Reinforcement in hybrids among once isolated semispecies of Danaus chrysippus (L.) and evidence for sex chromosome evolution

Ecological Entomology

Volumn 35, Issue SUPPL. 1, 2010, Pages 77-89

  Smith, David A S ^a   Gordon, Ian J ^b   Allen, John A ^c  

^a DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

^b INTERNATIONAL CENTRE OF INSECT PHYSIOLOGY AND ECOLOGY ICIPE   (Kenya)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

Haldane rule; Hybrid zone; Pleistocene; Reproductive isolating barriers; Semispecies; Sex linkage; Spiroplasma; Superspecies; W linkage

Indexed keywords

BIOGEOGRAPHY; BUTTERFLY; CHROMOSOME; CLIMATE CHANGE; ENDOSYMBIONT; GENE EXPRESSION; GENE FLOW; HOLOCENE; HYBRID ZONE; ISOLATED POPULATION; KARYOTYPE; PLEISTOCENE; REFUGIUM; REPRODUCTIVE ISOLATION;

DANAUS CHRYSIPPUS; SPIROPLASMA;

EID: 74549160302     PISSN: 03076946     EISSN: 13652311     Source Type: Journal    
DOI: 10.1111/j.1365-2311.2009.01143.x     Document Type: Article

References (77)

1. Ackery, P.R. & Vane-Wright, R.I. (1984) Milkweed Butterflies. British Museum (Natural History), London, U.K.
2. Avise, J.C. (1986) Mitochondrial DNA and the evolutionary genetics of higher animals. Philosophical Transactions of the Royal Society of London B, 312, 325 342.
3. Avise, J.C. (1994) Molecular Markers, Natural History and Evolution, 1st edn. Chapman & Hall, New York, New York.
4. Ayala, F.J., Tracey, M.L., Hedgecock, D. & Richmond, R.C. (1975) Genetic differentiation during the speciation process in Drosophila. Evolution, 28, 576 592.
5. Bates, H.W. (1864) The Naturalist on the River Amazons, 2nd edn. John Murray, London, U.K.
6. Boppré, M. (1981) Adult Lepidoptera 'feeding' at withered Heliotropium plants (Boraginaceae) in East Africa. Ecological Entomology, 6, 449 452.
7. Boppré, M. (1983) Leaf scratching-a specialized behaviour of danaine butterflies for gathering plant substances. Oecologia, 59, 414 416.
8. Brower, L.P., Edmunds, M. & Moffitt, C.M. (1975) Cardenolide content and palatability of a population of Danaus chrysippus butterflies from West Africa. Journal of Entomology (A), 49, 183 196.
9. Brower, L.P., Gibson, D.O., Moffitt, C.M. & Panchen, A.L. (1978) Cardenolide content of Danaus chrysippus butterflies from three areas of East Africa. Biological Journal of the Linnean Society, 10, 251 273.
10. Brown, K.S., Sheppard, P.M. & Turner, J.R.G. (1974) Quaternary refugia in tropical America: evidence from race formation in Heliconius butterflies. Proceedings of the Royal Society of London B, 187, 369 378.
11. Clarke, C.A., & Sheppard, P.M. (1962) The genetics of the mimetic butterfly Papilio glaucus. Ecology, 43, 159 161.
12. Clarke, C.A., Sheppard, P.M. & Mittwoch, U. (1976) Heterochromatin polymorphism and colour pattern in the tiger swallow tail butterfly Papilio glaucus. Nature, 263, 585 587.
13. Clarke, C.A., Sheppard, P.M. & Smith, A.G (1973) The genitics of fore and hindwing colour in crosess between Danaus chrysippus from Australia and from Sierra Leone (Danaidae). Journal of the Lepidopterists' Society, 27, 73 77.
14. Cross, P. (2003) The Butterflies of Wondo Genet: An Introduction to the Butterflies of Ethiopia. Mega Printing Enterprises, Addis Ababa, Ethiopia.
15. Darwin, C.R. (1859) The Origin of Species, 1st edn. John Murray, London, U.K. [Consulted in Penguin Classics edn, 1968].
16. Deacon, J. & Lancaster, N. (1988) Late Quaternary Palaeoenvironments of Southern Africa. Clarendon Press, Oxford, U.K.
17. Engelstädter, J. & Hurst, G.D.D. (2007) The impact of male-killing bacteria on host evolutionary processes. Genetics, 175, 245 254.
18. Fisher, R.A. & Ford, E.B. (1928) The variability of species in the Lepidoptera, with reference to abundance and sex. Transactions of the Royal Entomological Society of London, 76, 367 379.
19. Flenley, J.R. (1979) The Equatorial Rain Forest: A Geological History. Butterworths, London, U.K.
20. Gazarve, E., Catalan, J., da Graca Ramalino, M., da Luz Mathias, M., Nunes, A.C., Britton-Davidian, J., et al. (2006) Do chromosomal hybrids necessarily suffer from developmental instability? Biological Journal of the Linnean Society, 88, 33 43.
21. Gordon, I.J. (1984) Polymorphism of the tropical butterfly Danaus chrysippus L. in Africa. Heredity, 53, 583 593.
22. Gordon, I.J. (1987) Natural selection for rare and mimetic colour pattern combinations in wild populations of the diadem butterfly Hypolimnas misippus L. Biological Journal of the Linnean Society, 31, 1 23.
23. Gupta, Y. (1964) Chromosomal studies of some Indian lepidoptera. Chromosoma, Berlin, 15, 540 561.
24. Haldane, J.B.S. (1922) Sex-ratio and unisexual sterility in hybrid animals. Journal of Genetics, 12, 101 109.
25. Hamilton, A.C. (1982) Environmental History of East Africa. Academic Press, London, U.K.
26. Herren, J.K., Gordon, I.J., Holland, P.W.H. & Smith, D.A.S. (2007) The butterfly Danaus chrysippus (Lepidoptera: Nymphalidae) in Kenya is variably infected with respect to genotype and body size by a maternally transmitted male-killing endosymbiont (Spiroplasma). International Journal of Tropical Insect Science, 27, 62 69.
27. Hurst, G.D.D., Hurst, L.D. & Majerus M. (1997) Cytoplasmic sex ratio distorters. Influential passengers (ed. by S. L. O'Neill, A. A. Hoffman and J. H. Werren pp. 125 154. Oxford University Press, Oxford, U.K.
28. Jaenike, J. (2007) Fighting back against male killers. Trends in Ecology & Evolution, 22, 167 169.
29. Jaenike, J. & Dyer, K.A. (2008) No resistance to male-killing Wolbachia after thousands of years of infection. Journal of Evolutionary Biology, 21, 1570 1577.
30. Jiggins, F.M., Hurst, G.D.D., Jiggins, C.D., von der Schulenburg, J.H.G. & Majerus, M.E.N. (2000) The butterfly Danaus chrysippus is infected by a male-killing Spiroplasma bacterium. Parasitology, 120, 439 446.
31. Kingdon, J.S. (1997) The Kingdon Field Guide to African Mammals. Academic Press, London, U.K.
32. Kitching, I.J. (1986) Allozyme variation in the milkweed butterflies (Lepidoptera: Danainae). Zoological Journal of the Linnean Society, 86, 367 389.
33. Larsen, T.B. (1968) Butterflies migrating on Ikoyi Island (Lagos). Nigerian Entomological Magazine, 1, 62.
34. Larsen, T.B. (1978) A mixed butterfly migration in West Africa (Bénin). Atalanta, 9, 191 198.
35. Lushai, G., Allen, J.A., Goulson, D., Maclean, N. & Smith, D.A.S. (2005a) The butterfly Danaus chrysippus (L.) in East Africa comprises polyphyletic, sympatric lineages that are, despite behavioural isolation, driven to hybridization by female-biased sex ratios. Biological Journal of the Linnean Society, 86, 117 131.
36. Lushai, G., Zalucki, M.P., Smith, D.A.S., Goulson, D. & Daniels, G. (2005b) The lesser wanderer butterfly, Danaus petilia (Stoll 1790) stat. rev. (Lepidoptera: Danainae), reinstated as a species. Australian Journal of Entomology, 44, 6 14.
37. Lushai, G., Smith, D.A.S., Gordon, I.J., Goulson, D., Allen, J.A. & Maclean, N. (2003a) Incomplete sexual isolation in sympatry between subspecies of the butterfly Danaus chrysippus (L.) and the creation of a hybrid zone. Heredity, 90, 236 246.
38. Lushai, G., Gordon, I.J. & Smith, D.A.S. (2003b) Evidence from mitochondrial DNA supports earlier records of African queen butterflies (Danaus chrysippus) migrating in East Africa. Journal of East African Natural History, 92, 119 125.
39. Lushai, G., Smith, D.A.S., Goulson, D., Allen, J.A. & Maclean, N. (2003c) Mitochondrial DNA clocks and the phylogeny of Danaus butterflies. Insect Science and its Applications, 23, 309 315.
40. Majerus, M.E.N. (2003) Sex Wars. Princeton University Press, Princeton, New Jersey.
41. Mallet, J. (1989) The genetics of warning colour in Peruvian hybrid zones of Heliconius erato and H. melpomene. Proceedings of the Royal Society of London B, 236, 163 185.
42. Mayr, E. (1942) Systematics and the Origin of Species. Columbia University Press, New York.
43. Mayr, E. (1963) Animal Species and Evolution. Harvard University Press, Cambridge, Massachusetts.
44. Moreau, R.E. (1966) The Bird Faunas of Africa and Its Islands. Academic Press, London, U.K.
45. Noor, M.A.F., Grams, K.L., Bertucci, L.A., Almendarez, Y., Reiland, J. & Smith, K.R. (2001) The genetics of reproductive isolation and the potential for gene exchange between Drosophila pseudoobscura and D. persimilis via backcross hybrid males. Evolution, 55, 512 521.
46. Owen, D.F. (1971) Tropical Butterflies. Clarendon Press, Oxford, U.K.
47. Owen, D.F. & Chanter, D.O. (1968) Population biology of tropical African butterflies. 2. Sex ratio and polymorphism in Danaus chrysippus L. Revues Zoologiques et Botaniques Africaines, 78, 81 97.
48. Pliske, T.E. (1975) Attraction of Lepidoptera to plants containing pyrrolizidine alkaloids. Environmental Entomology, 4, 455 473.
49. Poulton, E.B. (1904) [Notes on an exhibit]. Proceedings of the Entomological Society of London, 1903, liv lvi.
50. Rothschild, M., Von Euw, J., Reichstein, J., Smith, D.A.S. & Pierre, J. (1975) Cardenolide storage in Danaus chrysippus with additional notes on D. plexippus. Proceedings of the Royal Society of London B: Biological Sciences, 190, 1 31.
51. Samadi, S. & Barberousse, A. (2006) The tree, the network, and the species. Biological Journal of the Linnean Society, 89, 509 521.
52. Smith, D.A.S. (1975a) Genetics of some polymorphic forms of the African butterfly Danaus chrysippus L. (Lepidoptera: Danaidae). Entomologica Scandinavica, 6, 134 144.
53. Smith, D.A.S. (1975b) All-female broods in Danaus chrysippus L. and their ecological significance. Heredity, 34, 363 371.
54. Smith, D.A.S. (1976a) Phenotypic diversity, mimicry and natural selection in the African butterfly Hypolimnas misippus L. (Lepidoptera: Nymphalidae). Biological Journal of the Linnean Society, 8, 183 204.
55. Smith, D.A.S. (1976b) Evidence for autosomal meiotic drive in the butterfly Danaus chrysippus L. Heredity, 36, 139 142.
56. Smith, D.A.S. (1980) Heterosis, epistasis and linkage disequilibrium in a wild population of the polymorphic butterfly Danaus chrysippus (L.). Zoological Journal of the Linnean Society, 69, 87 109.
57. Smith, D.A.S. (1984) Mate selection in butterflies: competition, coyness, choice and chauvinism. The Biology of Butterflies, Symposia of the Royal Entomological Society of London, Vol. 11 (ed. R.I. Vane-Wright and P.R. Ackery pp. 225 244. Academic Press, London, U.K.
58. Smith, D.A.S. (1998) Non-Mendelian segregation and variable penetrance of colour genes in the polymorphic butterfly Danaus chrysippus (L.). Heredity, 80, 474 480.
59. Smith, D.A.S., Gordon, I.J., Depew, L.A. & Owen, D.F. (1998) Genetics of the butterfly Danaus chrysippus (L.) in a broad hybrid zone, with special reference to sex ratio, polymorphism and intragenomic conflict. Biological Journal of the Linnean Society, 65, 1 40.
60. Smith, D.A.S., Gordon, I.J., Lushai, G., Goulson, D., Allen, J.A. & Maclean, N. (2002) Hybrid queen butterflies from the cross Danaus chrysippus (L.)×D. gilippus (Cramer): confirmation of species status for the parents and further support for Haldane's Rule. Biological Journal of the Linnean Society, 76, 535 544.
61. Smith, D.A.S., Lushai, G. & Allen, J.A. (2005) A classification of Danaus butterflies (Lepidoptera: Nymphalidae) based upon data from morphology and DNA. Zoological Journal of the Linnean Society, 144, 191 212.
62. Smith, D.A.S. & Owen, D.F. (1997) Colour genes as markers for migratory activity: the butterfly Danaus chrysippus in Africa. Oikos, 78, 127 135.
63. Smith, D.A.S., Owen, D.F., Gordon, I.J. & Lowis, N.K. (1997) The butterfly Danaus chrysippus (L.) in East Africa: polymorphism and morph-ratio clines within a complex, extensive and dynamic hybrid zone. Zoological Journal of the Linnean Society, 120, 51 78.
64. Suomalainen, E., Cook, L.M. & Turner, J.R.G. (1973) Achiasmatic oögenesis in heliconiine butterflies. Hereditas, 74, 302 304.
65. Talbot, G. (1943) Revisional notes on the genus Danaus Kluk (Lep. Rhop. Danaidae). Transactions of the Royal Entomological Society of London, 93, 115 148.
66. Thomaz, D., Guillar, A. & Clarke, B. (1996) Extreme divergence of mitochondrial DNA within species of pulmonate land snails. Proceedings of the Royal Society of London B, 263, 363 368.
67. Traut, A. (1986) A genetic linkage study of W-chromosome-autosome fusions, breakage, and kinetic organization of chromosomes in Ephestia (Lepidoptera). Genetica, 69, 69 79.
68. Turner, J.R.G. & Sheppard, P.M. (1975) Absence of crossing-over in female butterflies (Heliconius). Heredity, 34, 265 269.
69. Velasco, J.D. (2008) The internodal species concept: a response to 'The tree, the network, and the species'. Biological Journal of the Linnean Society, 93, 865 869.
70. Wallace, A.R. (1865) On the phenomena of variation and geographical distribution as illustrated by the Papilionidae of the Malayan Region. Transactions of the Linnean Society, 25, 1 71.
71. Wallace, A.R. (1889) Darwinism. Macmillan, London, U.K.
72. White, M.J.D. (1973) Animal Cytology and Evolution, 3rd edn. Cambridge University Press, Cambridge, U.K.
73. White, M.J.D. (1978) Modes of Speciation. W. H. Freeman, San Francisco, California.
74. Whitmore, T.C. & Prance, G.T. (ed.) (1987) Biogeography and Quaternary History in Tropical America. Clarendon Press, Oxford, U.K.
75. Williams, C.B. (1930) Insect Migration. Collins, London, U.K.
76. Williams, M.A.J. & Faure, H. (ed.) (1980) The Sahara and the Nile: Quaternary Environments and Occupation in Northern Africa. A.A. Balkema, Rotterdam, the Natherlands.
77. Wright, S., 1968. Evolution and the Genetics of Populations, The Theory of Gene Frequencies, Vol. 2. Chicago University Press, Chicago, Illinois.