Abstract
—Molecular clocks based on sequence change in mitochondrial (mt) DNA have been useful for placing molecular phylogenies 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 moléculaires 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 l’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 début du Pliocène.
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References
Ackery P. R. and Vane-Wright R. L (1984) Milkweed Butterflies. British Museum (Natural History), London. 425 pp.
Avise J. C. (1994) Molecular Markers, Natural History and Evolution. Chapman and Hall, New York. 511 pp.
Avise J. C. (2000) Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge. 447 pp.
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, 2734–2738.
Bremer K. (1994) Branch support and tree stability. Cladistics 10, 295–304.
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, 6491–6495.
Brown W. M. (1983) Evolution of animal mitochondrial DNA, pp. 62–88. In Evolution of Genes and Proteins (Edited by M. Nei and R. K. Koehn). Sinauer, Sunderland.
Brown W. M., George M. Jr and Wilson A. C. (1979) Rapid evolution of animal mitochondrial DNA. Proc. Natl Acad. Sci. USA 76, 1967–1971.
Cracraft J. (1983) Species concepts and speciation analysis. Current Ornithology 1, 159–187.
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, 157–164.
Felsenstein J. (1993) PHYLIP (phylogeny inference package) version 3.5. Distributed by the author, Department of Genetics, University of Washington, Seattle.
Goldman N. (1993) Statistical tests of models of DNA substitution. J. Moi. Evol 36, 182–198.
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. 515–543. In Molecular Systematics (2nd edn) (Edited by D. M. Hillis, C. Moritz and B. K. Mable). Sinauer, Sunderland.
Hopkins D. M. (1967) The Cenozoic history of Beringia: A synthesis, pp. 451–484. In The Bering Land Bridge (Edited by D. M. Hopkins). Stanford University Press, Stanford.
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, 1629–1632.
Lessios H. A. (1979) Use of Panamian sea urchins to test the molecular clock. Nature 280, 599–601.
Lessios H. A. (1998) The first stage of speciation as seen in organisms separated by the isthmus of Panama, pp. 186–201. In Endless Forms: Species and Speciation (Edited by D. J. Howard and S. H. Berlocher). Oxford University Press, New York.
Li W.-H. (1997) Molecular Evolution. Sinauer, Sunderland. 487 pp.
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, 236–246.
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).
Mayr E. (1942) Systematics and the Origin of Species. Columbia University Press, New York. 450 pp.
Page R. D. M. and Holmes E. G. (1998) Molecular Evolution. Blackwell, Oxford. 346 pp.
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. Sec. Lond. B 351, 877–895.
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, 91–97.
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, 620–623.
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, 1–40.
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.) x D. gilippus (Cramer): Confirmation of species status for the parents and further support for Haldane’s Rule. Biol J. Linn. Soc. 76, 535–544.
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, 51–78.
Swofford D. L. (1998) PAUP*, Phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer, Sunderland.
Wilson A. C., Cann R. L., Carr S. M., George M. Jr., Gyllensten U. B., HelnvBychowski 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, 375–400.
Zuckerhandl E. and Pauling L. (1965) Evolutionary divergence and convergence in proteins, pp. 97–166. In Evolving Genes and Proteins (Edited by V. Bryson and H. L. Vogel). Academic Press, New York.
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Lushai, G., Smith, D.A.S., Goulson, D. et al. Mitochondrial DNA Clocks and the Phylogeny of Danaus Butterflies. Int J Trop Insect Sci 23, 309–315 (2003). https://doi.org/10.1017/S1742758400012376
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DOI: https://doi.org/10.1017/S1742758400012376