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Genetic diversity hotspot of the amphi-Pacific macroalga Gloiopeltis furcata sensu lato (Gigartinales, Florideophyceae)

  • 23rd INTERNATIONAL SEAWEED SYMPOSIUM, JEJU
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Abstract

Genetic diversity patterns around the North Pacific received attention for marine organisms and have been used to infer biodiversity “hotspots” in the region. We conducted a phylogeographic study of the red alga Gloiopeltis furcata, investigating cryptic species diversity and comparing population genetic structure in the north Pacific. A phylogenetic tree and haplotype networks were constructed on the basis of 201 mitochondrial COI-5P sequences and 149 plastid rbcL sequences from G. furcata specimens. Eight distinct cryptic lineages (A–H) were identified within G. furcata. These lineages showed high genetic diversity and complex geographic distributions. All eight lineages of G. furcata sensu lato were present in the NW Pacific; however, only a single lineage (A) was present in the NE Pacific, suggesting that the NW Pacific is a center of genetic diversity for G. furcata sensu lato. Habitat discontinuities of G. furcata sensu lato in the high rocky intertidal zone may have been responsible for the high level of genetic differentiation of G. furcata sensu lato in the NW Pacific by impeding genetic exchange between adjacent populations. Our phylogenetic diversity suggests that the NW Pacific, especially Jeju Island, was a genetic diversity hotspot involving species diversity of Gloiopeltis.

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References

  • Bringloe T, Saunders GW (2018) Mitochondrial DNA sequence data reveal the origins of postglacial marine macroalgal flora in the Northwest Atlantic. Mar Ecol Prog Ser 589:45–58

    Google Scholar 

  • Boo GH, Lindstrom SC, Klochkova NC, Yotsukura N, Yang EC, Kim HG, Waaland JR, Cho GY, Miller KA, Boo SM (2011) Taxonomy and biogeography of Agarum and Thalassiophyllum (Laminariales, Phaeophyceae) based on sequences of nuclear, mitochondrial, and plastid markers. Taxon 60:831–840

    Google Scholar 

  • Cheang CC, Chu KT, Ang PO (2010) Phylogeography of the marine macroalga Sargassum hemiphyllum (Phaeophyceae, Heterokontophyta) in northwestern Pacific. Mol Ecol 19:2933–2948

    CAS  PubMed  Google Scholar 

  • Cox LN, Zaslavskaya NI, Marko PB (2014) Phylogeography and trans-Pacific divergence of the rocky shore gastropod Nucella lima. J Biogeogr 41:615–627

    Google Scholar 

  • Coyer JA, Hoarau G, Schaik JV, Luijckx P, Olsen JL (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

    Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Psada D (2012) jModelTest 2: more model, new heuristics and parallel computing. Nat Meth 9:772

    CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin version 3.0: an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50

  • Gavio B, Fredericq S (2002) Grateloupia turuturu (Halymeniaceae, Rhodophyta) is the correct name of the non-native species in the Atlantic known as Grateloupia doryphora. Eur J Phycol 37:349–360

    Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 52:696–704

    PubMed  Google Scholar 

  • Guiry MD, Guiry GM (2019) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Available at: http://www.algaebase.org (last accessed 5 January 2019)

  • Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc Lond B 270:313–321

    CAS  Google Scholar 

  • Hu ZM, Uwai S, Yu SH, Komatsu T, Ajisaka T, Duan DL (2011) Phylogeographic heterogeneity of the brown macroalga Sargassum horneri (Fucaceae) in the northwestern Pacific in relation to late Pleistocene glaciation and tectonic configurations. Mol Ecol 20:894–3909

    Google Scholar 

  • Hu ZM, Li JJ, Sun ZM, Oak JH, Zhang FP, Grant WS, Duan DL (2015) Phylogeographic structure and deep lineage diversification of the red alga Chondrus ocellatus Holmes in the Northwest Pacific. Mol Ecol 24:5020–5033

    PubMed  Google Scholar 

  • Hu ZM, Li JJ, Sun ZM, Gao X, Yao JT, Choi HG, Endo H, Duan DL (2017) Hidden diversity and phylogeographic history provide conservation insights for the edible seaweed Sargassum fusiforme in the Northwest Pacific. Evol Appl 10:366–378

    PubMed  PubMed Central  Google Scholar 

  • Ilves KL, Taylor EB (2008) Evolutionary and biogeographical patterns within the smelt genus Hypogesus in the North Pacific Ocean. J Biogeogr 35:48–64

    Google Scholar 

  • Kelly RP, Palumbi SR (2010) Genetic structure among 50 species of the northeastern Pacific rocky intertidal community. PLoS One 5:e0008591

    Google Scholar 

  • Kim MS, Kim SY, 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

    Google Scholar 

  • Kim KM, Hoarau GG, Boo SM (2012) Genetic structure and distribution of Gelidium elegans (Gelidiales, Rhodophyta) in Korea based on mitochondrial cox1 sequence data. Aquat Bot 98:27–33

    Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    CAS  Google Scholar 

  • Le Gall L, Saunders GW (2010) DNA barcoding is a powerful tool to uncover algal diversity: a case study of the Phyllophoraceae (Gigartinales, Rhodophyta) in the Canadian flora. J Phycol 46:374–389

    Google Scholar 

  • Lee JW, Oh BG, Lee HB (1996) Morphological variation of Gloiopeltis furcata (Postels et Ruprecht) J. Agardh (Rhodophyta) in the East Coast of Korea. Algae 11:91–94

    Google Scholar 

  • Lee YP (2008) Marine algae of Jeju. Academy Publication, Seoul pp. [i]-xvi, 1-477 [2], map

  • Lee KM, Boo GH, Riosmena-Rodrigue R, Shi JA, Boo SM (2009) Classification of the genus Ishige (Ishigeales, Phaeophyceae) in the North Pacific Ocean with recognition of Ishige foliacea based on plastid rbcL and mitochondrial cox3 gene sequences. J Phycol 45:905–913

    Google Scholar 

  • Lee KM, Yang EC, Coyer JA, Zuccarello GC, Wang WL, Choi CG, Boo SM (2012) Phylogeography of the seaweed Ishige okamurae (Phaeophyceae): evidence for glacial refugia in the northwest Pacific region. Mar Biol 159:1021–1028

    Google Scholar 

  • Leliaert F, Payo DA, Gurgel CFD, Shils T, Draisma SGA, Saunders GW, Kamiya M, Sherwood AR, Lin SM, Huisman JM, Le Gall L, Anderson RJ, Bolton JJ, Matti L, Zubia M, Spoke T, Viera C, Payri CE, Coppejans E, D'hondt S, Verbruggen H, De Clerck O (2018) Patterns and drivers of species diversity in the Indo-Pacific red seaweed Portieria. J Biogeogr 2018:1–15

    Google Scholar 

  • Librad P, Rozas J (2009) DnaSP V5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Google Scholar 

  • Lindstrom SC (2008) Cryptic diversity and phylogenetic relationships within the Mastocarpus papillatus species complex (Rhodophyta, Phyllophoraceae). J Phycol 44:1300–1308

    PubMed  Google Scholar 

  • Lindstrom SC, Hughey J, Martone P (2011) New, resurrected and redefined species of Mastocarpus (Phyllophoraceae, Rhodophyta) from the northeast Pacific. Phycologia 50:661–683

    Google Scholar 

  • López BA, Tellier F, Retamal-Alarcón JC, Pérez-Araneda K, Fierr AO, Macaya EC, Tala F, Thiel M (2017) Phylogeography of two intertidal seaweeds, Gelidium lingulatum and G. rex (Rhodophyta: Gelidiales), along the South East Pacific: patterns explained by rafting dispersal? Mar Biol 164:188

    Google Scholar 

  • Miller KG, Wright JD, Fairbanks RG (1991) Unlocking the ice house: Oligocene-Miocene Oxygen isotopes, eustasy, and margin erosion. J Geophys Res 96:6829–6848

  • Montecinos A, Broitma BR, Faugeron S, Haye PA, Tellier F, Guillemin ML (2012) Species replacement along a linear coastal habitat: phylogeography and speciation in the red alga Mazzaella laminarioides along the south east Pacific. BMC Evol Biol 12:97

    PubMed  PubMed Central  Google Scholar 

  • Muangmai N, von Ammon I, Zuccarello GC (2016) Cryptic species in sympatry: non-random small-scale distribution patterns in Bostrychia intricata (Ceramiales, Rhodophyta). Phycologia 55:424–430

    Google Scholar 

  • Oh BG, Lee HB (1996) Morphology of three species of Gloiopeltis (Endocladiaceae, Rhodophyta) in Korea. Algae 11:81–90

    Google Scholar 

  • Okamura K (1927) Icones of Japanese algae. Kazamashobo, Tokyo Vol. V pp. 135-180, plates CCXXXVI-CCXLV

  • Otofuji YI, Kambara A, Matsuda T, Nohda S (1994) Counterclockwise rotation of Northeast Japan: Paleomagnetic evidence for regional extent and timing of rotation. Earth Planet Sci Lett 121:503–518

    Google Scholar 

  • Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol 25:547–572

    Google Scholar 

  • Payo DA, Leliaert F, Verbruggen H, D’hondt S, Calumpong HP, De Clerck O (2013) Extensive cryptic species diversity and fine-scale endemism in the marine red alga Portieria in the Philippines. Proc R Soc B 280:20122660

    PubMed  Google Scholar 

  • Postels A, Ruprecht F (1840) Illustrationes algarum in itinere circum orbem jussu imperatoris Nicolai I. Atque auspiciis navarchi Friderici Lütke annis 1826, 1827, 1828 et 1829 celoce Seniavin exsecuto in Oceano pacifico, inprimis septemtrionale ad littora rossica asiatico-americana collectarum. Typis Eduardi Pratz, Petropoli [St. Petersburg] pp. [i-vi ], [i]- iv, 1-28 [1-2, index], [Latin:] [−iv], [1]-22, [1-2, index], 40 pls

  • Saunders GW, McDevit DC (2012) Acquiring DNA sequence data from dried archival red algae (Florideophyceae) for the purpose of applying available names to contemporary genetic species: a critical assessment. Botany 90:191–203

    CAS  Google Scholar 

  • Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539

    PubMed  PubMed Central  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    CAS  Google Scholar 

  • Tronholm A, Sansón M, Afonso-Carrillo J, Verbruggen H, De Clerk O (2010) Niche partitioning and the coexistence of two cryptic Dictyota (Dictyotales, Phaeophyceae) species from the Canary Islands. J Phycol 46:1075–1087

    Google Scholar 

  • von der Heydt A, Dijkstra HA (2006) Effect of ocean gateways on the global ocean circulation in the late Oligocene and early Miocene. Paleoceanography 21:PA1011

    Google Scholar 

  • Yang EC, Lee SY, Lee WJ, Boo SM (2009) Molecular evidence for recolonization of Ceramium japonicum (Ceramiaceae, Rhodophyta) on the west coast of Korea after the last glacial maximum. Bot Mar 52:307–315

    CAS  Google Scholar 

  • Yang MY, Macaya EC, Kim MS (2015) Molecular evidence for verifying the distribution of Chondracanthus chamissoi and C. teedei (Gigartinaceae, Rhodophyta). Bot Mar 58:103–113

    Google Scholar 

  • Yang MY, Kim MS (2018) DNA barcoding of the funoran-producing red algal genus Gloiopeltis (Gigartinales) and description of a new species, Gloiopeltis frutex sp. nov. J Appl Phycol 30:1381–1392

    CAS  Google Scholar 

  • Zheng J, Chen Y, Yao F, Chen W, Shi G (2012) Chemical composition and antioxidant/antimicrobial activities in supercritical carbon dioxide fluid extract of Gloiopeltis tenax. Mar Drugs 10:2634–2647

    PubMed  PubMed Central  Google Scholar 

  • Zuccarello GC, West JA (2003) Multiple cryptic species: molecular diversity and reproductive isolation in the Bostrychia radicans/B. moritziana complex (Rhodomelaceae, Rhodophyta) with focus on North American isolates. J Phycol 39:948–959

    CAS  Google Scholar 

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Acknowledgments

We thank Dr. G. W. Saunders, Dr. Olga Selivanova and Dr. Zhong-Min Sun for providing samples from Canada, Kamchatka and China, and all members of the molecular phylogeny team of the marine algal laboratory at Jeju National University.

Funding

This research was supported by the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT and Future Planning (2017R1A2B4009420), Basic Science Research Program funded by the Ministry of Education (2019R1A6A1A10072987) of the Republic of Korea, and the 2019 scientific promotion program funded by Jeju National University.

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Correspondence to Myung Sook Kim.

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Yang, M.Y., Yang, E.C. & Kim, M.S. Genetic diversity hotspot of the amphi-Pacific macroalga Gloiopeltis furcata sensu lato (Gigartinales, Florideophyceae). J Appl Phycol 32, 2515–2522 (2020). https://doi.org/10.1007/s10811-019-02017-y

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