Complete mitochondrial DNA sequence of the Japanese spiny lobster, Panulirus japonicus (Crustacea: Decapoda)

Gene 295 (2002) 89–96 www.elsevier.com/locate/gene

Complete mitochondrial DNA sequence of the Japanese spiny lobster, Panulirus japonicus (Crustacea: Decapoda) Mitsugu M. Yamauchi a,*, Masaki U. Miya b, Mutsumi Nishida a a

b

Ocean Research Institute, University of Tokyo, 1-15-1 Minamidai, Nakano-ku, Tokyo 164-8639, Japan Department of Zoology, Natural History Museum and Institute, Chiba, 955-2 Aoba-cho, Chuo-ku, Chiba 260-8682, Japan Received 21 February 2002; received in revised form 7 June 2002; accepted 25 June 2002 Received by T. Sekiya

Abstract We determined the complete nucleotide sequence of the mitochondrial genome for a Japanese spiny lobster, Panulirus japonicus (Crustacea: Decapoda). The entire genome was amplified using long polymerase chain reaction, and the products were subsequently used as templates for direct sequencing using a primer-walking strategy. The genome (15,717 base pairs) contained the same 37 genes (two ribosomal RNA, 22 transfer RNA, and 13 protein-coding genes) plus the putative control region as found in other arthropods, with the gene order identical to that of typical arthropods. Preliminary phylogenetic analyses of selected arthropods using concatenated amino acid sequences of the 13 protein-coding genes strongly supported monophyly of Decapoda species and confidently rejected ‘Macroura’, a conventional taxon that shares an elongated abdominal body. q 2002 Elsevier Science B.V. All rights reserved. Keywords: Mitochondrial genome; Long polymerase chain reaction; Decapod phylogeny

1. Introduction Nearly all eukaryotic cells contain a mitochondrial genome, in addition to nuclear genome. For animals, this usually is a single circular duplex molecule ranging in size from approximately 14 kb in some nematodes and tapeworms (Okimoto et al., 1992; von Nickisch-Rosenegk et al., 2001) to 42 kb in the scallop Placopecten magellanisus (LaRoche et al., 1990). In spite of the threefold range in size, the gene content is a nearly identical set of 13 proteins, 22 transfer RNAs (tRNAs), and two ribosomal RNAs (rRNAs), plus the so-called control region (Wolstenholme, 1992). Because of lack of intermolecular genetic recombination, maternal inheritance, and relatively rapid evolutionary rate, mitochondrial DNA (mtDNA) has been extensively used for studying population structures and phylogenetic relationships at various taxonomic levels. The Japanese spiny lobster Panulirus japonicus (Crustacea: Decapoda) inhabits shallow coastal waters on rocky Abbreviations: ATPase6 and 8, ATPase subunits 6 and 8; bp, base pair (s); COI–III, cytochrome c oxidase subunits I–III; CR, control region; cyt b, cytochrome b; mtDNA, mitochondrial DNA; ND1–6 and 4L, NADH dehydrogenase subunits 1–6 and 4L; PCR, polymerase chain reaction; srRNA and lrRNA, small and large subunits ribosomal RNA; tRNA, transfer RNA * Corresponding author. Tel.: 181-3-5351-6489; fax: 181-3-5351-6488. E-mail address: [email protected] (M.M. Yamauchi).

bottoms, being distributed in the western North Pacific around southern Japan, Korea, East China Sea, China, Xiamen ( ¼ Amoy), and Taiwan (George and Holthuis, 1965; Holthuis, 1991). This species is an important fisheries resource in Japan, with an annual catch reaching 1600 tons (Holthuis, 1991). Because of its commercial importance, many studies have been conducted regarding larval culture (e.g. Kittaka and Abrunhosa, 1997), larval distribution and migration process (Yoshimura et al., 1999), reproductive biology (Minagawa, 1999), and resource management (Tuiki et al., 1999). Consequently, there have been growing interests in genetic structure of P. japonicus with respect to stock identification, management, and conservation. Furthermore, DNA information is useful for larval identification, because larvae within P. japonicus species-group are morphologically very similar (McWilliam, 1995). In this study, we report the complete nucleotide sequence of the mitochondrial genome for the Japanese spiny lobster, P. japonicus. In addition, we perform phylogenetic analyses using selected arthropod species. The new sequence provides genetic marker for crustacean researches, because there are only few complete (or nearly complete) mtDNA sequences from these animals: two branchiopods, Artemia franciscana (Valverde et al., 1994) and Daphnia pulex (Crease, 1999); a maxillopod, Tigriopus japonicus (Machida et al., 2002); and two malacostracans, Penaeus monodon (Wilson et al., 2000)

0378-1119/02/$ - see front matter q 2002 Elsevier Science B.V. All rights reserved. PII: S 0378-111 9(02)00824-7

90

M.M. Yamauchi et al. / Gene 295 (2002) 89–96

and Pagurus longicarpus (Hickerson and Cunningham, 2000). 2. Materials and methods 2.1. Sample and DNA extraction A P. japonicus specimen was obtained from a commercial source and abdominal muscle tissues were excised and immediately preserved in 99.5% ethanol. Total genomic DNA was extracted from the tissues using a DNeasy tissue kit (Qiagen) following the manufacturer’s protocol. A voucher specimen preserved in 99.5% ethanol was deposited in the Natural History Museum and Institute, Chiba (CBM-ZC 5914).

1.5 ml 10£ Z PCR buffer (Takara), 1 ml dNTP (2.5 mM), 1 ml each primer (5 mM), 0.1 ml Taq polymerase (Z Taq, Takara), and 1 ml DNA template. The thermal cycle profile was as follows: denaturation at 98 8C for 1 s, annealing at 45 8C for 5 s, and extension at 72 8C for 10 s. The PCR products were electrophoresed on a 1.0% L 03 agarose gel (Takara) and stained with ethidium bromide for band characterization via ultraviolet transillumination. Double-stranded PCR products were purified using a PreSequencing Kit (USB) and subsequently used for direct cycle sequencing with dye-labeled terminators (Applied Biosystems Inc.). Primers used were the same as those for PCR. All sequencing reactions were performed according to the manufacturer’s instructions. Labeled fragments were analysed on a Model 377 DNA sequencer (Applied Biosystems Inc.).

2.2. PCR and sequencing 2.3. Long-PCR and sequencing by primer-walking Partial sequences for the cytochrome c oxidase subunit I (COI), cytochrome b (cyt b), and small subunit ribosomal RNA (srRNA) genes for the P. japonicus were determined by polymerase chain reaction (PCR) using the following primer pairs: LCO1490 1 HCO2198 (Folmer et al., 1994) for the COI gene; L10061-CYB (5 0 -GGA TTW TTT TTA GCK ATR CAT TAC AC-3 0 ) 1 H10699-CYB (5 0 -GCA AAT AGA AAA TAT CAT TCW GGT TG-3 0 ) for the cyt b gene; and L13337-12S (5 0 -YCT ACT WTG YTA CGA CTT ATC TC-3 0 ) 1 H13845-12S (5 0 -GTG CCA GCA GCT GCG GTT A-3 0 ) for the srRNA gene. L10061CYB was newly designed with reference to aligned sequences from several crustacean and insect species deposited in DDBJ/EMBL/GenBank. H10699-CYB, L1333712S, and H13845-12S were designed by Machida et al. (2002). Numbers of primer names refer to the position of 3 0 ends of the oligonucleotide with reference to the Artemia franciscana mtDNA sequence (Valverde et al., 1994). PCR was done in a Perkin Elmer Model 9700 thermal cycler and reaction carried out with 30 cycles of 15-ml reaction volume containing 9.4 ml sterile distilled H2O,

The mitochondrial genome of P. japonicus was amplified in its entirety using a long-PCR technique (Miya and Nishida, 1999). On the basis of the three partial sequences (COI, cyt b, and srRNA genes), six species-specific primers, Paja-CO1-L (5 0 -GCC TAT CAT AAT TGG GGG ATT CGG AAA TTG ACT AGT TCC G-3 0 ), Paja-CO1-H (5 0 CAA ATA GAG GCA TAC GGT CAA GAG TTA TAC CAG AAG ATC G-3 0 ), Paja-CYB-L (5 0 -GAG ACG TAA ATT ACG GCT GAT TTT TGC GAA CTC TTC ACG C3 0 ), Paja-CYB-H (5 0 -GCG TTT CCC ACT GAG AAT CCA CCT CAA ATC CAT TGG-3 0 ), Paja-12S-L (5 0 -GGT ATA CTG GCT CGA CAA GAA CAA GAA AGA TTC TAC G3 0 ) and Paja-12S-H (5 0 -GTA ATT GAG TTC TTG TAG GGG TAG ACT TAG GTT GAA GCC-3 0 ), were designed so as to amplify the entire mitochondrial genome in three long-PCR reactions (COI/cyt b, cyt b/srRNA, and srRNA/ COI regions; Fig. 1). Long-PCR was done in a Perkin Elmer Model 9700 thermal cycler, reactions being carried out with 40 cycles of a 25-ml reaction volume containing 12.75 ml sterile distilled

Fig. 1. Linearized representation of the mitochondrial gene arrangement for the Japanese spiny lobster, Panulirus japonicus. Protein-coding genes are transcribed from left-to-right except ND1, ND4L, ND4 and ND5 genes (indicated by underbars). The two ribosomal RNA genes encoded by L strands (indicated by underbars). Transfer RNA genes are designated by single-letter amino acid codes, those encoded by the H and L strands are shown above and below the gene map, respectively. L1, L2, S1 and S2 denote for the tRNA Leu(UCN), tRNA Leu(UUR), tRNA Ser(AGN), and tRNA Ser(UCN) genes, respectively. Three pairs of long-PCR primers (Paja-CO1-L 1 Paja-CYB-H, Paja-CYB-L 1 Paja-12S-H, and Paja-12S-L 1 Paja-CO1-H) amplify three segments that cover the entire mitochondrial genome. COI–III indicate genes of cytochrome c oxidase subunits I–III; ATPase6 and 8, ATPase subunits 6 and 8; ND1–6 and 4L, NADH dehydrogenase subunits 1–6 and 4L; cyt b, cytochrome b; srRNA and lrRNA, small and large subunits rRNA; CR, control region.

M.M. Yamauchi et al. / Gene 295 (2002) 89–96

H2O, 2.5 ml 10£ LA PCR buffer (Takara), 4 ml dNTP (2.5 mM), 2.5 ml MgCl2 (25 mM), 1 ml each primer (5 mM), 0.25 ml Taq polymerase (LA Taq, Takara), and 1 ml DNA template. The thermal cycle profile was that of ‘shuttle PCR’: denaturation at 98 8C for 10 s, with annealing and extension combined at the same temperature (68 8C) for 18 min. The long-PCR products were electrophoresed on a 1.0% L 03 agarose gel (Takara) and stained with ethidium bromide for band characterization via ultraviolet transillumination. Sequencing was carried out as above, initially using the same primers as those for long-PCR, with subsequent sequencing being performed by primers designed with reference to previously-determined sequences (primer-walking).

91

ford, 2001). All phylogenetically uninformative sites were ignored. Gaps were considered as missing data. ML analyses were conducted with 100 bootstrap replicate searches using the program Proml in PHYLIP version 3.6 (Felsenstein, 2000). The model of amino acid sequence evolution according to Dayhoff et al. (1979) was used. All other parameters were set at default options in the program. Minimum evolution tree was estimated using NJ method with 2000 bootstrap replicates implemented in MEGA version 2.1 (Kumar et al., 2001). Pairwise P-distances were adjusted by gamma model with shape parameter ðaÞ ¼ 0:42 (inferred from TREE-PUZZLE 5.0; Strimmer and von Haeseler, 1996), and pairwise deletion option for gaps and missing data were employed.

2.4. Sequence analysis 3. Results and discussion DNA sequences were analysed using the computer software DNASIS ver. 3.7 (Hitachi Software Engineering Co. Ltd). Locations of the 13 protein-coding genes were determined by comparisons of nucleotide or amino acid sequences of the previously-determined complete mtDNA sequences for other crustaceans. The 22 tRNA genes were identified by their proposed cloverleaf secondary structures and anticodon sequences (Kumazawa and Nishida, 1993; Wilson et al., 2000; Hickerson and Cunningham, 2000) or using tRNAscan-SE 1.1 (Lowe and Eddy, 1997). The two rRNA genes were identified by sequence homology and proposed secondary structures (Crease, 1999). Sequence data are available from DDBJ/EMBL/GenBank under accession number AB071201. 2.5. Phylogenetic analysis In addition to the complete mtDNA sequences from P. japonicus, those from four crustaceans, brine shrimp (Artemia franciscana, X69067), water flea (Daphnia pulex, AF117817), giant tiger prawn (Penaeus monodon, AF217843), hermit crab (Pagurus longicarpus, AF150756), and three insects, African malaria mosquito (Anopheles gambiae, L20934), fruit fly (Drosophila yakuba, X03240), and migratory locust (Locusta migratoria, X80245), were used in phylogenetic analysis. Two branchiopod crustaceans (A. franciscana and D. pulex) were selected as collective outgroups with reference to the recent analyses of the arthropod phylogenies (e.g. Wilson et al., 2000; Hwang et al., 2002). Amino acid sequences from the individual protein-coding genes were aligned using CLUSTAL X (Thompson et al., 1997) with default gap penalties. Ambiguous alignment regions, such as the N- and C-terminus, were excluded from the alignments. The concatenated amino acid sequences from the 13 protein-coding genes were subjected to maximum parsimony (MP), maximum likelihood (ML), and neighbor-joining (NJ) analyses. Branch-and-bound MP analyses were conducted with 1000 bootstrap replicate searches using PAUP4b8a (Swof-

3.1. Genome organization The mitochondrial genome of P. japonicus was 15,717 bp in length. The genome content of P. japonicus included the 13 protein-coding, 22 tRNA, and two rRNA genes (Figs. 1 and 2) as found in other metazoan animals. Some of the genes overlapped as in other animal mtDNA. In addition, there was a 786 bp noncoding region between the srRNA and tRNA Ile genes, which apparently corresponds to the control regions of the Drosophila yakuba and D. melanogaster mitochondrial genomes (Wolstenholme, 1992) because of its position in the mitochondrial genome and a sequence characteristic (A 1 T rich). This putative control region was less than half as long as the control region of Artemia franciscana (Table 1). Gene order was identical to those so far determined for several other arthropods, such as Penaeus monodon (Wilson et al., 2000), Daphnia pulex (Crease, 1999), Drosophila yakuba (Clary and Wolstenholme, 1985), D. melanogaster (U37541), and so on, although remarkable deviations from such order was recently observed for Pagurus longicarpus (Hickerson and Cunningham, 2000) and Tigriopus japonicus (Machida et al., 2002). 3.2. Base composition The overall A 1 T content in P. japonicus mitochondrial genome was 64.5% (L-strand: A ¼ 32:0%; C ¼ 21:0%; G ¼ 14:5%; T ¼ 32:5%), lower than that of Penaeus monodon (70.6%) and similar to that of Artemia franciscana (64.5%) (Table1). This value was not so high compared with those of some other arthropods, particularly insects (Apis mellifera, 84.9%; Crozier and Crozier, 1993). This pattern of base composition held for the protein coding, rRNA, and tRNA genes, as well as the control region (Table 1). In the protein-coding genes, first and third codon positions were especially A 1 T rich (Table 2) as observed in other arthropods (Crease, 1999; Wilson et al., 2000). The

92

M.M. Yamauchi et al. / Gene 295 (2002) 89–96

Fig. 2. The complete L-strand nucleotide sequence of the Japanese spiny lobster, P. japonicus. Position 1 corresponds to the first nucleotide of the COI gene. Direction of the transcription for each gene is shown by arrows. Beginning and end of each gene is indicated by vertical bars. Transfer RNA genes are boxed; corresponding anticodons are indicated by black boxes. Amino acid sequences presented below the nucleotide sequence were derived using invertebrate mitochondrial genetic code (one-letter amino acid abbreviations placed below the first nucleotide of each codon). Stop codons are overlined and indicated by asterisks. Numbers within brackets indicate first and last position number of nucleotides omitted from this figure. Sequence data are available from DDBJ/ EMBL/GenBank with accession number AB071201.

M.M. Yamauchi et al. / Gene 295 (2002) 89–96

93

Table 1 Characteristics of crustacean mitochondrial DNAs Species

Panulirus japonicus Penaeus monodon Pagurus longicarpus Artemia franciscana Daphnia pulex

L strand

13 Protein-coding genes

srRNA

Putative control region

Length (bp)

A1T (%)

No. of amino acids

A1T (%)

Length (bp)

A1T (%)

Length (bp)

A1T (%)

Length (bp)

A 1 T (%)

15,717 15,984 – 15,770 15,333

64.5 70.6 – 64.5 62.3

3715 3716 3698 3521 3681

62.6 69.3 69.6 63.9 60.4

1355 1365 1303 1153 1314

69.2 74.9 77.1 64.0 68.3

855 852 789 712 753

67.1 71.6 77.2 61.4 67.2

786 991 – 1770 689

70.6 81.5 – 68.0 67.1

extreme bias in the use of A and T in the third codon position has been observed in invertebrate mtDNA proteincoding genes, especially in Drosophila yakuba (93.8%) and Caenorhabditis elegans (Nematoda; 86.3%), and Apis mellifera (95.2%) (Crease, 1999). Further, remarkable difference of C/G compositions between protein-cording genes on each strand was found (Table 2). These traits were also observed in Limulus polyphemus (Lavrov et al., 2000), although the process responsible for creating strand asymmetry of base compositions in mtDNA is unknown. 3.3. Protein-coding genes Among the 13 protein-coding genes of P. japonicus, there were two reading-frame overlaps on the same strand. ATPase subunit 8 (ATPase8) and ATPase6 shared seven nucleotides, NADH dehydrogenase subunit 4L (ND4L) and ND4 shared seven nucleotides (Fig. 2). Nine proteincoding genes (ATPase6, ATPase8, COII, COIII, cyt b, ND1, ND4L, ND4, and ND5) started with ATG, ND2 with GTG, ND3 with ATT, and ND6 with ATC (Table 1), which have commonly been found as start codons in other animal mtDNAs (Wolstenholme, 1992). The start codon of COI gene in P. japonicus was supposed to be ACG based on comparisons with the Penaeus monodon (Wilson et al., 2000) and Pagurus longicarpus (Hickerson and Cunningham, 2000), but this has not been confirmed experimentally. Although the start codon of COI gene is unclear in several arthropod species, the ACG has been regarded as a putative start codon in P. monodon (Wilson et al., 2000). Open-reading frames of P. japonicus ended with TAA (ATPase8, Table 2 Base composition (%) of 13 protein-coding genes for mitochondrial genome of Japanese spiny lobster, Panulirus japonicus

All genes 1st 2nd 3rd Total L-strand genes H-strand genes

lrRNA

A

C

G

T

27.6 17.3 29.4 24.9 25.5 24.0

16.2 21.5 17.3 19.2 22.2 14.5

24.2 16.0 16.2 18.2 16.0 21.6

32.0 45.2 37.1 37.7 36.3 39.9

ND1, and ND4L), and the remainder had incomplete stop codons, either TA (ATPase6, COIII, and ND6) or T (COI, COII, cyt b, ND2, ND3, ND4, and ND5). 3.4. Transfer RNA genes Pannulirus japonicus mtDNA encoded 22 tRNA genes which can fold into clover-leaf secondary structures (Fig. 3). The anticodon nucleotides were identical to those commonly found for the corresponding tRNA genes in other mtDNAs with two exceptions. The tRNA Lys and the tRNA Ser(AGN) genes in P. japonicus possessed the TTT and TCT anticodons instead of the more common CTT and GCT, respectively, in invertebrate mitochondrial genomes. The differences of these anticodons correspond to the third wobble position. Both variations of anticodon were also found in Pagurus longicarpus (Hickerson and Cunningham, 2000) and Tigriopus japonicus (Machida et al., 2002). 3.5. Ribosomal RNA genes The small and large subunit ribosomal RNA genes (srRNA and lrRNA, respectively) of P. japonicus were 855 and 1355 nucleotides long, as long as that of Penaeus monodon (Wilson et al., 2000) (Table1). Those were located in the same relative locations as in many other mtDNAs (Fig. 1). Preliminary assessment of the secondary structure of P. japonicus indicated that the present sequence could be reasonably superimposed on the proposed secondary structure of the Daphnia pulex srRNA and lrRNA genes (Crease, 1999). 3.6. Phylogenetic analysis Maximum parsimony (MP) analysis of the amino acid sequences from the concatenated 13 protein-coding genes yielded a single most parsimonious tree (Fig. 4), with a length of 3600 steps (consistency index ¼ 0:769; retention index ¼ 0:474; rescaled consistency index ¼ 0:365). Maximum likelihood (ML) and neighbor-joining (NJ) analyses produced the same trees as found in the MP analysis. All internal branches were supported by moderate to high (73– 100%) bootstrap values in all analyses. Monophyly of Decapoda species was supported by 100% bootstrap values in all analyses. Although Reptantia (P.

94

M.M. Yamauchi et al. / Gene 295 (2002) 89–96

japonicus 1 Pagurus longicarpus) was supported by moderate to high bootstrap values (73–92%), ‘Macroura’ (P. japonicus 1 Penaeus monodon), a group of the

shrimp-like forms with an elongated abdominal body and long tail (shrimps and lobsters in earlier classifications; e.g. Dana, 1852), appears to be a paraphyletic group. Macroura

Fig. 3. Putative secondary structures for the 22 transfer RNA genes of the P. japonicus mitochondrial genome. Watson–Crick and GT bonds are denoted by ‘ 2 ’ and ‘ 1 ’, respectively.

M.M. Yamauchi et al. / Gene 295 (2002) 89–96

95

Fig. 4. A single most-parsimonious (MP) tree for the selected arthropod taxa inferred from concatenated amino acid sequences of the 13 protein-coding genes (tree length ¼ 3600; consistency index ¼ 0:769; retention index ¼ 0:474; rescaled consistency index ¼ 0:365). Topology of the maximum likelihood (ML) and neighbor-joining (NJ) trees were identical to that of the MP tree. Numbers beside internal branches indicate bootstrap values for each analysis obtained for 1000 (MP), 100 (ML), and 2000 (NJ) replicates. A single number indicates that values were the same for all the analyses. For details see Section 2.5.

monophyly was confidently rejected by the mtDNA data (Templeton test (Z ¼ 23:286, P , 0:001); Templeton, 1983), indicating that elongated abdominal body in the Decapoda is a shared primitive feature (symplesiomorphy). Acknowledgements We thank T. Komai for confirming identification of the P. japonicus specimen, R.J. Machida for technical support in various phases of experiments, and N. Suzuki for technical instruction for phylogenetic analyses. We also thank H. Morino, Y. Yamazaki, and graduate students at Molecular Marine Biology Laboratory, Ocean Research Institute, University of Tokyo, for their helpful suggestions during this study. A portion of this study was supported by Grantsin-Aid from the Ministry of Education, Culture, Sports, Science, and Technology, Japan (12NP0201 and 13640711). References Clary, D.O., Wolstenholme, D.R., 1985. The mitochondrial DNA molecular of Drosophila yakuba: nucleotide sequence, gene organization and genetic codes. J Mol. Evol. 2, 52–271. Crease, T.J., 1999. The complete sequence of the mitochondrial genome of Daphnia pulex (Cladocea: Crustacea). Gene 233, 89–99. Crozier, R.H., Crozier, Y.C., 1993. The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. Genetics 133, 97–117. Dana, J.D., 1852. Crustacea. United States Exploring Expedition during the

years 1838, 1839, 1840 1841, 1842 under the command of Charles Wilkes. USN XIII, 1–635. Dayhoff, M.O., Schwartz, R.M., Orcutt, B.C., 1979. A model of evolutionary change in proteins. In: Dayhoff, M.O. (Ed.). Atlas of Protein Sequence and Structure, Vol. 5, suppl. 3. National Biomedical Research Foundation, Washington, DC, pp. 345–352. Felsenstein, J., 2000. PHYLIP (Phylogeny Inference Package) version 3.6, Department of Genetics, University of Washington, Seattle, WA distributed by the author. Folmer, O., Black, M., Hoeh, R., Lutz, R.A., Vrijenhoek, R., 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3, 294–299. George, R.W., Holthuis, L.B., 1965. A revision of the Indo-West Pacific spiny lobsters of the Panulirus japonicus group. Zool. Verh. Leiden 72, 3–36. Hickerson, M.J., Cunningham, C.W., 2000. Dramatic mitochondrial gene rearrangements in the hermit crab Pagurus longicarpus (Crustacea, Anomura). Mol. Biol. Evol. 17, 639–644. Holthuis, L.B., 1991. Marine Lobsters of the World. An Annotated and Illustrated Catalogue of Species of Interest to Fisheries Known to Date, , FAO Species Catalogue, Vol. 13, FAO Fisheries Synopsis No. 125, Rome. Hwang, U.W., Friedrich, M., Tautz, D., Park, C.J., Kim, W., 2002. Mitochondrial protein phylogeny joins myriapods with chelicerates. Nature 413, 154–157. Kittaka, J., Abrunhosa, F.A., 1997. Characteristics of palinurids (Decapoda; Crustacea) in larval culture. Hydrobiologia 358, 305–311. Kumar, S., Tamura, K., Jakobsen, I.B., Nei, M., 2001. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17, 1244–1245. Kumazawa, Y., Nishida, M., 1993. Sequence evolution of mitochondrial tRNA genes and deep-branch animal phylogenetics. J. Mol. Evol. 37, 380–398. LaRoche, J., Snyder, M., Cook, D.I., Fuller, K., Zouros, E., 1990. Mole-

96

M.M. Yamauchi et al. / Gene 295 (2002) 89–96

cular characterization of a repeat element causing large-scale size variation in the mitochondrial DNA of the sea scallop Placopecten megellanicus. Mol. Biol. Evol. 7, 456–464. Lavrov, D.V., Boore, J.L., Brown, W.M., 2000. The complete mitochondrial DNA sequence of the horsehoe crab Limulus polyphemus. Mol. Biol. Evol. 17, 813–824. Lowe, T., Eddy, S.R., 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25, 955–964. Machida, R.J., Miya, M.U., Nishida, M., Nishida, S., 2002. Complete mitochondrial DNA sequence of Tigriopus japonicus (Crustacea: Copepoda). Mar. Biotechnol. 4, 406–417. McWilliam, P.S., 1995. Evolution in the phyllosoma and puerulus phases of the spiny lobster genus Panulirus White. J. Crustacean Biol. 15, 542– 557. Minagawa, M., 1999. Quantitative analysis of the seasonality of male reproduction in the spiny lobster Panulirus japonicus (Decapoda: Palinuridae). J. Crustacean Biol. 19, 276–282. Miya, M., Nishida, M., 1999. Organization of the mitochondrial genome of a deep-sea fish, Gonostoma gracile (Teleostei: Stomiiformes): first example of transfer RNA gene rearrangements in bony fishes. Mar. Biotechnol. 1, 416–426. Okimoto, R., MacFarlane, J.L., Clary, D.O., Wolstenholme, D.R., 1992. The mitochondrial genomes of two nematodes, Caenorhabditis elagans and Ascaris suum. Genetics 130, 471–498. Strimmer, K., von Haeseler, A., 1996. Quartet puzzling: a quartet maximum likelihood method for reconstructing tree topologies. Mol. Biol. Evol. 13, 964–969. Swofford, D.L., 2001. PAUP*: Phylogenetic Analysis Using Parsimony

(*and Other Methods), version 4.0, Sinauer Associates, Sunderland, MA. Templeton, A.R., 1983. Phylogenetic inference from restriction endonuclease cleavage site maps with particular reference to humans and apes. Evolution 37, 221–244. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., Higgins, D.J., 1997. The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876–4882. Tuiki, H., Yamakawa, T., Aoki, I., Taniuchi, T., 1999. Fisheries management of juveniles of the Japanese spiny lobster. Nippon Suisan Gakkaishi 65, 464–472. Valverde, J.R., Batuecas, B., Moratilla, C., Marco, R., Garesse, R., 1994. The complete mitochondrial DNA sequence of the crustacean Artemia franciscana. J. Mol. Evol. 39, 400–408. von Nickisch-Rosenegk, M., Brown, W.M., Boore, J.L., 2001. Complete sequence of the mitochondrial genome of the tapeworm Hymenolepis diminuta: gene arrangements indicate that platyhelminths are eutrochozoans. Mol. Biol. Evol. 18, 721–730. Wilson, K., Cahill, V., Ballment, E., Benzie, J., 2000. The complete sequence of the mitochondrial genome of the crustacean Penaeus monodon: are malacostracan crustaceans more closely related to insects than to branchiopods? Mol. Biol. Evol. 17, 863–874. Wolstenholme, D.R., 1992. Animal mitochondrial DNA: structure and evolution. Int. Rev. Cytol. 141, 173–216. Yoshimura, T., Yamakawa, H., Kozasa, E., 1999. Distribution of final stage phyllosoma larvae and free-swimming pueruli of Panulirus japonicus around the Kuroshio Current off southern Kyusyu. Jpn. Mar. Biol. 133, 293–306.