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Phylogeny of Drosophila and Related Genera: Conflict Between Molecular and Anatomical Analyses1 Jan Kwiatowski*,† and Francisco J

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Phylogeny of Drosophila and Related Genera: Conflict Between Molecular and Anatomical Analyses1 Jan Kwiatowski*,† and Francisco J Molecular Phylogenetics and Evolution Vol. 13, No. 2, November, pp. 319–328, 1999 Article ID mpev.1999.0657, available online at http://www.idealibrary.com on Phylogeny of Drosophila and Related Genera: Conflict between Molecular and Anatomical Analyses1 Jan Kwiatowski*,† and Francisco J. Ayala† *Institute of Botany, Warsaw University, 00-478 Warszawa, Poland; and †Department of Ecology and Evolutionary Biology, University of California, Irvine, California 92697-2525 Received August 6, 1998; revised March 10, 1999 phylogenetic relationships among the species, whether Drosophila species are extensively used in biological the inferences are based on morphology (Throckmor- research; yet, important phylogenetic relationships ton, 1975; Grimaldi, 1990) or molecular data (DeSalle, within the genus and with related genera remain 1992a,b; Kwiatowski et al., 1994, 1997; Pe´landakis and unresolved. The combined data for three genes (Adh, Solignac, 1993; Powell, 1997; Remsen and DeSalle, Sod, and Gpdh) statistically resolves outstanding is- 1998; Russo et al., 1995; Tatarenkov et al., 1999; sues. We define the genus Drosophila inclusively so as Thomas and Hunt, 1993). Throckmorton (1975) con- to include Scaptomyza and Zaprionus (considered dis- cluded, based on morphological, behavioral, and biogeo- tinct genera in the taxonomy of Wheeler, 1981) but graphical data, that the standard taxonomy implies excluding Scaptodrosophila. The genus Drosophila so defined is monophyletic. The subgenus Sophophora numerous paraphyletic relationships but he did not (including the melanogaster, obscura, and willistoni advance a new taxonomy. Grimaldi (1990) analyzed groups) is monophyletic and the sister clade to all cladistically 217 morphological characters in a represen- other Drosophila subgenera. The Hawaiian Drosophila tative set of 120 species and advanced a revised tax- (including Scaptomyza) is a monophyletic group, but onomy for the family. Notable in Grimaldi’s (1990) the subgenus Drosophila is not monophyletic, because analysis is the proposal that the subgenera Drosophila the immigrans group is more closely related to the and Sophophora are sister clades and the exclusion subgenus Hirtodrosophila than to other species of the from the genus Drosophila of the previous subgenus subgenus Drosophila, such as the virilis and repleta Hirtodrosophila, the Hawaiian species of Drosophila groups. ௠ 1999 Academic Press (which he classified as the genus Idiomyia), and the Key Words: Chymomyza; Drosophila; Hawaiian Dro- genera Zaprionus and Scaptomyza. Grimaldi’s (1990) sophila; Scaptodrosophila; molecular systematics; Adh; proposal contrasts with Throckmorton’s (1975), who Gpdh; Sod proposed an early divergence of the subgenus So- phophora, which would be the sister group to a complex of taxa that included the subgenus Drosophila, as well INTRODUCTION as Hirtodrosophila, Dorsilopha, Zaprionus, Scapto- myza, and the Hawaiian Drosophila. The family Drosophilidae is among the most diverse Introduction of molecular data into taxonomic dis- of the Diptera, encompassing more than 2500 species course should help in resolving some perplexing ques- (Wheeler, 1986). Species of this family are often used in tions but has so far left unresolved some key relation- many areas of contemporary biological research. Under- ships. Generally, molecular data (Kwiatowski et al., standing the phylogenetic relationships among the 1994, 1997; Pe´landakis and Solignac, 1993; Remsen species is crucial to many of these studies. However, despite extensive investigations, the taxonomy of the and DeSalle, 1998; Tatarenkov et al., 1999; Thomas and Drosophilidae remains controversial. Wheeler’s (1981, Hunt, 1993) contradict in very many important aspects 1986) standard classification is inconsistent with the Grimaldi’s revisions of the Drosophila phylogeny, while they often support Throckmorton’s hypothesis. The molecular studies have, however, paid relatively less 1 The sequences reported in this paper have been submitted to the attention to several taxa, including Zaprionus, Scapto- GenBank/EMBL Data Libraries under Accession Nos. AF021825– myza, Hirtodrosophila, and Dorsilopha. We have ob- AF021832 and AF022218. tained the nucleotide sequence of two genes, Cu,Zn 2 Abbreviations used: Adh, alcohol dehydrogenase gene; Gpdh, 2 glycerol-3-phosphate dehydrogenase gene; ML, maximum likelihood; superoxide dismutase (Sod) and alcohol dehydroge- MP, maximum parsimony; NJ, neighbor joining; nt, nucleotide; s.g., nase (Adh) in several critical species. We have com- subgenus; Sod, superoxide dismutase gene. bined our data with preexisting sequences of the same 319 1055-7903/99 $30.00 Copyright ௠ 1999 by Academic Press All rights of reproduction in any form reserved. 320 KWIATOWSKI AND AYALA two genes, as well as of glycerol-3-phosphate dehydroge- and Engiscaptomyza as Drosophila subgenera, follow- nase (Gpdh), seeking to resolve the phylogeny of these ing Tatarenkov et al. (1999), but Scaptodrosophila as a and other taxa within the Drosophilidae. genus, following Grimaldi (1990) and Tatarenkov et al. (1999; see also Kwiatowski et al., 1994, 1997; Remsen MATERIALS AND METHODS and DeSalle, 1998; Russo et al., 1995). Species DNA Preparation, Amplification, Cloning, Table 1 lists the 29 Drosophilidae species that we and Sequencing have investigated. Strains of Chymomyza procnemis, Genomic DNA from about 10 to 20 flies was prepared D. mimica, D. immigrans, D. (Hirtodrosophila) pictiven- following the method of Kawasaki (1990). The amplifi- tris, D. (Scaptomyza) adusta, and D. (Zaprionus) tuber- cation, cloning, and sequencing of Sod fragments used culatus were obtained from the National Drosophila for most species are described elsewhere (Kwiatowski Species Stock Center at Bowling Green, Ohio; the rest et al., 1994). Sod fragments from D. teissieri, D. paulis- were from cultures available in our laboratory. We list torum, D. nebulosa, and D. immigrans were amplified Scaptomyza and Zaprionus, classified as genera by with primers N (5Ј-CCTCTAGAAATGGTGGTTAAAGC- Wheeler (1981), as well as Hirtodrosophila, Dorsilopha, TGTNTGCGT-3Ј) and O (5Ј-ACGGAAGTCTAGAAGG- TABLE 1 The 31 Species Studied, with GenBank Accession Nos. for the Gene Sequences Accession no. Family Genus Subgenus Group Species Adh Sod Gpdh Drosophilidae Drosophila Sophophora melanogaster melanogaster X78384 X13780 X14179 simulans X15685 L41248 teissieri X54118 AF021828 U47809 yakuba X54120 obscura subobscura X55545 U38233 U47877 pseudoobscura X62181 U47871 L41249 ambigua X54813 U47868 U47880 willistoni willistoni L08648 L13281 L37038 paulistorum AF021829 L41648 nebulosa AF021830 L41250 saltans saltans U37590 Drosophila virilis virilis U26846 X13831 D10697 repleta hydei X58694 U37714 L41650 mulleriAdh1 X03048 immigrans immigrans M97638 AF021825 quinaria guttifera AF021826 Hawaiianb mimica M60792 AF022218 nigra M60793 differens M36785 heteroneura M36781 picticornis M63392 Scaptomyzaa albovittata M80925 adusta AF021827 Engiscaptomyza crassifemur M60790 Hirtodrosophila pictiventris AF021832 AF021824 L41649 Dorsilopha busckii U39445 R. S. Wells Zaprionusa tuberculatus X63955 AF021823 L37039 Scaptodrosophilaa lebanonensis M97637 AF021822 R. S. Wells Chymomyza amoena X61687 L36961 procnemis AF021831 AF021821 L41252 Tephritidae Ceratitis capitata Z30194 M76975 L36960 Note. Sequences newly obtained in this study are underlined. The busckii and lebanonensis Gpdh sequences are courtesy of Dr. Wells and available on-line (see Materials and Methods). a Scaptodrosophila was classified by Wheeler (1981) as a subgenus of Drosophila but has been raised to genus by Grimaldi (1990). Scaptomyza and Zaprionus are classified as genera by Wheeler (1981); in this paper we shall refer to them, as well as to Engiscaptomyza, Hirtodrosophila and Dorsilopha, as subgenera within the genus Drosophila. b The Hawaiian Drosophila groups are: modified mouthparts (mimica); white tip scutellum (nigra); and picture wing (differens, heteroneura, picticornis). MOLECULAR PHYLOGENY OF Drosophila 321 GCTTTTTGGGCTTTGCCACCTG-3Ј), resulting in 441 were obtained and tested according to Templeton (1983) nt of coding sequence. The Sod of D. (S.) adusta was and Kishino and Hasegawa (1989), respectively, using obtained with the previous N primer and a C primer, the PHYLIP 3.572c package programs DNAPARS and (5Ј-CTTGCTGAGCTCGTGTCCACCCTTGCCCAGAT- DNAML (Felsenstein, 1989). We give equal weights to CATC-3Ј), resulting in 345 nt of coding sequence. all sites in MP trees and use empirical base frequencies The Adh gene fragments were amplified by PCR, and a transition/transversion ratio of 2 in the ML cloned into the pCRII vector from the Invitrogen TA- calculations. No saturation was observed for the third cloning kit, and sequenced using standard methods codon position for Adh and Sod genes (Tatarenkov et (Ausubel et al., 1987), as previously described (Kwia- al., 1999) or for synonymous nucleotide replacement in towski et al., 1994). The 576-nt-long coding fragment the Gpdh gene (Ayala et al., 1996). Kimura’s (1980) from C. procnemis was obtained with primers L3 two-parameter distances were used for constructing NJ (5Ј-GAACTGAAGGCAAT(CT)AATCC(AC)AA-3Ј), de- trees. Using other distance measures for NJ trees or rived from a conserved protein region ELKAINPK, changing the transition/transversion ratio in ML trees corresponding to the beginning of exon 2, and R1 did not affect the topologies in any substantial way. Our (5Ј-TTAGATGCC(GC)GA(AG)TCCCA(AG)TG(TC)T- alignments of the coding sequences are available
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