.
46. Matsubayashi, K.W., Ohshima, I. & Nosil, P. 2010. Ecological speciation in phytophagous insects. Entomol. Exp. Appl. 134: 1-27.
47. Maynard Smith, J. 1966. Sympatric speciation. Am. Nat. 100: 637-650.
48. Mayr, E. 1963. Animal Species and Evolution. Belknap Press, Cambridge, MA.
49. Mendelson, T.C. 2003. Sexual isolation evolves faster than hybrid inviability in a diverge and sexually dimorphic genus of freshwater fish (Percidae: Etheostoma). Evolution 57: 317-327.
50. Nosil, P. 2004. Reproductive isolation caused by visual predation on migrants between divergent environments. Proc. R. Soc. Lond. B 271: 1521-1528.
51. Nosil, P. 2007. Divergent host plant adaptation and reproductive isolation between ecotypes of Timema cristinae walking sticks. Am. Nat. 169: 151-162.
52. Nosil, P. & Harman, L. 2009. Niche dimensionality and ecological speciation. In: Speciation and Patterns of Diversity (R.B. Butlin, J.R. Bridle & D. Schluter, eds), pp. 127-154. Cambridge Univ. Press, Cambridge, UK.
53. Nosil, P., Vines, T.H. & Funk, D.J. 2005. Reproductive isolation caused by natural selection against immigrants from divergent habitats. Evolution 59: 705-719.
54. Ohshima, I. 2008. Host race formation in the leaf-mining moth Acrocercops transecta (Lepidoptera: Gracillariidae). Biol. J. Linn. Soc. 93: 135-145.
55. Pappers, S.M., van der Velde, G., Ouborg, N.J. & van Groenendael, J.M. 2002. Genetically based polymorphisms in morphology and life history associated with putative host races of the water lily leaf beetle, Galerucella nymphaeae. Evolution 56: 1610-1621.
56. R Development Core Team 2009. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL.
57. Rice, W.R. 1989. Analyzing tables of statistical tests. Evolution 43: 223-225.
58. Rice, W.R. & Hostert, E.E. 1993. Laboratory experiments on speciation: what have we learned in 40years? Evolution 47: 1637-1653.
59. Rice, W.R. & Salt, G. 1990. The evolution of reproductive isolation as a correlated character under sympatric conditions: experimental evidence. Evolution 44: 1140-1152.
60. Rolán-Alvarez, E. & Caballero, A. 2000. Estimating sexual selection and sexual isolation effects from mating frequencies. Evolution 54: 30-36.
61. Rundle, H.D. & Nosil, P. 2005. Ecological speciation. Ecol. Lett. 8: 336-352.
62. Schluter, D. 1998. Ecological causes of speciation. In: Endless Forms: Species and Speciation (D.J. Howard & S.H. Berlocher, eds), pp. 114-129. Oxford Univ. Press, Oxford, UK.
63. Schluter, D. 2000. The Ecology of Adaptive Radiation. Oxford Univ. Press, Oxford, UK.
64. Schluter, D. 2001. Ecology and the origin of species. Trends Ecol. Evol. 16: 372-380.
65. Sokal, R.R. & Rohlf, F.J. 1995. Biometry, 3rd edn. Freeman, New York.
66. Tamura, K., Dudley, J., Nei, M. & Kumar, S. 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software. Mol. Biol. Evol. 24: 1596-1599.
67. Via, S. 1999. Reproductive isolation between sympatric races of pea aphids, I. Gene flow restriction and habitat choice. Evolution 53: 1446-1457.
68. Via, S., Bouck, A.C. & Skillman, S. 2000. Reproductive isolation between divergent races of pea aphids in two hosts. II. Selection against migrants and hybrids in the parental environments. Evolution 54: 1626-1637.
69. Wang, B., Park, J., Watabe, H., Gao, J., Xiangyu, J., Aotsuka, T., Chen, H. & Zhang, Y. 2006. Molecular phylogeny of the Drosophila virilis section (Diptera: Drosophilidae) based on mitochondrial and nuclear sequences. Mol. Phyl. Evol. 40: 484-500.
70. Wardani, M. 2001. Leucas R. Br. In: Plant Resources of South-East Asia No. 12(2) Medical and Poisonous Plants 2 (J.L.C.H. van Valkenburg & N. Bunyapraphatsara, eds), pp. 337-341. Backhuys Publishers, Leiden.
71. White, T.J., Bruns, T., Lee, S. & Taylor, J.W. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR Protocols: A Guide to Methods & Applications (M.A. Innis, D.H. Gelfand, J. Sninsky & T. White, eds), pp. 315-322. Academic Press, San Diego, USA.
72. Whitten, T., Soeriaatmadja, R.E. & Afiff, S.A. 1996. The Ecology of Java and Bali. Periplus Editions, Singapore.