DOI QR코드

DOI QR Code

Phylogeography of the economic seaweeds Chondrus (Gigartinales, Rhodophyta) in the northwest Pacific based on rbcL and COI-5P genes

  • Yang, Mi Yeon (Department of Biology and Research Institute for Basic Sciences, Jeju National University) ;
  • Kim, Myung Sook (Department of Biology and Research Institute for Basic Sciences, Jeju National University)
  • 투고 : 2021.09.12
  • 심사 : 2022.05.29
  • 발행 : 2022.06.15

초록

The red algal genus Chondrus have long been used as raw materials for carrageenan and dietary fiber in health foods. Despite the importance of genetic information in safeguarding natural seaweed resources, knowledge of the population genetics of Chondrus in the northwest Pacific is limited. In this study, genetic diversity and phylogeographic structure of 45 populations (777 specimens) of Chondrus from Korea, China, and Japan were evaluated based on mitochondrial COI-5P gene sequences, and phylogenetic relationships were confirmed based on plastid rbcL gene sequences. Molecular analyses assigned the specimens in this study to three Chondrus species: C. nipponicus, C. ocellatus, and C. giganteus; phenotype-based species classification was impossible owing to their high morphological plasticity. We found moderate intraspecific genetic diversity and a shallow phylogeographic structure in both for C. nipponicus and C. ocellatus, and low intraspecific genetic diversity in C. giganteus. Each of the three species exhibited high-level intraspecific gene flow among regions based on the most common haplotypes (CN1 for C. nipponicus, CO1 for C. ocellatus, and CG1 for C. giganteus). Our comprehensive genetic information provides insights into the phylogeographic patterns and intraspecific diversity of the economically important Chondrus species. It also highlights the need to conserve existing natural Chondrus resources through continuous monitoring of genetic diversity and phylogeographic pattern.

키워드

과제정보

We thank Dr. Daisuke Fujita for collecting samples from Japan and all members of the molecular phylogeny team of the Marine Algae Laboratory at Jeju National University. This research was supported by the 2021 Scientific Promotion Program funded by Jeju National University.

참고문헌

  1. Arbelaez-Cortes, E., Mila, B. & Navarro-Siguenza, A. G. 2014. Multilocus analysis of intraspecific differentiation in three endemic bird species from the northern Neotropical dry forest. Mol. Phylogenet. Evol. 70:362-377. https://doi.org/10.1016/j.ympev.2013.10.006
  2. Aris-Brosou, S. & Excoffier, L. 1996. The impact of population expansion and mutation rate heterogeneity on DNA sequence polymorphism. Mol. Biol. Evol. 13:494-504. https://doi.org/10.1093/oxfordjournals.molbev.a025610
  3. Avise, J. C., Arnold, J., Ball, R. M., Bermingham, E., Lamb, T., Neigel, J. E., Reeb, C. A. & Saunders, N. C. 1987. Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu. Rev. Ecol. Syst. 18:489-522. https://doi.org/10.1146/annurev.es.18.110187.002421
  4. Brodie, J., Guiry, M. D. & Masuda, M. 1991. Life history and morphology of Chondrus nipponicus (Gigartinales, Rhodophyta) from Japan. Br. Phycol. J. 26:33-50. https://doi.org/10.1080/00071619100650041
  5. Brodie, J., Guiry, M. D. & Masuda, M. 1993. Life history, morphology and crossability of Chondrus ocellatus forma ocellatus and C. ocellatus forma crispoides (Gigartinales, Rhodophyta) from the north-western Pacific. Eur. J. Phycol. 28:183-196. https://doi.org/10.1080/09670269300650281
  6. Brodie, J., Masuda, M. & Guiry, M. D. 1994. Life history and photoperiodic responses in Chondrus giganteus forma flabellatus (Gigartinaceae, Rhodophyta) from Japan. Eur. J. Phycol. 29:159-164. https://doi.org/10.1080/09670269400650601
  7. Brodie, J., Masuda, M., Mine, I. & Guiry, M. D. 1997. Two morphologically similar biological species: Chondrus pinnulatus and C. armatus (Gigartinaceae, Rhodophyta). J. Phycol. 33:682-698. https://doi.org/10.1111/j.0022-3646.1997.00682.x
  8. Cakil, Z. V., Garlasche, G., Iakovenko, N., Cesare, A. D., Eckert, E. M., Guidetti, R., Hamdan, L., Janko, K., Lukashanets, D., Rebecchi, L., Schiaparelli, S., Sforzi, T., Kasparova, E. S., Velasco-Castrillon, A., Walsh, E. J. & Fontaneto, D. 2021. Comparative phylogeography reveals consistently shallow genetic diversity in a mitochondrial marker in Antarctic bdelloid rotifers. J. Biogeogr. 48:1797-1809. https://doi.org/10.1111/jbi.14116
  9. Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797. https://doi.org/10.1093/nar/gkh340
  10. Excoffier, L. & Lischer, H. E. L. 2010. Arlequin suite ver. 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10:564-567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
  11. Fu, Y. X. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915-925. https://doi.org/10.1093/genetics/147.2.915
  12. Furfaro, G., Salvi, D., Triainito, E., Vitale, F. & Mariottini, P. 2021. When morphology does not match phylogeny: the puzzling case of two sibling nudibranchs (Gastropoda). Zool. Scr. 50:439-454. https://doi.org/10.1111/zsc.12484
  13. Gasiorek, P., Voncina, K., Zajac, K. & Michalczyk, L. 2021. Phylogeography and morphological evolution of Pseudechiniscus (Heterotardigrada: Echiniscidae). Sci. Rep. 11:7606. https://doi.org/10.1038/s41598-021-84910-6
  14. Guiry, M. D. & Guiry, G. M. 2021. Algaebase. Word-wide electronic publication, National University of Ireland, Galway. Available from: https://www.algaebase.org. Accessed May 13, 2021.
  15. Hommersand, M. H., Fredericq, S. & Freshwater, D. W. 1994. Phylogenetic systematics and biogeography of the Gigartinaceae (Gigartinales, Rhodophyta) based on sequence analysis of rbcL. Bot. Mar. 37:193-203.
  16. Hommersand, M. H., Fredericq, S., Freshwater, D. W. & Hughey, J. 1999. Recent developments in the systematics of the Gigartinaceae (Gigartinales, Rhodophyta) based on rbcL sequence analysis and morphological evidence. Phycol. Res. 47:139-151. https://doi.org/10.1111/j.1440-1835.1999.tb00294.x
  17. Hu, Z., Guiry, M. D., Critchley, A. T. & Duan, D. 2010. Phylogeographyic patterns indicate transatlantic migration from Europe to north America in the red seaweed Chondrus crispus (Gigartinales, Rhodophyta). J. Phycol. 46:889-900. https://doi.org/10.1111/j.1529-8817.2010.00877.x
  18. Hu, Z. -M., Li, J. -J., Sun, Z. -M., Gao, X., Yao, J. -T., Choi, H. -G., Endo, H. & Duan, D. -L. 2016. Hidden diversity and phylogeographic history provide conservation insights for the edible seaweed Sargassum fusiforme in the Northwest Pacific. Evol. Appl. 10:366-378.
  19. Hu, Z. -M., Li, J. -J., Sun, Z. -M., Oak, J. -H., Zhang, J., Fresia, P., Grant, W. S. & Duan, D. -L. 2015. Phylogeographic structure and deep lineage diversification of the red algal Chondrus ocellatus Holmes in the Northwest Pacific. Mol. Ecol. 24:5020-5033. https://doi.org/10.1111/mec.13367
  20. Hu, Z. M., Li, W., Li, J. J. & Duan, D. L. 2011. Post-Pleistocene demographic history of the North Atlantic endemic Irish moss Chondrus crispus: glacial survival, spatial expansion and gene flow. J. Evol. Biol. 24:505-517. https://doi.org/10.1111/j.1420-9101.2010.02186.x
  21. Hu, Z., Zeng, X., Critchley, A. T., Morrell, S. L. & Duan, D. 2007. Phylogeography of the Northern Atlantic species Chondrus crispus (Gigartinales, Rhodophyta) inferred from nuclear rDNA internal transcribed spacer sequences. 575:315-327.
  22. Kamiya, M., Inoue, N., Suzuki, C. & Abe, S. 2021. Ecological, physiological, and biomechanical differences between gametophytes and sporophytes of Chondrus ocellatus (Gigartinales, Rhodophyta). J. Phycol. 57:1590-1603. https://doi.org/10.1111/jpy.13193
  23. Kang, J. C., Yang, M. Y., Lin, S. -M. & Kim, M. S. 2015. Reappraisal of nine species of Martensia (Delesseriaceae, Rhodophyta) reported from Korea based on morphology and molecular analyses. Bot. Mar. 58:151-166. https://doi.org/10.1515/bot-2014-0075
  24. Kang, P. J., An, J. W. & Nam, K. W. 2020. New record of Chondrus retortus (Gigartinales, Rhodophyta) in Korea. Korean J. Environ. Biol. 38:481-485. https://doi.org/10.11626/KJEB.2020.38.3.481
  25. Kim, D. H. 1976. A study of the development of cystocarps and tetrasporangial sori in Gigartinaceae (Rhodophyta, Gigartinales). Nova Hedwigia 27:1-146.
  26. Kim, K. M., Hoarau, G. G. & Boo, S. M. 2012. Genetic structure and distribution of Gelidium elegans (Gelidiales, Rhodophyta) in Korea based on mitochondrial cox1 sequence data. Aquat. Bot. 98:27-33. https://doi.org/10.1016/j.aquabot.2011.12.005
  27. Kim, M. S., Kim, S. Y. & Nelson, W. 2010. Symphyocladia lithophila sp. nov. (Rhodomelaceae, Ceramiales), a new Korean red algal species based on morphology and rbcL sequences. Bot. Mar. 53:233-241. https://doi.org/10.1515/BOT.2010.031
  28. Kim, S. Y., Manghisi, A., Morabito, M., Yang, E. C., Yoon, H. S., Miller, K. A. & Boo, S. M. 2014. Genetic diversity and haplotype distribution of Pachymeniopsis gargiuli sp. nov. and P. lanceolata (Halymeniales, Rhodophyta) in Korea, with notes on their non-native distributions. J. Phycol. 50:885-896. https://doi.org/10.1111/jpy.12218
  29. Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35:1547-1549. https://doi.org/10.1093/molbev/msy096
  30. Lamont, T. & McSweeney, M. 2021. Consumer acceptability and chemical composition of whole-wheat breads incorporated with brown seaweed (Ascophyllum nodosum) or red seaweed (Chondrus crispus). J. Sci. Food Agric. 101:1507-1514. https://doi.org/10.1002/jsfa.10765
  31. Liang, Y., Zhang, J., Song, X., Choi, H. -G., Gao, X., Duan, D. & Hu, Z. -M. 2021. Low genetic diversity in the endangered marine alga Silvetia siliquosa (Ochrophyta: Fucaceae) and the implication to conservation. J. Oceanol. Limnol. 40:216-225.
  32. Matsumoto, K. & Shimada, S. 2013. Taxonomic reassessment of Chondrus verrucosus (Rhodophyta, Gigartinales), with a description of Chondrus retortus sp. nov. Phycol. Res. 61:299-309. https://doi.org/10.1111/pre.12028
  33. Mikami, H. 1965. A systematic study of the Phyllophoraceae and Gigartinaceae from Japan and its vicinity. Sci. Pap. Inst. Algol. Res. Fac. Sci. Hokkaido Univ. 5:181-285.
  34. Nam, K. W. & Kang, P. J. 2015. Algal flora of Korea. Vol. 4, No. 11. National Institute of Biological Resources, Incheon, 146 pp.
  35. Nauer, F., Gurgel, C. F. D., Ayres-Ostrock, L. M., Plastino, E. M. & Oliveira, M. C. 2019. Phylogeography of the Hypnea musciformis species complex (Gigartinales, Rhodophyta) with the recognition of cryptic species in the western Atlantic Ocean. J. Phycol. 55:676-687. https://doi.org/10.1111/jpy.12848
  36. Neiva, J., Assis, J., Coelho, N. C., Fernandes, F., Pearson, G. A. & Serrao, E. A. 2015. Genes left behind: climate change threatens cryptic genetic diversity in the canopy-forming seaweed Bifurcaria bifurcata. PLoS ONE 10:e0131530. https://doi.org/10.1371/journal.pone.0131530
  37. Okamura, K. 1932. Icones of Japanese algae, Vol. 6. The Author, Tokyo, 96 pp.
  38. Okamura, K. 1936. Nippon kaiso shi [Descriptions of Japanese algae]. Uchida Rokakuho, Tokyo, 964 pp.
  39. Pauls, S. U., Nowak, C., Balint, M. & Pfenninger, M. 2013. The impact of global climate change on genetic diversity within populations and species. Mol. Ecol. 22:925-946. https://doi.org/10.1111/mec.12152
  40. Payo, D. A., Leliaert, F., Verbruggen, H., D'Hondt, S., Calumpong, H. P. & De Clerck, O. 2013. Extensive cryptic species diversity and fine-scale endemisms in the marine red alga Portieria in the Philippines. Proc. R. Soc. B 280:20122660. https://doi.org/10.1098/rspb.2012.2660
  41. Pinsky, M. L., Selden, R. L. & Kitchel, Z. J. 2020. Climate-driven shifts in marine species ranges: scaling from organisms to communities. Annu. Rev. Mar. Sci. 12:153-179. https://doi.org/10.1146/annurev-marine-010419-010916
  42. Preuss, M., Nelson, W. A. & D'Archino, R. 2022. Cryptic diversity and phylogeographic patterns in the Asparagopsis armata species complex (Bonnemaisoniales, Rhodophyta) from New Zealand. Phycologia 61:89-96. https://doi.org/10.1080/00318884.2021.2015223
  43. Provan, J., Glendinning, K., Kelly, R. & Maggs, C. A. 2013. Levels and patterns of population genetic diversity in the red seaweed Chondrus crispus (Florideophyceae): a direct comparison of single nucleotide polymorphisms and microsatellites. Biol. J. Linn. Soc. 108:251-262. https://doi.org/10.1111/j.1095-8312.2012.02010.x
  44. Stamatakis, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312-1313. https://doi.org/10.1093/bioinformatics/btu033
  45. Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595. https://doi.org/10.1093/genetics/123.3.585
  46. Taylor, A. R. A. & Chen, L. C. M. 1994. Chondrus Stackhouse. In Akatsuka, I. (Ed.) Biology of Economic Algae. SPB Academic Publishing, Hague, pp. 35-76.
  47. Wernberg, T., Coleman, M. A., Bennett, S., Thomsen, M. S., Tuya, F. & Kelaher, B. P. 2018. Genetic diversity and kelp forest vulnerability to climatic stress. Sci. Rep. 8:1851. https://doi.org/10.1038/s41598-018-20009-9
  48. Yang, M. Y., Fujita, D. & Kim, M. S. 2021a. Phylogeography of Gloiopeltis furcata sensu lato (Gigartinales, Rhodophyta) provides the evidence of glacial refugia in Korea and Japan. Algae 36:13-24. https://doi.org/10.4490/algae.2021.36.3.3
  49. Yang, M. Y. & Kim, M. S. 2018. Cryptic species diversity of ochtodenes-producing Portieria species (Gigartinales, Rhodophyta) from the northwest Pacific. Algae 33:205-214. https://doi.org/10.4490/algae.2018.33.7.30
  50. Yang, M. Y., Kim, S. Y. & Kim, M. S. 2021b. Population genetic structure and phylogeography of co-distributed Pachymeniopsis species (Rhodophyta) along the coast of Korea and Japan. Diversity 13:336. https://doi.org/10.3390/d13080336
  51. Yang, M. Y., Kim, S. Y. & Kim, M. S. 2021c. Verification of hotspots of genetic diversity in Korean population of Grateloupia asiatica and G. jejuensis (Rhodophyta) show low genetic diversity and similar geographic distribution. Genes Genomics 43:1463-1469. https://doi.org/10.1007/s13258-021-01168-y
  52. Yang, M. Y., Yang, E. C. & Kim, M. S. 2020. Genetic diversity hotspot of the amphi-Pacific macroalga Gloiopeltis furcata sensu lato (Gigartinales, Florideophyceae). J. Appl. Phycol. 32:2515-2522. https://doi.org/10.1007/s10811-019-02017-y
  53. Yoshida, Y. & Yoshinaga, K. 2010. Checklist of marine algae of Japan. Jpn. J. Phycol. 58:69-122.
  54. Zhang, J., Yao, J. -T., Sun, Z. -M., Fu, G., Galanin, D. A., Nagasato, C., Motomura, T., Hu, Z. -M. & Duan, D. -L. 2015. Phylogeographic data revealed shallow genetic structure in the kelp Saccharina japonica (Laminariales, Phaeophyta). BMC Evol. Biol. 15:237. https://doi.org/10.1186/s12862-015-0517-8