Systematics and Biogeography of the Red Algal Genus Yonagunia (Halymeniaceae, Rhodophyta) from the Indo-Pacific Including the Description of Two New Species from Taiwan.
Carpopeltis maillardii
Halymeniaceae
Indo-Pacific
Taiwan
Yonagunia palmata sp. nov.
Yonagunia taiwani-borealis sp. nov
phylogenetic analyses
species diversity
Journal
Journal of phycology
ISSN: 1529-8817
Titre abrégé: J Phycol
Pays: United States
ID NLM: 9882935
Informations de publication
Date de publication:
12 2020
12 2020
Historique:
received:
17
02
2020
accepted:
11
06
2020
pubmed:
28
7
2020
medline:
2
3
2021
entrez:
27
7
2020
Statut:
ppublish
Résumé
Carpopeltis maillardii has been regarded as a widely distributed species in the Indo-Pacific region. In this study, we analyzed the genetic diversity of C. maillardii and related species collected from Taiwan and the Indian Ocean based on rbcL sequences, in order to elucidate species boundaries, diversity, and biogeographic patterns. Our analyses show that C. maillardii specimens are only distantly related to the genus Carpopeltis (type: C. phyllophora) but instead form a clade together with species of Yonagunia. We therefore propose the new combination Yonagunia maillardii comb. nov. In addition, two new species (Yonagunia palmata sp. nov. and Yonagunia taiwani-borealis sp. nov.) are described from Taiwan. The close relationship of Yonagunia to Grateloupia is corroborated by detailed observations of the female reproductive structures, which demonstrate that the development of auxiliary cell ampullae before and after diploidization is similar to that of Grateloupia sensu stricto. Namely, the ampullae are composed of only two orders of unbranched filaments in which only a few ampullar cells are incorporated into a basal fusion cell after diploidization of the auxiliary cell and the pericarp consists almost entirely of secondary medullary filaments. Of all Yonagunia species, Y. maillardii has the widest distribution in the Indo-Pacific, and can be identified in the field by its relatively thin, feathery, and highly branched morphology. Most other species, including those that occur in Taiwan, are seemingly more range-restricted. Our phylogenetic analyses resulted in a well-resolved phylogeny of Yonagunia, with an origin estimated in the Eocene-Oligocene, and diversification of species mainly in the Miocene.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1542-1556Informations de copyright
© 2020 Phycological Society of America.
Références
Agardh, J. G. 1876. Species genera et ordines algarum. Vol. 3, Part 1. Epicrisis systematis floridearum. Weigel, Leipzig, 724 pp.
Boo, G. H., Park, J. K., Gerung, G. S. & Boo, S. M. 2013. Transfer of the red alga Gelidium zollingeri Sonder (Gelidiales) to Yonagunia (Halymeniales) based on morphological and molecular evidence. Phycologia 52:279-87.
Børgesen, F. 1936. Some marine algae from Ceylon. Ceylon J. Sci. Sec. A Bot. 12:57-96.
Børgesen, F. 1943. Some marine algae from Mauritius. III. Rhodophyceae. Part 2. Gelidiales, Cryptonemiales, Gigartinales. Kon. Dan. Vid. Selsk. Biol. Medd. 19:1-85.
Calderon, M. S., Boo, G. H. & Boo, S. M. 2014. Morphology and phylogeny of Ramirezia osornoensis gen. & sp. nov. and Phyllymenia acletoi sp. nov. (Halymeniales, Rhodophyta) from South America. Phycologia 53:23-36.
Chiang, Y. M. 1970. Morphological studies of red algae of the family Cryptonemiaceae. Univ. Calif. Publ. Bot. 58:1-95.
Coppejans, E. & Millar, A. J. K. 2000. Marine red algae from the North coast of Papua New Guinea. Bot. Mar. 43:315-46.
De Clerck, O., Bolton, J., Anderson, R. & Coppejans, E. 2005c. Guide to the seaweeds of KwaZulu-Natal. Scripta Botanica Belgica, 33 (pp. 1-294). National Botanic Garden of Belgium, Meise.
De Clerck, O., Gavio, B., Fredericq, S., Bárbara, I. & Coppejans, E. 2005b. Systematics of Grateloupia filicina (Halymeniaceae, Rhodophyta), based on rbcL sequence analyses and morphological evidence, including the reinstatement of G. minima and the description of G. capensis sp. nov. J. Phycol. 41:391-410.
De Clerck, O., Gavio, B., Fredericq, S., Cocquyt, E. & Coppejans, E. 2005a. Systematic reassessment of the red algal genus Phyllymenia (Halymeniaceae, Rhodophyta). Eur. J. Phycol. 40:169-78.
Drummond, A. J., Ho, S. Y. W., Phillips, M. J. & Rambaut, A. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4:699-710.
Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29:1969-73.
Edgar, R. C. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:1-19.
Farghaly, M. S. 1980. Algues benthiques de la Mer Rouge et du bassin occidental de l'Océan Indien (étude taxinomique et essai de répartition, notamment des Udotéacées). Thesis, Université des Sciences et Techniques du Langedoc, Montpellier, 274 pp.
Faye, E. T., Wang, H. W., Kawaguchi, S., Shimada, S. & Masuda, M. 2004. Reinstatement of Grateloupia subpectinata (Rhodophyta, Halymeniaceae) based on morphology and rbcL sequences. Phycol. Res. 52:59-68.
Gargiulo, G., Morabito, M. & Manghisi, A. 2013. A re-assessment of reproductive anatomy and postfertilization development in the systematics of Grateloupia (Halymeniales, Rhodophyta). Crypt. Algol. 34:3-35.
Gernhard, T. 2008. The conditioned reconstructed process. J. Theor. Biol. 253:769-78.
Guiry, M. D. & Guiry, G. M. 2020. AlgaeBase. World-wide electronic publication. National University of Ireland, Galway. Available at https://www.algaebase.org (searched on 30 June 2020).
Hommersand, H. M. & Fredericq, S. 1990. Sexual reproduction and cystocarp development. In Cole, K. M. & Sheath, R. G. [Eds.] Biology of the Red Algae. Cambridge University Press, Cambridge, pp. 305-45.
Hommersand, M. H., Leister, G. L., Ramírez, M. E., Gabrielson, P. W. & Nelson, W. A. 2010. A morphological and phylogenetic study of Glaphyrosiphon gen. nov. (Halymeniaceae, Rhodophyta) based on Grateloupia intestinalis with descriptions of two new species: Glaphyrosiphon lindaueri from New Zealand and Glaphyrosiphon chilensis from Chile. Phycologia 49:554-73.
Kawaguchi, S. 1989. The genus Prionitis (Halymeniaceae, Rhodophyta) in Japan. J. Fac. Sci., Hokkaido Univ. Ser. V (Bot.) 16:193-257.
Kawaguchi, S. 1997. Taxonomic notes on the Halymeniaceae (Gigartinales, Rhodophyta) from Japan. III. Synonymization of Pachymeniopsis Yamada in Kawabata with Grateloupia C. Agardh. Phycol. Res. 45:9-21.
Kawaguchi, S., Shimada, S., Wang, H. W. & Masuda, M. 2004. The new genus Yonagunia Kawaguchi & Masuda (Halymeniaceae, Rhodophyta), based on Y. tenuifolia Kawaguchi & Masuda sp. nov. from southern Japan and including Y. formosana (Okamura) Kawaguchi & Masuda comb. nov. from southeast Asia. J. Phycol. 40:180-92.
Kawaguchi, S., Wang, H. W., Horiguchi, T., Sartoni, G. & Masuda, M. 2001. A comparative study of the red alga Grateloupia filicina (Halymeniaceae) from the northwestern Pacific and Mediterranean with the description of Grateloupia asiatica, sp. nov. J. Phycol. 37:433-42.
Kraft, G. T. 1981. Rhodophyta: morphology and classification. In Lobban, C. S. & Wynne, M. [Eds.] Biology of Marine Plants. Longman Cheshire, Melbourne, Australia, pp. 41-85.
Kützing, F. T. 1868. Tabulae phycologicae; oder, Abbildungen der Tange (Vol. XVIII). Gedruckt auf kosten des Verfassers, Nordhausen, 35 pp + 100 pl.
Kützing, F. T. 1869. Tabulae phycologicae; oder, Abbildungen der Tange (Vol. XIX). Gedruckt auf kosten des Verfassers, Nordhausen, 36 pp + 100 pl.
Kylin, H. 1923. Studien über die Entwicklungsgeschichte der Florideen. K. Svensk. Vetensk.-Akad. Hand. 63:1-139.
Kylin, H. 1956. Die Gattungen der Rhodophyceen. Gleerups, Lund, 673 pp.
Leliaert, F., Payo, D. A., Gurgel, C. F. D., Shils, T., Draisma, S. G. A., Saunders, G. W., Kamiya, M. et al. 2018. Patterns and drivers of species diversity in the Indo-Pacific red seaweed Portieria. J. Biogeogr. 45:2299-313.
Lewis, J. E. & Norris, J. N. 1987. A History and annotated account of the benthic marine algae of Taiwan. Smithsonian Contrib. Mar. Sci. 29:1-38.
Lin, S. M., D'Archino, R. & Hommersand, M. H. 2012. A new method of cystocarp development in the red algal genus Callophyllis (Kallymeniaceae) from Chile. J. Phycol. 48:784-972.
Lin, S. M., Fredericq, S. & Hommersand, M. H. 2001. Systematics of the Delesseriaceae (Ceramiales, Rhodophyta) based on LSU rDNA and rbcL sequences, including the Phycodryoideae, subfam. nov. J. Phycol. 37:881-99.
Lin, S. M., Hommersand, M. H. & Fredericq, S. 2004. Two new species of Martensia (Delesseriaceae, Rhodophyta) from Kenting National Park, southern Taiwan. Phycologia 43:13-25.
Lin, S. M. & Liang, H. Y. 2011. Grateloupia huangiae (Halymeniaceae, Rhodophyta), a new species from Taiwan previously confused with Polyopes lancifolius, with emphasis on the development of the auxiliary-cell ampullae. Phycologia 50:232-40.
Lin, S. M., Liang, H. Y. & Hommersand, M. H. 2008. Two types of auxiliary cell ampullae in Grateloupia (Halymeniaceae, Rhodophyta), including G. taiwanensis Lin et Liang sp. nov. and G. orientalis Lin et Liang sp. nov. from Taiwan based on rbcL sequence analysis and cystocarp development. J. Phycol. 44:196-214.
Manghisi, A., Morabito, M., Boo, G. H., Boo, S. M., Bonillo, C., De Clerck, O. & Le Gall, L. 2015. Two novel species of Yonagunia (Halymeniales, Rhodophyte) were uncovered in the South of Madagascar during the Atimo-Vatae expedition. Cryptogamie Algol. 36:199-217.
Millar, A. J. K. & Prud'homme van Reine, W. F. 2005. Marine benthic macroalgae collected by Vieillard from New Caledonia and described as new species by Kützing. Phycologia 44:536-49.
Montagne, C. & Millardet, M. 1862. Botanique, Cryptogamie, Algues. In Maillard, L. [Ed.] Notes sur I'île de Réunion (Bourbon). Annexe O, Paris. 25 pp, pls 24-27.
Ng, P. K., Chiou, Y. S., Liu, L. C., Sun, Z. M., Shimabukuro, H. & Lin, S. M. 2019. Phylogeography and genetic connectivity of the marine macro-alga Sargassum ilicifolium (Phaeophyceae, Ochrophyta) in the northwestern Pacific. J. Phycol. 55:7-24.
Okamura, K. 1931. On the marine algae from Kôtôsho (Botel Tobago). Bul. Biogeogr. Soc. Japan 2:95-122.
Rambaut, A. 2014. Figtree v1.4.2. Available from http://tree.bio.ed.ac.uk/software/figtree/.
Rambaut, A., Suchard, M. A., Xie, D. & Drummond, A. J. 2014. Tracer v1.6. Available at http://beast.bio.ed.ac.uk/Tracer.
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., 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. 61:539-42.
Schmitz, F. 1895. Marine Florideen von Deutsch-Ostafrica. Bot. Jahrb. Syst. 21:137-77.
Sonder, O. G. 1871. Die Algen des tropischen Australiens. Abh. Naturwiss. Verein Hamburg 5:33-74.
Stamatakis, A. 2006. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-90.
Stamatakis, A. 2014. RAxML Version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312-13.
Tornabene, L., Valdez, S., Erdmann, M. & Pezold, F. 2015. Support for a ‘center of origin’ in the coral triangle: cryptic diversity, recent speciation, and local endemism in a diverse lineage of reef fishes (Gobiidae: Eviota). Mol. Phylogenet. Evol. 82:200-10.
Ukuwela, K. D. B., Lee, M. S. Y., Rasmussen, A. R., de Silva, A., Mumpuni Fry, B. G., Ghezellou, P., Rezaie-Atagholipour, M. & Sanders, K. L. 2016. Evaluating the drivers of Indo-Pacific biodiversity: speciation and dispersal of sea snakes (Elapidae: Hydrophiinae). J. Biogeogr. 43:243-55.
Vieira, C., Camacho, O., Sun, Z., Fredericq, S., Leliaert, F., Payri, C. & De Clerck, O. 2017. Historical biogeography of the highly diverse brown seaweed Lobophora (Dictyotales, Phaeophyceae). Mol. Phylogenet. Evol. 110:81-92.
Wang, H. W., Kawaguchi, S., Horiguchi, T. & Masuda, M. 2001. A morphological and molecular assessment of the genus Prionitis J. Agardh (Halymeniaceae, Rhodophyta). Phycol. Res. 49:251-62.
Wilkes, R. J., McIvor, L. M. & Guiry, M. D. 2005. Using rbcL sequence data to reassess the taxonomic position of some Grateloupia and Dermocorynus species (Halymeniaceae, Rhodophyta) from the north-eastern Atlantic. Eur. J. Phycol. 40:53-60.
Williams, S. T. & Duda, T. F. 2008. Did tectonic activity stimulate Oligo-Miocene speciation in the Indo-West Pacific? Evolution 62:1618-34.
Wilson, M. E. J. & Rosen, B. R. 1998. Implications of paucity of corals in the Paleogene of SE Asia: plate tectonics or centre of origin? In Hall, R. & Holloway, J. D. [Eds.] Biogeography and Geological Evolution of SE Asia. Backhuys Publishers, Leiden, pp. 165-95.
Wittmann, W. 1965. Aceto-iron-haematoxylin-chloral hydrate for chromosome staining. Stain Tech. 40:161-64.
Womersley, H. B. S. 1994. The marine benthic flora of southern Australia - Part IIIA - Bangiophyceae and Florideophyceae (Acrochaetiales, Nemaliales, Gelidiales, Hildenbrandiales and Gigartinales sensu lato). Australian Biological Resources Study published, Canberra, Australia, 508 pp.
Yang, E. C., Boo, S. M., Bhattacharya, D., Saunders, G. W., Knoll, A. H., Fredericq, S., Graf, L. & Yoon, H. S. 2016. Divergence time estimates and the evolution of major lineages in the florideophyte red algae. Sci. Rep. 6:21361.
Yip, Z. T., Quek, R. Z. B. & Huang, D. 2020. Historical biogeography of the widespread macroalga Sargassum (Fucales, Phaeophyceae). J. Phycol. 56:300-9.