Phylogenetic relationships within the genus Hypnea (Cystocloniaceae, Rhodophyta): convergent evolution and its implications in the infrageneric classification

Botanica Marina - Tập 62 Số 6 - Trang 563-575 - 2019
Priscila Barreto de Jesus1,2, Fábio Nauer3, Goia de Mattos Lyra1, Valter Loureiro de Araújo1,2, Igor Araújo Santos de Carvalho4, José Marcos de Castro Nunes1, Valéria Cassano3, Mariana C. Oliveira3, Alessandra Selbach Schnadelbach4
1Laboratório de Algas Marinhas, Instituto de Biologia, Universidade Federal da Bahia, Rua Barão de Jeremoabo, s/n, Salvador, BA, 40.170-115, Brazil
2Programa de Pós-Graduação em Botânica , Universidade Estadual de Feira de Santana , Av. Transnordestina, s/n , Feira de Santana , BA, 44031-460 , Brazil
3Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, Rua do Matão 277, São Paulo, SP, 05508-090, Brazil
4Laboratório de Genética e Evolução de Plantas, Instituto de Biologia , Universidade Federal da Bahia , Rua Barão de Jeremoabo, s/n , Salvador , BA, 40.170-115 , Brazil

Tóm tắt

Abstract

Hypnea is a monophyletic genus with a complex nomenclatural and taxonomic history, and is an important commercial source of carrageenan. Phylogenies of this genus have been accessed based primarily on Asian species; however, recent studies performed in South America revealed a great diversity of species, for which phylogenetic relationships need to be evaluated. Three infrageneric sections are recognized in the genus: Pulvinatae, Spinuligerae, and Virgatae; however, morphological and molecular circumscriptions within each section lack clarity. In this study, we analyzed three distinct markers to establish phylogenetic relationships among Hypnea species. To assign each species to the correct section, morphological data were obtained from original descriptions, reference literature, and comparisons with type/topotype and herbaria specimens. Our analyses recovered robust phylogenies for the genus and provided new insights on the taxonomic status and relationships among and within Hypnea species. The combination of three genetic markers increased the resolution and support, resulting in the largest and best-resolved phylogeny of the genus to date. Single and combined analyses revealed that the three sections of the genus Hypnea are taxonomically irrelevant, as currently recognized. Morphological differences are not associated with monophyletic groups and similarities among clades could be better explained by convergent evolution in thallus habit.

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Tài liệu tham khảo

Abbott, I.A. 1999. Marine red algae of the Hawaiian Islands. Bishop Museum Press, Honolulu, Hawaii. pp. 477.

Agardh, J.G. 1852. Species genera et ordines algarum. Volume 2. Pars 2. Gleerup, Lund. pp. 337–720.

Biomatters. Geneious v6.0.6. Available at: http://www.geneious.com (last accessed October 20, 2017).

Cardoso, D., L.P. Queiroz, H.C. Lima, E. Suganuma, C. van den Berg and M. Lavin. 2013. A molecular phylogeny of the vataireoid legumes underscores floral evolvability that is general to many early-branching papilionoid lineages. Amer. J. Bot. 100: 403–421.

Cianciola, E., T.R. Popolizio, C.W. Schneider and C.E. Lane. 2010. Using molecular-assisted alpha taxonomy to better understand red algal biodiversity in Bermuda. Diversity 2: 946–958.

Dawes, C.J. and A.C. Mathieson. 2008. The seaweeds of Florida. University Press of Florida, Gainesville, USA. pp. 591.

De Toni, G.B. 1897. Sylloge algarum omnium hucusque cognitarum. Volume IV: Florideae. Sectio II. pp. 337–776.

Doyle, J.J. and J.L. Doyle. 1987. A rapid DNA isolation method for small quantities of fresh tissues. Phytochem. Bull. Soc. Amer. 19: 11–15.

Freshwater, D.W. and J. Rueness. 1994. Phylogenetic relationships of some European Gelidium (Gelidiales, Rhodophyta) species, based on rbcL nucleotide sequence analysis. Phycologia 33: 187–194.

Freshwater, D.W., S. Fredericq, B.S. Butler, M.H. Hommersand and M.W. Chase. 1994. A gene phylogeny of the red algae (Rhodophyta) based on plastid rbcL. Proc. Natl. Acad. Sci. USA 91: 7281–7285.

Geraldino, P.J.L., E.C. Yang and S.M. Boo. 2006. Morphology and molecular phylogeny of Hypnea flexicaulis (Gigartinales, Rhodophyta) from Korea. Algae 21: 417–423.

Geraldino, P.J.L., E.C. Yang, M.S. Kim and S.M. Boo. 2009. Systematics of Hypnea asiatica sp. nov. (Hypneaceae, Rhodophyta) based on morphology and nrDNA SSU, plastid rbcL, and mitochondrial cox1. Taxon 58: 606–616.

Geraldino, P.J.L., R. Riosmena-Rodriguez, L.M. Liao and S.M. Boo. 2010. Phylogenetic relationships within the genus Hypnea (Gigartinales, Rhodophyta), with a description of Hypnea caespitosa sp. nov. J. Phycol. 46: 336–345.

Guiry, M.D. and G.M. Guiry. 2019. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Available at: http://www.algaebase.org (last accessed March 01, 2019).

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.

Hillis, D.M. and J.J. Bull. 1993. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Syst. Biol. 42: 182–192.

Hommersand, M.H. and S. Fredericq. 2003. Biogeography of the marine red algae of the South African West Coast: a molecular approach. In: (A.R.O. Chapman, R.J. Anderson, V.J. Vreeland and I.R. Davison, eds) Proceedings XVIIth International Seaweed Symposium. Oxford University Press, Oxford, UK. pp. 325–336.

Jesus, P.B. and J.M.C. Nunes. 2012. Estudos morfológicos e taxonômicos em Hypnea cornuta (Kützing) J. Agardh (Gigartinales, Rhodophyta) no litoral da Bahia Brasil. Acta Bot. Bras. 26: 973–978.

Jesus, P.B., A.S. Schnadelbach and J.M.C. Nunes. 2013. O gênero Hypnea (Cystocloniaceae, Rhodophyta) no litoral do estado da Bahia, Brasil. Sitientibus, Sér. Ciênc. Biol. 13: 1–21.

Jesus, P.B., M.S. Silva, G.M. Lyra, J.M.C. Nunes and A.S. Schnadelbach. 2015. Extension of the distribution range of Hypnea stellulifera (Cystocloniaceae, Rhodophyta) to the South Atlantic: morphological and molecular evidence. Aquat. Bot. 123: 26–36.

Jesus, P.B., F. Nauer, G.M. Lyra, V. Cassano, M.C. Oliveira, J.M.C. Nunes and A.S. Schnadelbach. 2016. Species delimitation and phylogenetic analyses of some cosmopolitan species of Hypnea (Rhodophyta) reveal synonyms and misapplied names to H. cervicornis, including a new species from Brazil. J. Phycol. 52: 774–792.

Jesus, P.B., A.L. Costa, J.M.C. Nunes, A. Manghisi, G. Genovese, M. Morabito and A.S. Schnadelbach. 2018. Species delimitation methods reveal cryptic diversity in the Hypnea cornuta complex (Cystocloniaceae, Rhodophyta). Eur. J. Phycol. 54: 135–153.

Kearse, M., R. Moir, A. Wilson, S. Stones-Havas, M. Cheung, S. Sturrock, S. Buxton, A. Cooper, S. Markowitz, C. Duran, T. Thierer, B. Ashton, P. Mentjies and A. Drummond. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647–1649.

Kimura, M. 1980. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16: 111–120.

Lamouroux, J.V.F. 1813. Essai sur les genres de la famille des Thalassiophytes non articulées. Ann. Mus. Hist. Nat. Paris 20: 21–47, 115–139, 267–293, pls. 7–13.

Lyra, G.M., E.S. Costa, P.B. Jesus, J.C.G. Matos, T.A. Caires, M.C. Oliveira, E.C. Oliveira, Z. Xi, J.M.C. Nunes and C.C. Davis. 2015. Phylogeny of Gracilariaceae (Rhodophyta): evidence from plastid and mitochondrial nucleotide sequences. J. Phycol. 51: 356–366.

Miller, M.A., W. Pfeiffer and T. Schwartz. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE). The Institute of Electrical and Electronics Engineers (IEEE), New Orleans, Los Angeles. pp. 1–8.

Nauer, F., N.R. Guimarães, V. Cassano, N.S. Yokoya and M.C. Oliveira. 2014. Hypnea species (Gigartinales, Rhodophyta) from the southeastern coast of Brazil based on molecular studies complemented with morphological analyses, including descriptions of Hypnea edeniana sp. nov. and H. flava sp. nov. Eur. J. Phycol. 49: 550–575.

Nauer, F., V. Cassano and M.C. Oliveira. 2015. Description of Hypnea pseudomusciformis sp. nov., a new species based on molecular and morphological analyses, in the context of the H. musciformis complex (Gigartinales, Rhodophyta). J. Appl. Phycol. 27: 2405–2417.

Nauer, F., V. Cassano and M.C. Oliveira. 2016. Hypnea wynnei and Hypnea yokoyana (Cystocloniaceae, Rhodophyta), two new species revealed by a DNA barcoding survey on the Brazilian coast. Phytotaxa 268: 123–134.

Nylander, J.A.A. 2008. MrModeltest v2.3. Program distributed by the author. Evolutionary Biology Centre, Uppsala University. Available at: http://www.abc.se/~nylander/mrmodeltest2/mrmodeltest2.html.

Posada, D. and T.R. Buckley. 2004. Model selection and model averaging in phylogenetics: analysis of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst. Biol. 53: 793–808.

Price, J.H., D.M. John and G.W. Lawson. 1992. Seaweeds of the western coast of tropical Africa and adjacent islands: a critical assessment. IV. Rhodophyta (Florideae) 3. Genera H–K. Bull. Br. Mus. Nat. Hist. (Bot.) 22: 123–146.

Ronquist, F., M. Teslenko, P. Mark, D.L. Ayres, A. Darling, S. Höhna, B. Larget, L. Liu, M.A. Suchard and J.P. Huelsenbeck. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61: 539–542.

Saunders, G.W. 2005. Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Phil. Trans. R. Soc. B 360: 1879–1888.

Schneider, C.W. and R.B. Searles. 1976. North Carolina marine algae. VII. New species of Hypnea and Petroglossum (Rhodophyta, Gigartinales) and additional records of other Rhodophyta. Phycologia 15: 51–60.

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

Stamatakis, A., P. Hoover and J. Rougemont. 2008. A rapid bootstrap algorithm for the RAxML web servers. Syst. Biol. 57: 758–771.

Tamura, K., G. Stecher, D. Peterson, A. Filipski and S. Kumar. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30: 2725–2729.

Tanaka, T. 1941. The genus Hypnea from Japan. Sci. Pap. Inst. Algol. Res. Fac. Sci. Hokkaido Univ. 2: 227–250.

Tanaka, T. 1960. Studies on some marine algae from Southern Japan, III. Mem. Fac. Fish. Kagoshima Univ. 9: 91–105.

Thiers, B. [continuously updated]. Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. http://sweetgum.nybg.org/science/ih/(last accessed March 01, 2019).

Thompson, J.D., D.G. Higgins and T.J. Gibson. 1994. Clustal, W: improving the sensitivity of progressive weighting position–specific gap penalties and weight matrix choice. Nucl. Acids Res. 22: 4673–4680.

Vázquez-Delfín, E., G.H. Boo, D. Rodriguez, S.M. Boo and D. Robledo. 2016. Hypnea musciformis (Cystocloniaceae) from the Yucatan Peninsula: morphological variability in relation to life-cycle phase. Phycologia 55: 230–242.

Wiens, J.J. 1998. Combining data sets with different phylogenetic histories. Syst. Biol. 47: 568–581.

Yamagishi, Y. and M. Masuda. 1997. Species of Hypnea from Japan. In: (I.A. Abbott, ed) Taxonomy of economic seaweeds with reference to some Pacific species 6. California Sea Grant College System, La Jolla. pp. 135–162.

Yamagishi, Y. and M. Masuda. 2000. A taxonomic revision of Hypnea charoides-valentiae complex (Rhodophyta Gigartinales) in Japan with a description of Hypnea flexicaulis sp. nov. Phycol. Res. 48: 27–35.

Yamagishi, Y., M. Masuda, T. Abe, S. Uwai, K. Kogame, S. Kawaguchi and S.M. Phang. 2003. Taxonomic notes on marine algae from Malaysia XI. Four species of Rhodophyceae. Bot. Mar. 46: 534–547.

Yang, E.C. and S.M. Boo. 2004. Evidence for two independent lineages of Griffithsia (Ceramiaceae, Rhodophyta) based on plastid protein–coding psaA, psbA, and rbcL gene sequences. Mol. Phylogenet. Evol. 31: 680–688.

Yoon, H.S., J.D. Hackett and D. Bhattacharya. 2002. A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proc. Natl. Acad. Sci. USA 99: 11724–11729.