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Doi: 10.7831/ras.4.8 c REVIEWS OPEN ACCESS MEDAKA IN JAPANESE AGRICULTURAL WATER CHANNELS: GENETIC DIVERSITY AND CONSERVATION M.S.A. Mamun1, Koji Tsuchida2, Takeo Onishi2, Ken Hiramatsu2, Atsushi Iwasawa2 and Shinichi Nishimura2
1 United Graduate School of Agricultural Science, Gifu University, 1-1 Yanagido, Gifu 501-1193, Japan 2 Faculty of Applied Biological Sciences, Gifu University, 1-1 Yanagido, Gifu 501-1193, Japan
ABSTRACT Medaka is familiar to Japanese people as a small fish inhabiting paddy fields, agricultural water channels and ponds. This would be a consequence of adaptation of medaka to the agricultural management calendar during the long history of Japanese paddy production. However, medaka has been categorized as “vulnerable” in the Red List of Threatened Wildlife of Japan since 1999. Habitat deterioration due to the recent modernization of paddy fields and agricultural channels is suggested as a likely cause. On the other hand, medaka has a history of more than a century as an excellent experimental model vertebrate like zebrafish, and a draft nucleotide sequence of the whole genome was released in 2007. Such biological information can be successfully applied to the conservation of medaka in paddy fields and channels. We summarize genetic analyses of medaka including our own research to elucidate the effects of the modernization of agricultural water channels to the subpopulation structure of medaka. We also focus on the analytical methods such as PCR-RFLP, RAPD and microsatellite and examples of their use in population structure analyses of various organisms that are much more detailedly examined for conservation purpose than medaka. Conservation efforts of medaka in paddy fields would be most successful if they are harmonized with the paddy production there. Practices to promote production and add values to the products such as “medaka rice” are mentioned in this context. Keywords: Irrigation and drainage channels, Freshwater fish, Multifunctionality of paddy field, Biodiversity conservation, DNA analysis
1. Introduction 1999). Deterioration of habitat due to rural development, land Medaka is familiar to Japanese people as a small fish inhabiting consolidation, modernization of agricultural channels, decrease of paddy fields, agricultural water channels and ponds. Historically, it natural farm ponds, lining of channels with three-sided concrete, was caught and reared as an ornamental fish from as early as Edo decrease of aquatic plants serving as laying bed, large drops era and has been depicted in various paintings since then (Sawara between paddy fields and drainage channels, adverse effects of and Hosomi, 2003; Sasado et al., 2010). It was also incorporated invasive alien species, etc. are suggested as likely causes of the into modern children’s songs composed in Meiji and Showa era decline of medaka (Hosoya, 2000; Hayashi, 2003; Takehana and that are still well known to Japanese people. Although most of Kitagawa, 2010). Since the citation of medaka in the Red List, them were forgotten, there used to be 2,800 or 5,000 local names of people of various sectors such as governments, NPOs, local medaka throughout Japan depending on the report (see Sawara and communities, schools and kindergartens have taken part in a variety Hosomi, 2003). All these suggest that medaka has been an important of conservation activities of medaka and its habitat throughout the component of the cultural landscape (sensu UNESCO World nation, which may have led not only to the conservation per se but Heritage Centre, 2012) of Japanese rural area. to the encouragement of children to be conscious of biodiversity However, medaka is categorized as “vulnerable” in the Red and environment surrounding themselves. List of Threatened Wildlife of Japan (Ministry of Environment, In many cases, medaka requires both a site of spawning
8 Received: November 30, 2015. Revised: February 3, 2016. Accepted: February 25, 2016. Published on line: May 9, 2016. Correspondence to A.I.: [email protected] ©2016 Reviews in Agricultural Science n ★ En tio v c ir u o d n
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Doi: 10.7831/ras.4.8 c and growing of juveniles (such as paddy fields) and that of spontaneous and induced mutants, 18 inbred lines, 85 transgenic overwintering (such as agricultural channels), and hence an lines, 22 medaka-related species and 67 wild stock lines of importance of conservation of these specific habitats for the medaka (as of July, 2014) are provided under the program survival of medaka (Abe and Hirota, 2006). Besides, since medaka Medaka Bioresource Project (NBRP: http://www.shigen.nig. inhabits rural area, overall promotion of paddy production along ac.jp/medaka) sponsored by the Japanese government (Sasado with eco-friendly, sustainable farming might play a key role in et al., 2010). When “medaka” was searched in the literature the conservation of medaka. It would also be important for the database PubMed (http://www.ncbi.nlm.nih.gov/pubmed), conservation of local medaka populations to consider genetic more than 2,800 articles were reached (as of November, 2015). characteristics within and between the populations. Some of these articles include mechanisms of sex determination In this paper, for the ultimate purpose of contribution to the (Herpin and Schartl, 2009), gonadal development (Nishimura and conservation of medaka and concurrent promotion of paddy field Tanaka, 2014), ovulation (Takahashi et al., 2013) and crosstalk of production, we first briefly summarize what kind of fish medaka is endocrine systems in reproduction (Flood et al., 2013); descriptive and then concentrate on the recent advancement of the evaluation (Iwamatsu, 2004) and molecular developmental biology (Wittbrodt of genetic property and diversity of medaka (including our own et al., 2002); functions of transposable elements of DNA (Koga et findings) and other organisms for comparison purpose. We finally al., 2002); studies of endocrine toxic substances in environment discuss the relationship between medaka and sustainable agricultural (Urushitani et al., 2007); models of human diseases (Asaoka et al., production that is of increasing importance in recent years. 2013; Schartl, 2014). See Parenti (2008) for the review of citations covering the use of medaka as well as the recent popularity of 2. Biology of medaka medaka in various fields. Whole genome draft sequences have Japanese medaka (Orizias latipes and O. sakaizumii) is a been determined for the inbred strain medaka Hd-rR and HNI small fish that belongs to the family Adrianichthyidae of the (Kasahara et al., 2007; Ahsan et al., 2008; Kobayashi and Takeda, order Beloniformes. It is distributed in all main islands of Japan, 2008), which are available online at the University of Tokyo i.e., Hokkaido (non-indigenous), Honshu, Shikoku, Kyushu and Genome Browser (http://utgenome.org), for example. Okinawa (Ministry of Environment, 1999). The genus name Oryzias came from the rice (Oryza sativa), the preferred habitat of 3. Taxonomic status and genetic diversity of madaka medaka being the rice paddy. 3.1. The family Adrianichthyidae Although medaka mostly inhabits freshwater, it can adapt to The family Adrianichthyidae (ricefishes) is composed of two seawater unlike the strictly stenohaline zebrafish (Danio rerio), genera and 36 species (genus Oryzias with 32 species and genus a ranking experimental model fish (Inoue and Takei, 2003). In Adrianichthys with four species) (Mokodongan and Yamahira, reality, medaka is sometimes found in brackish water. It is thus an 2015). Members of this family live in fresh and brackish waters excellent model for the studies of seawater adaptation of fishes. and are broadly distributed throughout Southeast and East Asia Actually, medaka has been another most widely used model fish in from India along the Malay Archipelago to Japan (Naruse, experimental vertebrate biology for more than a century (Parenti, 1996; Parenti, 2008). Most species inhabit tropical regions and 2008). Advantageous features of medaka as an experimental 20 species (16 Oryzias species and four Adrianichthys species) animal include small size (so that a large number of individuals are distributed in Sulawesi, one of the Greater Sunda Islands of can be kept in a laboratory), short generation time (two to three Malay Archipelago. Since 19 of these 20 species are endemic months), external sexual dimorphism, easy maintenance and to Sulawesi, this island is considered a biodiversity hotspot for breeding under laboratory conditions, transparent egg membrane Adrianichthyidae; Mokodongan and Yamahira (2015) attributed (favorable for the observation of embryonic development), and this to the complex geological history of Sulawesi that is located relatively small genomic size (approximately 800 million base in the region whose geography has changed considerably over the pairs, about the half of the genome of zebrafish) (Shima and past 50 million years (Lohman et al., 2011). Mitani, 2004; Parenti, 2008; Sasado et al., 2010). Due to a high 3.2.The genus Oryzias tolerance to inbreeding, many highly inbred strains have been Based on karyological analyses of the genus Oryzias, Uwa established (Kirchmaier et al., 2015). Various naturally occurred and his colleagues proposed that this genus be divided into three mutants such as albino have been known, while induced mutants groups (mono-armed, bi-armed and fused chromosome groups) (for and genetically modified medaka are widely used to clarify example, Uwa, 1990; reviewed by Naruse, 1996). Takehata et al. the function of specific genes and also to apply as models of (2005) divided the genus Oryzias into three major species groups human diseases. Of these, more than 490 strains including 300 (the javanicus, latipes, and celebensis groups), based on molecular
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c Doi: 10.7831/ras.4.8 phylogenetic analyses using the nuclear tyrosinase and mitochondrial by divergent DNA sequences (see Freeland et al., 2011). Based on 12S and 16S rRNA genes. They found that these three groups the results of the allozyme studies, Sakaizumi (1990) subdivided corresponded to the three karyotype groups, i.e., mono-armed, bi- the Southern population into nine regional types, namely, Eastern armed and fused chromosome groups, respectively. Medaka belongs Japan, Eastern Setouchi (or Eastern Inland Sea), Western Setouchi, to the latipes group that includes O. luzonensis native to north Luzon San-in, Northern Kyushu, Oosumi, Ariake, Satsuma and Ryukyu in the Philippines, O. curvinotus native to China and Vietnam and O. types. Between the Northern and the Southern populations lies a mekongensis native to the Mekon River basin (Takehata et al., 2005). major mountain range of Japanese Archipelago and this seems to On the other hand, Parenti (2008) thoroughly investigated 85 different have been a firm barrier against the movements of medaka whose morphological features of Oryzias and Adrianichthys species and habitat is wet lowlands (Sakaizumi, 1985). Similarly, borders claimed that, in Oryzias species, it was only the latipes group that between the regional types seem to correspond to geological monophyly was unambiguously supported; The morphological factors such as the existence of mountain ranges and straits data showed javanicus group was monophyletic only in part and (Sakaizumi et al., 1983; Takehana and Sakaizumi, 2002). The the celebensis group was paraphyletic. Parenti (2008) attributed allozyme analyses revealed a hybrid population termed “boundary this discordance to inappropriate taxon sampling and outgroup region population” in Tango and Tajima districts (i.e. the districts comparison conducted in the study of Takehata et al. (2005) and its along the Japan Sea coast of Kyoto and Hyogo Prefectures) at the preceding study of Naruse (1996). boundary between the Northern and the Southern populations; The 3.3. Classification of medaka allozyme results suggested this boundary region population was Takehana et al. (2003, 2004a, 2004b) reported that medaka not the result of recent hybridization, but “goes back to fairly old (O. latipes as described) in East Asia (Japan, Korea and China) times, for instance, to the last glacial period” (Sakaizumi, 1984). could be divided into four genetic populations by allozyme Matsuda et al. (1997) performed restriction fragment length and mitochondria DNA analyses, i.e., the Northern and the polymorphism (RFLP) analysis of entire mitochondrial DNA Southern populations of Japan, the East Korean population and (mtDNA) using mtDNA extracted from medaka whose head, the China-West Korean population. It has long been known that intestine and fins were removed, and six different restriction the Northern and the Southern populations of Japan are not only enzymes. The RFLPs are the first widespread markers that isolated geographically but differentiated genetically (Sakaizumi quantified variation in DNA sequences. The RFLP data are et al., 1980, 1983; Sakaizumi, 1984; Takehana et al., 2003, 2004a, generated using restriction enzymes that cut DNA at specific 2004b), and the Northern population has finally been proposed sequences, whose presence or absence depends on individuals, to describe as a new species, O. sakaizumii by Asai et al. (2011) populations, species, etc. (Freeland et al., 2011). In their RFLP based on taxonomical evidences. Asai et al. (2011) also suggested study, Matsuda et al. (1997) found that the mtDNA haplotypes (a that the China-West Korean population was considered to be O. total of 63) formed three distinct clusters (A, B and C) supported by sinensis (Chinese medaka sensu Parenti, 2008) and East Korean high bootstrap values more than 90%, and that the cluster A could be population could be a subspecies of O. sakaizumii or another subdivided into two subclusters, the cluster B could be subdivided unnamed species. The two species, O. latipes and O. sakaizumii, into 11 subclusters and the cluster C (whose haplotype found in were estimated to have diverged from the common ancestor 4.0-4.7 only two sites in the Kanto district) could not be subdivided. The million years ago using a molecular clock of cytochrome b gene geographic distributions of the clusters A and B corresponded to (Takehana et al., 2003) and 18 million years ago by a Bayesian the Northern and the Southern population, respectively, defined by relaxed molecular-clock analysis (Setiamarga et al., 2009). the allozyme studies (Matsuda et al., 1997). This was followed by 3.4. Local populations/types of medaka in Japan the study of Takehana et al. (2003), who conducted a phylogenetic Series of extensive studies by Sakaizumi and his colleagues analysis based on the nucleotide sequence analysis of the complete have revealed genetic diversity of the local populations of mitochondrial cytochrome b gene. Their analysis revealed 67 medaka in Japan. Their allozyme studies in 1980s showed wild mitotypes in total that could be divided into three major clades populations of medaka in Japan consisted of two genetically (A, B and C). The clades A and B were subdivided into three and different groups, namely, the Northern population (presently O. 11 subclades, respectively. The clades A, B and C completely sakaizumii) from the northern coast of the Sea of Japan, and the corresponded to the clusters A, B and C, respectively, revealed by Southern population (presently O. latipes) from eastern, western the RFLP analysis (Matsuda et al., 1997) of the entire mtDNA. and southern Japan (Sakaizumi et al., 1980, 1983; Sakaizumi, The relationship between the regional types revealed by allozyme 1986). Allozymes, classic genetic markers first used in 1960s, studies (Sakaizumi, 1990), subclusters revealed by RFLP of entire refer to multiple variants of the same protein that are generated mtDNA (Matsuda et al., 1997), and the subclades revealed by
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Doi: 10.7831/ras.4.8 c sequence analysis of cytochrome b gene (Takehana et al., 2003) is Development Bureau of the Ministry of Land, Infrastructure, summarized in Table 1. The cluster (clade) C is classified into the Transport and Tourism of Japan conducted the “School of Medaka Southern population by allozyme analysis. Survey in Aichi” from 2000 to 2002, a prefecture-wide survey of 3.5. Application of PCR-RFLP for conservation of medaka distribution and habitat condition of medaka, ranging 320 sampling The PCR-RFLP is a modification of RFLP, where PCR- points in 62 municipalities of Aichi Prefecture (Chubu Technical amplified DNA, instead of original DNA sample, is subjected to and Engineering Office, 2003). Nine different mitotypes were restriction enzyme reaction (reviewed by Rasmussen, 2012). An detected in Aichi Prefecture, each with a characteristic geographical attribute of PCR that encourages its use would be small amount distribution pattern. For example, Types 2.2 and 14 were found of sample necessary for the analysis; A small piece of the caudal only in the basin of the Kiso River. These nine mitotypes, although fin from medaka, for example, is sufficient for PCR-RFLP, RAPD analysis methods are not specified in the literature, seem to (see further) and microsatellite (see further) analyses, so that one correspond to the mitotypes obtained by PCR-RFLP (the method does not need to kill this endangered fish. Takehana et al. (2003) of Takehana et al., 2003) when only HaeIII was used out of the five conducted PCR-RFLP analysis of the complete mitochondrial restriction enzymes (Sakaizumi, 2015, personal communication). cytochrome b gene of medaka using five different restriction Koyama and Kitagawa (2009) investigated wild medaka enzymes, HaeIII, MboI, MspI, RsaI and TaqI, as a method that populations in Yamato River system, Nara Prefecture, by PCR- is simpler than DNA sequencing and could be applied to genetic RFLP (the method of Takehana et al., 2003) and warned that not monitoring for conservation of local medaka populations. Their only commercial, orange-red type strain of medaka (himedaka) was study, as well as their previous study, revealed that among the escaping from local fish farms to the river, but genetic introgression populations of medaka in Kanto district mitotypes from other occurred from himedaka to wild medaka populations. Koyama et districts such as Setouchi and Northern Kyushu were detected, al. (2011) investigated the mitotype of commercial strain of medaka which were possibly introduced by releasing medaka derived purchased from aquarium fish shops in various prefectures of Japan from these districts (Takehana and Sakaizumi, 2002; Takehana et by PCR-RFLP (the method of Takehana et al., 2003) and found al., 2003). They argued that there could be a possibility of river that the commercial medaka was characterized by a few specific captures in the past if populations in the upper and lower reaches mitotypes regardless of the shop locations. They warned again that of the river had different genetic types from each other but that the release of commercial medaka should be avoided to conserve the existence of the genetic types far beyond districts was not local medaka mitotypes (Koyama et al., 2011). accountable unless anthropogenic effects were assumed. They 3.6. Genetic analyses of wild populations of medaka in Wanouchi sometimes found such probably introduced types of individuals in Town, Gifu Prefecture park ponds (Takehana and Sakaizumi, 2002). 3.6.1. Introduction to the study and summary of the study area As expected by Takehana et al. (2003), this PCR-RFLP analysis Wanouchi Town is located in the southwest part of Gifu of medaka cytochrome b gene has been widely used for genetic Prefecture, Japan. The town is situated in the west part of the large monitoring for conservation. For example, the Chubu Regional delta formed by three big rivers, the Ibi, the Nagara and the Kiso.
Table 1: Comparison of the classification of medaka populations in Japan according to three different analyses Allozyme types Subclusters of mtDNA RFLP Subclades of cytochrome b gene (Sakaizumi, 1990) (Matsuda et al., 1997) (Takehana et al., 2003) Northen population A-1, 2 A-I, II Southern population Eastern Japan B-3, 4, 5, 7, 8, 9, C B-I, II, III, IV, V, C Eastern Setouchi B-8 B-VII Western Setouchi B-2, 5, 6, 8 B-VII, IX San-in B-1, 5 B-IX, X Northern Kyushu B-5, 11 B-IX Oosumi B-6 B-VIII Ariake B-11 B-XI Satsuma B-11 B-XI Ryukyu B-11 B-XI Hybrid population A-2, B-1 A-III, B-X Based on the original tables in Sakaizumi (2000) and Takehana and Sakaizumi (2002).
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The town consists of lowlands enclosed by a waju embankment primers (10 pmoles each), DNA sample, and ultrapure water. in the north and three rivers (the Ibi, the Nagara and the Oogure) Denaturation was performed at 94°C for 3 min, then 30 cycles of in the east, west and south. Historically, this area was prone to denaturation-annealing-extension (94°C for 1.5 min, 55°C for 2 flooding for centuries and many web-like tributaries changed their min, 72°C for 2 min), and the final extension at 72°C for 2 min. The ways repeatedly. The Government of Meiji Japan, advised by a PCR products were digested with four restriction enzymes HaeIII, Dutch civil engineer Johannis de Rijke (1842-1913), conducted MboI, MspI, and RsaI (Takara Bio) separately in different tubes for massive river restructuring between 1887 and 1911, which led to a 3 hours according to the manufacturer’s instructions. The resultant marked decrease of flooding throughout the basin of the three big products were electrophoresed in a 6% polyacrylamide gel. The rivers. However, most paddy fields in Wanouchi Town had still gel stained with CYBR Green (Life Technologies, Tokyo, Japan) been inundated most of the year and insufficiently drained even was visualized under ultraviolet light. The electrophoretogram during non-irrigation periods. Reclamation of the damp lowlands was recorded by a digital camera and analyzed for the molecular and land consolidation were started after the World War II and weights by ImageJ (Schneider et al., 2012). were completed by around 1965. The latest modernization of As is shown in Fig. 1B, mitotypes B11, B12 and B40 as paddy fields with separation of irrigation and drainage channels described by Takehana et al. (2003) were detected. The mitotypes has been performed in the recent 25 years (See Wanouchi Town, B12 and B40 were found in all sampling points whereas B11 was 1981 and Gifu Prefectural Museum, 1990 for the history of found in three sampling points. The B12 and B40 are mitotypes flooding, river restructuring and land consolidation in Wanouchi). that characterize medaka populations in the Kiso River basin and Therefore, it is a suitable study site to investigate effects of B11 is widely distributed in Eastern to Central Japan (Takehana channel improvements on genetic diversity of medaka. et al., 2003). Our results were consistent with these mitotype In Wanouchi Town, most drainage water from paddy fields flows distribution patterns. We could not find mitotypes that seemed to into four trunk channels called the Nishie, Naka-nishie, Nakae and be non-native, while non-native mitotypes probably introduced, Higashie Rivers, and these rivers flow into the Oogure River (Fig. for example by fish releases, have been found in some localities 1A). Since the water level of the Oogure is much lower than the rivers (Takehana and Sakaizumi, 2002; Takehana et al., 2003; Koyama outside the waju area except at the low tide, the water is forcedly and Kitagawa, 2009). We could not find mitotype B11 in sampling discharged by drainage pumps upward into the Ibi River. Irrigation points 2, 4 and 5. This might be because of small percentage of water is drawn mainly from the Ibi River only by pump facilities fish bearing B11 in points 2, 4 and 5. (Conference of the Integrated Plan for the Oogure River Internal Prefecture-wide survey of genetic diversity of medaka like Water, 2011). The recent and present possibility of the entry of new “School of Medaka Survey in Aichi” has never been undertaken individuals of medaka from outside this waju area is, therefore, in the adjoining Gifu Prefecture and our study is the first to reveal assumed to be low, hence the importance of conservation measures the mitotypes of medaka in Wanouchi Town. We plan to extend to prevent medaka from decreasing. Our series of investigations this survey to the neighboring towns; they are separated from in Wanouchi Town have been conducted to provide basic data for Wanouchi Town by large rivers and a waju embankment (see conservation of medaka and also to contribute to a consideration for Fig. 1A), and hence, it is worth evaluating the genetic features of environment on paddy field improvement. Medaka samples were medaka in Wanouchi Town in relation to the surrounding towns. collected from six different locations (Fig. 1A). See Mamun et al. Our present study would also contribute to an environmental (2015) for detailed description about the six sampling points. education to prevent the release of commercial medaka in paddy 3.6.2. PCR-RFLP fields and channels, which is of great importance in conservation We conducted PCR-RFLP analysis of local populations of of local genetic diversity. medaka in Wanouchi Town. DNA was extracted from caudal fins 3.6.3. Random amplified polymorphic DNA (RAPD) (about 1.5 × 3 mm) of medaka (n=14-18 for each sampling point) As mentioned above, allozyme, RFLP and PCR-RFLP according to Miller et al. (1988). The PCR-RFLP was performed analyses have contributed to elucidate genetic structures of as described by Takehana et al. (2003). Briefly, amplifications of wild populations of medaka in Japan. It seems also suitable for specific medaka DNA by PCR were performed in a 50 µl reaction detecting introduced medaka among individuals in a population. volume containing ExTaq Polymerase (1.25 units; Takara Bio Inc., However, more informative methods, such as DNA sequencing, Shiga, Japan), ExTaq buffer, dNTPs (2.5 nmols each of dATP, than the variations of protein and DNA fragment length would be dCTP, dGTP and dTTP), forward (5'-AGGACCTGTGGCTTG necessary if one seek for a detailed genetic comparison between AAAAACCAC-3'; Cytb Fa, Takehana et al., 2003) and reverse individuals and between populations. (5'-TYCGACYYCCGRWTTACAAGACCG-3'; Cytb RVa, id.) As a trial for further analyses of population genetics of wild
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Fig.1. (A) Map showing six sampling points of medaka, rivers and agricultural channels (in part) in Wanouchi Town, Gifu Prefecture. Pie charts show proportion of assignment of medaka (n=11 for each sampling point) to four genetic clusters estimated using the software STRUCTURE. Adopted from Mamun et al. (2015) with minor modification. (B) Number of individuals that belong to the genetic types (mitotypes) revealed by PCR-RFLP analysis of medaka collected in Wanouchi Town, Gifu Prefecture. Sampling points correspond to those in panel A. The insert map shows distribution of two Japanese medaka species (Orizias latipes and O. sakaizumii) according to Asai et al. (2011), and the location of Wanouchi Town.
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c Doi: 10.7831/ras.4.8 medaka in Wanouchi Town, we conducted a random amplified regions (Sathishkumar et al., 2011). Although several online polymorphic DNA (RAPD) experiment as a method that costs software programs are available for bioinformatical data mining less than DNA sequencing. The RAPD is a polymorphism of the based on these sequence data (Sharma et al., 2007; Tong et al., segments of amplified DNA (such as the presence/absence of a 2009), we employed a simple, in-house software program written segment) based on the amplification of random DNA segments with, in FORTRAN to find microsatellite regions from a public medaka normally, a single primer of arbitrary nucleotide sequence (Welsh genome database (Mamun et al., 2015). In our study of medaka and McClelland, 1990; Williams et al., 1990). The RAPD technique collected at the six sampling points (n=11 for each) in Wanouchi has been used in wide range of applications such as: analyses Town (Fig. 1A), we used ten primer sets to amplify microsatellite of genetic diversity of buffalograss (Buchloe dactyloides) for regions that consist of 12-28 repeats of tetranucleotides, for breeding plans (Zhang et al., 2007); identification of clonal spread example, (AACT)17. Our study was the first report where of the alpine willow (Salix herbacea) for the study of its strategy microsatellite analysis was applied to study meta-population of clonal/sexual reproduction (Reisch et al., 2007); estimations of structure of medaka around relatively small area (about 5 x 5 km) genetic structuring and gene flow between the populations of the of paddy fields. It revealed that 1) genetic diversity was relatively corn leafhopper (Dalbulus maidis) in Brazil, an important pest of high within each population possibly due to a large number of maize (de Oliveira et al., 2007); species identification of lamprey medaka present in each population; 2) there were weak (with the larvae that is difficult from their morphological features (Yamazaki values of pairwise FST ranging from 0.023-0.086) but significant et al., 2005); identification of natural hybrids (F1, F2, F3,... hybrids) genetic differentiation between populations possibly due to between two Japanese toads Bufo japonicus formosus and Bufo the obstacles such as sluice gates and drop works that caused torrenticola (Yamazaki et al., 2008). difficulties in free movements of medaka between populations; We conducted a RAPD analysis using medaka collected from 3) The individual medaka was assigned into four genetic clusters the above-mentioned, six sampling points (n= 20 for each) in by the STRUCTURE (Pritchard et al., 2000) analysis and each Wanouchi Town. We tried 12 different RAPD primers but only sampling point was characterized by one major cluster; Points one of them generated reproducible profiles, and consequently, 1 and 2, 3 and 4, and 5 and 6 had the same major cluster in we could not carry out detailed genetic analyses. The occasional common, respectively (Fig. 1A). Our study raised a possibility poor reproducibility of RAPD bands is sometimes regarded that genetic structuring of medaka in this study area has not been as a drawback of this method (Marois et al., 2001). However, remarkable until recently, and suggested a significance to promote numerous successful studies obviously indicate RAPD is still an free movements of medaka on planning further correction of important option for genetic analysis. irrigation/drainage channels in this area (Mamun et al., 2015). 3.6.4. Microsatellite analysis 3.6.5. Perspectives of genetic analyses of medaka populations in Although RAPD has an advantage that specific knowledge of Wanouchi Town the template DNA nucleotide sequence is not necessary (Williams Microsatellite analyses have uncovered many interesting et al. 1990), it could be more advantageous to use microsatellites population structures of fish as well as other organisms. There if nucleotide sequence is known. Microsatellites, also known as have been plenty of reports suggesting that genetic differentiation simple sequence repeats (SSRs), are genomic DNA sequences between fish populations is large if the populations are located in containing tandemly repeated short (1-10 base pairs) motifs of different river basins or, even in the same basin, if free movements nucleotides. For example, dinucleotide repeat (GT)10 consists of ten of individuals between the populations are physically restricted: for repeats of GT, like GTGTGTGTGTGTGTGTGTGT. Microsatellite example, Kawamura et al., 2007 (Oncorhynchus masou ishikawae), DNA loci have high levels of length polymorphism and generally Ornelas-García et al., 2012 (Neotoca bilineata) and Bartáková et provide high-resolution data, and thus are useful for the studies of al., 2013 (Nothobranchius furzeri). Genetic distance between the genetic diversity of populations (Bruford et al., 1996; Chistiakov et populations of threespine stickleback (Gasterosteus aculeatus) that al., 2006; Freeland et al., 2011; Abdul-Muneer, 2014). inhabit a scattered pond complex in Iceland is likely to correlate more These advantages prompted us to conduct microsatellite strongly to the landscape connectivity provided by flooding rather analysis of medaka in Wanouchi Town (Mamun et al., 2015). than to the geographical distance between the ponds (Seymour et Information of microsatellite regions in the genomic DNA as well al., 2013). A study on killifish (Aphanius baeticus) inhabiting Iberian as their flanking sequences is necessary for conducting genetic onshore rivers reported that periodic floods allowed dispersal of fish analysis using microsatellites. An increasing number of genomic between different costal streams and that genetic differentiations and expressed sequences (ESTs) in public databases have enabled between these populations were not very high with the values of researchers to use these sequences for finding microsatellite pairwise FST ranging from 0.001 to 0.471 (mean: 0.180) (Gonzalez
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Doi: 10.7831/ras.4.8 c et al., 2014). Ancient DNA analysis of a population of Atlantic to the river where it was reared) over contemporary timescales, sturgeon (Acipenser oxyrinchus) once inhabited but now extinct in such patterns can be reversed over evolutionary, coalescent- the Baltic Sea suggested that the Baltic population had been founded derived timescales, hence the importance of conservation efforts by migrants from Canadian population (Ludwig et al., 2008). In spite of small populations (Palstra et al., 2007). Although MIGRATION of the very large geographical distance between the ancient Baltic is reported to have some drawbacks in estimating migration rates and Canadian populations, their genetic distance was small with the (Abdo et al., 2004) and BAYESASS assume relatively large genetic value of pairwise FST (0.02) showing no significant difference from differentiation among populations (Wilson and Rannala, 2003), 0 (Ludwig et al., 2008). Altogether, these reports suggest that the these methods seem worth applying for more detailed evaluation of genetic distance is generally influenced by a degree of movements population structures of medaka with careful consideration whether of individuals between populations or, in other terms, connectivity the analyses reflect biological reality. The question how agricultural between the populations, even if geographical distance is large. We facilities such as sluice gates and drop works changed small- plan to study further how connectivity of the agricultural channels scale population structures of madaka in Wanouchi Town seems and geographical distance influence genetic population structures of worth pursuing for us and we plan to continue our investigations medaka in Wanouchi Town using microsatellites by increasing the with the use of these two analytical programs besides a long-term number of SSR primers, sampling points and individuals. observation of the population structures. It is of paramount importance in terms of freshwater fish conservation to know how the population structure changes 4. Ecological features of medaka and sustainable paddy chronologically, i.e., before and after the installation of irrigation/ production drainage facilities that are possible obstructors for the free The Food, Agriculture and Rural Areas Basic Act of Japan (1999) movements of fish. Direct estimates of individuals that migrate notes in the Article 3 “Multiple functions of agricultural production from one station to another by mark-recapture methods might activities in rural areas, other than the function of supplying food and be useful for this purpose, but they could be impractical if the other agricultural products, such as the conservation of national land, percentage of migrants exchanged between the population is very water resources and natural environment, formation of favorable low, because the expected number of recaptures is too low (Wilson landscapes, and the passing down of culture (hereinafter referred and Rannala, 2003). Furthermore, we cannot go back in time and to as “Multiple Functions”) must be performed appropriately and mark-recapture the fish before the installation of irrigation/drainage sufficiently into the future”. Since the implementation of this act, there facilities when they are already installed. The program MIGRATE has been a growing interest in the promotion of multifunctionality of (Beerli and Felsenstein, 2001) available at http://evolution.genetics. paddy fields and related facilities, among which is the conservation of washington.edu/lamarc.html based on coalescent theory (Kingman, diverse organisms inhabiting there like medaka (Hata, 2002; Matsuno 1982) estimates long-term gene flow of about 4Ne (Ne: effective et al., 2006; Miyamoto, 2007). population size; Wright, 1931) generations in the past. On the Medaka has adapted to the agro-ecosystem where periodic other hand, the program BAYESASS (Wilson and Rannala, 2003) disturbance is inherent according to the traditional agricultural available at http://rannala.org uses a Bayesian method and estimates management calendar (Sawara and Hosomi, 2003). Medaka mostly rates of recent migrations within several generations. These two spawns in paddy fields in spring and the larvae may either stay programs based on different principles have been jointly used by there as their lifelong habitat or migrate into channels in autumn for some authors who intend to compare historical and contemporary overwintering if water is drained out of the paddy fields in the non- gene flow among fish populations. For example, Yamazaki et al. irrigation period (Hata, 2002; Sawara and Hosomi, 2003; Takehana (2011) indicated that historical gene flow among subpopulations and Kitagawa, 2010). In paddy fields where water is drained out of a fluvial lamprey, Lethenteron sp. N, living in a paddy water temporarily in late spring (a practice called nakaboshi), medaka also system had been frequent and bidirectional, whereas contemporary migrates down into the channels in tandem (Abe and Hirota, 2006). gene flow was unidirectional. They suggested that the installation Hata (2002) classified Japanese freshwater fishes from the viewpoint of sluice gates hindered the free movements of individuals, and of migration. For example, ocean-migrating threespine stickleback hence gene flow between subpopulations. Palstra et al. (2007) also migrates down to the ocean and up rivers to agricultural water used MIGRATION and BAYESASS to show that the relationship channels. Carp (Cyprinus carpio) usually migrates between rivers of source and sink in meta-population structure of Atlantic salmon and channels. Catfish (Silurus asotus) migrates similarly but prefers (Salmo salar) in North American rivers was not constant over paddy fields to channels for spawning. Medaka and loach (Misgurnus longer timescales; Whereas large populations tend to function anguillicaudatus) migrate between channels and paddy fields (or as sources (of straying fish in the context of homing of salmon stay lifelong in paddy fields if water remains). Securement of the site
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c Doi: 10.7831/ras.4.8 of spawning and growing of juveniles (i.e. paddy fields), the site of and services aimed at multifunctional agriculture); 4) support to overwintering (i.e. channels) and a connection between the two sites the agriculture sector (such as promotion of researches to meet are suggested as requisites for the conservation of medaka in the the needs for ecology-oriented agriculture). Along with other areas, especially after consolidations (Abe and Hirota, 2006). Since measures, these governmental supports seem also necessary for the swimming capability of medaka is low, it is difficult for medaka to conservation of biological diversity (including medaka) of paddy swim in concrete channels whose flow velocity tends to rise high. fields that is a part of the multifunctionality of agriculture. Some Thus, measures preventing medaka from falling into rivers through municipalities in Japan (for example, Gifu Prefecture as of 2015) channels are also necessary (Abe and Hirota, 2006). financially support installations of fish passes in paddy fields under Medaka is an important intermediate species of food webs certain conditions. For successful survival of medaka, installations in the paddy field ecosystem, since it feeds on plankton, small of waterway bottoms that are lower than those of other parts (like aquatic arthropods and insects fallen into the water, while being a pit) with enough water during the non-irrigation period would prey of various larger organisms (Sawara and Hosomi, 2003). This also be necessary for overwintering. Even in the paddy fields with can lead to the implication that a paddy field where madaka lives fish passes, appropriate regulations of the water level of (generally) healthy life and constantly produces its offspring is ecologically the drainage channels in irrigation periods would be important sound, or in other words, medaka is an indicator species (see for the free movement of medaka between the paddy fields and Primack, 2006) of ecologically sound paddy fields. Thus, there are a the channels. Studies for the verification of these effects on the number of examples throughout Japan of commercial packed rice, population of medaka should preferably be promoted with financial rather more expensive than the ordinary one, with regional brand aids of municipalities and conducted in corporation with local names baring medaka (for example, Gifu Medaka Rice) to show farmers, NPOs, schoolchildren and their parents. the value added to the rice that was produced medaka-friendlily Pham (2015) investigated the role of trees in paddy field safe, for example, with the least use of pesticides. It is also landscapes (rice-producing forests) in northeast Thailand and worth mentioning an example (Munakata et al., 2013; Yagiyama stressed the paramount importance of preserving biological Zoological Park, 2014) that medaka might play an indispensable diversity in human-managed landscape like paddy fields and the role as a symbol of the restoration from disasters. The paddy fields necessity of comprehensive strategies to achieve this purpose. and channels inhabited by medaka along the Pacific coast of Sendai Combined with infrastructure development, increase in people's City were utterly destroyed by the tsunami caused by the Great income and stability of lives, creation of new jobs, etc. for East Japan Earthquake occurred in 2011. Researchers of the Miyagi sustainable agriculture in paddy rural area, medaka seems most University of Education who happened to have collected about 50 likely to be conserved for the next generations. In doing so, we individuals of medaka in this area in 2010 and kept them in their believe that the accurate and detailed assessments of genetic labs, launched the “Sendai Medaka Rice Project” in collaboration diversity of medaka will provide scientific basis for policy with the Yagiyama Zoological Park, Sendai and the farmers of the decision and its implementation to promote multifunctionality of stricken area. The project ultimately aims at restoring paddy fields paddy agriculture. inhabited by medaka by inviting local volunteers to breed and rear the survived medaka in their homes, offices, etc. until paddy Acknowledgements fields are resumed. Some paddy fields that are already resumed This study was supported in part by a Grant-in-Aid for are used to produce “Sendai Medaka Rice” without pesticides. In Scientific Research from the Japan Society for the Promotion of this sense, medaka serves not only as an indicator species of sound Science (No. 22380128 to K.H., K.T., A.I. and S.N.). We thank our paddy ecosystem but also as a flagship species (Primack, 2006) for former students, Shigeru Sato, Yuka Okada and Chika Uchida for promotion of ecologically friendly farming and possibly for the their valuable help in sampling and data analyses. unity of people in a local community. Finally, what are the requirements for successful conservation References of medaka in paddy fields? Groenfeldt (2005) enumerated four Abe A and Hirota J (2006) Measures for preservation of Japanese necessary supports by the administrative agency for the promotion killifish in land consolidation projects and farmers’ opinions of of multifunctional service of agriculture: 1) support to individual the measures -Case study of Kanzaki project area in Ichinoseki- farmers (such as incentives to farmers who take production city, Iwate prefecture-. Abstract of the Meeting of JSIRDE, regimens that will enhance multifunctional features); 2) support to 2006: 350-351. the rural communities (to yield outcomes that create rural amenities Abdo Z, Crandall KA and Joyce P (2004) Evaluating the and jobs); 3) support to the rural area (such as infrastructure performance of likelihood methods for detecting population
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