DOI QR코드

DOI QR Code

Cryptic diversity and phylogeographic patterns of Plocamium telfairiae and P. cartilagineum (Plocamiales, Rhodophyta) in the Northwest Pacific

  • Mi Yeon Yang (Research Institute for Basic Sciences, Jeju National University) ;
  • Myung Sook Kim (Research Institute for Basic Sciences, Jeju National University)
  • Received : 2023.04.17
  • Accepted : 2023.08.04
  • Published : 2023.09.15

Abstract

Cryptic diversity refers to two or more distinct species classified as a single species due to lack of morphological difference. Although Plocamium Lamouroux has potential applications in biotechnology, several phylogenetic studies suggest the presence of cryptic diversity within the genus that requires further phylogenetic evaluation. Here, we investigated two species of Plocamium, P. "cartilagineum" and P. "telfairiae", in the Northwest (NW) Pacific. The aims of this study are to identify potential cryptic species by analyzing the genetic differences between the species from their type localities and specimens from the NW Pacific, to characterize their population genetic diversity and structure, and to find potential hotspots with high intraspecific genetic diversity in Korea. A reconstructed phylogenetic tree based on mitochondrial 5' region of cytochrome c oxidase subunit I (COI-5P) and plastid ribulose-1,5-bisphosphate carboxylase / oxygenase large subunit (rbcL) with molecular delimitation methods revealed significant differences as distinct species in the genus Plocamium. Comparison with specimens from their type localities indicated the presence of two cryptic species in the NW Pacific, including Plocamium luculentum sp. nov. The phylogeographic study for both species showed low genetic differences among populations, demonstrating genetic connectivity within the NW Pacific. These findings could promote the discovery of other morphologically and ecologically similar but phylogenetically different Plocamium species worldwide, which is essential for conservation assessments.

Keywords

Acknowledgement

This research was supported by the 2022 scientific promotion program funded by Jeju National University.

References

  1. Benson, J., Stewart, B., Close, P. & Lymbery, A. 2022. Evidence for multiple refugia and hotspots of genetic diversity for Westralunio carteri, a threatened freshwater mussel in south-western Australia. Aquat. Conserv. Mar. Freshw. Ecosyst. 32:559-575. https://doi.org/10.1002/aqc.3780
  2. Bickford, D., Lohnan, D. J., Sodhi, N. S., Ng, P. K. L., Meier, R., Winker, K., Ingram, K. K. & Das, I. 2007. Cryptic species as a window on diversity and conservation. Trends Ecol. Evol. 22:148-155. https://doi.org/10.1016/j.tree.2006.11.004
  3. Boo, G. H., Leliaert, F., Le Gall, L., Coppejans, E., De Clerck, O., Nguyen, T. V., Payri, C. E., Miller, K. A. & Yoon, H. S. 2022. Ancient Tethyan vicariance and long-distance dispersal drive global diversification and cryptic speciation in the red seaweed Pterocladiella. Front. Plant Sci. 13:849476.
  4. Chiocchio, A., Arntzen, J. W., Martinez-Solano, I., de Vries, W., Bisconti, R., Pezzarossa, A., Maiorano, L. & Canestrelli, D. 2021. Reconstructing hotspots of genetic diversity from glacial refugia and subsequent dispersal in Italian common toads (Bufo bufo). Sci. Rep. 11:260.
  5. Cremades, J., Barreiro, R., Maneiro, I. & Saunders, G. W. 2011. A new taxonomic interpretation of the type of Plocamium cartilagineum (Plocamiales, Florideophyceae) and its consequences. Eur. J. Phycol. 46:125-142. https://doi.org/10.1080/09670262.2011.565129
  6. De Clerck, O., Engledow, H. R., Bolton, J. J., Anderson, R. J. & Coppejans, E. 2002. Twenty marine benthic algae new to South Africa, with emphasis on the flora of Kwazulu-Natal. Bot. Mar. 45:413-431. https://doi.org/10.1515/BOT.2002.042
  7. Diaz-Tapia, P., Ly, M. & Verbruggen, H. 2020. Extensive cryptic diversity in the widely distributed Polysiphonia scopulorum (Rhodomelaceae, Rhodophyta): molecular species delimitation and morphometric analyses. Mol. Phylogenet. Evol. 152:106909.
  8. Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29:1969-1973. https://doi.org/10.1093/molbev/mss075
  9. Excoffier, L., Laval, G. & Schneider, S. 2005. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol. Bioinform. Online 1:47-50.
  10. Fujisawa, T. & Barraclough, T. G. 2013. Delimiting species using single-locus data and the Gneralized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets. Syst. Biol. 62:707-724. https://doi.org/10.1093/sysbio/syt033
  11. Grant, W. S. & Bowen, B. W. 1998. Shallow population histrories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation. J. Hered. 89:415-426. https://doi.org/10.1093/jhered/89.5.415
  12. Guiry, M. D. & Guiry, G. M. 2023. Algaebase. World-wide electronic publication, National University of Ireland, Galway. Available from: https://www.algaebase.org. Accessed Mar 20, 2023.
  13. Kang, J. C. & Kim, M. S. 2012. Seasonal variation in depth-stratified macroalgal assemblage patterns on Marado, Jeju Island, Korea. Algae 27:269-281. https://doi.org/10.4490/algae.2012.27.4.269
  14. Kang, J. C., Lin, S. -M., Miller, K. A. & Kim, M. S. 2021. Taxonomic revision of hook-forming Acrosorium (Delesseriaceae, Rhodophyta) from the Northwestern Pacific based on morphology and molecular data. Plants 10:2269.
  15. Kim, H. S. & Hwang, I. K. 2015. Algal flora of Korea. Vol. 4, No. 10. Marine red algae. Rhodophyta: Florideophyceae: Gelidiales, Gracilariales, Procamiales. National Institute of Biological Resources, Incheon, 140 pp.
  16. Kim, J. -Y., Yoon, M. -Y., Cha, M. -R., Hwang, J. -H., Park, E., Choi, S. -U., Park, H. -R. & Hwang, Y. -I. 2007. Methoanolic extracts of Plocamium telfairiae induce cytotoxicity and caspase-dependent apoptosis in HT-29 human colon carcinoma cells. J. Med. Food 10:587-593. https://doi.org/10.1089/jmf.2007.002
  17. 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
  18. 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
  19. Lane, C. E., Lindstrom, S. C. & Saunders, G. W. 2007. A molecular assessment of northeast Pacific Alaria species (Laminariales, Phaeophyceae) with reference to the utility of DNA barcoding. Mol. Phylogenet. Evol. 44:634-648. https://doi.org/10.1016/j.ympev.2007.03.016
  20. Lee, H. W., Kang, J. C. & Kim, M. S. 2019. Taxonomy of Ulva causing blooms from Jeju Island, Korea with new species, U. pseudo-ohnoi sp. nov. (Ulvales, Chlorophyta). Algae 34:253-266. https://doi.org/10.4490/algae.2019.34.12.9
  21. Lee, S. J. & Kim, M. S. 2022. Morphology of Plocamium cartilagineum (Plocamiales, Rhodophyta) from Korea. Aquat. Nat. 2:59-68.
  22. Montecinos, A. E., Huanel, O. R., Ramirez, M. E. & Guillemin, M. -L. 2021. Molecular data reveal the presence of three Plocamium Lamouroux species with complex patterns of distribution in Southern Chile. Cryptogam. Algol. 42:1-19. https://doi.org/10.5252/cryptogamie-algologie2021v42a1
  23. Muangmai, N., Preuss, M., West, J. A. & Zuccarello, G. C. 2022. Cryptic diversity and phylogeographic patterns of the Bostrychia intricata species complex (Rhodomelaceae, Rhodophyta) along the coast of southeastern Australia. Phycologia 61:27-36. https://doi.org/10.1080/00318884.2021.1994768
  24. 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
  25. Park, S. Y., Kang, H. M., Song, W. C., Oh, J. -W., Park, G. & Choi, Y. -W. 2022. Characterization of Plocamium telfairiae extract-functionalized Au nanostructures and their anti-adipogenic activity through PLD1. Mar. Drugs 20:421.
  26. Payo, D. A., Colo, J., Calumpong, H. & De Clerck, O. 2011. Variability of non-polar secondary metabolites in the red alga Portieria. Mar. Drugs 9:2438-2468. https://doi.org/10.3390/md9112438
  27. Puillandre, N., Brouillet, S. & Achaz, G. 2021. ASAP: assemble species by automatic partitioning. Mol. Ecol. Resour. 21:609-620. https://doi.org/10.1111/1755-0998.13281
  28. Rambaut, A., Drummond, A. J., Xie, D., Baele, G. & Suchard, M. A. 2018. Posterior summarization in Bayesian phylogenetic using tracer 1.7. Syst. Biol. 67:901-904. https://doi.org/10.1093/sysbio/syy032
  29. Reddy, M. M., du Plessis, J., Roodt-Wilding, R., Anderson, R. J. & Bolton, J. J. 2023. The reinstatement of Plocamium robertiae (Rhodophyta, Plocamiales) and an updated species inventory of the genus in South Africa. Phycologia 62:194-202. https://doi.org/10.1080/00318884.2023.2174342
  30. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. K., Darling, A., Hohna, S., Larget, B., Liu, L., Suchard, M. A. & Huelsenbeck, J. P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61:539-542. https://doi.org/10.1093/sysbio/sys029
  31. Rovirosa, J., Soler, A., Blanc, V., Leon, R. & San-Martin, A. 2013. Bioactive monoterpenes from Antarctic Plocamium cartilagineum. J. Chil. Chem. Soc. 58:2025-2026. https://doi.org/10.4067/S0717-97072013000400026
  32. Sabry, O. M. M., Goeger, D. E., Valeriote, F. A. & Gerwick, W. H. 2017. Cytotoxic halogenated monoterpenes from Plocamium cartilagineum. Nat. Prod. Res. 31:261-267. https://doi.org/10.1080/14786419.2016.1230115
  33. Saunders, G. W. 2005. Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360:1879-1888. https://doi.org/10.1098/rstb.2005.1719
  34. 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
  35. Saunders, G. W. & Lehmkuhl, K. V. 2005. Molecular divergence and morphological diversity among four cryptic species of Plocamium (Plocamiales, Florideophyceae) in northern Europe. Eur. J. Phycol. 40:293-312. https://doi.org/10.1080/09670260500192935
  36. Shilling, A. J., Heiser, S., Amsler, C. D., McClintock, J. B. & Baker, B. J. 2021. Hidden diversity in an Antarctic algal forest: metabolomic profiling linked to patterns of genetic diversification in the antarctic red alga Plocamium sp. Mar. Drugs 19:607.
  37. Shilling, A. J., von Salm, J. L., Sanchez, A. R., Kee, Y., Amsler, C. D., McClintock, J. B. & Baker, B. J. 2019. Anverenes B-E, new polyhalogenated monoterpenes from the Antarctic red alga Plocamium cartilagineum. Mar. Drugs 17:230.
  38. Struck, T. H., Feder, J. L., Bendiksby, M., Birkeland, S., Cerca, J., Gusarov, V. I., Kistenich, S., Larsson, K. -H., Liow, L. H., Nowak, M. D., Stedji, B., Bachmann, L. & Dimitrov, D. 2018. Finding evolutionary processes hidden in cryptic species. Trends Ecol. Evol. 33:153-163. https://doi.org/10.1016/j.tree.2017.11.007
  39. Suchard, M. A., Lemey, P., Baele, G., Ayres, D. L., Drummond, A. J. & Rambaut, A. 2018. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 4:vey016.
  40. Vieira, C., De Clerck, O., De Ramon N'Yeurt, A., D'hondt, S., Millet, L., Kim, M. S., Payri, C. & Zubia, M. 2022. Diversity, systematics, and biogeography of French Polynesian Lobophora (Dictyotales, Phaeophyceae). Eur. J. Phycol. 58:226-253. https://doi.org/10.1080/09670262.2022.2092216
  41. Wei, X., Fu, Z., Li, J., Guo, B. & Ye, Y. 2023. Genetic structure and phylogeography of commercial Mytilus unguiculatus in China based on mitochondrial COI and Cytb sequences. Fishes 8:89.
  42. Womersley, H. B. S. 1994. The marine benthic flora of southern Australia Rhodophyta. Part IIIA. Australian Biological Resources Study, Canberra, 508 pp.
  43. Wynne, M. J. 2002. A description of Plocamium fimbriatum sp. nov. (Plocamiales, Rhodophyta) from the Sultanate of Oman, with a census of currently recognized species in the genus. Nova Hedwigia 75:333-356. https://doi.org/10.1127/0029-5035/2002/0075-0333
  44. 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
  45. 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
  46. Yang, M. Y. & Kim, M. S. 2022. Phylogeography of the economic seaweeds Chondrus (Gigartinales, Rhodophyta) in the northwest Pacific based on rbcL and COI-5P genes. Algae 37:135-147. https://doi.org/10.4490/algae.2022.37.5.29
  47. 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.
  48. 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
  49. 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
  50. Yano, T., Kamiya, M., Arai, S. & Kawai, H. 2004. Morphological homoplasy in Japanese Plocamium species (Plocamiales, Rhodophyta) inferred from the Rubisco spacer sequence and intracellular acidity. Phycologia 43:383-393. https://doi.org/10.2216/i0031-8884-43-4-383.1
  51. Yano, T., Kamiya, M., Murakami, A., Sasaki, H. & Kawai, H. 2005. Biochemical phenotypes corresponding to molecular phylogeny of the red algae Plocamium (Plocamiales, Rhodophyta): implications of incongruence with the conventional taxonomy. J. Phycol. 42:155-169. https://doi.org/10.1111/j.1529-8817.2006.00178.x
  52. Zampiglia, M., Bisconti, R., Maiorano, L., Aloise, G., Siclari, A., Pellegrino, F., Martino, G., Pezzarossa, A., Chiocchio, A., Martino, C., Nascetti, G. & Canestrelli, D. 2019. Drilling down hotspots of intraspecific diversity to bring them into on-ground conservation of threatened species. Front. Ecol. Evol. 7:205.
  53. Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. 2013. A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29:2869-2876. https://doi.org/10.1093/bioinformatics/btt499