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On the Evolution of Dopa Decarboxylase (Ddc) and Drosophila Systematics

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On the Evolution of Dopa Decarboxylase (Ddc) and Drosophila Systematics J Mol Evol (1999) 48:445–462 © Springer-Verlag New York Inc. 1999 On the Evolution of Dopa decarboxylase (Ddc) and Drosophila Systematics Andrey Tatarenkov, Jan Kwiatowski,* Douglas Skarecky, Eladio Barrio,† Francisco J. Ayala Department of Ecology and Evolutionary Biology, 321 Steinhaus Hall, University of California, Irvine, CA 92697-2525, USA Received: 2 June 1998 / Accepted: 3 September 1998 Abstract. We have sequenced most of the coding re- Key words: Dopa decarboxylase (Ddc) — Diver- gion of the gene Dopa decarboxylase (Ddc) in 24 fruitfly gence — Drosophila — Scaptodrosophila — Chymo- species. The Ddc gene is quite informative about Dro- myza — Zaprionus — Scaptomyza sophila phylogeny. Several outstanding issues in Dro- sophila phylogeny are resolved by analysis of the Ddc sequences alone or in combination with three other Introduction genes, Sod, Adh, and Gpdh. The three species groups, melanogaster, obscura, and willistoni, are each mono- phyletic and all three combined form a monophyletic The received classification of the Drosophilidae (e.g., group, which corresponds to the subgenus Sophophora. Wheeler 1981) is inconsistent with the phylogenetic re- The Sophophora subgenus is the sister group to all other lationships among the species, whether these are based Drosophila subgenera (including some named genera, on morphology (Throckmorton 1975; Grimaldi 1990) or previously considered outside the Drosophila genus, molecular data (Kwiatowski et al. 1997; Powell 1997). namely, Scaptomyza and Zaprionus, which are therefore Throckmorton (1975) advanced a comprehensive downgraded to the category of subgenus). The Hawaiian scheme of the phylogenetic relationships in the Dro- Drosophila and Scaptomyza are a monophyletic group, sophilidae and showed that paraphyly is widespread which is the sister clade to the virilis and repleta groups among the various groups. However, he did not make of the subgenus Drosophila. The subgenus Drosophila any attempt to bring the classification of the Drosophi- appears to be paraphyletic, although this is not definitely lidae in correspondence with his hypothesis of phyloge- resolved. The two genera Scaptodrosophila and Chymo- netic relationships. Grimaldi (1990) has more recently myza are older than the genus Drosophila. The data favor constructed a phylogeny of the family, using a number the hypothesis that Chymomyza is older than Scaptodro- of morphological characters and relying on strict cladis- sophila, although this issue is not definitely resolved. tic methods, concluding also that Wheeler’s classifica- Molecular evolution is erratic. The rates of nucleotide tion implies extensive paraphyly. Grimaldi (1990) has substitution in 3rd codon position relative to positions 1 accordingly proposed a new classification of the Dro- + 2 vary from one species lineage to another and from sophilidae, which is consistent with his hypothesis of gene to gene. phylogenetic relationships. Grimaldi’s phylogenetic hy- pothesis displays important disparities with Throckmor- ton’s and has been shown also to be inconsistent with extensive molecular data (DeSalle 1992; Thomas and *Present address: Institute of Botany, Warsaw University, 00-478 Hunt 1993; Kwiatowski et al. 1994, 1997; Powell 1997; Warszawa, Al. Ujazdowskie 4, Poland; e-mail: jmkwiato@ Remsen and DeSalle 1998). PLEARN.EDU.PL †Present address: Department de Genetica, Universitat de Valencia, One particularly noteworthy discrepancy between Dr. Moliner 50, 46100 Valencia, Spain; e-mail: [email protected] Grimaldi’s and Throckmorton’s phylogenies concerns Correspondence to: F.J. Ayala; e-mail: [email protected] the position of the subgenus Sophophora (which includes 446 D. melanogaster). Grimaldi (1990) considers So- following the procedure described by Palumbi et al. (1991). The pub- phophora to be a sister-taxon of the subgenus (s.g.) Dro- lished sequences from a moth (Manduca sexta; GenBank U03909), a sophila, which together with the s.g. Dorsilopha, would fly (Drosophila melanogaster; X04661), and a mosquito (Aedes ae- gypti; U27581) were used to design PCR primers. Two slightly differ- make up the genus Drosophila. In contrast, Throckmor- ent methods (a and b) were followed for amplification and sequencing. ton (1975) considered the s.g. Drosophila to be phylo- Method a was used for species 1–12, 14, 22, and 24; method b, for genetically closer to several genera and subgenera (such species 13 and 15–23 (see Table 1 for ID numbers; Scaptodrosophila as Zaprionus, Samoaia, Dorsilopha, Hirtodrosophila, was analyzed with both methods). and Scaptomyza) than to Sophophora. Molecular data have, on the whole, favored Throckmorton’s rather than Method a. The amplifying primers were 5Ј-CACTGGTACCGNC- Ј Grimaldi’s hypothesis in this respect (e.g., Kwiatowski et CCAASTTYCAYGCCTACTTCCCCAC-3 (APF; forward primer), and 5Ј-CCGCTCGTTGGTACCCTTNAGCCGGAAGCAGACCA-3Ј al. 1994, 1997; Russo et al. 1995; Powell 1997; Remsen (APR; reverse primer). The amplified fragment is 963–966 bp long and and DeSalle 1998) but have left unresolved the relation- encompasses most of the Ddc exon 4 gene, accounting for 68% of the ships among several genera and subgenera (and brought total Ddc coding sequence in D. melanogaster. The shorter fragments into question whether the willistoni group, usually in- (963 rather than 966 bp) are due to a 3-bp deletion shared by all cluded in the subgenus Sophophora, may actually be a species of the Sophophora subgenus. All PCR reactions were con- ducted as described by Kwiatowski et al. (1991). Amplification param- sister taxon to the Drosophila genus (e.g., Pe´landakis and eters were as follows: initial denaturation at 94°C for 5 min, followed Solignac 1993). These unsettled issues are significant, by 31 cycles of denaturation, annealing, and extension at 94°C for 30 particularly the phylogenetic position of Sophophora, be- s, 60°C for 30 s, and 72°C for 2 min, respectively; after 30 cycles, the cause this subgenus includes D. melanogaster, which is reaction was additionally kept at 72°C for 7 min to complete exten- so extensively used as a model species for many evolu- sion. PCR products were purified with Wizard PCR preps DNA puri- fication system (Promega corporation) and cloned using the TA cloning tionary, developmental, and molecular biology investi- kit (Invitrogen, San Diego, CA). DNA sequencing was done by the gations. dideoxy chain-termination technique with Sequenase Version 2.0 T7 In this paper we study the phylogenetic relationships DNA polymerase (Amersham Life Sciences Inc., USA) using 32P- among 24 species of the family Drosophilidae, using the labeled dATP. The internal sequencing primers were as follows: A1F, Ј Ј Ј nucleotide sequences of Dopa decarboxylase (Ddc), a 5 -ATAGGCAAGCTGGTGGGCTA-3 ; A2F, 5 -ATCCAGATTGG- GAYGARCACAC-3Ј;A3F,5Ј-TGGTGAATTTCGACTGCTCGGC- nuclear gene involved in morphological differentiation CATGTGG-3Ј;A1R,5Ј-AGAGCCACCAAGGTGGATACA- and in the production of the neurotransmitters, dopamine CTGGC-3Ј;A2R,5Ј-TCRAAGTTSACCAGCATCCA-3Ј; and A3R, and serotonin. The product of this gene, DDC, catalyzes 5Ј-ASCCACATGGCMGAGCAGTC-3Ј. the decarboxylation of dopa to dopamine and is essential for the sclerotization and melanization of the cuticle Method b. The amplifying primers were 5Ј-GAYATYGARC- (Wright 1996, and references therein). This gene is con- GNGTSATCATGCCKGG-3Ј (BPF; forward primer) and 5Ј- Ј served between Drosophila and humans and is expressed TSRGTGAATCGNGARCADAYKGCCAT-3 (BPR; reverse primer). The amplified fragments were longer than with method a, but we in the central nervous system (CNS) as well as in the analyze here only the nucleotide sequence corresponding to the PCR peripheral nervous system of insects and mammals fragments of method a. PCR amplifications were performed in a 100-␮l (Wright et al. 1982; Konrad et al. 1993; Wang and Marsh volume of the ExTAKARA buffer, containing 2.5 U of ExTAKARA 1995; Wang et al. 1996; Wright 1996). The only Dro- Taq polymerase, 0.2 mM dNTP (all from TAKARA), a 0.5 ␮M con- ␮ sophilid nucleotide sequence of Ddc already published is centration of primers, and 3 l of template DNA. The cycling param- eters for the amplification were as follows: initial denaturation at 95°C that of D. melanogaster (Eveleth et al. 1986). We have for 5 min, followed by 31 cycles with denaturation for 30 s at 95°C, sequenced this gene in another 22 Drosophilid species annealing for 30 s at 59°C, and extension for 2 min at 72°C; after 30 and in the medfly Ceratitis capitata. The Ddc gene has cycles the reaction was additionally kept at 72°C for 7 min to complete been found to be a highly appropriate marker for phylo- extension. PCR products were purified with Wizard PCR preps DNA genetic analysis in a subfamily of Lepidoptera that arose purification system (Promega corporation), and both strands of the PCR fragments were sequenced directly with an ABI Model 377 autose- within the last 20 million years (Fang et al. 1997). Com- quencer using the Dye Terminator Ready Reaction Kit according to the parison of D. melanogaster Ddc with that of other ani- manufacturer’s protocol (Perkin Elmer). The two amplification primers mals (such as mosquito, moth, and some mammals) in- were also used for sequencing. Internal primers used for sequencing dicates that it can be informative at deeper taxonomic were as follows: B1F, 5Ј-CNCAYTCNTCNGTGGARCG-3Ј; B2F, 5Ј- Ј Ј levels as well. YGAYTGYTCNGCYATGTGG-3 ; B1R, 5 -CGYAGNCKATTRT- KCTCATC-3Ј; and B2R, 5Ј-TTRAANGCRTTNACCACCCA-3Ј. The sequence of Ceratitis capitata
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