Genetic characteristics and possible introduced origin of the paradise fish Macropodus opercularis in the Ryukyu Archipelago, Japan

  • Yuichi Kano
  • Ryoichi Tabata
  • Jun Nakajima
  • Mikumi Takada-Endo
  • Chunguang Zhang
  • Yahui Zhao
  • Tomomi Yamashita
  • Katsutoshi Watanabe
Full Paper

Abstract

It has hitherto been unknown whether the paradise fish Macropodus opercularis that inhabits the Ryukyu Archipelago, Japan, is native to the region or was introduced. This study examined the genetic identity of fish from five islands in the Ryukyu Archipelago (Okinoerabu, Okinawa, Yagaji, Kume, and Minamidaito islands) and compared it with those from Taiwan Island, mainland China, and Hainan Island. Analyses of the mtDNA control (760 bp) and cytb (660 bp) regions showed that haplotypes of specimens from the Ryukyu Archipelago were the same as or were very similar (with a 1- or 2-bp difference) to those from Taiwan. In addition, haplotypes from the Ryukyu Archipelago also showed lower genetic diversity than those from Taiwan Island, mainland China, and Hainan Island. These results suggest a high likelihood that the fish in the Ryukyu Archipelago were artificially introduced from Taiwan. However, the possibility that the fish is indigenous to the Ryukyu Archipelago cannot be completely ruled out, because some haplotypes and a clade from the Ryukyu Archipelago have not been found in the other areas. Regardless of its origin, we emphasize the importance of the conservation of the paradise fish in the Ryukyu Archipelago as an indicator of the threatened wetland environment as well as for its cultural value.

Keywords

Mitochondrial DNA Endangered Conservation Okinawa Paddy fields 

References

  1. Ankei Y (2007) Iriomote-jima no noukoubunka (Agrarian cultures in Iriomote Island). Hosei University Press, TokyoGoogle Scholar
  2. Ankei Y, Toyama M (2011) Amami-Okinawa kankyoshi shiryo shusei (The corpus of environmentology of Amami-Okinawa). Nanposhinsha, KagoshimaGoogle Scholar
  3. Aoyagi M (1948) Ryukyu-rettou san tansuigyorui sousetsu (A review of freshwater fishes in the Ryukyu Islands). Zool Mag 58:13–14Google Scholar
  4. Baba H, Narasaki S (1991) Minatogawa man, the oldest type of modern Homo sapiens in East Asia. Quat Res 30:221–230Google Scholar
  5. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9: 772Google Scholar
  6. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10: 564–567Google Scholar
  7. Hammer Ø, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education. https://folk.uio.no/ohammer/past/. Accessed 1 July 2017
  8. Harada S, Jeon SR, Kinoshita I, Tanaka M, Nishida M (2002) Phylogenetic relationships of four species of floating gobies (Gymnogobius) as inferred from partial mitochondrial cytochrome b gene sequences. Ichthyol Res 49:324–332Google Scholar
  9. Hosoya K (2013) Belontiidae. In: Nakabo T (ed) Fishes of Japan with pictorial keys to the species, third edition. Tokai Univ Press, Hadano, p 1655Google Scholar
  10. Iguchi K, Yodo T, Katano O (2003) Habitat conditions for freshwater fishes found in a paddy water system on Iriomote Island. Jpn J Ichthyol 50:115–121Google Scholar
  11. Ingvarsson PK (2001) Restoration of genetic variation lost – the genetic rescue hypothesis. Trends Ecol Evol 16:62–63Google Scholar
  12. Inoue JG, Miya M, Tsukamoto K, Nishida M (2000) Complete mitochondrial DNA sequence of the Japanese sardine, Sardinops melanostictus. Fish Sci 66:924–932Google Scholar
  13. Inui T, Kuwabara T, Suzuki K, Kawase S, Maegata M (2013) A report of the biological research on butterflies, inland water fishes and birds in the Yaeyama Islands, Okinawa, Japan. Mem Fac Agric Kinki Univ (46):277–298Google Scholar
  14. Ishikawa C, Matsuura K (1897) Preliminary catalogue of fishes including Dipnoi, Cyclostomi and Cephalochorda in the collection of the natural history department, imperial museum. Imperial Museum, TokyoGoogle Scholar
  15. Kagoshima Kankyogaku Kenkyukai (2010) Kagoshima Kankyougaku II. Nanposhinsha, KagoshimaGoogle Scholar
  16. Kano Y, Nakajima J (2014) Non-killing simple photography techniques of small–middle freshwater fishes in the field. Jpn J Ichthyol 61:123–125Google Scholar
  17. Kano Y, Nakajima J, Mizutani H, Nakazato Y, Nakazato N, Kaji Y, Huang L, Nishida S, Hashiguchi Y (2012) Critical status of the genetically-district, oriental weather loach (Misgurnus anguillicaudatus) population on Iriomote Island, Japan. Jpn J Ichthyol 59:37–43Google Scholar
  18. Kano Y, Adnan MSB, Grudpan C, Grudpan J, Magtoon W, Musikasinthorn P, Natori Y, Ottomanski S, Praxaysonbath B, Phongsa K, Rangsiruji A, Shibukawa K, Shimatani Y, So N, Suvarnaraksha A, Thach P, Thanh PN, Tran DD, Utsugi K, Yamashita T (2013) An online database on freshwater fish diversity and distribution in Mainland Southeast Asia. Ichthyol Res 60:293–295Google Scholar
  19. Kano Y, Watanabe K, Nishida S, Kakioka R, Chris W, Shimatani Y, Kawaguchi Y (2011) Population genetics structure, diversity, and stocking effect of the oriental weatherloach (Misgurnus anguillicaudatus) in an isolated island. Environ Biol Fishes 90:211–222Google Scholar
  20. Kanou M (2009) Is the paradise fish endangered or alien? In: Japan Wildlife Research Center (ed) A photographic guide to the invasive alien species in Japan, Heibon-sha, Tokyo, p 173Google Scholar
  21. Kimura M (2004) Paleogeography of Ryukyu Islands. In: Nishida M, Shikatani N, Shokita S (eds) The flora and fauna of inland waters in the Ryukyu Islands (2nd edn). Tokai University Press, Tokyo, pp 17–24Google Scholar
  22. Kimura S (1937) Distribution and some notes on the two Chinese labyrinth fishes. J Shanghai Sci Inst Sec III 7:47–69Google Scholar
  23. Kitagawa T, Hosoya K (2016) Origin of the Ryukyuan paradise fish Macropodus opercularis inferred from literature survey. Biogeography 18:11–16Google Scholar
  24. Kitagawa T, Oda Y, Hosoya K (2013) Reproductive characteristics of captive paradise fish Macropodus opercularis from Okinawa, Japan. Mem Fac Agric Kinki Univ 46:31–36Google Scholar
  25. Kouchi Y (2004) Fishes in ponds and dams. In Nishida M, Shikatani N and Shokita S (eds) The flora and fauna of inland waters in the Ryukyu Islands. Tokai University Press, Tokyo pp 482–487Google Scholar
  26. Kuroiwa H (1927) Summary of sampling freshwater fishes in the Ryukyu Islands. Zool Mag 39:355–368Google Scholar
  27. Löytynoja A, Milinkovitch MC (2003) A hidden Markov model for progressive multiple alignment. Bioinformatics 19:1505–1513Google Scholar
  28. Maehata M (2001) Taiwan-kingyo (Paradise fish). In: Kawanabe K, Mizuno N, Hosoya K (eds) Freshwater fishes of Japan (3rd edn). Yamatokeikoku-sha, Tokyo, pp 468–469Google Scholar
  29. Man SH, Hodgkiss IJ (1981). Hong Kong freshwater fishes. Urban Council, Wishing Printing Company, Hong KongGoogle Scholar
  30. Matsumoto S, Kon T, Yamaguchi M, Takeshima H, Yamazaki Y, Mukai T, Kuriiwa K, Kohda M, Nishida M (2010) Cryptic diversification of the swamp eel Monopterus albus in East and Southeast Asia, with special reference to the Ryukyuan populations. Ichthyol Res 57:71–77Google Scholar
  31. MOE (Ministry of the Environment, Japan) (2013). Red list, brackish-water / freshwater fishes. Ministry of the Environment, Japan, TokyoGoogle Scholar
  32. Mu X, Liu Y, Lai M, Song H, Wang X, Hu Y, Luo J (2015) Characterization of the Macropodus opercularis complete mitochondrial genome and family Channidae taxonomy using Illumina-based de novo transcriptome sequencing. Gene 559:189–195Google Scholar
  33. Ohshima M (1934) An osphronemid fish in Japan. Shokubutsu oyobi Dobutsu 3:671Google Scholar
  34. Oka M, Ohashi A (1997) Investigation of the fish-fighting research – Presentation of the example in Southeast Asia and East Asia. Tenri Bull South Asian Stud 24:139–161Google Scholar
  35. Okudo H (2000) Nature of Minamidaito Island. Nirai-sha, NahaGoogle Scholar
  36. Ota H (1998) Geographic pattern of endemism and speciation in amphibians and reptiles of the Ryukyu Archipelago, Japan, with special reference to their paleogeographical implications. Res Popul Ecol 40:189–204Google Scholar
  37. Sakai AK, Allendorf FW, Holt JS, Lodge DM, Molofsky J, With KA, Baughman S, Cabin RJ, Cohen JE, Ellstrand NC, McCauley DE, O’Neil P, Parker IM, Thompson JN, Weller SG (2001) The population biology of invasive species. Annu Rev Ecol Syst 32:305–332Google Scholar
  38. Sakaguchi S (1922) Tougyo Macropodus opercularis nit suite (About paradise fish Macropodus opercularis). Zool Mag 34:915–920Google Scholar
  39. Sakuma I, Miyamoto T (2005) The encyclopedia of aquatic alien species in Japan. Kashiwa-shobo, TokyoGoogle Scholar
  40. Sakurai K, Sunagawa K, Nakanishi M, Matsushima T, Miwa D (2012) Environmental concerns of Ryukyu Islands. Kobunken, TokyoGoogle Scholar
  41. Senou H (2015) Paradise fish. In: Ministry of the Environment Japan (ed) Red data book Japan 2014 – Threatened wildlife of Japan –, vol 4, Pisces–brackish and fresh water fishes. Gyosei Corporation, Tokyo, pp 146–147Google Scholar
  42. Swofford DL, Olsen GJ, Waddell PJ (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, SunderlandGoogle Scholar
  43. Tabata, R, Kakioka R, Tominaga K, Komiya T, K Watanabe (2016) Phylogeny and historical demography of endemic fishes in Lake Biwa: the ancient lake as a promoter of evolution and diversification of freshwater fishes in western Japan. Ecol Evol 6: 2601–2623Google Scholar
  44. Tachihara K (2005) Fishes in the Ryukyu Islands. In: Katano O, Mori S (eds) Kisho tansuigyo no genzai to mirai. Shinzan-sha, Tokyo, pp 295–310Google Scholar
  45. Takada M, Tachihara K, Kon T, Yamamoto G, Iguchi K, Miya M, Nishida M (2010a) Biogeography and evolution of the Carassius auratus-complex in East Asia. BMC Evol Biol 10:7Google Scholar
  46. Takada M, Tachihara K, Nishida M (2010b) Distribution and habitats of Carassius auratus in the Ryukyu Archipelago: comparisons between indigenous and introduced populations. Jpn J Ichthyol 57:113–123Google Scholar
  47. Toda M, Shokita S, Nishida M (2004) Historical formation of the biota of Ryukyu Islands. In: Nishida M, Shikatani N, Shokita S (eds) The flora and fauna of inland waters in the Ryukyu Islands (2nd edn). Tokai University Press, Tokyo, pp 25–32Google Scholar
  48. Tsukagoshi H, Yokoyama R, Goto A (2011) Mitochondrial DNA analysis reveals a unique population structure of the amphidromous sculpin Cottus pollux middle-egg type (Teleostei: Cottidae). Mol Phylogenet Evol 60:265–270Google Scholar
  49. Tzeng CS, Lin YS, Lin SM, Wang TY, Wang FY (2006) The phylogeography and population demographics of selected freshwater fishes in Taiwan. Zool Stud 45:285–297Google Scholar
  50. Wang T-Y, Tzeng C-S, Shen S-C (1999) Conservation and phylogeography of Taiwan paradise fish, Macropodus opercularis Linnaeus. Acta Zool Taiwan 10:121–134Google Scholar
  51. Wang PX, Luo JR, Bai JJ, Ye X, Hu YC, Wang XJ (2009) Cytochrome b complete sequences and RAPD analysis of phylogenetic relationships among the fishes of the genus Macropodus. Chin J Zool 44:14–23Google Scholar
  52. Wang M, Zhong L, Bian W, Qin Q, Chen X (2016) Complete mitochondrial genome of paradise fish Macropodus opercularis (Perciformes: Macropodusinae). Mitochondrial DNA A DNA Mapp Seq Anal 27:4146–4148Google Scholar
  53. Watanabe K, Kano Y, Takahashi H, Mukai T, Kakioka R, Tominaga K (2009) GEDIMAP: a database of genetic diversity for Japanese freshwater fishes. Ichthyol Res 57:107–109Google Scholar
  54. Watanobe T, Okumura N, Ishiguro N, Nakano M, Matsui A, Sahara M (1999) Genetic relationship and distribution of the Japanese wild boar (Sus scrofa leucomystax) and Ryukyu wild boar (Sus scrofa riukiuanus) analysed by mitochondrial DNA. Mol Ecol 8:1509–1512Google Scholar
  55. Yu P, Ding S, Yang Q, Bi Z, Chen L, Liu X, Song X, Wan Q (2016) Complete sequence and characterization of the paradise fish Macropodus erythropterus (Perciformes: Macropodusinae) mitochondrial genome. Mitochondrial DNA B Resour 1:54–55Google Scholar
  56. Zhang C, Zhao Y (2016) Species diversity and distribution of inland fishes in China. Science Press, BeijingGoogle Scholar

Copyright information

© The Ichthyological Society of Japan 2017

Authors and Affiliations

  • Yuichi Kano
    • 1
  • Ryoichi Tabata
    • 2
    • 6
  • Jun Nakajima
    • 3
  • Mikumi Takada-Endo
    • 4
  • Chunguang Zhang
    • 5
  • Yahui Zhao
    • 5
  • Tomomi Yamashita
    • 1
  • Katsutoshi Watanabe
    • 2
  1. 1.Institute of Decision Science for Sustainable SocietyKyushu UniversityFukuokaJapan
  2. 2.Department of Zoology, Division of Biological Science, Graduate School of ScienceKyoto UniversityKyotoJapan
  3. 3.Fukuoka Institute of Health and Environmental SciencesDazaifuJapan
  4. 4.Shizuoka Medical Research Center for DisasterJuntendo UniversityIzunokuniJapan
  5. 5.Key Laboratory of Zoological Systematics and Evolution, Institute of ZoologyChinese Academy of SciencesBeijingChina
  6. 6.Lake Biwa MuseumKusatsuJapan

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