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Mitochondrial Genetic Diversity of the Freshwater Snail Melanoides Tuberculata

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Mitochondrial Genetic Diversity of the Freshwater Snail Melanoides Tuberculata Biochemical Genetics (2019) 57:323–337 https://doi.org/10.1007/s10528-018-9892-3 ORIGINAL ARTICLE Mitochondrial Genetic Diversity of the Freshwater Snail Melanoides tuberculata Yuh‑Wen Chiu1,2 · Ye‑Chen Gan3 · Po‑Hsun Kuo4 · Kui‑Ching Hsu5 · Mian‑Shin Tan6 · Yu‑Min Ju7,8 · Hung‑Du Lin9 Received: 25 June 2018 / Accepted: 12 October 2018 / Published online: 26 October 2018 © Springer Science+Business Media, LLC, part of Springer Nature 2018 Abstract According to geological history, Peninsular Malaysia and Borneo formed at difer- ent times and were once connected during Quaternary glaciations. To determine how this history has infuenced phylogeography, our study examined the population genetic structure of the tropical freshwater gastropod Melanoides tuberculata across Peninsular Malaysia and Borneo using the sequences from mitochondrial DNA 16S rRNA and cytochrome oxidase subunit I genes (1168 bp). In total, 104 specimens were collected from seventeen populations. All mtDNA haplotypes were identi- fed as belonging to two highly divergent lineages, and these lineages were almost allopatric in their distributions. Our study found that the freshwater fauna in Malay- sia might be divided into four regions: northeast Peninsular Malaysia, northwest Peninsular Malaysia, south Peninsular Malaysia, and Borneo. The phylogeography of M. tuberculata in Malaysia was shaped by the landforms of Peninsular Malaysia and by the paleo-river systems in the Sunda continental shelf. In addition, our study found that these two lineages in Malaysia have invaded the globe. These results sug- gest that Malaysia is located in important shipping lanes throughout the world, and the populations of M. tuberculate might be widely distributed throughout the world by shipping. Keywords Malaysia · Melanoides tuberculate · Population genetics · Snail · Sundaland Electronic supplementary material The online version of this article (https​://doi.org/10.1007/s1052​ 8-018-9892-3) contains supplementary material, which is available to authorized users. * Hung‑Du Lin [email protected] Extended author information available on the last page of the article Vol.:(0123456789)1 3 324 Biochemical Genetics (2019) 57:323–337 Fig. 1 Map showing the sampling localities of Melanoides tuberculata used in this study (asterisks). The pie charts are the frequencies of the mtDNA lineages (Fig. 3) in each population Introduction Peninsular Malaysia, Borneo, southern Thailand, southern Indo-China, Sumatra, Java, and the Sunda continental shelf (the present-day shallow sea) are defned as Sundaland in Paleogeology (Hanebuth et al. 2011). Sundaland is considered a bio- diversity hotspot by the organization Conservation International based in Washing- ton DC (Cox and Moore 2000). It has been documented that this high biodiversity is because of the complex geological history of this area and the efects of Pleis- tocene sea-level changes (Voris 2000). During Quaternary glaciations, the Sunda continental shelf was exposed by the sea-level dropping. At this time, four major drainage systems existed on the Sunda continental shelf (Fig. 1a; Voris 2000). The Siam River system (SRS) collected from the south to the tip of Peninsular Malaysia, and the North Sunda River system (NSR) collected from eastern Sumatra, western Borneo, and possibly south Peninsular Malaysia. These two rivers emptied into the present-day South China Sea. The East Sunda River (ESR) was located from the present-day Java Sea and eastward. The Malacca Straits River (MSR) drained north- westward between northern Sumatra and western Peninsular Malaysia. Many phylo- geographic studies of freshwater species have shown that these paleo-river systems in the Sunda continental shelf caused gene fow among islands during Pleistocene glaciations (e.g., Inger and Chin 2002; McConnell 2004; De Bruyn et al. 2004; Ryan and Esa 2006). In addition, the longitudinal Main Range of Peninsular Malaysia might play an important role in isolating populations on either side of the mountains. Yeo et al. (2007) proposed that two largely peninsular groups of the freshwater crab genus 1 3 Biochemical Genetics (2019) 57:323–337 325 Johora appeared to have fairly distinct distributions on either side of the Main Range of Peninsular Malaysia. To determine how this complex system has infuenced phylogeography, our study examines the genetic patterns of the tropical freshwater snail Melanoides tuberculata (Müller 1774) since it is restricted to freshwater systems and there- fore provides opportunities for testing the infuences of geological events on the distribution of genetic variations (e.g., Chen et al. 2007; Hsu et al. 2014). Mel- anoides tuberculata, red-rimmed Melania, is a tropical freshwater gastropod in the family Thiaridae. This taxon was originally described from India and is com- mon to freshwaters within its native distributional range, which covers tropical regions, although it has been introduced in many other tropical and subtropical areas worldwide (e.g., Dundee and Pain 1977; Madsen and Frandsen 1989; Dug- gan 2002; Santos et al. 2007; Reeves et al. 2008; Lasso et al. 2009; Vázquez and Perera 2010). Thus, the objectives in our study are to (1) establish the DNA bar- codes of M. tuberculata in Malaysia, (2) characterize the phylogeography of M. tuberculata in Malaysia, and (3) examine the relationships among populations of M. tuberculata in Malaysian accessions and other worldwide accessions available at GenBank. To achieve the above objectives, genetic variability was analyzed by the mitochondrial DNA (mtDNA) cytochrome oxidase subunit I (COI) and 16S rRNA (16S) genes. mtDNA sequences are usually analyzed in studies of animal phylogeography (e.g., Chen et al. 2007; Hsu et al. 2014). Among mtDNA genes, the COI gene is used in DNA barcodes (e.g., Folmer et al. 1994; Hebert et al. 2003), and 16S rRNA is used to resolve phylogenies (e.g., Guo et al. 2005; Liu et al. 2018). Methods Study Site and Taxon Sampling The territories of Malaysia include two parts: East (Sarawak, Borneo of Malaysia) and West (Peninsular Malaysia) Malaysia, which are separated by the South China Sea. Peninsular Malaysia is the most southern region in Asia, and Borneo is a large island between Asia and Australia. To examine the relationships within and between Borneo and Peninsular Malaysia, our study sampled specimens in Malaysia. In total, specimens were collected from seventeen populations (Fig. 1). These seventeen populations were divided into three regions, two regions in Peninsu- lar Malaysia, i.e., western Peninsular Malaysia (WPM) and eastern Peninsular Malaysia (EPM), and one in Sarawak (SRW; Borneo part of Malaysia). A total of 104 specimens were collected (Table 1; Fig. 1). These samples were fxed and stored in 100% ethanol. All specimens were stored in the National Museum of National Science in Taiwan. Sequences of M. tuberculata from other regions were also directly obtained from GenBank for comparison (Tables S1 and S2). Tarebia granifera (COI: AY958760; 16S: EF382644) was used as an outgroup. 1 3 326 Table 1 Samples of Melanoides tuberculata used for mtDNA analyses, location, code, haplotype diversity (h), and nucleotide diversity (%, θπ and θω) (for sampling site number see Fig. 1) Region Drainage Population Code Size Latitude (N) Longitude (E) H θπ θω Habitat Sarawak (SRW) 18 0.647 0.745 0.500 Sarawak River Sarawak River Barrage (1) SB 6 1°34′24.33″ 110°24′33.54″ 0.000 0.000 0.000 ditch Kampong Iboi (2) KI 6 1°31′9.24″ 110°42′38.91″ 0.000 0.000 0.000 ditch Pisang Garden (3) PG 6 1°32′35.92″ 110°19′24.46″ 0.600 0.258 0.188 ditch East of Peninsular Malaysia (EPM) 43 0.849 5.795 2.792 Kelantan River Pulai Chondong (4) PC 6 5°54′52.44″ 102°12′8.02″ 0.000 0.000 0.000 ditch Besut River Jertih (5) JT 6 5°44′17.64″ 102°29′30.31″ 0.333 0.029 0.038 ditch Dungun River Tanjong Jara (6) TJ 7 4°49′11.81″ 103°25′9.89″ 0.286 3.229 4.613 stream Pahang River Gambang (7) GB 6 3°41′59.99″ 103°7′20.78″ 0.533 0.046 0.038 stream Chini (8) CN 6 3°23′23.02″ 102°56′35.09″ 0.333 0.057 0.075 ditch Endau River Endau (9) ED 6 2°36′56.36″ 103°40′23.00″ 0.000 0.000 0.000 ditch Johor River Tanjong Surat (10) TS 6 1°34′36.49″ 104°7′9.18″ 0.000 0.000 0.000 ditch West of Peninsular Malaysia (WPM) 43 0.672 4.846 2.872 Biochemical Genetics (2019)57:323–337 Lenek River Sungai Suloh (11) SS 5 1°46′55.75″ 102°57′26.61″ 0.000 0.000 0.000 ditch Sungai Ayam (12) AY 7 1°47′1.94″ 102°56′31.27″ 0.571 0.049 0.035 stream Langat River Kajang (13) KJ 6 3°0′56.22″ 101°46′24.33″ 0.000 0.000 0.000 ditch Selangor River Rawang (14) RW 8 3°19′30.67″ 101°33′34.97″ 0.571 6.459 4.359 ditch Perak River Tambun (15) TB 6 4°37′9.44″ 101°9′35.40″ 0.000 0.000 0.000 ditch Tasik Chenderoh (16) TC 6 4°58′22.06″ 100°56′0.03″ 0.000 0.000 0.000 ditch Juru River Bukit Mertajam (17) BM 5 5°21′27.69″ 100°28′27.27″ 0.000 0.000 0.000 stream Total 104 0.889 5.707 2.630 Bold values indicate the statistics in the region 1 3 Biochemical Genetics (2019) 57:323–337 327 Genetic Analyses Genomic DNA was extracted from muscle tissue by a Tissue & Cell Genomic DNA Purifcation Kit (GeneMark-DP021). The COI and 16S genes were amplifed using polymerase chain reaction (PCR) with primers adapted from Folmer et al.
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