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Mitochondrial DNA Differentiation in the Japanese Brown Frog Rana Japonica As Revealed by Restriction Endonuclease Analysis

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Mitochondrial DNA Differentiation in the Japanese Brown Frog Rana Japonica As Revealed by Restriction Endonuclease Analysis Genes Genet. Syst. (1997) 72, p. 79–90 Mitochondrial DNA differentiation in the Japanese brown frog Rana japonica as revealed by restriction endonuclease analysis Masayuki Sumida Laboratory for Amphibian Biology, Faculty of Science, Hiroshima University, Higashihiroshima, Hiroshima 739, Japan (Received 17 February 1997, accepted 28 April 1997) To elucidate mtDNA differentiation in the Japanese brown frog Rana japonica, and compare it with results from allozyme analysis and crossing experiments, RFLP analysis was conducted on 78 frogs from 16 populations in Honshu. Purified mtDNA was digested with eight six-base recognizing restriction enzymes and analyzed by 1% agarose-slab gel electrophoresis. Cleavage patterns of the mtDNA showed three distinct genome size classes: small (18.5 kb), middle (20.0 kb) and large (21.5 kb). Ten haplotypes (I~X) were observed among the 16 populations. The expected nucleotide divergences within populations ranged from 0 to 0.47% with a mean of 0.08%. The net nucleotide divergences among 16 populations ranged from 0 to 7.74% with a mean of 3.49%. The UPGMA dendrogram and NJ tree, which were constructed based on the net nucleotide divergences, showed that R. japonica diverged first into the eastern and western groups. The eastern group subsequently differentiated into a subgroup containing six populations and the Akita population, and the western group divided into several subgroups. These results, as well as the results of allozyme analysis and crossing experiments, suggest that the eastern and western groups have experienced secondary contact, and introgression has occurred in the Akita population. eastern, western and northwestern groups, were repro- INTRODUCTION ductively isolated from one another by male hybrid steril- The Japanese brown frog, Rana japonica, is widely dis- ity (Sumida, 1996). tributed through Japan, from Honshu (except for the Mitochondrial genomes of higher animals are mater- northern end) to Kyushu and into China (except for the nally inherited, closed circular duplex DNA molecules. northeastern regions) (Okada, 1931, 1966; Maeda and They are compact in organization, conserved in gene con- Matsui, 1989). In Japan, the Ichinoseki population (east- tent, and range in size, among species, from 15,000 to ern Japan) of R. japonica is reproductively isolated from 23,000 base pairs (Brown, 1983; Kessler and Avise, 1985; the Hiroshima population (western Japan) by sterility in Moritz and Brown, 1986). The evolutionary rate at the male hybrids (Sumida, 1981). These male hybrids show nucleotide sequence level for animal mtDNA is rapid, per- varying degrees of testicular abnormality, and in the first haps 1-10 times faster than a typical single copy nuclear spermatogenetic meiosis, homologous chromosomes fail to DNA (Brown et al., 1979; Vawter and Brown, 1986). pair, resulting in the formation of univalents and varying Variations in fragment patterns revealed following diges- degrees of degeneration of the spermatids (Sumida, 1994). tion with restriction enzymes are referred to as restriction Starch-gel electrophoretic analyses of 25 loci encoding 15 fragment length polymorphisms (RFLPs). Base substitu- enzymes and three blood proteins of 505 individuals be- tion can create or eliminate cleavage sites for a particular longing to 25 populations showed distinct differentiation enzyme, thereby altering the number and size of frag- between the eastern and western groups. The introgres- ments detected by that enzyme alone (Dowling et al., sion of eastern alleles was noted at several loci in the 1996). A great deal of attention has been given to RFLP northwestern populations such as the Akita and Joetsu analyses of animal mtDNA within and among populations populations (Sumida and Nishioka, 1994a). The locus (Harrison, 1989; Avise, 1994; Moritz, 1994). Mitochon- linked with the sex-determining gene differed with the lo- drial DNA markers, originally used mainly for the analy- cal populations (Sumida and Nishioka, 1994b). Extensive sis of population structure and matriarchal phylogeny, crossing experiments among 20 populations from Honshu have also been used to elucidate the phenomena of hybrid- and Kyushu showed that three population groups, the ization and introgression (Streit et al., 1994). In the con- 80 M. SUMIDA text of hybridization, the most frequently used approach was centrifuged at 36,000 rpm (Hitachi RPS-40 rotor) for has been to apply nuclear markers (mostly allozymes and 40 h at 20°C. The fraction containing closed circular ribosomal DNA sequences) and an RFLP analysis of mtDNA was collected, extracted three times with CsCl- mtDNA in concert to reveal the process and directionality saturated isopropanol to remove the dye and dialyzed of hybridization. against 0.1 mM EDTA (pH 8.0) for 20 h with two changes In the present study, the restriction fragment analysis of the medium. The mtDNA solutions were stored at of mtDNA was used to examine intraspecific variation in -20°C until used. Rana japonica and to compare the results with those obtained from crossing hybridization experiments and Restriction endonuclease digestion. Eight six-base allozyme analysis. recognizing restriction endonucleases, BglII, EcoRI, EcoRV, HpaI, PstI, SacI, SmaI and XhoI, were purchased from TaKaRa. The mtDNA was digested by incubating MATERIALS AND METHODS at 37°C for 2 h with appropriate amounts of the enzymes Animals and mtDNA preparation. A total of 78 adult under conditions described by the suppliers. Agarose- Rana japonica (66 females and 12 males) was collected slab gel (1% Sigma agarose) electrophoresis was carried from 16 localities throughout Honshu (Table 1). Most of out in the standard TAE buffer (0.04 M Tris, 0.001 M them were also used for allozyme analysis (Sumida and EDTA, 0.02 M sodium acetate, pH 8.3). After electro- Nishioka, 1994a) and crossing experiments (Sumida, phoresis, the gels were stained with 0.1 µg/ml ethidium 1996). Mitochondria were isolated from fresh livers or bromide and photographed under ultraviolet light. λ- ovaries. Tissues were homogenized in a decuple volume DNA digested with HindIII was used as molecular weight of STE buffer (0.25 M sucrose, 0.03 M Tris-HCl, 0.01 M standards. The cleavage patterns with each enzyme EDTA, 0.11 M NaCl, pH 7.6) cooled with ice, and centri- were designated by A, B, C, etc., in the order of discovery. fuged at 800 ×g for 10 min at 2°C. The supernatant was centrifuged at 10,000 ×g for 10 min at 2°C. MtDNA was Nucleotide sequence divergence and dendrogram. purified by CsCl ethidium bromide density gradient cen- Nucleotide sequence divergence between mtDNA haplo- trifugation described by Yonekawa et al. (1980) as follows types was calculated by the method of Gotoh et al. (1979). (Sumida, 1997). Mitochondria obtained from each frog The expected value for the nucleotide sequence divergence were lysed completely by suspending the pellet in 3.6 ml within a population (nucleotide diversity; π) was calcu- (final volume) of 0.6% sarcosyl, 10 mM EDTA and 10 mM lated from the estimated nucleotide divergence and fre- Tris-HCl (pH 8.0). The lysate was then dialyzed against quencies (Nei and Tajima, 1981). The nucleotide diver- the same buffer for 4 h at room temperature. The volume gence (πxy) and the net nucleotide divergence (δ) between of lysate was adjusted to 3.6 ml by the same buffer, and 3.6 populations were estimated according to the method of Nei g of solid CsCl and 0.24 ml of 4.6 mg/ml ethidium bromide and Tajima (1981). Based on the net nucleotide diver- were added to the lysate and mixed well. Then the lysate gences, dendrograms were constructed by two different Table 1. Specimens of Rana japonica used in the present study No. of specimens Prefecture Locality Population Total Female Male Eastern Iwate Ichinoseki-shi, Sannoseki 11 10 1 Ichinoseki Fukushima Onuma-gun, Aizutakada-machi 2 2 0 Aizutakada Tochigi Yaita-shi 3 2 1 Yaita Chiba Sawara-shi 4 4 0 Sawara Chiba Mobara-shi 6 6 0 Mobara Kanagawa Isehara-shi, Sannomiya 5 4 1 Isehara Northwestern Akita Akita-shi, Toyoiwaishidazaka 7 6 1 Akita Niigata Kitakanbara-gun, Nakajo-machi 5 5 0 Nakajo Niigata Santo-gun, Izumozaki-machi 1 1 0 Izumozaki Niigata Joetsu-shi 2 2 0 Joetsu Western Fukui Sakai-gun, Mikuni-cho 2 2 0 Mikuni Shizuoka Fujieda-shi 3 1 2 Fujieda Aichi Ama-gun, Tatsuta-mura 2 1 1 Tatsuta Shimane Ochi-gun, Ochi-cho 3 3 0 Ochi Hiroshima Higashihiroshima-shi, Saijo-cho 12 11 1 Saijo Hiroshima Saiki-gun, Saiki-cho, Iinoyama 10 6 4 Saiki Total 78 66 12 Mitochondrial DNA differentiation in Rana japonica 81 methods: the unweighted pair-group arithmetic average cleases. The cleavage patterns of each enzyme except clustering method (Sneath and Sokal, 1973) and the BglII, SacI, and SmaI, with which no site variations were neighbor-joining method (Saitou and Nei, 1987). found among individuals, are shown in Fig. 1. Hetero- plasmy was not observed in any individuals. The num- bers of cleavage patterns produced by site variation were RESULTS three (A~C) in HpaI and XhoI, four (A~D) in EcoRI and Cleavage pattern and genome size of mtDNA. PstI, and eight (A~H) in EcoRV (Fig. 1). Fragment Restriction enzyme cleavage patterns of R. japonica lengths of each cleavage pattern were determined by their mtDNA were analyzed with eight restriction endonu- mobilities relative to those of λ-DNA fragments digested Fig. 1. Cleavage patterns of Rana japonica mtDNA digested with five restriction enzymes. A~H = types of cleavage patterns with each enzyme; M = λ-DNA digested with HindIII as molecular weight standards. l, m, s = three genome size (large, middle, and small) classes. 82 M. SUMIDA with HindIII (Table 2). kb, and the large type (l) having about 21.5 ± 0.4 kb (Table Cleavage patterns of mtDNA showed three genome size 2, Fig.
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