Abstract
The phylogeny and taxonomy of the drosophilids have been the subject of extensive investigations. Recently, Grimaldi (1990) has challenged some common conceptions, and several sets of molecular data have provided information not always compatible with other taxonomic knowledge or consistent with each other. We present the coding nucleotide sequence of the Cu,Zn superoxide dismutase gene (Sod) for 15 species, which include the medfly Ceratitis capitata (family Tephritidae), the genera Chymomyza and Zaprionus, and representatives of the subgenera Dorsilopha, Drosophila, Hirtodrosophila, Scaptodrosophila, and Sophophora. Phylogenetic analysis of the Sod sequences indicates that Scaptodrosophila and Chymomyza branched off the main lineage before the major Drosophila radiations. The presence of a second intron in Chymomyza and Scaptodrosophila (as well as in the medfly) confirms the early divergence of these two taxa. This second intron became deleted from the main lineage before the major Drosophila radiations. According to the Sod sequences, Sophophora (including the melanogaster, obscura, saltans, and willistoni species groups) is older than the subgenus Drosophila; a deep branch splits the willistoni and saltans groups from the melanogaster and obscura groups. The genus Zaprionus and the subgenera Dorsilopha and Hirtodrosophila appear as branches of a prolific “bush” that also embraces the numerous species of the subgenus Drosophila. The Sod results corroborate in many, but not all, respects Throckmorton's (King, R.C. (ed) Handbook of Genetics. Plenum Press, New York, pp. 421–469, 1975) phylogeny; are inconsistent in some important ways with Grimaldi's (Bull. Am. Museum Nat. Hist. 197:1–139, 1990) cladistic analysis; and also are inconsistent with some inferences based on mitochondrial DNA data. The Sod results manifest how, in addition to the information derived from nucleotide sequences, structural features (i.e., the deletion of an intron) can help resolve phylogenetic issues.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Ayala FJ (1986) On the virtues and pitfalls of the molecular evolutionary clock. J Hered 77:226–235
Beverley SM, Wilson AC (1984) Molecular evolution in Drosophila and higher Diptera. II. Time scale for fly evolution. J Mol Evol 21:1–13
Collier GE, MacIntyre RJ (1977) Microcomplement fixation studies on the evolution of α-glycerophosphate dehydrogenase within the genus Drosophila. Proc Natl Acad Sci USA 74:684–688
Dayhoff MD (1978) Atlas of protein sequence and structure. Natl Biomed Res Found, Washington, DC
DeSalle R (1992) The phylogenetic relationships of flies in the family Drosophilidae deduced from mtDNA sequences. Mol Phylogenet Evol 1:31–40
DeSalle R, Grimaldi DA (1991) Morphological and molecular systematics of the Drosophilidae. Annu Rev Ecol Syst 22:447–475
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–374
Felsenstein J (1985a) Confidence limits on phylogenies with a molecular clock. Syst Zool 34:152–161
Felsenstein J (1985b) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Felsenstein J (1988) Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet 22:521–565
Felsenstein J (1989) PHYLIP—Phylogeny inference package (version 3.2). Cladistics 5:164–166
Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155:279–287
Fridovich I (1986) Superoxide dismutases. Adv Enzymol 58:61–97
Gillespie JH (1986) Rates of molecular evolution. Annu Rev Ecol Syst 17:637–655
Grimaldi D (1990) A phylogenetic revised classification of genera in the Drosophilidae. Bull Am Museum Nat Hist 197:1–139
Hillis DM, Bull JJ (1993) An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst Biol 42:182–192
Hudson RR, Bailey K, Skarecky D, Kwiatowski J, Ayala FJ (1994) Evidence for positive selection at the superoxide dismutase (Sod) locus of Drosophila rnelanogaster. Genetics (in press)
Kawasaki ES (1990) Sample preparation from blood, cells, and other fluids. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 146–152
Kimura M (1980) A simple method for estimating evolutionary rate of base substitution through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J Mol Evol 29:170–179
Kwiatowski J, Ayala FJ (1989) Drosophila virilis Cu,Zn superoxide dismutase gene sequence. Nucleic Acids Res 17:2133
Kwiatowski J, Gonzalez F, Ayala FJ (1989a) Drosophila simulans Cu,Zn superoxide dismutase gene sequence. Nucleic Acids Res 17:6735
Kwiatowski J, Patel M, Ayala FJ (1989b) Drosophila melanogaster Cu,Zn superoxide dismutase gene sequence. Nucleic Acids Res 17:1264
Kwiatowski J, Hudson RR, Ayala FJ (1991a) The rate of Cu,Zn superoxide dismutase evolution. Free Radic Res Common 12–13: 363–370
Kwiatowski J, Skarecky D, Hernandez S, Pham D, Quijas F, Ayala FJ (1991b) High fidelity of the polymerase chain reaction. Mol Biol Evol 8:884–887
Kwiatowski J, Skarecky D, Ayala FJ (1992a) Structure and sequence of the Cu, Zn Sod gene in the Mediterranean fruit-fly, Ceratitis capitata: intron insertion/deletion and evolution of the gene. Mol Phyl Evol 1:72–82
Kwiatowski J, Skarecky D, Burgos M, Ayala FJ (1992b) Structure and sequence of the Cu,Zn superoxide dismutase gene of Chymomyza amoena: phylogeny of the genus and codon-use evolution. Insect Mol Biol 1:3–13
Lee YM, Friedman DJ, Ayala FJ (1985) Superoxide dismutase: an evolutionary puzzle. Proc Natl Acad Sci USA 82:824–828
Lloyd AT, Sharp PM (1992) CODONS: a microcomputer program for codon usage analysis. J Hered 83:239–240
Patterson JT, Stone WS (1952) Evolution in the genus Drosophila. MacMillan, New York
Pelandakis M, Higgins DH, Solignac M (1991) Molecular phylogeny of the subgenus Sophophora of Drosophila derived from large subunit of ribosomal RNA sequences. Genetica 84:87–94
Rousset FM, Pelandaks M, Solignac M (1991) Evolution of compensatory substitutions through G-U intermediate state in Drosophila rRNA. Proc Natl Acad Sci USA 88:10032–10036
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Sharp PM, Cowe E, Higgins DG, Shields DC, Wolfe KH, Wright F (1988) Codon usage patterns in Escherichia coli, Bacillus subtilis, Saccharomyces cerevisiae, Schistosaccharomyces pombe, Drosophila melanogaster and Homo sapiens: a review of the considerable within-species diversity. Nucleic Acids Res 16:8207–8211
Spicer GS (1988) Molecular evolution among some Drosophila species groups as indicated by two-dimensional electrophoresis. J Mol Evol 27:250–260
Starmer WT, Sullivan DT (1989) A shift in the third-codon-position nucleotide frequency in alcohol dehydrogenase genes in the genus Drosophila. Mol Biol Evol 6:546–552
Sturtevant AH (1921) The North American species of Drosophila. Carnegie Institution, Washington, DC
Templeton AR (1983) Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to the evolution of humans and apes. Evolution 37:221–244
Thomas RH, Hunt JA (1993) Phylogenetic relationships in Drosophila: a conflict between molecular and morphological data. Mol Biol Evol 10:362–374
Throckmorton LH (1975) The phylogeny, ecology and geography of Drosophila. In: King RC (ed) Handbook of genetics. Plenum Press, New York, pp 421–469
Villarroya A, Juan E (1991) ADH and phylogenetic relationships of Drosophila lebanonensis (Scaptodrosophila). J Mol Evol 32:421–428
Wheeler MR (1981) The Drosophilidae: a taxonomic overview. In: Ashburner M, Carson HL, Thompson JN Jr (eds) The genetics and biology of drosophila. Academic Press, New York, pp 1–97
Wheeler MR (1986) Additions to the Catalog of the World's Drosophilidae. In: Ashburner M, Carson HL, Thompson JN Jr (eds) The genetics and biology of drosophila, vol 3e. Academic Press, New York, pp 395–409
Woese CR (1991) The use of ribosomal RNA in reconstructing evolutionary relationships among bacteria. In: Selander RK, Clark AG, Whittam TS (eds) Evolution at the molecular level. Sinauer Associates, Sunderland, MA, pp 1–24
Author information
Authors and Affiliations
Additional information
Correspondence requests to: F. J. Ayala
Rights and permissions
About this article
Cite this article
Kwiatowski, J., Skarecky, D., Bailey, K. et al. Phylogeny of Drosophila and related genera inferred from the nucleotide sequence of the Cu,Zn Sod gene. J Mol Evol 38, 443–454 (1994). https://doi.org/10.1007/BF00178844
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00178844