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Genetic diversity and population structure of Corollospora maritima sensu lato: new insights from population genetics

  • Patricia Velez

    Patricia Velez earned her PhD in Fungal Ecology from the National Autonomous University of Mexico in 2014 for her work on the community structure of marine arenicolous fungi from the Gulf of Mexico and the population genetics of Corollospora maritima. She has previously worked on the comparative transcriptomics of this cosmopolitan marine fungus, and in the fungal ecology of an oligotrophic freshwater system. Currently she is a postdoctoral researcher at the Centro de Investigación Científica y Educación Superior de Ensenada (CICESE) and her work focuses on the molecular ecology of marine fungal communities from deep-sea sediments.

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    , Jaime Gasca-Pineda

    Jaime Gasca-Pineda is currently a postdoctoral researcher at the Centro de Investigación Científica y Educación Superior de Ensenada (CICESE). He received his PhD in Biomedical Sciences from the National Autonomous University of Mexico in 2015 for his work on the population genetics of bighorn sheep and bison from Mexico. He has also conducted research on the molecular ecology of wild maize and microbial communities. More recently, his postdoctoral research has focused on the population genomics of ichthyoplankton from the Gulf of Mexico.

    , Akira Nakagiri

    Akira Nakagiri is a Professor at the Faculty of Agriculture, Fungus/Mushroom Resource and Research Center, University of Tottori. In 2014, he received an award from the former Japan Society for Culture Collections (current Japan Society for Microbial Resources and Systematics) for his contributions to fungal taxonomy and to the preservation of fungal cultures. His research areas range from fungal taxonomy and ecology of marine taxa to the preservation of fungal cultures. He is a specialist in marine fungal taxonomy and biology, having described several new taxa including members of the genus Corollospora.

    , Richard T. Hanlin

    Richard T. Hanlin, Professor Emeritus at the University of Georgia, retired in 2001 after 41 years in the Department of Plant Pathology. He continues to serve as a part-time curator of the Miller Mycology Herbarium in the Museum of Natural History. He is a member of the Mycological Society of America, served as vice president and president, and is a recipient of the society’s W. H. Weston Award for Teaching Excellence in Mycology and Distinguished Mycologist Award.

    and María C. González

    María C. González received her DSc from the National Autonomous University of Mexico. She is presently a permanent researcher at the Institute of Biology at the same university, where she teaches mycology in graduate level courses and conducts research on the biology of microscopic fungi from freshwater and marine habitats in Mexico.

Published/Copyright: September 26, 2016

Abstract

The study of genetic variation in fungi has been poor since the development of the theoretical underpinnings of population genetics, specifically in marine taxa. Corollospora maritima sensu lato is an abundant cosmopolitan marine fungus, playing a crucial ecological role in the intertidal environment. We evaluated the extent and distribution of the genetic diversity in the nuclear ribosomal internal transcribed spacer region of 110 isolates of this ascomycete from 19 locations in the Gulf of Mexico, Caribbean Sea and Pacific Ocean. The diversity estimates demonstrated that C. maritima sensu lato possesses a high genetic diversity compared to other cosmopolitan fungi, with the highest levels of variability in the Caribbean Sea. Globally, we registered 28 haplotypes, out of which 11 were specific to the Caribbean Sea, implying these populations are genetically unique. We detected populations inhabiting human-impacted sites with null genetic variation. As long-term exposure to contaminants has been proven to decrease genetic diversity, a conservation genetics approach to assess this matter is urgent. Our results revealed the occurrence of five genetic lineages with distinctive environmental preferences and an overlapping geographical distribution, agreeing with previous studies reporting physiological races within this species.

About the authors

Patricia Velez

Patricia Velez earned her PhD in Fungal Ecology from the National Autonomous University of Mexico in 2014 for her work on the community structure of marine arenicolous fungi from the Gulf of Mexico and the population genetics of Corollospora maritima. She has previously worked on the comparative transcriptomics of this cosmopolitan marine fungus, and in the fungal ecology of an oligotrophic freshwater system. Currently she is a postdoctoral researcher at the Centro de Investigación Científica y Educación Superior de Ensenada (CICESE) and her work focuses on the molecular ecology of marine fungal communities from deep-sea sediments.

Jaime Gasca-Pineda

Jaime Gasca-Pineda is currently a postdoctoral researcher at the Centro de Investigación Científica y Educación Superior de Ensenada (CICESE). He received his PhD in Biomedical Sciences from the National Autonomous University of Mexico in 2015 for his work on the population genetics of bighorn sheep and bison from Mexico. He has also conducted research on the molecular ecology of wild maize and microbial communities. More recently, his postdoctoral research has focused on the population genomics of ichthyoplankton from the Gulf of Mexico.

Akira Nakagiri

Akira Nakagiri is a Professor at the Faculty of Agriculture, Fungus/Mushroom Resource and Research Center, University of Tottori. In 2014, he received an award from the former Japan Society for Culture Collections (current Japan Society for Microbial Resources and Systematics) for his contributions to fungal taxonomy and to the preservation of fungal cultures. His research areas range from fungal taxonomy and ecology of marine taxa to the preservation of fungal cultures. He is a specialist in marine fungal taxonomy and biology, having described several new taxa including members of the genus Corollospora.

Richard T. Hanlin

Richard T. Hanlin, Professor Emeritus at the University of Georgia, retired in 2001 after 41 years in the Department of Plant Pathology. He continues to serve as a part-time curator of the Miller Mycology Herbarium in the Museum of Natural History. He is a member of the Mycological Society of America, served as vice president and president, and is a recipient of the society’s W. H. Weston Award for Teaching Excellence in Mycology and Distinguished Mycologist Award.

María C. González

María C. González received her DSc from the National Autonomous University of Mexico. She is presently a permanent researcher at the Institute of Biology at the same university, where she teaches mycology in graduate level courses and conducts research on the biology of microscopic fungi from freshwater and marine habitats in Mexico.

Acknowledgments

This research was supported by the Institute of Biology, National Autonomous University of Mexico, and by the Consejo Nacional de Ciencia y Tecnología (CONACyT), project number CB 60502. Patricia Velez also thanks the fellowship provided by the CONACyT. The authors recognize the help provided during the fieldwork in the Mexican states of Tabasco, Campeche and Veracruz by Edmundo Rosique-Gil and Silvia Capello from the División Académica de Ciencias Biológicas, Universidad Juárez Autónoma de Tabasco, as well as Sergio Martínez from the Centro de Biodiversidad y Descubrimiento de Drogas, INDICASAT-AIP, Xavier Alvarez from the Facultad de Ciencias Naturales, Universidad de Guayaquil, staff of the Instituto de Oceanología, Christian Quintero and Jan Hanlin for the assistance in the sample collection of Panama, Ecuador, Cuba, Sonora State in Mexico, and Hawaii, respectively. We would also like to extend our sincere appreciation to anonymous reviewers for their valuable comments.

References

Abdel-Wahab, M.A. 2011. Marine fungi from Sarushima Island, Japan, with a phylogenetic evaluation of the genus Naufragella. Mycotaxon 115: 443–456.10.5248/115.443Search in Google Scholar

Abdel-Wahab, M.A., K.L. Pang, H.M. El-Sharouney and E.B.G. Jones. 2001. Halosarpheia unicellularis sp. nov., (Halosphaeriales, Ascomycota) based on morphological and molecular evidence. Mycoscience 42: 255–260.10.1007/BF02463916Search in Google Scholar

Alberte, R.S., G.K. Suba, G. Procaccini, R.C. Zimmerman and S.R. Fain. 1994. Assessment of genetic diversity of seagrass populations using DNA fingerprinting: Implications for population stability and management. Proc. Natl. Acad. Sci. USA 91: 1049–53.10.1073/pnas.91.3.1049Search in Google Scholar

Amos, W., J. Harwood. 1998. Factors affecting levels of genetic diversity in natural populations. Philos. Trans. R. Soc. Lon. B. Biol. Sci. 353: 177–186.10.1098/rstb.1998.0200Search in Google Scholar

Bebout, B., S. Schatz, J. Kohlmeyer and M. Haibach. 1987. Temperature-dependent growth in isolates of Corollospora maritima Werderm. (Ascomycetes) from different geographical regions. J. Exp. Mar. Biol. Ecol. 106: 203–210.10.1016/0022-0981(87)90093-1Search in Google Scholar

Belsley, D., E. Kuh and R. Welsch. 1980. Regression diagnostics. Wiley, New York. pp. 292.10.1002/0471725153Search in Google Scholar

Biegert, A., C. Mayer, M. Remmert, J. Söding and A. Lupas. 2006. The MPI Toolkit for protein sequence analysis. Nucleic Acids Res. 34: W335–W339.10.1093/nar/gkl217Search in Google Scholar PubMed PubMed Central

Bowen, B.W., L.A. Rocha, R.J. Toonen and S.A. Karl. 2013. The origins of tropical marine biodiversity. Trends Ecol. Evol. 28: 359–366.10.1016/j.tree.2013.01.018Search in Google Scholar PubMed

Brewer, M.T. and M.G. Milgroom. 2010. Phylogeography and population structure of the grape powdery mildew fungus, Erysiphe necator, from diverse Vitis species. BMC Evol. Biol. 10: 268.10.1186/1471-2148-10-268Search in Google Scholar PubMed PubMed Central

Brown, A.C., K. Nordstorm, A. McLachlan, N.L. Jackson and D.J. Sherman. 2008. Sandy shores of the near future. Aquatic Ecosystems. In: (N.V.C. Polunin, ed.) Trends and Global Prospects. Cambridge University Press, New York. pp. 263–280.10.1017/CBO9780511751790.024Search in Google Scholar

Caballero, H., G. Varona, Y. García. 2004. Estructura ecológica de las comunidades de corales de la costa oriental de Bahía de Cochinos, Cuba. Rev. Invest. Mar. 25: 23–36.Search in Google Scholar

Campbell, J., B. Volkmann-Kohlmeyer, T. Gräfenhan, J.W. Spatafora and J. Kohlmeyer. 2005. A reevaluation of Lulworthiales: relationships based on 18S and 28S rDNA. Mycol. Res. 109: 556–568.10.1017/S0953756205002716Search in Google Scholar

Carpenter, K.E., P.H. Barber, E.D. Crandall, M.C.A. Ablan-Lagman, Ambariyanto, G.N. Mahardika, B.M. Manjaji-Matsumoto, M.A. Juinio-Meñez, M.D. Santos, C.J. Starger and A.H.A. Toha. 2011. Comparative phylogeography of the Coral Triangle and implications for marine management. J. Mar. Biol.2011: 1–14.10.1155/2011/396982Search in Google Scholar

Carranza-Edwards, A. and M. Caso-Chávez. 1994. Zonificación del perfil de playa. Geo-UNAM 2: 26–32.Search in Google Scholar

Carriconde, F., H. Gryta, P. Jargeat, B. Mouhamadou and M. Gardes. 2008. High sexual reproduction and limited contemporary dispersal in the ectomycorrhizal fungus Tricholoma scalpturatum: new insights from population genetics and spatial autocorrelation analysis. Mol. Ecol. 17: 4433–4445.10.1111/j.1365-294X.2008.03924.xSearch in Google Scholar PubMed

Casteleyn, G., V.A. Chepurnov, F. Leliaert, D.G. Mann, S.S. Bates, N. Lundholm, L. Rhodes, K. Sabbe and W. Vyverman. 2008. Pseudo-nitzschia pungens (Bacillariophyceae): a cosmopolitan diatom species? Harmful Algae 7: 241–257.10.1016/j.hal.2007.08.004Search in Google Scholar

Chalkley, D.B., S.O. Suh, B. Volkmann-Kohlmeyer, J. Kohlmeyer and J.J. Zhou. 2010. Diatrypasimilis australiensis, a novel xylarialean fungus from mangrove. Mycologia 102: 430–437.10.3852/09-142Search in Google Scholar PubMed

Charlesworth, B. and D. Charlesworth. 2010. Elements of evolutionary genetics. Roberts and Company Publishers, Greenwood Village, CO. pp. 734.Search in Google Scholar

Choi, Y.W., K.D. Hyde and W.H. Ho. 1999. Single spore isolation of fungi. Fungal Divers. 3: 29–38.Search in Google Scholar

Crow, J. F. and M. Kimura. 1970. An introduction to population genetics theory. Harper and Row, New York. pp. 591.Search in Google Scholar

Darriba, D., G.L. Taboada, R. Doallo and D. Posada. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9: 772.10.1038/nmeth.2109Search in Google Scholar PubMed PubMed Central

Defeo, O., A. McLachlan, D.S. Schoeman, T.A. Schlacher, J. Dugan, A. Jones, M. Lastra and F. Scapini. 2009. Threats to sandy beach ecosystems: a review. Estuar. Coast. Shelf S. 81: 1–12.10.1016/j.ecss.2008.09.022Search in Google Scholar

Domaschke, S., F. Fernández-Mendoza, M.A. Garcia, M.P. Martín and C. Printzen. 2012. Low genetic diversity in Antarctic populations of the lichenforming ascomycete Cetraria aculeata and its photobiont. Polar Res. 31: 17353.10.3402/polar.v31i0.17353Search in Google Scholar

Douhan, G.W., L. Vincenot, H. Gryta and M.A. Selosse. 2011. Population genetics of ectomycorrhizal fungi: from current knowledge to emerging directions. Fungal Biol. 115: 569–597.10.1016/j.funbio.2011.03.005Search in Google Scholar PubMed

Doyle, J.J. and J.L. Doyle. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. 19: 11–15.Search in Google Scholar

Dray, S. and A.B. Dufour. 2007. The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw. 22: 1–20.10.18637/jss.v022.i04Search in Google Scholar

Durand, P. and F. Blanc. 1988. Genetic diversity in a tropical marine bivalve: Pinctada margaritifera (Linne, 1758). Bull. Soc. Zool. France 113: 293–304.Search in Google Scholar

Edgar, R.C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32: 1792–1797.10.1093/nar/gkh340Search in Google Scholar PubMed PubMed Central

Edwards, A.W.F. 1971. Distances between populations on the basis of gene frequencies. Biometrics. 27: 873–881.10.2307/2528824Search in Google Scholar

Ellstrand, N.C. and D.R. Elam. 1993. Population genetic consequences of small population size: implications for plant conservation. Annu. Rev. Ecol. Syst.24: 217–242.10.1146/annurev.es.24.110193.001245Search in Google Scholar

Ewens, W.J. 1990. The minimum viable population size as a genetic and a demographic concept. In: (J. Adams, D.A. Lam, A.I. Hermalin and P.E. Smouse, eds) Convergent issues in genetics and demography. Oxford University Press, New York. pp. 307–316.Search in Google Scholar

Ewing, B. and P. Green. 1998. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8: 186–194.10.1101/gr.8.3.186Search in Google Scholar

Ewing, B., L. Hillier, M. Wendl and P. Green. 1998. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8: 175–185.10.1101/gr.8.3.175Search in Google Scholar PubMed

Excoffier, L. and H.E. Lischer. 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Res. 10: 564–567.10.1111/j.1755-0998.2010.02847.xSearch in Google Scholar PubMed

Figueira, D. and M. Barata. 2007. Marine fungi on two sandy beaches. Mycologia 99: 20–23.10.1080/15572536.2007.11832596Search in Google Scholar

Fisher, R.A. 1930. The distribution of gene ratios for rare mutations. P. Roy. Soc. Edinb. 50: 205–220.10.1017/S0370164600044886Search in Google Scholar

González, M.C. and R.T. Hanlin. 2010. Potential use of marine arenicolous ascomycetes as bioindicators of ecosystem disturbance on sandy Cancun beaches: Corollospora maritima as a candidate species. Bot. Mar. 53: 577–580.10.1515/bot.2010.073Search in Google Scholar

González, M.C., T. Herrera, M. Ulloa and R.T. Hanlin. 1998. Abundance and diversity of microfungi in three coastal beaches of Mexico. Mycoscience 39: 115–121.10.1007/BF02464049Search in Google Scholar

Gordon, D., C. Desmarais and P. Green. 2001. Automated finishing with autofinish. Genome Res.11: 614–625.10.1101/gr.171401Search in Google Scholar PubMed PubMed Central

Grant, W.D., M. Atkinson, B. Burke and C. Molloy. 1996. Chitinolysis by the marine ascomycete Corollospora maritima Werdermann: purification and properties of a chitobiosidase. Bot. Mar. 39: 177–186.10.1515/botm.1996.39.1-6.177Search in Google Scholar

Graves, J.E. 1998. Molecular insights into the population structures of cosmopolitan marine fishes. J. Hered. 89: 427–437.10.1093/jhered/89.5.427Search in Google Scholar

Gray, J.S. 1997. Marine biodiversity: patterns, threats and conservation needs. Biodivers. Conserv. 6: 153–175.10.1023/A:1018335901847Search in Google Scholar

Hedrick, P.W. 2011. Genetics of populations. 4th Edition. Jones & Bartlett Learning, Massachusetts. pp. 675.Search in Google Scholar

Hendrickx, J. 2012. perturb: Tools for evaluating collinearity. R package version 2.05. http://CRAN.R-project.org/package=perturb.Search in Google Scholar

Hijmans, R.J., S.E. Cameron, J.L. Parra, P.G. Jones and A. Jarvis. 2005. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25: 1965–1978.10.1002/joc.1276Search in Google Scholar

Hosoya, T., D. Hirose, M. Fujisaki, T. Osono, T. Kubono, S. Tokumasu and M. Kakishima. 2010. Internal transcribed spacer haplotype diversity and their geographical distribution in Dasyscyphella longistipitata (Hyaloscyphaceae, Helotiales) occurring on Fagus crenata cupules in Japan. Mycoscience 51: 116–122.10.1007/S10267-009-0020-4Search in Google Scholar

Husson, F., J. Josse, S. Le and J. Mazet. 2016. FactoMineR: Multivariate Exploratory Data Analysis and Data Mining. R package version 1.31.5. http://CRAN.R-project.org/package=FactoMineR.Search in Google Scholar

Inderbitzin, P., J. Kohlmeyer, B. Volkmann-Kohlmeyer and M.L. Berbee. 2002. Decorospora, a new genus for the marine ascomycetes Pleospora gaudefroyi. Mycologia 91: 651–659.10.2307/3761716Search in Google Scholar

Inderbitzin, P., S.R. Lim, B. Volkmann-Kohlmeyer, J. Kohlmeyer and M.L. Berbee. 2004. The phylogenetic position of Spathulospora based on DNA sequences from dried herbarium material. Mycol. Res. 108: 737–748.10.1017/S0953756204000206Search in Google Scholar

James, T.Y., D. Porter, J.L. Hamrick and R. Vilgalys. 1999. Evidence for limited intercontinental gene flow in the Cosmopolitan mushroom, Schizophyllum commune. Evolution 53: 1665–1677.10.1111/j.1558-5646.1999.tb04552.xSearch in Google Scholar PubMed

Jombart, T. and I. Ahmed. 2011. adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27: 3070–3071.10.1093/bioinformatics/btr521Search in Google Scholar PubMed PubMed Central

Jones, E.B.G. 2000. Marine fungi. Some factors influencing biodiversity. Fungal Divers. 4: 53–73.Search in Google Scholar

Jones, E.B.G., A. Pilantanapak, I. Chatmala, J. Sakayaroj, S. Phongpaichit and R. Choeyklin. 2006. Thai marine fungal diversity. Songklankarin J. Sci. Technol. 28: 687–708.Search in Google Scholar

Jones, E.B.G., J. Sakayaroj, S. Suetrong, S. Somrithipol and K.L. Pang. 2009. Classification of marine Ascomycota, anamorphic taxa and Basidiomycota. Fungal Divers. 35: 1–187.Search in Google Scholar

Jones, E.B.G., S. Suetrong, J. Sakayaroj, A.H. Bahkali, M.A. Abdel-Wahab, T. Boekhout and K.L. Pang. 2015. Classification of marine Ascomycota, Basidiomycota, Blastocladiomycota and Chytridiomycota. Fungal Divers. 73: 1–72.10.1007/s13225-015-0339-4Search in Google Scholar

Kirk, P.W. and A.S. Gordon. 1988. Hydrocarbon degradation by filamentous marine higher fungi. Mycologia 80: 776–782.10.2307/3807554Search in Google Scholar

Kirk, P.W., B.J. Dyer and J. Noé. 1991. Hydrocarbon utilization by higher marine fungi from diverse habitats and localities. Mycologia 83: 227–230.10.2307/3759940Search in Google Scholar

Kohlmeyer, J. 1968. Marine fungi from the tropics. Mycologia 60: 252–270.10.2307/3757156Search in Google Scholar

Kohlmeyer, J. 1983. Geography of marine fungi. Aust. J. Bot. Suppl. 13, 67–76.Search in Google Scholar

Kohlmeyer, J. and T.M. Charles. 1981. Sclerocarps: undescribed propagules in a sand-inhabiting marine fungus. Can. J. Bot. 59: 1787–1791.10.1139/b81-238Search in Google Scholar

Kohlmeyer, J. and E. Kohlmeyer. 1979. Marine Mycology: The Higher Fungi. Academic Press, New York. pp. 685.Search in Google Scholar

Kohlmeyer, J. and B. Volkmann-Kohlmeyer. 1991. Illustrated key to the filamentous higher marine fungi. Bot. Mar. 34: 1–61.10.1515/botm.1991.34.1.1Search in Google Scholar

Kohlmeyer, J., J.W. Spatafora and B. Volkmann-Kohlmeyer. 2000. Lulworthiales, a new order of marine Ascomycota. Mycologia 92: 453–458.10.2307/3761504Search in Google Scholar

Kriticos, D.J., B.L. Webber, A. Leriche, N. Ota, I. Macadam, J. Bathols and J.K. Scott. 2012. CliMond: global high resolution historical and future scenario climate surfaces for bioclimatic modelling. Methods Ecol. Evol. 3: 53–64.10.1111/j.2041-210X.2011.00134.xSearch in Google Scholar

Legendre, P. and L. Legendre. 2012. Numerical Ecology. 3rd Edition. Elsevier, Amsterdam. pp. 1006.Search in Google Scholar

Lewontin, R.C. 1991. Twenty-five years ago in Genetics: electrophoresis in the development of evolutionary genetics: milestone or millstone? Genetics 128: 657–662.10.1093/genetics/128.4.657Search in Google Scholar PubMed PubMed Central

Liberra, K., R. Jansen and U. Lindequist. 1998. Corollosporine, a new phthalide derivative from the marine fungus Corollospora maritima Werderm. 1069. Pharmazie 53: 578–581.10.1002/chin.199847275Search in Google Scholar

Librado, P. and J. Rozas. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452.10.1093/bioinformatics/btp187Search in Google Scholar PubMed

Lindblom, L. and S. Ekman. 2006. Genetic variation and population differentiation in the lichen-forming ascomycete Xanthoria parietina on the island Storfosna, central Norway. Mol. Ecol. 15: 1545–1559.10.1111/j.1365-294X.2006.02880.xSearch in Google Scholar PubMed

McLachlan, A. and A.C. Brown. 2006. The Ecology of Sandy Shores. 2nd edition. Academic Press, Massachusetts. pp. 373.Search in Google Scholar

Michaelis, K.C., R.V. Gessner and M.A. Romano. 1987. Population genetics and systematics of marine species of Dendryphiella.Mycologia 79: 514–518.10.2307/3807589Search in Google Scholar

Millberg, H., J. Boberg and J. Stenlid. 2015. Changes in fungal community of Scots pine (Pinus sylvestris) needles along a latitudinal gradient in Sweden. Fungal Ecol. 17: 126–139.10.1016/j.funeco.2015.05.012Search in Google Scholar

Murphy, S. J., H.E. Hurlburt, J.J. O’Brien. 1999. The connectivity of eddy variability in the Caribbean Sea, the Gulf of Mexico, and the Atlantic Ocean. J. Geophys. Res. 104: 1431–1453.10.1029/1998JC900010Search in Google Scholar

Murtagh, F. and P. Legendre. 2014. Ward’s hierarchical agglomerative clustering method: which algorithms implement Ward’s criterion? J. Classif. 3: 274–295.10.1007/s00357-014-9161-zSearch in Google Scholar

Nagy, L. G., S. Kocsubé, Z. Csanádi, G.M. Kovács, T. Petkovits, C. Vágvölgyi and T. Papp. 2012. Re-mind the gap! insertion–deletion data reveal neglected phylogenetic potential of the nuclear ribosomal internal transcribed spacer (ITS) of fungi. PLoS One 7: e49794.10.1371/journal.pone.0049794Search in Google Scholar PubMed PubMed Central

Nei, M. 1972. Genetic distance between populations. Am. Nat. 106: 283–292.10.1086/282771Search in Google Scholar

Nei, M. 1978. Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 23: 341–369.10.1093/genetics/89.3.583Search in Google Scholar PubMed PubMed Central

Nevo, E., A. Beiles and R. Ben-Shlomo. 1984. The evolutionary significance of genetic diversity: ecological, demographic and life history correlates. In: (G.S. Mani, ed) Evolutionary dynamics of genetic diversity. Lecture notes in biomathematics. Springer-Verlag, New York. pp. 13–213.10.1007/978-3-642-51588-0_2Search in Google Scholar

Ngamskulrungroj, P., F. Gilgado, J. Faganello, A.P. Litvintseva, A.L. Leal, K.M. Tsui, T.G. Mitchell, M.H. Vainstein and W. Meyer. 2009. Genetic diversity of the Cryptococcus species complex suggests that Cryptococcus gattii deserves to have varieties. PLoS One 4: e5862.10.1371/journal.pone.0005862Search in Google Scholar PubMed PubMed Central

Oksanen, J., F., G. Blanchet, R. Kindt, P. Legendre, P.R. Minchin, R.B. O’Hara, G.L. Simpson, P. Solymos, M. Henry, H. Stevens and H. Wagner. 2015. vegan: Community Ecology Package. R package version 2.3-1. http://CRAN.R-project.org/package=vegan.Search in Google Scholar

Pang, K.L., J.S. Jheng and E.B.G. Jones. 2011. Marine mangrove fungi of Taiwan. National Taiwan Ocean University Press, Taiwan. pp. 131.Search in Google Scholar

Pang, K.L., L.L. Vrijmoed and E.B.G. Jones. 2013. Genetic variation within the cosmopolitan aquatic fungus Lignincola laevis (Microascales, Ascomycota). Org. Divers. Evol.13: 301–309.10.1007/s13127-013-0132-8Search in Google Scholar

Pantoja, D.A., S.G. Marinone, A. Parés-Sierra and F. Gómez-Valdivia. 2012. Numerical modeling of seasonal and mesoscale hydrography and circulation in the Mexican Central Pacific. Cienc. Mar. 38: 363–379.10.7773/cm.v38i2.2007Search in Google Scholar

Pugh, G.J.F. and E.B.G. Jones. 1986. Antarctic marine fungi, a preliminary account. In: (S.T. Moss, ed) The biology of marine fungi. Cambridge University Press, Cambridge. pp. 323–330.Search in Google Scholar

R Core Team. 2015. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.Search in Google Scholar

Rämä, T., J. Nordén, M.L. Davey, G.H. Mathiassen, J.W. Spatafora and H. Kauserud. 2014. Fungi ahoy! Diversity on marine wooden substrata in the high North. Fungal Ecol. 8: 46–58.10.1016/j.funeco.2013.12.002Search in Google Scholar

Rambaut, A. 2009. FigTree v1. 3.1: Tree figure drawing tool. http://tree.bio.ed.ac.uk/software/figtree.Search in Google Scholar

Ratcliff, W.C., R.F. Denison, M. Borrello and M. Travisano. 2012. Experimental evolution of multicellularity. Proc. Natl. Acad. Sci. USA109: 1595–1600.10.1073/pnas.1115323109Search in Google Scholar

Ray, G.C. 1991. Coastal-zone biodiversity patterns. Bioscience 41: 490–498.10.2307/1311807Search in Google Scholar

Roberts, C.M. and J.P. Hawkins. 1999. Extinction risk in the sea. Trends Ecol. Evol. 14: 241–246.10.1016/S0169-5347(98)01584-5Search in Google Scholar

Roberts, P.L., J.I. Mitchell, S.T. Moss and E.B.G. Jones. 1995. Morphological and molecular taxonomy of marine ascomycetes: Corollospora. In: (L. Rossen, V. Rubio, M.T. Dawson and J. Frisvad, eds) Abstracts. VI. International marine mycology symposium. Office for Official Publications of the European Communities, Luxembourg. pp. 103–109.Search in Google Scholar

Ronquist, F., M. Teslenko, P. van der Mark, D. L. Ayres, A. Darling, S. Höhna and J. P. Huelsenbeck. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61: 539–542.10.1093/sysbio/sys029Search in Google Scholar PubMed PubMed Central

Rosales-Hoz, L., A. Carranza-Edwards, S. Santiago-Pérez, C. Méndez-Jaime, R. Doger-Badillo. 1994. Study of anthropogenically induced trace metals on the continental shelf in the southeastern part of the Gulf of Mexico. Rev. Int. Contam. Ambie.10: 9–13.Search in Google Scholar

Rosendahl, S., P. Mcgee and J.B. Morton. 2009. Lack of global population genetic differentiation in the arbuscular mycorrhizal fungus Glomus mosseae suggests a recent range expansion which may have coincided with the spread of agriculture. Mol. Ecol. 18: 4316–4329.10.1111/j.1365-294X.2009.04359.xSearch in Google Scholar PubMed

Rydholm, C., G. Szakacs and F. Lutzoni. 2006. Low genetic variation and no detectable population structure in Aspergillus fumigatus compared to closely related Neosartorya species. Eukaryot. Cell 5: 650–657.10.1128/EC.5.4.650-657.2006Search in Google Scholar PubMed PubMed Central

Schlacher, T.A. and R.M. Connolly. 2009. Land-ocean coupling of carbon and nitrogen fluxes on sandy beaches. Ecosystems 12: 311–321.10.1007/s10021-008-9224-2Search in Google Scholar

Schlacher, T.A., D.S. Schoeman, M. Lastra, A. Jones, J. Dugan, F. Scapini and A. McLachlan. 2006. Neglected ecosystems bear the brunt of change. Ethol. Ecol. Evol. 18: 349–351.10.1080/08927014.2006.9522701Search in Google Scholar

Schoch, C.L., G.H. Sung, B. Volkmann-Kohlmeyer, J. Kohlmeyer and J.W. Spatafora. 2007. Marine fungal lineages in the Hypocreomycetidae. Mycol. Res. 111: 154–162.10.1016/j.mycres.2006.10.005Search in Google Scholar PubMed

Solé-Cava, A.M., M. Klautau, N. Boury-Esnault, R. Borojecic and J.P. Thorpe. 1991. Genetic evidence for cryptic speciation in allopatric populations of two cosmopolitan species of the calcareous sponge genus Clathrina. Mar. Biol. 111: 381–386.10.1007/BF01319410Search in Google Scholar

Spatafora, J.W., B. Volkmann-Kohlmeyer and J. Kohlmeyer. 1998. Independent terrestrial origins of the Halosphaeriales (marine Ascomycota). Am. J. Bot. 85: 1569–1580.10.2307/2446483Search in Google Scholar

Stoeck, T. and S. Epstein. 2003. Novel eukaryotic lineages inferred from small-subunit rRNA analyses of oxygen depleted marine environments. Appl. Environ. Microb. 69: 2657–2663.10.1128/AEM.69.5.2657-2663.2003Search in Google Scholar PubMed PubMed Central

Tamura, K. and M. Nei. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10: 512–526.Search in Google Scholar

Teacher, A.G.F. and D.J. Griffiths. 2011. HapStar: Automated haplotype network layout and visualisation. Mol. Ecol. Res. 11: 151–153.10.1111/j.1755-0998.2010.02890.xSearch in Google Scholar PubMed

Ter Braak, C.J.F. 1986. Canonical correspondence analysis: a new Eigenvector technique for multivariate direct gradient analysis. Ecology 67: 1167–1179.10.2307/1938672Search in Google Scholar

Velez, P., M.C. González, E. Rosique-Gil, J. Cifuentes, M.R. Reyes-Montes, S. Capello-García and R.T. Hanlin. 2013. Community structure and diversity of marine ascomycetes from coastal beaches of the southern Gulf of Mexico. Fungal Ecol. 6: 513–521.10.1016/j.funeco.2013.10.002Search in Google Scholar

Velez, P., N.D. Alejandri-Ramírez, M.C. González, K.J. Estrada, A. Sanchez-Flores and T.D. Dinkova. 2015a. Comparative transcriptome analysis of the cosmopolitan marine fungus Corollospora maritima under two physiological conditions. G3-Genes Genom. Genet. 5: 1805–1814.10.1534/g3.115.019620Search in Google Scholar PubMed PubMed Central

Velez, P., M.C. González, S. Capello-García, E. Rosique-Gil, R.T. Hanlin. 2015b. Diversity of marine ascomycetes from the disturbed sandy beaches of Tabasco, Mexico. J. Mar. Biol. Assoc. UK 95: 897–903.10.1017/S0025315414002112Search in Google Scholar

Velez, P., C.A. Quintero, G. Merino, J. Gasca-Pineda, M.C. González. 2016. An ISSR-based approach to assess genetic diversity in the marine arenicolous fungus Corollospora maritima sensu lato. Mycoscience. 57: 187–195.10.1016/j.myc.2016.01.002Search in Google Scholar

Volkmann-Kohlmeyer, B. and J. Kohlmeyer. 1993. Biogeographic observations on Pacific marine fungi. Mycologia 85: 337–346.10.2307/3760692Search in Google Scholar

Ward, R.D., M. Woodwark and D.O.F. Skibinski. 1994. A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes. J. Fish. Biol. 44: 213–32.10.1111/j.1095-8649.1994.tb01200.xSearch in Google Scholar

Werdermann, E. 1922. Corollospora maritima Werd., ein salzliebender Pilz von der Nordseeküste. Notizbl. Bot. Gart. Berlin-Dahlem 73: 248–250.Search in Google Scholar

White, T.J., T. Bruns, S. Lee and J. Taylor. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: (M.A. Innis, D.H. Gelfand, J.J. Sninsky and T.J. White, eds.) PCR protocols: a guide to methods and applications. Academic Press, New York. pp. 315–322.10.1016/B978-0-12-372180-8.50042-1Search in Google Scholar

Wood, A.M. 1989. Population genetic studies of algae. J. Phycol. 25: 11.Search in Google Scholar

Wright, S. 1931. Evolution in Mendelian populations. Genetics 16: 97–159.10.1093/genetics/16.2.97Search in Google Scholar PubMed PubMed Central

Zhang, Y., L. Xu, S. Zhang, X. Liu, Z. An, M. Wang and Y. Guo. 2009. Genetic diversity of Ophiocordyceps sinensis, a medicinal fungus endemic to the Tibetan Plateau: implications for its evolution and conservation. BMC Evol. Biol. 9: 290.10.1186/1471-2148-9-290Search in Google Scholar PubMed PubMed Central

Zuccaro, A., C.L. Schoch, J.W. Spatafora, J. Kohlmeyer, S. Draeger and J.I. Mitchel. 2008. Detection and identification of fungi intimately associated with the brown seaweed Fucus serratus. Appl. Environ. Microbiol. 74: 931–941.10.1128/AEM.01158-07Search in Google Scholar PubMed PubMed Central


Supplemental Material:

The online version of this article (DOI: 10.1515/bot-2016-0058) offers supplementary material, available to authorized users.


Received: 2016-6-22
Accepted: 2016-8-24
Published Online: 2016-9-26
Published in Print: 2016-10-1

©2016 Walter de Gruyter GmbH, Berlin/Boston

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