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Conservation and Phylogeography of Taiwan Paradise Fish, Macropodus Opercularis Linnaeus

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Conservation and Phylogeography of Taiwan Paradise Fish, Macropodus Opercularis Linnaeus Acta Zoologica Taiwanica 10(2): 121-134 (1999) Conservation and Phylogeography of Taiwan Paradise Fish, Macropodus opercularis Linnaeus Tzi-Yuan Wang1, Chyng-Shyan Tzeng1, and Shih-Chieh Shen2 1Department of Life Science, National Tsing Hua University, Hsinchu, Taiwan 30043, R.O.C. 2Department of Zoology, National Taiwan University, Taipei, Taiwan 10617, R.O.C. ABSTRACT The paradise fish (Macropodus opercularis) is naturally distributed in western Taiwan, but is rare now because of such factors as environment pollution and habitat loss. Conservation of this animal in Taiwan is becoming more urgent. Some closely related species, such as Chinese paradise fish (M. chinensis), are difficult to distinguish with morphological charac- ters. We sequenced and compared the control region of mitochondrial DNA (mtDNA) to reveal the genetic distance and molecular phylogeny of paradise fish populations from dif- ferent geographical regions: Taiwan, Singapore, and mainland China. The interspecific dis- tance between M. opercularis (Taiwan, Singapore) and M. chinensis (Zhejiang, Jilin) is 0.1341 ±0.0124, much more highly divergent than the distance between the Taiwanese and Singaporean populations, or within the Chinese populations. Five haplotypes from 11 specimens of the Taiwanese native population have been identified from a 1034-bp-length of mtDNA. However, the lower haplotypic diversity (H = 0.68) indicates a decreasing pop- ulation in Taiwan, in contrast with the M. chinensis (H = 0.89). In addition, the unique genotype in Miaoli and Taichung may imply their subdivision because of exotic input of fish from a different geographic region. Thus conservation work should focus on avoiding the random release of paradise fishes into the wild. Key words: Macropodus opercularis, Paradise fish, Mitochondrial DNA, Taiwan of the first tropical fishes that 19th century INTRODUCTION Europeans kept as pets (Shen et al., 1991). Tai- Only three species of Anabantoidei fishes wan paradise fish can be further divided into occur in Taiwan: Anabas testudineus, Macropo- four groups, according to their body color: dus opercularis, and Tricogaster trichopterus. A. Nankang (Taipei) type, Sanyi (Miaoli) type, testudineus is close to extirpation on this Shyrshoeike (Taichung) type, and Malaysia island, while the last species is assumed to have peninsula type (Jan et al., 1992). The natural been introduced from other areas. As a result, distribution of paradise fish has been in west- paradise fish, M. opercularis, is the only species ern Taiwan, but is now limited because of envi- of the Subfamily Macropodinae, Perciformes: ronment pollution, habitat loss, etc. Belontiidae (Forselius, 1957; Liem, 1963; Nel- M. opercularis is dispersed extensively in son, 1994) in Taiwan. The so-called colorful plain and lower-elevation hills of western and rabbit sold for aquariumuse is actually an northeastern Taiwan. Natural ponds, minor introduced man-bred paradise fish strain. creeks, and farm drains areas-slow-moving, Some strains of paradise fish interbred with nearly quiescent waters are the preferred habi- other species have also become popular in the tats. However, the broad distribution has aquatic pet market. Paradise fish was also one dwindled to a sporadic occurrence according 121 Tzi-Yuan Wang, Chyng-Shyan Tzeng, and Shih-Chieh Shen Table 1. Collection data and sample information. Bold letters indicate that the samples are collected from aquarium. The others are all native populations in this investigation. Scientific name Region, Country Colony Specimens number (analyzed number) Macropodus opercularis (Mo) Taipei, Taiwan MN 2 (1) Hsinchu, Taiwan MB 3 (2) Miaoli, Taiwan MS 4 (2) Taichung, Taiwan MK 3 (3) Chiayi, Taiwan MJ 3 (2) Pingtung, Taiwan MP 3 (1) Aquarium, Taiwan MU 3 (1) Duan, Guangxi DA 5 (*) Juhae, Guangdong JH 4 (*) Aquarium, Singapore SG 2 (2) Macropodus chinensis (Mc) Wuyih, Zhejiang WE 5 (3) Jyrlin, Jyrlin GL 2 (2) Trichopsis pumilus (Tp) Aquarium TP 3 (2) Betta splendens (Bs) Aquarium BS 3 (3) * Sample was preserved in formalin without successful mtDNA sequence data. to a 1991 investigation (Shen et al., 1991; Jan Korean peninsula in 1914, and have proven and Wu, 1994), despite the government's capable of reproducing in the wild. Recently, announcement to place the paradise fish in the Wakiyama (1997) employed 12 allozyme mark- list of rare and valuable species on 31 Aug. ers to analyze the relationships among 17 1990. species of Anabantoid fishes. The result con- Kimura (1937) first reported and estab- firmed anatomy-based classification of five lished data of the Anabantidae fishes in China. Macropodinae species: Betta splendens and M. Chen (1969) reported A. scandens and M. oper- opercularis were grouped together with cularis (Synonyms names: M. polyacanthus Parosphromenus deissneri, whereas Trichopsis Linnaeus, M. viridiauratus Oshima) in Taiwan vittatus and Pseduosphromenus dayi constituted thereafter. Chen (1969) stated that M. opercu- a separate group. laris could be found in Taipei, Taichung, and Jan and Wu (1994) investigated M. opercu- Luotung. Fig. 1A illustrates the distribution of laris since 1992, and 12 isolated, native, but the species native to southern China, the small populations are found in this investiga- Malaysia peninsula, Hainan I., Okinawa, and tion. Conservation of M. opercularis remains Taiwan (Oshima, 1934; Nelson, 1994). Both pressing, and conserving the genetic diversity Hong Kong- and Japan-inhabiting paradise between populations will directly influence fishes belong to either M. opercularis or M. chi- their long-term chance of survival. Resolving nensis (Oshima, 1934; Wen, 1981). Some simi- molecular phylogeny between two paradise lar species, such as Chinese paradise fish (M. fishes (M. opercularis and M. chinensis) appears chinensis) and M. opercularis, are difficult to to be the key to these problems, because they distinguish solely with morphological charac- are confused by traditional taxonomic meth- ters. The Chinese paradise fish originally ods. The mitochondrial DNA (mtDNA) con- spread from the western Korean peninsula, trol region has been shown to be a powerful then west of the Luohtung River to mainland marker in the analysis of inter- and intra-spe- China, to the north of the Yangtze River. The cific genetic differentiation owing to the imple- specimens in Japan were introduced from the mentation of rapid evolution rates than 122 Conservation and Phylogeography of Taiwan Paradise Fish, Macropodus opercularis Linnaeus (A) (B) Figure 1. Distribution of Macropodinae fishes in Asia (A); and (B) sampling locations of paradise fishes in Sin- gapore (SG), China (DA, JH, WE, GL), and Taiwan (MN, MB, MS, MJ, MP). Detailed information is given in table 1. remainder of the mtDNA genome (Brown et at 45 to 55 °C. Proteins and lipids were al., 1986; Lee et al., 1995; Sbisae et al., 1997). removed by phenol-chloroform extraction. Maternal inheritance of mtDNA genes also DNA was precipitated at -20 °C by adding two provides a sensitive tool for the detection of volumes of 100% ethanol. Pellets were washed population subdivision (Birky et al., 1989). with 70% ethanol, dried and resuspended in 50 In this study, we examine the genetic diver- µl TE (10 mM Tris-HCl, pH8.0; 1 mM EDTA, gence among samples of M. opercularis and M. pH 8.0). chinensis using the entire mtDNA control region to reveal the genetic information of M. PCR amplification and sequencing opercularis. Betta splendens and Trichopsis A segment of mtDNA that encompasses a pumilus are utilized as outgroups to compare part of the cytochrome b gene, tRNAThr gene, the molecular phylogeography among different tRNAPro gene, the control region, and a part of populations of M. opercularis. tRNAPhe gene, was chosen for sequencing analysis. The primers, Ec7, G22A, PE3, and MATERIALS AND METHODS PK3-2A, were modified from Tzeng et al. Sample collection and DNA extraction (1992); the primer PU was modified from Jean A total of 45 fully grown fishes were col- et al. (1995); the primers, PE4-1, PU4-1 and lected from western Taiwan, Zhejiang, Jilin, PU4-2, were used only for sequencing (Fig. 2, Guangdong, Guangxi, and Singapore from Sep. Table 2). 1996 to Dec. 1999 (Fig. 1, Table 1). Specimens PCR amplifications were performed in a 50- from Taiwan were kept alive in the laboratory. µl reaction volume containing 0.2 mM of Total genomic DNA was extracted from muscle dNTP, 0.2 µM of each primers and 10-500 ng or fin tissue, using a protocol modified from of genomic DNA, 1 unit of Taq polymerase Kocher et al. (1989). Approximately 50 mg of (HT Biotechnology Ltd., England), and the muscle tissue was placed in 700 µl of digestion buffer supplied by the manufacturers. The buffer (10 mM Tris-HCl, pH 8.0; 2 mM EDTA, amplification conditions were as follows: 30- 10 mM NaCl, 1% SDS, 10 mg/ml DTT, 0.5 40 cycles at 93 °C for 1 min of denaturation, mg/ml Proteinase K) and incubated overnight annealing at 45 to 55 °C for 1 min, and exten- 123 Tzi-Yuan Wang, Chyng-Shyan Tzeng, and Shih-Chieh Shen Table 2. List of primers used in this study. Name Primer sequence Location of mtDNA Ec7 5’-ATYCTACGRTCAATYCC-3’ Cytochrome b PE3 5’-AACTTCCATCCTCAACTCCCAAAGC-3’ Pro-tRNA PE4-1 5’-TAATAATTATWCAGGAC-3’ Control region PK3-2A 5’-CTATTACTGGCATCTGG-3’ Control region G22A 5’-TGKWCCTGAAATAGGAACC-3’ Control region PU4-2 5’-TYYTAGGAGTTTAGGGGG-3’ Control region PU4-1 5’-GCTTTAATTAAGCTACG-3’ Phe-tRNA PU 5’-GGGCATTCTCACGGGGATGCG-3’ Phe-tRNA Figure 2. Schematic diagram of partial mtDNA and the locations of eight primers. The primers, indicated by arrows, were used for amplification and sequencing. For the sequence of each primer see table 2. Table 3. Specimen number and their haplotypes of mtDNA among different colonies. MN MB MS MK MJ MP MU SG WE GL TP BS Mo1 1 2 1 1 2 Mo2 2 Mo3 2 Mo4 1 Mo5 1 Mo6 1 Mc1 1 Mc2 1 Mc3 1 Mc4 1 Mc5 1 Tp1 2 Bs1 3 sion at 72 °C for 1 min; a final extension reac- stranded PCR product mixtures were used as tion of 10 min at 72 °C was always added.
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