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Biogeographic pattern of four endemic Pyropia from the east coast of Korea, including a new species, Pyropia retorta (Bangiaceae, Rhodophyta)

  • Kim, Sun-Mi (Division of Polar Life Sciences, Korea Polar Research Institute) ;
  • Choi, Han-Gu (Division of Polar Life Sciences, Korea Polar Research Institute) ;
  • Hwang, Mi-Sook (Aquatic Plant Variety Center, National Institute of Fisheries Science) ;
  • Kim, Hyung-Seop (Department of Biology, Gangneung-Wonju National University)
  • Received : 2017.12.19
  • Accepted : 2018.02.26
  • Published : 2018.03.15

Abstract

Foliose species of the Bangiaceae (Porphyra s. l.) are very important in Korean fisheries, and their taxonomy and ecophysiology have received much attention because of the potential for developing or improving aquaculture techniques. Although 20 species of foliose Bangiales have been listed from the Korean coast, some of them remain uncertain and need further comparative morphological studies with molecular comparison. In this study, we confirm the distribution of four Pyropia species from the east coast of Korea, Pyropia kinositae, P. moriensis, P. onoi, and P. retorta sp. nov., based on morphology and rbcL sequence data. Although P. onoi was listed in North Korea in old floral works, its occurrence on the east coast of South Korea is first revealed in this study based on molecular data. P. kinositae and P. moriensis, which were originally described from Hokkaido, Japan, are first reported on the east coast of Korea in this study. Pyropia retorta sp. nov. and P. yezonesis share a similar thallus color and narrow spermatangial patches in the upper portion of the frond, and they have a sympatric distribution. However, P. retorta can be distinguished by the curled or twisted thalli and by molecular data. The biogeographic pattern of the two native species, P. kinositae and P. retorta, suggests that the east coast of Korea may have been a place of refugia during the Last Glacial Maximum (LGM), and then recolonized to the northern part of Japan through the restored East Korean Warm Current after the LGM.

Keywords

References

  1. Agardh, C. A. 1824. Systema Algarum. Literis Berlingiana, Lund, 312 pp.
  2. Anisimova, M. & Gascuel, O. 2006. Approximate likelihoodratio test for branches: a fast, accurate, and powerful alternative. Syst. Boil. 55:539-552. https://doi.org/10.1080/10635150600755453
  3. Barbara, I., Choi, H. -G., Secilla, A., Diaz-Tapia, P., Gorostiaga, J. M., Seo, T. -K., Jung, M. -Y. & Berecibar, E. 2013. Lampisiphonia iberica gen. et sp. nov. (Ceramiales, Rhodophyta) based on morphology and molecular evidence. Phycologia 52:137-155. https://doi.org/10.2216/12-009.1
  4. Broom, J. E. S., Nelson, W. A., Farr, T. J., Phillips, L. E. & Clayton, M. 2010. Relationships of the Porphyra (Bangiales, Rhodophyta) flora of the Falkland Islands: a molecular survey using rbcL and nSSU sequence data. Aust. Syst. Bot. 23:27-37. https://doi.org/10.1071/SB09033
  5. Butterfield, N. I. 2000. Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/Neoproterozoic radiation of eukaryotes. Paleobiology 26:386-404. https://doi.org/10.1666/0094-8373(2000)026<0386:BPNGNS>2.0.CO;2
  6. Coyer, J. A., Hoarau, G., Van Schaik, J., Luijckx, P. & Olsen, J. L. 2011. Trans‐Pacific and trans‐Arctic pathways of the intertidal macroalga Fucus distichus L. reveal multiple glacial refugia and colonizations from the North Pacific to the North Atlantic. J. Biogeogr. 38:756-771. https://doi.org/10.1111/j.1365-2699.2010.02437.x
  7. Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9:772.
  8. Dumilag, R. V. & Aguinaldo, Z. -Z. A. 2017. Genetic differentiation and distribution of Pyropia acanthophora (Bangiales, Rhodophyta) in the Philippines. Eur. J. Phycol. 52: 104-115. https://doi.org/10.1080/09670262.2016.1230786
  9. Dumilag, R. V. & Monotilla, W. D. 2017. Molecular diversity and biogeography of Philippine foliose Bangiales(Rhodophyta). J. Appl. Phycol. Online version (doi. org/10.1007/s10811-017-1201-8).
  10. Engler, A. 1892. Syllabus der Vorlesungen Über Specielle und Medicinisch-Pharmaceutische Botanik. Eine Uebersicht Uber das Ganze Pflanzensystem mit Berucksichtigung der Medicinal- und Nutzpflanzen. Grosse Ausgabe, Berlin, 184 pp.
  11. Freshwater, D. W. & Rueness, J. 1994. Phylogenetic relationships of some European Gelidium (Gelidiales, Rhodophyta) species based upon rbcL nucleotide sequences analysis. Phycologia 33:187-194. https://doi.org/10.2216/i0031-8884-33-3-187.1
  12. Fukuhara, E. 1968. Studies on the taxonomy and ecology of Porphyra of Hokkaido and its adjacent waters. Bull. Hokkaido Reg. Fish. Res. Lab. 34:40-99.
  13. Gerard, K., Bierne, N., Borsa, P., Chenuil, A. & Feral, J. -P. 2008. Pleistocene separation of mitochondrial lineages of Mytilus spp. mussels from Northern and Southern Hemispheres and strong genetic differentiation among southern populations. Mol. Phylogenet. Evol. 49:84-91. https://doi.org/10.1016/j.ympev.2008.07.006
  14. Guillemin, M. -L., Contreras-Porcia, L., Ramírez, M. E., Macaya, E. C., Contador, C. B., Woods, H., Wyatt, C. & Brodie, J. 2016. The bladed Bangiales (Rhodophyta) of the South Eastern Pacific: molecular species delimitation reveals extensive diversity. Mol. Phylogenet. Evol. 94:814-826. https://doi.org/10.1016/j.ympev.2015.09.027
  15. Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W. & Gascuel, O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Boil. 59:307-321. https://doi.org/10.1093/sysbio/syq010
  16. Guiry, M. D. & Guiry, G. M. 2017. AlgaeBase. World-wide electronic publication, National University of Ireland,Galway. Available from: http://www.algaebase.org. Accessed Feb 15, 2017.
  17. Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95-98.
  18. Harden, L. K., Morales, K. M. & Hughey, J. R. 2015. Identification of a new marine algal species Pyropia nitida sp. nov. (Bangiales: Rhodophyta) from Monterey, California. Mitochondrial DNA A DNA Mapp. Seq. Anal. 27:3058-3062.
  19. Hommersand, M. H. & Fredericq, S. 2003. Biogeography of the marine red algae of the South Africa west coast: a molecular approach. In Chapman, A. R. O., Anderson, R. J., Vreeland, V. J. & Davison, I. R. (Eds.) Proc. 17th Int. Seaweed Symp., Oxford University Press, Oxford, pp. 325-336.
  20. Huelsenbeck, J. P. & Ronquist, F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754-755. https://doi.org/10.1093/bioinformatics/17.8.754
  21. Hwang, M. S. & Lee, I. K. 2001. Taxonomy of the genus Porphyra (Bangiales, Rhodophyta) from Korea. Algae16:233-273.
  22. Kim, H. -S., Boo, S. M., Lee, I. K. & Sohn, C. H. 2013. National list of species of Korea Marine algae. National Institute of Biological Resources, Incheon, 336 pp.
  23. Kim, H. -S. & Kim, S. -M. 2011. Algal flora of Korea. Vol. 4, Npo. 1. Rhodophyta: Stylonematophyceae, Compsopogonophyceae, Bangiophyceae. Primitive red algae. National Institute of Biological Resources, Incheon, 138 pp.
  24. Kim, S. -M. 2005. Morphology and molecular phylogeny of Porphyra yezoensis Ueda and its related species in Korea. M.S. thesis, Gangneung National University, Wonju, 61 pp.
  25. Kim, Y., Choi, S. -J. & Choi, C. 2017. An efficient PCR-RFLP method from the rapid identification of Korean Pyropia species. Molecules 22:E2182. https://doi.org/10.3390/molecules22122182
  26. Korean Hydrographic and Oceanographic Agency. Quasireal-time ocean current using satellite altimetry data. Available from: http://www.khoa.go.kr/koofs/kor/seawf/sea_wflow.do?menuNo. Accessed Feb 15, 2017.
  27. Kucera, H. & Saunders, G. W. 2012. A survey of Bangiales (Rhodophyta) based on multiple molecular markers reveals cryptic diversity. J. Phycol. 48:869-882. https://doi.org/10.1111/j.1529-8817.2012.01193.x
  28. Kunimoto, M., Kito, H., Yamamoto, Y., Cheney, D. P., Kaminishi, Y. & Mizukami, Y. 1999. Discrimination of Porphyra species based on small subunit ribosomal RNA gene sequence. J. Appl. Phycol. 11:203-209. https://doi.org/10.1023/A:1008019409008
  29. Lindstrom, S. C. 2001. The Bering Strait connection: dispersal and speciation in boreal macroalgae. J. Biogeogr. 28:243-251. https://doi.org/10.1046/j.1365-2699.2001.00529.x
  30. Lindstrom, S. C. 2008. Cryptic diversity, biogeography and genetic variation in Northeast Pacific species of Porphyra sensu lato (Bangiales, Rhodophyta). J. Appl. Phycol. 20:951-962. https://doi.org/10.1007/s10811-008-9313-9
  31. Lindstrom, S. C. & Fredericq, S. 2003. rbcL gene sequences reveal relationships among north-east Pacific species of Porphyra (Bangiales, Rhodophyta) and a new species, P. aestivalis. Phycol. Res. 51:211-224. https://doi.org/10.1111/j.1440-1835.2003.tb00189.x
  32. Lindstrom, S. C., Hughey, J. R. & Aguilar Rosas, L. E. 2015a. Four new species of Pyropia (Bangiales, Rhodophyta) from the west coast of North America: the Pyropia lanceolata species complex updated. PhytoKeys 52:1-22. https://doi.org/10.3897/phytokeys.52.5009
  33. Lindstrom, S. C., Lindeberg, M. R. & Guthrie, D. A. 2015b. Marine macroalgae of the Aleutian Islands: I. Bangiales. Algae 30:247-263. https://doi.org/10.4490/algae.2015.30.4.247
  34. Lopez-Vivas, J. M., Muniz-Salazar, R., Riosmena-Rodriguez, R., Pacheco-Ruiz, I. & Yarish, C. 2015. Endemic Pyropia species (Bangiales, Rhodophyta) from the Gulf of California, Mexico. J. Appl. Phycol. 27:1029-1041. https://doi.org/10.1007/s10811-014-0366-7
  35. Lyngbye, H. C. 1819. Tentamen Hydrophytologiae Danicae Continens Omnia Hydrophyta Cryptogama Daniae, Holsatiae, Faeroae, Islandiae, Groenlandiae Hucusque Cognita, Systematice Disposita, Descripta et Iconibus Illustrata, Adjectis Simul Speciebus Norvegicis. Typis Schultzianis, in commissis Librariae Gyldendaliae, Copenhagen, 248 pp.
  36. Mabuchi, K., Nakabo, T. & Nishida, M. 2004. Molecular phylogeny of the antitropical genus Pseudolabrus (Perciformes: Labridae): evidence for a Southern Hemisphere origin. Mol. Phylogent. Evol. 32:375-382. https://doi.org/10.1016/j.ympev.2004.01.008
  37. Mateo-Cid, L. E., Mendoza-Gonzalez, A. C., Diaz-Larrea, J., Senties, A., Pedroche, F. F. & Sanchez Heredia, J. D. 2012. A new species of Pyropia (Rhodophyta, Bangiaceae), from the Pacific coast of Mexico, based on morphological and molecular evidence. Phytotaxa 54:1-12. https://doi.org/10.11646/phytotaxa.54.1.1
  38. Milstein, D., Medeiros, A. S., Oliveira, E. C. & Oliveira, M. C. 2012. Will a DNA barcoding approach be useful to identify Porphyra species (Bangiales, Rhodophyta)? A case study with Brazilian taxa. J. Appl. Phycol. 24:837-845. https://doi.org/10.1007/s10811-011-9702-3
  39. Milstein, D., Medeiros, A. S., Oliveira, E. C. & Oliveira, M. C. 2015. Native or introduced? A re-evaluation of Pyropia species (Bangiales, Rhodophyta) from Brazil based on molecular analyses. Eur. J. Phycol. 50:37-45. https://doi.org/10.1080/09670262.2014.982202
  40. Mindell, D. P. & Thacker, C. E. 1996. Rates of molecular evolution: phylogenetic issues and applications Annu. Rev. Ecol. Syst. 27:279-303. https://doi.org/10.1146/annurev.ecolsys.27.1.279
  41. Mishler, B. D., Knerr, N., González-Orozco, C. E., Thornhill, A. H., Laffan, S. W. & Miller, J. T. 2014. Phylogenetic measures of biodiversity and neo- and paleo-endemism in Australian Acacia. Nat. Commun. 5:4473. https://doi.org/10.1038/ncomms5473
  42. Mols-Mortensen, A., Neefus, C. D., Nielsen, R., Gunnarsson, K., Egilsdóttir, S., Pedersen, P. M. & Brodie, J. 2012. New insights into the biodiversity and generic relationships of foliose Bangiales (Rhodophyta) in Iceland and the Faroe Islands. Eur. J. Phycol. 47:146-159. https://doi.org/10.1080/09670262.2012.666678
  43. Mols-Mortensen, A., Neefus, C. D., Pedersen, P. M. & Brodie, J. 2014. Diversity and distribution of foliose Bangiales (Rhodophyta) in West Greenland: a link between the North Atlantic and North Pacific. Eur. J. Phycol. 49:1-10. https://doi.org/10.1080/09670262.2013.871062
  44. Nakamura, K., Denda, T., Kokubugata, G., Forster, P. I., Wilson, G., Peng, C. -I. & Yokota, M. 2012. Molecular phylogeography reveals an antitropical distribution and local diversification of Solenogyne (Asteraceae) in the Ryukyu Archipelago of Japan and Australia. Biol. J. Lin. Soc. 105:197-217. https://doi.org/10.1111/j.1095-8312.2011.01769.x
  45. Naughton, K. M., O'Hara, T. D., Appleton, B. & Cisternas, P. A. 2014. Antitropical distributions and species delimitation in a group of ophiocomid brittle stars (Echinodermata, Ophiuroidea: Ophiocomidae). Mol. Phylogenet. Evol. 78:232-244. https://doi.org/10.1016/j.ympev.2014.05.020
  46. Nekola, J. C. 1999. Paleorefugia and neorefugia: the influence of colonization history on community pattern and process. Ecology 80:2459-2473. https://doi.org/10.1890/0012-9658(1999)080[2459:PANTIO]2.0.CO;2
  47. Nelson, W. A. 2013. Pyropia plicata sp. nov. (Bangiales, Rhodophyta): naming a common intertidal alga from New Zealand. PhytoKeys 21:17-28. https://doi.org/10.3897/phytokeys.21.4614
  48. Nelson, W. A. & D'Archino, R. 2014. Three new macroalgae from the Three Kings Islands New Zealand including the first southern Pacific Ocean record of the Furcellariaceae (Rhodophyta). Phycologia 53:602-613. https://doi.org/10.2216/14-60R1.1
  49. Nikula, R., Strelkov, P. & Vainola, R. 2007. Diversity and transarctic invasion history of mitochondrial lineages in the North Atlantic Macoma balthica complex (Bivalvia: Tellinidae). Evolution 61:928-941. https://doi.org/10.1111/j.1558-5646.2007.00066.x
  50. Niwa, K., Iida, S., Kato, A., Kawai, H., Kikuchi, N., Kobiyama, A. & Aruga, Y. 2009. Genetic diversity and introgression in two cultivated species (Porphyra yezoensis and Porphyra tenera) and closely related wild species or Porphyra (Bangiales, Rhodophyta). J. Phycol. 45:493-502. https://doi.org/10.1111/j.1529-8817.2009.00661.x
  51. Niwa, K., Kikuchi, N., Hwang, M. S., Choi, H. -G. & Aruga, Y. 2014. Cryptic species in the Pyropia yezoensis complex (Bangiales, Rhodophyta): sympatric occurrence of two cryptic species even on same rocks. Phycol. Res. 62:36-43. https://doi.org/10.1111/pre.12035
  52. Niwa, K. & Kobiyama, A. 2014. Speciation in the marine crop Pyropia yezoensis (Bangiales, Rhodophyta). J. Phycol. 50:897-900. https://doi.org/10.1111/jpy.12220
  53. Niwa, K. & Sakamoto, T. 2010. Allopolyploidy in natural and cultivated populations of Porphyra (Bangiales, Rhodophta). J. Phycol. 46:1097-1105. https://doi.org/10.1111/j.1529-8817.2010.00897.x
  54. Notoya, M. & Miyashita, A. 1999. Life history, in culture, of the obligate epiphyte Porphyra moriensis (Bangiales,Rhodophyta). Hydrobiologia 398/399:121-125. https://doi.org/10.1023/A:1017023210883
  55. Ohmi, H. 1954. New species of Porphyra, epiphytic on Chorda filum from Hokkaido. Bull. Fac. Fish. Hokkaido Univ. 5:231-239.
  56. Ramirez, M. -E., Contreras-Porcia, L., Guillemin, M. -L., Brodie, J., Valdivia, C., Flores-Molina, M. R., Nunez, A., Bulboa Contador, C. & Lovazzano, C. 2014. Pyropia orbicularis sp. nov. (Rhodophyta, Bangiaceae) based on a population previously known as Porphyra columbina from the central coast of Chile. Phytotaxa 158:133-153. https://doi.org/10.11646/phytotaxa.158.2.2
  57. Sanchez, N., Verges, A., Peteiro, C., Sutherland, J. E. & Brodie, J. 2014. Diversity of bladed Bangiales (Rhodophyta) in western Mediterranean: recognition of the genus Themis and description of T. ballesterosii sp. nov., T. iberica sp. nov., and Pyropia parva sp. nov. J. Phycol. 50:908-929. https://doi.org/10.1111/jpy.12223
  58. Sanchez, N., Verges, A., Peteiro, C., Sutherland, J. E. & Brodie, J. 2015. Diversity of bladed Bangiales (Rhodophyta) in western Mediterranean: recognition of the genus Themis and description of T. ballesterosii sp. nov., T. iberica sp. nov., and Pyropia parva sp. nov. (Corrigendum). J. Phycol. 51:401. https://doi.org/10.1111/jpy.12289
  59. Saunders, G. W. & Kraft, G. T. 1994. Small-subunit rRNA gene sequences from representatives of selected families of the Gigartinales and Rhodymeniales (Rhodophyta). 1. Evidence for the Plocamiales ord.nov. Can. J. Bot. 72:1250-1263. https://doi.org/10.1139/b94-153
  60. Smith, D. R., Hua, J., Lee, R. W. & Keeling, P. J. 2012. Relative rates of evolution among the three genetic compartments of the red alga Porphyra differ from those of green plants and do not correlate with genome architecture. Mol. Phylogenet. Evol. 65:339-344. https://doi.org/10.1016/j.ympev.2012.06.017
  61. Stiller, J. W. & Waaland, J. R. 1993. Molecular analysis reveals cryptic diversity in Porphyra (Rhodophyta). J. Phycol. 29:506-517. https://doi.org/10.1111/j.1529-8817.1993.tb00152.x
  62. Sutherland, J. E., Lindstrom, S. C., Nelson, W. A., Brodie, J., Lynch, M. D. J., Hwang, M. S., Choi, H. -G., Miyata, M., Kikuchi, N., Oliveira, M. C., Farr, T., Neefus, C., Mols-Mortensen, A., Milstein, D. & Muller, K. M. 2011. A new look at an ancient order: generic revision of the Bangiales (Rhodophyta). J. Phycol. 47:1131-1151. https://doi.org/10.1111/j.1529-8817.2011.01052.x
  63. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Boil. Evol. 28:2731-2739. https://doi.org/10.1093/molbev/msr121
  64. Tanaka, T. 1952. The systematic study of the Japanese Protoflorideae. Mem. Fac. Fish. Kagoshima Univ. 2:1-92.
  65. Teasdale, B. W., West, A., Klein, A. S. & Mathieson, A. C. 2009. Distribution and evolution of variable group-I introns in the small ribosomal subunit of North Atlantic Porphyra (Bangiales, Rhodophyta). Eur. J. Phycol. 44:171-182. https://doi.org/10.1080/09670260802590877
  66. Ueda, S. 1932. Systematic study of the genus Porphyra in Japan. Suiko-Kenkyu-Kokoku 28:1-45.
  67. Verbruggen, H. 2014. Morphological complexity, plasticity, and species diagnosability in the application of old species names in DNA-based taxonomics. J. Phycol. 50:26-31. https://doi.org/10.1111/jpy.12155
  68. Williams, S. T., Reid, D. G. & Littlewood, D. T. J. 2003. A molecular phylogeny of the Littorininae (Gastropoda: Littorinidae): unequal evolutionary rates, morphological parallelism, and biogeography of the Southern Ocean.Mol. Phylogenet. Evol. 28:60-86. https://doi.org/10.1016/S1055-7903(03)00038-1
  69. Xie, Z. -Y., Lin, S. -M., Liu, L. -C., Ang, P. O. Jr. & Shyu, J. -F. 2015. Genetic diversity and taxonomy of foliose Bangiales (Rhodophyta) from Taiwan based on rbcL and cox1 sequences. Bot. Mar. 58:189-202.

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