Phylogeography of the Chinese False Gudgeon, Abbottina Rivularis, in East Asia, with Special Reference to the Origin and Artifcial Disturbance of Japanese Populations
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Ichthyological Research (2019) 66:460–478 https://doi.org/10.1007/s10228-019-00686-w FULL PAPER Phylogeography of the Chinese false gudgeon, Abbottina rivularis, in East Asia, with special reference to the origin and artifcial disturbance of Japanese populations Nian‑Hong Jang‑Liaw1,5 · Koji Tominaga1,6 · Chungung Zhang2 · Yahui Zhao2 · Jun Nakajima3 · Norio Onikura4 · Katsutoshi Watanabe1 Received: 7 September 2018 / Revised: 13 February 2019 / Accepted: 18 February 2019 / Published online: 8 March 2019 © The Ichthyological Society of Japan 2019 Abstract The Chinese false gudgeon, Abbottina rivularis, is a common cyprinid fsh that is widely distributed throughout continental East Asia, but exhibits a restricted, discontinuous distribution in western Japan, including Honshu and Kyushu islands. In this study, analyses of mitochondrial (cytochrome b) and nuclear (glyt, myh6, and RAG1) genes were conducted to investigate patterns and magnitudes of intraspecifc diferentiation among A. rivularis populations in Japan and adjacent continental areas. Phylogenetic analysis of the mitochondrial gene sequences resolved four major lineages—the Japan lineage (JL), a northern continental lineage (NCL), and two southern continental lineages (SCL1 and SCL2)—with uncorrected pairwise sequence distances of 9.4–15.2% (estimated divergence times, 7.9–17.1 Myr). Two lineages (JL and SCL1) occurred in both the Honshu and Kyushu districts of Japan. Compared with populations in continental areas, most Japanese populations exhib- ited less genetic diversity. The JL was divided into two well-diferentiated sub-lineages distributed on Honshu and Kyushu islands, respectively. Kyushu Island, as well as areas on Honshu where the species is known to have been introduced, also harbored the SCL1 lineage, which constituted most of the populations on Kyushu. The applied nuclear DNA data strongly suggest that hybridization between the Japan and continental lineages has occurred on Kyushu Island. The artifcial introduc- tion hypothesis, instead of a two-origin scenario, best explains the origin of the SCL1 in Japan. Keywords Abbottina rivularis · Freshwater fsh · Phylogeography · East Asia · Artifcial introduction · Mitochondrial DNA (mtDNA) · Nuclear DNA Introduction East Asia is a large region that includes several divergent geographic features. Land covers about 12,000,000 km2 (about 9% of all land on Earth) in this region, which includes Electronic supplementary material The online version of this part of the Russian Far East, China, the Korean Peninsula, article (https ://doi.org/10.1007/s1022 8-019-00686 -w) contains northern Vietnam, and surrounding islands, and several supplementary material, which is available to authorized users. * Nian-Hong Jang-Liaw 3 Fukuoka Institute of Health and Environmental Sciences, 39 [email protected] Mukaizano, Dazaifu, Fukuoka 818-0135, Japan * Katsutoshi Watanabe 4 Fishery Research Laboratory, Kyushu University, 2506 [email protected] Tsuyazaki, Fukutsu, Fukuoka 811-3304, Japan 5 Present Address: Conservation and Research Center, Taipei 1 Department of Zoology, Division of Biological Zoo, No. 30, Sec. 2, Xinguang Road, Wenshan District, Sciences, Graduate School of Science, Kyoto University, Taipei 11656, Taiwan Kitashirakawa-Oiwake, Sakyo, Kyoto 606-8502, Japan 6 Present Address: Kwansei Gakuin Senior High School, 1-155 2 Institute of Zoology, Chinese Academy of Sciences, 1-5 Uegahara-ichibancho, Nishinomiya, Hyogo 662-8501, Japan Beichen West Road, Chaoyang District, Beijing 100101, China Vol:.(1234567890)1 3 Phylogeography of Abbottina rivularis 461 large rivers (e.g., the Amur River, Yellow River, Changjiang accompanied by the stocking of commercially valuable fsh River, and Pearl River) run through the continental area. In (Tsukahara 1954; Hosoya 2001; Matsuzawa and Senou addition, climate patterns vary with latitude and altitude. 2008). In Lake Biwa, the largest lake in Japan, located in the Due to the complicated topography and climatic character- Kinki Region, the indigenousness of this cyprinid is unclear istics, the biota of East Asia is complex and provides ample because of its limited occurrence there (Miura1966; Naka- subject matter for biogeographic studies (Li and Li 1997; mura 1969; Nakajima and Nakagawa 2007; Matsuzawa and Xiao et al. 2001; Kita and Kato 2004; Motokawa and Kaji- Senou 2008). hara 2017). In addition to continental East Asia, thousands Over the past few decades, phylogenetic/phylogeographic of islands lie along the Pacifc coast, where high endemism studies using nucleotide sequence information have become is often observed (e.g., Ota 1998; Hsieh 2002; Shih and the most useful approach for the investigation of genetic Suzuki 2008). backgrounds in terms of population biogeography, evolu- Japan is an island country with more than 3,000 islands tionary systematics, and conservation (Avise 2000; Wata- extending along the Pacifc coast of East Asia, stretching nabe et al. 2006; Beheregary 2008). To reconstruct evolu- from the Sea of Okhotsk in the north to the East China Sea tionary lineages in animals, mitochondrial (mt) DNA is a and Taiwan in the south. The Japanese freshwater fsh fauna suitable candidate marker (Avise 1994; Kocher and Stepien exhibits close relationships to those in adjacent areas, as 1997) and is widely used for various purposes, including the these fsh communities formed as a result of repeated con- study of natural and artifcial processes driving the distribu- nections and separations between continental Asian and tion of animals (Beheregary 2008). The cytochrome b gene Japanese freshwater systems (Lindberg 1972; Nishimura (cytb) has been one of the most frequently utilized segments 1980; Watanabe et al. 2017). The four largest islands (Hok- of mtDNA because it is generally polymorphic within spe- kaido, Honshu, Shikoku, and Kyushu, from north to south; cies, easy to align, and has been characterized in various Fig. 1) together account for 97% of Japan’s land area. The vertebrates, including many fsh species (e.g., Doadrio and four major islands are separated by narrow straits that form Domìnguez 2004; Tang et al. 2006; Yang et al. 2006; Tomi- migration barriers, as do extensive mountain systems in the naga et al. 2016). However, mtDNA alone is often insuf- interiors of these islands. Due to the complex topography cient for phylogenetic/phylogeographic analyses, especially in Japan, the freshwater ichthyofauna shows remarkable in studies of complex evolutionary processes including geographic heterogeneity (Watanabe 2012; Watanabe et al. hybridization or selection (Chan and Levin 2005). Thus, 2017). Using phylogenetic and phylogeographic analyses of nuclear (nc) DNA sequences for phylogenetic reconstruction the widely distributed freshwater species, several attempts have also been increasingly used to address phylogenetic/ have been made to reconstruct the historical formation of the phylogeographic issues (e.g., Li and Ortí 2007; Kawahara Japanese freshwater fauna (Watanabe et al. 2006; Watanabe et al. 2009; Watanabe et al. 2010a). et al. 2017). The present study investigated intraspecifc variations The Chinese false gudgeon, Abbottina rivularis, is a good of A. rivularis in Japan and adjacent areas by sequencing candidate for phylogeographic surveys in Japan and East mtDNA and nuclear genes with three objectives: (1) to Asia. The fsh is a small cyprinid that inhabits shallow zones identify clear phylogenetic relationships within/between of slow or lentic ditches, rivers, and lakes with sandy or Japanese and continental populations, with inference of muddy bottoms (Hosoya 2001). The species occurs widely divergence times; (2) to clarify the native distribution pat- in the East Asian region, including Japan and continental tern of A. rivularis in Japan; and (3) to propose possible East Asia from the Amur River in the north to Fujian and dispersal scenarios of A. rivularis on the Japanese islands. Yunnan provinces of China in the south (Bǎnǎrescu and For a widely distributed species like A. rivularis, cryptic Nalbant 1973; Chu and Chen 1989; Neely et al. 2008); this lineage divergence is often detected by phylogeographic fsh was also introduced into the Mekong River and other analysis (Avise 2000; Watanabe et al. 2017). Knowledge of regions (Vidthayanon and Kottelat 1995; Kottelat 2001; the natural distribution and genetic structure of A. rivularis Tang and He 2015). Although A. rivularis is a common will be helpful in understanding the natural history of the species in China, it is somewhat rare in Japan and is lim- freshwater ichthyofauna of Japan and continental East Asia. ited to several discontinuous areas: the Kanto Plain, Nobi Plain, Kinki Region, and Sanyo Region on Honshu Island, and northwestern Kyushu Island (Miura 1966; Hosoya 2001; Materials and methods Nakajima and Nakagawa 2007; Fig. 1). Few studies have examined the ecology or biogeography of this fsh in Japan Specimens. In total, 209 specimens of Abbottina rivula- (Tsukahara 1954; Nakajima and Nakagawa 2007; Hayashi ris were collected from Japan and continental East Asia et al. 2013), and researchers generally accept that A. rivula- for analyses; in addition, data for eight specimens were ris of the Kanto Plain was artifcially introduced probably obtained from DDBJ/EMBL/GenBank (Table 1; Liu et al. 1 3 462 N.-H. Jang-Liaw et al. Fig. 1 Locations of sampling sites and lineages for Abbottina rivula- b Complete map of the study area. c, d Larger maps of Kyushu and ris in this study. a Map depicting