Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Botanica Marina

Editor-in-Chief: Dring, Matthew J.


IMPACT FACTOR 2018: 0.919
5-year IMPACT FACTOR: 1.336

CiteScore 2018: 1.22

SCImago Journal Rank (SJR) 2018: 0.399
Source Normalized Impact per Paper (SNIP) 2018: 0.672

Online
ISSN
1437-4323
See all formats and pricing
More options …
Ahead of print

Issues

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

Priscila Barreto de JesusORCID iD: https://orcid.org/0000-0001-6072-1422
  • Corresponding author
  • Programa de Pós-Graduação em Botânica, Universidade Estadual de Feira de Santana, Av. Transnordestina, s/n, Feira de Santana, BA, 44031-460, Brazil
  • Laboratório de Algas Marinhas, Instituto de Biologia, Universidade Federal da Bahia, Rua Barão de Jeremoabo, s/n, Salvador, BA, 40.170-115, Brazil
  • orcid.org/0000-0001-6072-1422
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Fabio Nauer
  • Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, Rua do Matão 277, São Paulo, SP, 05508-090, Brazil
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Goia de Mattos Lyra
  • Laboratório de Algas Marinhas, Instituto de Biologia, Universidade Federal da Bahia, Rua Barão de Jeremoabo, s/n, Salvador, BA, 40.170-115, Brazil
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Valter Loureiro de Araújo
  • Programa de Pós-Graduação em Botânica, Universidade Estadual de Feira de Santana, Av. Transnordestina, s/n, Feira de Santana, BA, 44031-460, Brazil
  • Laboratório de Algas Marinhas, Instituto de Biologia, Universidade Federal da Bahia, Rua Barão de Jeremoabo, s/n, Salvador, BA, 40.170-115, Brazil
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Igor Araújo Santos de Carvalho
  • Laboratório 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
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ José Marcos de Castro Nunes
  • Laboratório de Algas Marinhas, Instituto de Biologia, Universidade Federal da Bahia, Rua Barão de Jeremoabo, s/n, Salvador, BA, 40.170-115, Brazil
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Valéria Cassano
  • Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, Rua do Matão 277, São Paulo, SP, 05508-090, Brazil
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Mariana Cabral Oliveira
  • Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, Rua do Matão 277, São Paulo, SP, 05508-090, Brazil
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Alessandra Selbach Schnadelbach
  • Laboratório 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
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2019-08-14 | DOI: https://doi.org/10.1515/bot-2019-0018

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.

This article offers supplementary material which is provided at the end of the article.

Keywords: COI-5P; psaA; rbcL; sections; systematics

References

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

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

  • 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.CrossrefGoogle Scholar

  • 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.CrossrefGoogle Scholar

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

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

  • 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.Google Scholar

  • 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.CrossrefGoogle Scholar

  • 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.CrossrefGoogle Scholar

  • 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.CrossrefGoogle Scholar

  • 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.CrossrefWeb of ScienceGoogle Scholar

  • 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.CrossrefWeb of ScienceGoogle Scholar

  • 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.Google Scholar

  • 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.CrossrefGoogle Scholar

  • 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.Google Scholar

  • 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.CrossrefGoogle Scholar

  • 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.Google Scholar

  • 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.CrossrefWeb of ScienceGoogle Scholar

  • 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.CrossrefWeb of ScienceGoogle Scholar

  • 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.Web of ScienceGoogle Scholar

  • 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.CrossrefWeb of ScienceGoogle Scholar

  • 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.CrossrefGoogle Scholar

  • 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.Google Scholar

  • 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.CrossrefWeb of ScienceGoogle Scholar

  • 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.Google Scholar

  • 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.CrossrefWeb of ScienceGoogle Scholar

  • 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.CrossrefWeb of ScienceGoogle Scholar

  • 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.CrossrefWeb of ScienceGoogle Scholar

  • 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.CrossrefGoogle Scholar

  • 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.Google Scholar

  • 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.Web of ScienceCrossrefGoogle Scholar

  • 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.CrossrefGoogle Scholar

  • 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.CrossrefGoogle Scholar

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

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

  • 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.Web of ScienceCrossrefGoogle Scholar

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

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

  • 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.CrossrefGoogle Scholar

  • 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.CrossrefWeb of ScienceGoogle Scholar

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

  • 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.Google Scholar

  • 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.CrossrefGoogle Scholar

  • 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.Google Scholar

  • 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.CrossrefGoogle Scholar

  • 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.CrossrefGoogle Scholar

About the article

Priscila Barreto de Jesus

Priscila Barreto de Jesus is currently a temporary lecturer at the Department of Technology and Social Sciences (DTCS), Bahia State University (UNEB), Brazil. She was awarded a Master’s and a PhD degree in Botany from the State University of Feira de Santana, Brazil, and a postdoctoral degree from the University of São Paulo, Brazil. Her research interests are species delimitation, molecular systematics, phylogeography, phylogeny and genomics of marine macroalgae, especially the genus Hypnea.

Fabio Nauer

Fabio Nauer is a postdoctoral researcher at the Botany Institute of São Paulo. PhD degree in Science, Botany sub-area, obtained at the Botany Department of the Institute of Biosciences, University of São Paulo (IB-USP), under supervision of Dr. Mariana Cabral de Oliveira. He is a specialist in the genus Hypnea, focusing on biogeography and polyphasic taxonomy and joining molecular, morphological and eco-physiological data to understand the delimitations and distributions of the species along the Brazilian coast.

José Marcos de Castro Nunes

José Marcos de C. Nunes has been a Professor at the Universidade Federal da Bahia (UFBA), Brazil since 1990. With a PhD in Science from the Universidade de São Paulo, Brazil (2005), his research is focused on marine algal taxonomy, systematics and ecology. He is the curator of the Cryptogam collection of the Herbarium Alexandre Leal Costa (ALCB/UFBA), and the coordinator of the Laboratório de Algas Marinhas (LAMAR).

Mariana Cabral Oliveira

Mariana C. Oliveira is a Professor at the University of São Paulo, Brazil. She is interested in the origin, evolution, diversity, and distribution of different groups of algae. She was on the Editorial Board of Journal of Phycology, International Vice-President of the Phycological Society of America, Associate Editor of Phycologia, in the Botany committee of CNPq and on the coordination committee of the Biota-FAPESP Program. Presently She is part of Area Coordination for the Biosciences of FAPESP.

Alessandra Selbach Schnadelbach

Alessandra Selbach Schnadelbach is an Associate Professor at Biology Institute of the Federal University of Bahia (UFBA) and coordinator of the PPG Biodiversity and Evolution. She specializes in Genetics and Plant Evolution, mainly on the following topics: genetic variability, molecular markers, phylogeny, evolution, biosystematics and genetics of populations.


Received: 2019-03-29

Accepted: 2019-07-05

Published Online: 2019-08-14


Funding Source: Fundação de Amparo à Pesquisa do Estado de São Paulo

Award identifier / Grant number: 2013/11833-3

Funding Source: Fundação de Amparo à Pesquisa do Estado da Bahia

Award identifier / Grant number: PRONEM T.O. PNE. 0020/2011

Award identifier / Grant number: REDES T.O. RED006/2012

This research was funded by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, BrBOL 564945/2010-2 and UNIVERSAL 477614/2013-2), Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, Funder Id: http://dx.doi.org/10.13039/501100001807, Biota Program, 2013/11833-3), and Fundação de Amparo à Pesquisa do Estado da Bahia (FAPESB, Funder Id: http://dx.doi.org/10.13039/501100006181, PRONEM T.O. PNE. 0020/2011 and REDES T.O. RED006/2012). FN and ALC acknowledge scholarships from CNPq. IASC acknowledges scholarships from FAPESB. PBJ (150068/2017-4), JMCN (308542/2018-5), VC (302549/2017-0) and MCO (301491/2013-5) acknowledge CNPq. Many thanks to Dr. Kazuiro Kogame (SAP), Dr. Patrik Frödén (LD), Dr. Richard Searles (DUKE), Jo Wilbraham (BM), John Parnell (TCD), Dr. Heroen Verbruggen (MELU), and Dr. Daniel Robledo (MEXU) for the loan of sequences and samples.


Citation Information: Botanica Marina, 20190018, ISSN (Online) 1437-4323, ISSN (Print) 0006-8055, DOI: https://doi.org/10.1515/bot-2019-0018.

Export Citation

©2019 Walter de Gruyter GmbH, Berlin/Boston.Get Permission

Supplementary Article Materials

Comments (0)

Please log in or register to comment.
Log in