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Mitochondrial DNA Clocks and the Phylogeny of Danaus Butterflies

Published online by Cambridge University Press:  19 September 2011

Gugs Lushai
Affiliation:
Ecology and Biodiversity Division, School of Biological Sciences, University of Southampton, Bassett Crescent East, Southampton S016 7PX, UK
David A. S. Smith
Affiliation:
Natural History Museum, Eton College, Windsor SL4 6EW, UK
Dave Goulson
Affiliation:
Ecology and Biodiversity Division, School of Biological Sciences, University of Southampton, Bassett Crescent East, Southampton S016 7PX, UK
John A. Allen
Affiliation:
Ecology and Biodiversity Division, School of Biological Sciences, University of Southampton, Bassett Crescent East, Southampton S016 7PX, UK
Norman Maclean
Affiliation:
Ecology and Biodiversity Division, School of Biological Sciences, University of Southampton, Bassett Crescent East, Southampton S016 7PX, UK
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Abstract

Molecular clocks based on sequence change in mitochondrial (mt) DNA have been useful for placing molecular phytogenies in their historical context, thereby enhancing evolutionary insight. Nonetheless, despite their importance to phylogeographers, the methodology is controversial. Here we report on two mitochondrial clocks for the butterfly genus Danaus based on sequences from the cytochrome c oxidase subunit I (COI) and small subunit 12S rRNA (12S) genes. Both clocks are, within the context of Danaus, reliable time-keepers, mutually consistent and, respectively, in agreement with a crustacean COI clock and a molluscan 12S clock. Though we have no fossils with which directly to calibrate sequence divergence rates for Danaus, the 12S molluscan and COI crustacean clocks chosen for comparison were calibrated to radiometrically dated geomorphological events. Our results indicate that the Danaus COI clock evolves approximately four times faster than the 12S clock. Differences between rates of sequence change in terminal sister-taxa are small and likelihood ratio tests do not reject a hypothesis that evolution has been clock-like. The species Danaus chrysippus is paraphyletic and, therefore, invalid. Danaus probably split from its sister-genus Tirumala around 4.9 ± 0.3 million years ago in the early Pliocene.

Résumé

Les horloges moléculaires basées sur le changement de séquence de l'ADN mitochondrial (mt) ont été utiles pour replacer les phylogénies moléculaires dans leur contexte historique, et ainsi améliorer nos connaissances sur l'évolution. Cependant, malgré leur importance pour les phylogéographes, la méthodologie est contestée. Nous présentons ici deux horloges moléculaíres pour le papillon du genre Danaus établies sur les séquences des gènes du cytochrome c oxidase sous unité I (COI) et la petite sous unité 12S rRNA (12S). Les deux horloges sont, dans le contexte du genre Danaus, des chronomètres fiables, mutuellement compatibles et, respectivement, en accord avec 1'horloge de crustacé COI et l'horloge de mollusque 12S. Bien que nous n'ayons pas de fossile avec lequel calibrer les taux de divergence des séquences pour Danaus, les horloges de mollusque 12S et de crustacé COI choisis pour comparaison ont été calibrées avec des événements géomorphologiques datés par radiométrie. Nos résultats indiquent que chez Danaus l'horloge COI évolue approximativement 4 fois plus vite que l'horloge 12S. Les différences entre les taux de changement de séquence de taxons frères terminaux sont faibles et les tests du taux de vraisemblance ne rejettent pas l'hypothèse selon laquelle l'évolution a été régulière. L'espèce Danaus chrysippus est paraphylétique et, par conséquent non valide. Le genre Danaus s'est probablement séparé de son genre frère il y a environ 4,9 ± 0,3 millions d'années au debut du Pliocène.

Type
Research Articles
Copyright
Copyright © ICIPE 2003

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References

REFERENCES

Ackery, P. R. and Vane-Wright, R. I. (1984) Milkweed Butterflies. British Museum (Natural History), London. 425 pp.Google Scholar
Avise, J. C. (1994) Molecular Markers, Natural History and Evolution. Chapman and Hall, New York. 511 pp.CrossRefGoogle Scholar
Avise, J. C. (2000) Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge. 447 pp.CrossRefGoogle Scholar
Bermingham, E. and Lessios, H. (1993) Rate variation of protein and mtDNA evolution as revealed by sea urchins separated by the Isthmus of Panama. Proc. Natl. Acad. Sci. USA 90, 27342738.CrossRefGoogle ScholarPubMed
Bremer, K. (1994) Branch support and tree stability. Cladistics 10, 295304.CrossRefGoogle Scholar
Brower, A. Z. (1994) Rapid morphological radiation and convergence among races of Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc. Natl. Acad. Sci. USA 91, 64916495.CrossRefGoogle ScholarPubMed
Brown, W. M. (1983) Evolution of animal mitochondrial DNA, pp. 6288. In Evolution of Genes and Proteins (Edited by Nei, M. and Koehn, R. K.). Sinauer, Sunderland.Google Scholar
Brown, W. M., George, M. Jr and Wilson, A. C. (1979) Rapid evolution of animal mitochondrial DNA. Proc. Natl. Acad. Sci. USA 76, 19671971.CrossRefGoogle ScholarPubMed
Cracraft, J. (1983) Species concepts and speciation analysis. Current Ornithology 1, 159187.CrossRefGoogle Scholar
DeSalle, R., Freedman, T., Prager, E. M. and Wilson, A. C. (1987) Tempo and mode of sequence evolution in mitochondrial DNA of Hawaiian Drosophila. J. Mol. Evol. 26, 157164.CrossRefGoogle ScholarPubMed
Felsenstein, J. (1993) PHYLIP (phylogeny inference package) version 3.5. Distributed by the author, Department of Genetics, University of Washington, Seattle.Google Scholar
Goldman, N. (1993) Statistical tests of models of DNA substitution. J. Mol. Evol. 36, 182198.CrossRefGoogle ScholarPubMed
Hillis, D. M., Mable, B. K. and Moritz, C. (1996) Applications of molecular systematics: The state of the field and a look to the future, pp. 515543. In Molecular Systematics (2nd edn) (Edited by Hillis, D. M., Moritz, C. and Mable, B. K.). Sinauer, Sunderland.Google Scholar
Hopkins, D. M. (1967) The Cenozoic history of Beringia: A synthesis, pp. 451484. In The Bering Land Bridge (Edited by Hopkins, D. M.). Stanford University Press, Stanford.Google Scholar
Knowlton, N., Weight, L. A., Solorzano, L. A., Mills, D. K. and Bermingham, E. (1993) Divergence in proteins, mitochondrial DNA and reproductive compatibility across the Isthmus of Panama. Science 260, 16291632.CrossRefGoogle ScholarPubMed
Lessios, H. A. (1979) Use of Panamian sea urchins to test the molecular clock. Nature 280, 599601.CrossRefGoogle Scholar
Lessios, H. A. (1998) The first stage of speciation as seen in organisms separated by the isthmus of Panama, pp. 186201. In Endless Forms: Species and Speciation (Edited by Howard, D. J. and Berlocher, S. H.). Oxford University Press, New York.Google Scholar
Li, W.-H. (1997) Molecular Evolution. Sinauer, Sunderland. 487 pp.Google ScholarPubMed
Lushai, G., Smith, D. A. S., Gordon, I. J., Goulson, D., Allen, J. A. and Maclean, N. (2003a) Incomplete sexual isolation between subspecies of the butterfly Danaus chrysippus (L.) and the creation of a hybrid zone. Heredity 90, 236246.CrossRefGoogle ScholarPubMed
Lushai, G., Zalucki, M. P., Goulson, D. and Smith, D. A. S. (2003b) The lesser wanderer butterfly, formerly known as subspecies petilia (Stoll 1790) of Danaus chrysippus (L.) (1758) (Lepidoptera: Danainae), is a species. Austral. J. Entomol. (in press).Google Scholar
Mayr, E. (1942) Systematics and the Origin of Species. Columbia University Press, New York. 450 pp.Google Scholar
Page, R. D. M. and Holmes, E. G. (1998) Molecular Evolution. Blackwell, Oxford. 346 pp.Google Scholar
Reid, D. G., Rumbak, E. and Thomas, R. H. (1996) DNA, morphology and fossils: Phylogeny and evolutionary rates of the gastropod genus Littorina. Phil. Trans. R. Soc. Lond. B 351, 877895.Google ScholarPubMed
Rumbak, E., Reid, D. G. and Thomas, R. H. (1994) Reconstruction of phylogeny of 11 species of Littorina (Gastropoda: Littorinidae) using mitochondrial sequence data. Nautilus 2, 9197.Google Scholar
Shackleton, N. J., Backman, J., Zimmerman, H., Kent, D. V., Hall, M. A., Roberts, D. G., Schnitker, D., Baldauf, J. G., Despraires, A., Homrighausen, R., Huddlestun, P., Keene, J. B., Kaltenback, A. J., Krumsiek, K. A. O., Morton, A. C., Murray, J. W. and Westberg-Smith, J. (1984) Oxygen isotope calibration of the onset of ice-rafting and history of glaciation in the North Atlantic region. Nature 307, 620623.CrossRefGoogle Scholar
Smith, D. A. S., Gordon, I. J., Depew, L. A. and 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. Biol. J. Linn. Soc. 65, 140.Google Scholar
Smith, D. A. S., Gordon, I. J., Lushai, G., Goulson, D., Allen, J. A. and 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. Biol. J. Linn. Soc. 76, 535544.CrossRefGoogle Scholar
Smith, D. A. S., Owen, D. F., Gordon, I. J. and 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. Zool. J. Linn. Soc. 120, 5178.CrossRefGoogle Scholar
Swofford, D. L. (1998) PAUP*, Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer, Sunderland.Google Scholar
Wilson, A. C., Cann, R. L., Carr, S. M., George, M. Jr, Gyllensten, U. B., Helm-Bychowski, K. M., Higuchi, R. G., Palumbi, S. R., Prager, E. M., Sage, R. D. and Stoneking, M. (1985) Mitochondrial DNA and two perspectives on evolutionary genetics. Biol. J. Linn. Soc. 26, 375400.CrossRefGoogle Scholar
Zuckerhandl, E. and Pauling, L. (1965) Evolutionary divergence and convergence in proteins, pp. 97166. In Evolving Genes and Proteins (Edited by Bryson, V. and Vogel, H. L.). Academic Press, New York.CrossRefGoogle Scholar