A MOLECULAR PHYLOGENY OF THE DROSOPHILA WILLISTONI GROUP: CONFLICTS BETWEEN SPECIES CONCEPTS?
Jennifer M. Gleason
Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, 06520-8106
Present address: School of Environmental and Evolutionary Biology, Bute Medical Building, University of St. Andrews, St. Andrews, Fife KY16 9TS, United Kingdom.Search for more papers by this authorElizabeth C. Griffith
Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut, 06520-8106
Search for more papers by this authorJeffrey R. Powell
Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, 06520-8106
Search for more papers by this authorJennifer M. Gleason
Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, 06520-8106
Present address: School of Environmental and Evolutionary Biology, Bute Medical Building, University of St. Andrews, St. Andrews, Fife KY16 9TS, United Kingdom.Search for more papers by this authorElizabeth C. Griffith
Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut, 06520-8106
Search for more papers by this authorJeffrey R. Powell
Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, 06520-8106
Search for more papers by this authorAbstract
The six sibling species of the Neotropical Drosophila willistoni group have a long history in studies of evolutionary biology, yet to date only one molecular study, which used allozymes, has been published on the phylogeny of the group. Here we present a phylogeny of the siblings based on the sequences of two nuclear genes, period (per) and Alcohol dehydrogenase (Adh), as well as the mitochondrial gene Cytochrome oxidase I (COI). Taken individually, only per has a strong phylogenetic signal supporting a well-resolved phylogeny of the group, and this phylogeny is different from that obtained using allozymes. The COI dataset by itself produces trees that disagree with per, and neither that data nor the Adh data have a strong phylogenetic signal, as indicated by low bootstrap values for all analyses. Combining the Adh and COI datasets results in the same tree as per alone. Combining all three genes results in the same topology, which is strongly supported. Two problematic taxa, D. pavlovskiana and a “Carmody strain,” which were identified as potentially separate species based on reproductive isolation, clearly cluster in the phylogenetic analyses within D. paulistorum and D. equinoxialis, respectively. Thus, there appears to be a conflict between the biological species concept and the phylogenetic species concept.
Literature Cited
- Ayala, F. J. 1973. Two new subspecies of the Drosophila willistoni group. Pan-Pacific Entomol. 49: 273–279.
- Ayala, F. J., C. A. Mourão, S. Pérez–Salas, R. Richmond, and T. Dobzhansky. 1970. Enzyme variability in the Drosophila willistoni group. I. Genetic differentiation among sibling species. Proc. Nat. Acad. Sci. USA 67: 225–232.
- Ayala, F. J., M. L. Tracey, D. Hedgecock, and R. C. Richmond. 1974a. Genetic differentiation during the speciation process in Drosophila. Evolution 28: 576–592.
- Ayala, F. J., M. L. Tracey, L. G. Barr, and J. G. Ehrenfeld. 1974b. Genetic and reproductive differentiation of Drosophila equinoxialis caribbensis. Evolution 28: 24–41.
- Baker, R. H., and R. DeSalle. 1997. Multiple sources of character information and the phylogeny of Hawaiian Drosophilids. Syst. Biol. 46: 654–673.
- Bull, J. J., J. P. Huelsenbeck, C. W. Cunningham, D. L. Swofford, and P. J. Waddell. 1993. Partitioning and combining data in phylogenetic analysis. Syst. Biol. 42: 384–397.
- Carmody, G. 1965. Two unusual strains of the D. willistoni sibling species group. Drosophila Inf. Serv. 40: 53.
- Clark, J. B., W. P. Maddison, and M. G. Kidwell. 1994. Phylogenetic analysis supports horizontal transfer of P transposable elements. Mol. Biol. Evol. 11: 40–50.
- Clary, D. O., and D. R. Wolstenholme. 1985. The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization and genetic code. J. Mol. Evol. 22: 252–271.
- Cracraft, J. 1989. Speciation and its ontology: the empirical consequences of alternative species concepts for understanding patterns and processes of differentiation. Pp. 28–59 in D. Otte and J. A. Endler, eds. Speciation and its consequences. Sinauer, Sunderland, MA.
- Cunningham, C. W. 1997. Can three incongruence tests predict when data should be combined? Mol. Biol. Evol. 14: 733–740.
- da Cunha, A. B., Th. Dobzhansky, O. Pavlovsky, and B. Spassky. 1959. Genetics of natural populations. XXVIII. Supplemental data on the chromosomal polymorphism in Drosophila willistoni in relation to the environment. Evolution 13: 389–404.
- Daniels, S. B., K. R. Peterson, L. D. Strausbaugh, M. G. Kidwell, and A. Chovnick. 1990. Evidence for horizontal transmission of the P transposable element between Drosophila species. Genetics 124: 339–355.
- de Queiroz, A. 1993. For consensus (sometimes). Syst. Biol. 42: 368–372.
- de Queiroz, A., M. J. Donoghue, and J. Kim. 1995. Separate versus combined analysis of phylogenetic evidence. Annu. Rev. Ecol. Syst. 26: 657–681.
- Dobzhansky, Th. 1937. Genetics and the origin of species. Columbia Univ. Press, New York.
- Dobzhansky, Th. 1950. The chromosomes of Drosophila willistoni. J. Heredity 41: 156–158.
- Doyle, J. A., M. J. Donoghue, and E. A. Zimmer. 1994. Integration of morphological and rRNA data on the origin of angiosperms. Ann. Mo. Bot. Gard. 81: 419–450.
- Ehrman, L. 1961. The genetics of sexual isolation in Drosophila paulistorum. Genetics 46: 1025–1038.
- Ehrman, L. 1965. Direct observation of sexual isolation between allopatric and between sympatric strains of the different Drosophila paulistorum races. Evolution 19: 459–464.
- Ehrman, L., and J. R. Powell. 1982. The Drosophila willistoni species group. Pp. 193–225 in M. Ashburner, H. L. Carson, and J. N. Thompson., eds. The genetics and biology of Drosophila. Academic Press, New York.
- Farris, J. S. 1972. Estimating phylogenetic trees from distances matrices. Am. Nat. 106: 645–668.
- Farris, J. S., M. Källersjö, A. G. Kluge, and C. Bult. 1995. Testing significance of incongruence. Cladistics 10: 315–319.
10.1111/j.1096-0031.1994.tb00181.x Google Scholar
- Felsenstein, J. 1978. Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17: 368–376.
10.1007/BF01734359 Google Scholar
- Felsenstein, J. 1995. PHYLIP: phylogeny inference package. Vers. 3.57c. University of Washington, Seattle, WA.
- Gleason, J. M. 1996. Molecular evolution of the period locus and evolution of courtship song in the Drosophila willistoni sibling species. Ph.D. diss., Yale University, New Haven, CT.
- Gleason, J. M., and J. R. Powell. 1997. Interspecific and intraspecific variation in the period locus in the Drosophila willistoni group. Mol. Biol. Evol. 14: 741–753.
- Griffith, E. C., and J. R. Powell. 1997. Adh nucleotide variation in Drosophila willistoni: high replacement polymorphism in an electrophoretically monomorphic protein. J. Mol. Evol. 45: 232–237.
- Hein, J. 1989. A new method that simultaneously aligns and reconstructs ancestral sequences for any number of homologous sequences, when phylogeny is given. Mol. Biol. Evol. 6: 669–684.
- Huelsenbeck, J. P., J. J. Bull, and C. W. Cunningham. 1996. Combining data in phylogenetic analysis. Trends Ecol. Evol. 11: 152–158.
- Kastritsis, C. D., and Th. Dobzhansky. 1967. Drosophila pavlovskiana, a race or a species? Am. Midl. Nat. 78: 244–247.
- Kessler, S. 1962. Courtship rituals and reproductive isolation between the races or incipient species of Drosophila paulistorum. Am. Nat. 96: 117–121.
- Kim, J. 1993. Improving the accuracy of phylogenetic estimation by combining different methods. Syst. Biol. 42: 331–340.
- Kimura, M. 1980. A simple method of estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16: 111–120.
- Kluge, A. G., and A. J. Wolf. 1993. Cladistics: what's in a word? Cladistics 9: 183–199.
- Lakovaara, S., and A. Saura. 1972. Location of enzyme loci in chromosomes of Drosophila willistoni. Experientia 28: 355–356.
- Larson, A. 1994. The comparison of morphological and molecular data in phylogenetic systematics. Pp. 371–390 in B. Schierwater, B. Streit, G. P. Wagner, and R. DeSalle, eds. Molecular ecology and evolution: approaches and applications. Birkhäuser Verglag, Basel, Switzerland.
10.1007/978-3-0348-7527-1_22 Google Scholar
- Maddison, W. P., and D. R. Maddison. 1992. MacClade: Analysis of phylogeny and character evolution. Sinauer, Sunderland, MA.
- Mayr, E. 1963. Animal species and evolution. Harvard Univ. Press, Cambridge, MA.
10.1111/j.0022-1112.2004.00433.x Google Scholar
- Mickevich, M. F., and J. S. Farris. 1981. The implication of congruence in Medidia. Syst. Zool. 30: 351–370.
- Miyamoto, M. M., and W. M. Fitch. 1995. Testing species phylogenies and phylogenetic methods with congruence. Syst. Biol. 44: 64–76.
- Nei, M. 1972. Genetic distance between populations. Am. Nat. 106: 283–292.
- Nei, M. 1987. Molecular evolutionary genetics. Colombia Univ. Press, New York.
10.1111/j.1365-294X.2006.02908.x Google Scholar
- Nixon, K. C., and J. M. Carpenter. 1996. On simultaneous analysis. Cladistics 12: 221–241.
- Olmstead, R. G., and J. A. Sweere. 1994. Combining data in phylogenetic systematics: an empirical approach using three molecular data sets in the Solanaceae. Syst. Biol. 43: 467–481.
- Pamilo, P., and M. Nei. 1988. Relationships between gene trees and species trees. Mol. Biol. Evol. 5: 568–583.
- Powell, J. R., and J. M. Gleason. 1996. Codon usage and the origin of P-elements. Mol. Biol. Evol. 13: 278–279.
- Ritchie, M. G., and J. M. Gleason. 1995. Rapid evolution of courtship song pattern in Drosophila willistoni sibling species. J. Evol. Biol. 8: 463–479.
- Rohde, C., E. Abdelhay, H. Pinto Jr., A. Schrank, and V. L. S. Valente. 1995. Analysis and in situ mapping of the Adh locus in species of the willistoni group of Drosophila. Cytobios 81: 37–47.
- Saitou, N., and M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406–425.
- Spassky, B., R. C. Richmond, S. Pérez-Salas, O. Pavlovsky, C. A. Mourã∗o, A. S. Hunter, H. Hoenigsberg, Th. Dobzhansky, and F. J. Ayala. 1971. Geography of the sibling species related to Drosophila willistoni and of the semispecies of the Drosophila paulistorum complex. Evolution 25: 129–143.
- Sturtevant, A. H. 1916. Notes on North American Drosophilidae with descriptions of twenty-three new species. Ann. Ent. Soc. Am. 9: 323–343.
10.1093/aesa/9.4.323 Google Scholar
- Swofford, D. 1990. PAUP∗: phylogenetic analysis using parsimony. Vers. 3.0. Illinois Natural History Survey, Champaign.
- Swofford, D. In press. PAUP∗: phylogenetic analysis using parsimony. Vers. 4.0.0.d63. Sinauer, Sunderland, MA.
- Throckmorton, L. H. 1975. The phylogeny, ecology and geography of Drosophila. Pp. 421–469 in R. C. King, ed. Handbook of genetics. Plenum Press, New York.
10.1007/978-1-4613-4470-4_20 Google Scholar
- Werman, S. D., E. H. Davidson, and R. J. Britten. 1990. Rapid evolution in a fraction of the Drosophila nuclear genome. J. Mol. Evol. 30: 281–289.