Advertisement

Organisms Diversity & Evolution

, Volume 12, Issue 1, pp 17–37 | Cite as

Using haplotype networks, estimation of gene flow and phenotypic characters to understand species delimitation in fungi of a predominantly Antarctic Usnea group (Ascomycota, Parmeliaceae)

  • Nora Wirtz
  • Christian Printzen
  • H. Thorsten LumbschEmail author
Original Article

Abstract

Species delimitations in the predominantly Antarctic and South American group of neuropogonoid species of the lichen-forming fungal genus Usnea are poorly understood. Morphological variability has been interpreted as a result of harsh ecological conditions, but preliminary molecular data have led to doubts about the current species delimitations in these lichenized fungi. We examined species boundaries using a phylogenetic approach and a cohesion species recognition method generating haplotype networks and looking at associations of phenotypic characters with clades found in the networks. In addition, we estimated gene flow among detected clades and currently circumscribed species. We identified several clades that were significantly associated with phenotypic characters, but did not necessarily agree with current species circumscriptions. In one case (U. aurantiaco-atra/U. antarctica), network analysis and the estimation of gene flow provided no evidence of distinct species. The distinctness of another species pair (U. subantarctica/U. trachycarpa) remains dubious, showing evidence for gene flow among currently accepted species.

Keywords

Lichens Usnea Species delimitation Cohesion species 

Notes

Acknowledgments

The authors would like to thank all colleagues who provided fresh lichen material for this study. N,W, is indebted to María Inés Messuti, Andrés Diehl and Gernot Vobis (all S.C. de Bariloche, Argentina) for organizing and performing a field trip to Tierra del Fuego. N.W. and H.T.L. are grateful to Asuncion Cano and Angel Ramirez (Lima) for organizing and conducting a field trip to Huascaran NP in Peru and to the Women’s Board of the Field Museum in Chicago for financially supporting the trip. Most of the laboratory work was done at the Pritzker Laboratory for Molecular Systematics at the Field Museum. Financial support for this project was allocated by the Deutsche Forschungsgemeinschaft (DFG grant to H.T.L. and C.P.), the National Science Foundation (DEB-0949147, PI: HTL), a scholarship of the DAAD (German Exchange Service) to N.W., and a grant of the Women’s Board of the Field Museum.

Supplementary material

13127_2011_66_MOESM1_ESM.doc (580 kb)
ESM 1 (DOC 580 kb)

References

  1. Ané, C., Larget, B., Baum, D. A., Smith, S. D., & Rokas, A. (2007). Bayesian estimation of concordance among gene trees. Molecular Biology and Evolution, 24, 412–426.PubMedCrossRefGoogle Scholar
  2. Argüello, A., del Prado, R., Cubas, P., & Crespo, A. (2007). Parmelina quercina (Parmeliaceae, Lecanorales) includes four phylogenetically supported morphospecies. Biological Journal of the Linnean Society, 91, 455–467.CrossRefGoogle Scholar
  3. Articus, K., Mattsson, J. E., Tibell, L., Grube, M., & Wedin, M. (2002). Ribosomal DNA and beta-tubulin data do not support the separation of the lichens Usnea florida and U-subfloridana as distinct species. Mycological Research, 106, 412–418.CrossRefGoogle Scholar
  4. Avise, J. C., & Ball, R. M. (1990). Principles of genealogical concordance in species concepts and biological taxonomy. Oxford Surveys in Evolutionary Biology, 7, 45–67.Google Scholar
  5. Buschbom, J., & Barker, D. (2006). Evolutionary history of vegetative reproduction in Porpidia s. l. (lichen-forming ascomycota). Systematic Biology, 55, 471–484.PubMedCrossRefGoogle Scholar
  6. Buschbom, J., & Mueller, G. M. (2006). Testing "species pair" hypotheses: evolutionary processes in the lichen-forming species complex Porpidia flavocoerulescens and Porpidia melinodes. Molecular Biology and Evolution, 23, 574–586.PubMedCrossRefGoogle Scholar
  7. Clement, M., Posada, D., & Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology, 9, 1657–1659.PubMedCrossRefGoogle Scholar
  8. Clerc, P. (1984). Contribution a la revision de la systematique des usnees (Ascomycotina, Usnea) d'Europe I.--Usnea florida (L.) Wigg. emend. Clerc. Cryptogamie. Bryologie et Lichenologie, 5, 333–360.Google Scholar
  9. Clerc, P. (1998). Species concepts in the genus Usnea (lichenized Ascomycetes). The Lichenologist, 30, 321–340.Google Scholar
  10. Coyne, J. A., & Orr, H. A. (2004). Speciation. Sunderland: Sinauer Associates.Google Scholar
  11. Crandall, K. (1996). Multiple interspecies transmissions of human and simian T-cell leukemia/lymphoma virus type I sequences. Molecular Biology and Evolution, 13, 115–131.PubMedGoogle Scholar
  12. Crespo, A., & Lumbsch, H. T. (2010). Cryptic species in lichen-forming fungi. IMA Fungus, 1, 167–170.CrossRefGoogle Scholar
  13. Crespo, A., & Perez-Ortega, S. (2009). Cryptic species and species pairs in lichens: a discussion on the relationship between molecular phylogenies and morphological characters. Anales del Jardin Botánico de Madrid, 66, 71–81.CrossRefGoogle Scholar
  14. Cubero, O. F., Crespo, A., Esslinger, T. L., & Lumbsch, H. T. (2004). Molecular phylogeny of the genus Physconia (Ascomycota, Lecanorales) inferred from a Bayesian analysis of nuclear ITS rDNA sequences. Mycological Research, 108, 498–505.PubMedCrossRefGoogle Scholar
  15. de Queiroz, K. (2007). Species concepts and species delimitation. Systematic Biology, 56, 879–886.PubMedCrossRefGoogle Scholar
  16. Dettman, J. R., Jacobson, D. J., & Taylor, J. W. (2003). A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Evolution, 57, 2703–2720.PubMedGoogle Scholar
  17. Dettman, J. R., Jacobson, D. J., Turner, E., Pringle, A., & Taylor, J. W. (2003). Reproductive isolation and phylogenetic divergence in Neurospora: comparing methods of species recognition in a model eukaryote. Evolution, 57, 2721–2741.PubMedGoogle Scholar
  18. Dettman, J. R., Jacobson, D. J., & Taylor, J. W. (2006). Multilocus sequence data reveal extensive phylogenetic species diversity within the Neurospora discreta complex. Mycologia, 98, 436–446.PubMedCrossRefGoogle Scholar
  19. Divakar, P. K., Molina, M. C., Lumbsch, H. T., & Crespo, A. (2005). Parmelia barrenoae, a new lichen species related to Parmelia sulcata (Parmeliaceae) based on molecular and morphological data. The Lichenologist, 37, 37–46.CrossRefGoogle Scholar
  20. Dodge, C. W. (1973). Lichen flora of the Antarctic continent and adjacent islands. New Hampshire: Canaan.Google Scholar
  21. Elix, J. A., Wirtz, N., & Lumbsch, H. T. (2007). Studies on the chemistry of some Usnea species of the Neuropogon group (Lecanorales, Ascomycota). Nova Hedwigia, 85, 491–501.CrossRefGoogle Scholar
  22. Farris, J. S., Källersjö, M., Kluge, A. G., & Bult, C. (1994). Testing significance of incongruence. Cladistics, 10, 315–319.CrossRefGoogle Scholar
  23. Farris, J. S., Källersjö, M., Kluge, A. G., & Bult, C. (1995). Constructing a significance test for incongruence. Systematic Biology, 44, 570–572.Google Scholar
  24. Fisher, M. C., Koenig, G., White, T. J., & Taylor, J. W. (2000). A test for concordance between the multilocus genealogies of genes and microsatellites in the pathogenic fungus Coccidioides immitis. Molecular Biology and Evolution, 17, 1164–1174.PubMedGoogle Scholar
  25. Funk, D. J., & Omland, K. E. (2003). Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annual Review of Ecology, Evolution, and Systematics, 34, 397–423.CrossRefGoogle Scholar
  26. Geiser, D. M., Pitt, J. I., & Taylor, J. W. (1998). Cryptic speciation and recombination in the aflatoxin-producing fungus Aspergillus flavus. Proceedings of the National Academy of Sciences of the United States of America, 95, 388–393.PubMedCrossRefGoogle Scholar
  27. Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.Google Scholar
  28. Heled, J., & Drummond, A. J. (2009). Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution, 27, 570–580.PubMedCrossRefGoogle Scholar
  29. Hey, J., & Wakeley, J. (1997). A coalescent estimator of the population recombination rate. Genetics, 145, 833–846.PubMedGoogle Scholar
  30. Hird, S., Kubatko, L., & Carstens, B. (2010). Rapid and accurate species tree estimation for phylogeographic investigations using replicated subsampling. Molecular Phylogenetics and Evolution, 57, 888–898.PubMedCrossRefGoogle Scholar
  31. Honegger, R., & Zippler, U. (2007). Mating systems in representatives of Parmeliaceae, Ramalinaceae and Physciaceae (Lecanoromycetes, lichen-forming ascomycetes). Mycological Research, 111, 424–432.PubMedCrossRefGoogle Scholar
  32. Honegger, R., Zippler, U., Gansner, H., & Scherrer, S. (2004). Mating systems in the genus Xanthoria (lichen-forming ascomycetes). Mycological Research, 108, 480–488.PubMedCrossRefGoogle Scholar
  33. Hudson, R. R., & Coyne, J. A. (2002). Mathematical consequences of the genealogical species concept. Evolution, 56, 1557–1565.PubMedGoogle Scholar
  34. Hudson, R. R., Slatkin, M., & Maddison, W. P. (1992). Estimation of levels of gene flow fom DNA sequence data. Genetics, 132, 583–589.PubMedGoogle Scholar
  35. Huelsenbeck, J. P., & Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755.PubMedCrossRefGoogle Scholar
  36. Kasuga, T., White, T. J., Koenig, G., McEwen, J., Restrepo, A., Castaneda, E., Lacaz, C. D., Heins-Vaccari, E. M., De Freitas, R. S., Zancope-Oliveira, R. M., Qin, Z. Y., Negroni, R., Carter, D. A., Mikami, Y., Tamura, M., Taylor, M. L., Miller, G. F., Poonwan, N., & Taylor, J. W. (2003). Phylogeography of the fungal pathogen Histoplasma capsulatum. Molecular Ecology, 12, 3383–3401.PubMedCrossRefGoogle Scholar
  37. Kliman, R. M., Andolfatto, P., Coyne, J. A., Depaulis, F., Kreitman, M., Berry, A. J., McCarter, J., Wakeley, J., & Hey, J. (2000). The population genetics of the origin and divergence of the Drosophila simulans complex species. Genetics, 156, 1913–1931.PubMedGoogle Scholar
  38. Kroken, S., & Taylor, J. W. (2001). A gene genealogical approach to recognize phylogenetic species boundaries in the lichenized fungus Letharia. Mycologia, 93, 38–53.CrossRefGoogle Scholar
  39. Kubatko, L. S., Carstens, B. C., & Knowles, L. L. (2009). STEM: species tree estimation using maximum likelihood for gene trees under coalescence. Bioinformatics, 25, 971–973.PubMedCrossRefGoogle Scholar
  40. Lamb, I. M. (1939). A review of the genus Neuropogon (Nees & Flot.) Nyl., with special reference to the antarctic species. Journal of the Linnean Society (Botany), 52, 199–237.Google Scholar
  41. Lange, O. L. (1992). Pflanzenleben unter Stress. Flechten als Pioniere der Vegetation an Extremstandorten der Erde. Würzburg: Rostra Universitatis Wirceburgensis.Google Scholar
  42. Liu, L., & Pearl, D. K. (2007). Species trees from gene trees: reconstructing Bayesian posterior distributions of a species phylogeny using estimated gene tree distributions. Systematic Biology, 56, 504–514.PubMedCrossRefGoogle Scholar
  43. Liu, L., Yu, L. L., Pearl, D. K., & Edwards, S. (2009). Estimating species phylogenies using coalescence times among sequences. Systematic Biology, 58, 468–477.PubMedCrossRefGoogle Scholar
  44. Lohse, K. (2009). Can mtDNA barcodes be used to delimit species? A response to Pons et al. (2006). Systematic Biology, 58, 439–442.PubMedCrossRefGoogle Scholar
  45. Lohtander, K., Myllys, L., Sundin, R., Kallersjo, M., & Tehler, A. (1998). The species pair concept in the lichen Dendrographa leucophaea (Arthoniales): analyses based on ITS sequences. Bryologist, 101, 404–411.Google Scholar
  46. Lumbsch, H. T., & Leavitt, S. D. (2011). Goodbye morphology? A paradigm shift in the delimitation of species in lichenized fungi. Fungal Diversity, 50, 59–72.CrossRefGoogle Scholar
  47. Lumbsch, H. T., & Wirtz, N. (2011). Phylogenetic relationships of the neuropogonoid core group in the genus Usnea (Ascomycota, Parmeliaceae). The Lichenologist, 43, 553–559.CrossRefGoogle Scholar
  48. Lutzoni, F., Kauff, F., Cox, C., McLaughlin, D., Celio, G., Dentinger, B., Padamsee, M., Hibbett, D., James, T. Y., Baloch, E., Grube, M., Reeb, V., Hofstetter, V., Schoch, C., Arnold, A. E., Miadlikowska, J., Spatafora, J., Johnson, D., Hambleton, S., Crockett, M., Shoemaker, R., Sung, G.-H., Lücking, R., Lumbsch, H. T., O'Donnell, K., Binder, M., Diederich, P., Ertz, D., Gueidan, C., Hansen, K., Harris, R. C., Hosaka, K., Lim, Y.-W., Matheny, B., Nishida, H., Pfister, D., Rogers, J., Rossman, A., Schmitt, I., Sipman, H., Stone, J., Sugiyama, J., Yahr, R., & Vilgalys, R. (2004). Assembling the fungal tree of life: progress, classification, and evolution of subcellular traits. American Journal of Botany, 91, 1446–1480.PubMedCrossRefGoogle Scholar
  49. Mattsson, J. E., & Lumbsch, H. T. (1989). The use of the species pair concept in lichen taxonomy. Taxon, 38, 238–241.CrossRefGoogle Scholar
  50. Molina, M. C., Crespo, A., Blanco, O., Hladun, N., & Hawksworth, D. L. (2002). Molecular phylogeny and status of Diploicia and Diplotomma, with observations on Diploicia subcanescens and Diplotomma rivas-martinezii. The Lichenologist, 34, 509–519.CrossRefGoogle Scholar
  51. Molina, M. C., Crespo, A., Blanco, O., Lumbsch, H. T., & Hawksworth, D. L. (2004). Phylogenetic relationships and species concepts in Parmelia s. str. (Parmeliaceae) inferred from nuclear ITS rDNA and β-tubulin sequences. The Lichenologist, 36, 37–54.CrossRefGoogle Scholar
  52. Motyka, J. (1936–1938). Lichenum generis Usnea studium monographicum, pars systematica. 2 vols., Lviv.Google Scholar
  53. Murtagh, G. J., Dyer, P. S., & Crittenden, P. D. (2000). Sex and the single lichen. Nature, 404, 564.PubMedCrossRefGoogle Scholar
  54. Myllys, L., Lohtander, K., Källersjö, M., & Tehler, A. (1999). Sequence insertions and ITS data provide congruent information on Roccella canariensis and R. tuberculata (Arthoniales, Euascomycetes) Phylogeny. Molecular Phylogenetics and Evolution, 12, 295–309.PubMedCrossRefGoogle Scholar
  55. Myllys, L., Lohtander, K., & Tehler, A. (2001). beta-tubulin, ITS and group I intron sequences challenge the species pair concept in Physcia aipolia and P. caesia. Mycologia, 93, 335–343.CrossRefGoogle Scholar
  56. Myllys, L., Stenroos, S., Thell, A., & Ahti, T. (2003). Phylogeny of bipolar Cladonia arbuscula and Cladonia mitis (Lecanorales, Euascomycetes). Molecular Phylogenetics and Evolution, 27, 58–69.PubMedCrossRefGoogle Scholar
  57. Nei, M. (1987). Molecular evolutionary genetics. New York: Columbia University Press.Google Scholar
  58. Nylander, J. A. A., Wilgenbusch, J. C., Warren, D. L., & Swofford, D. L. (2008). AWTY (are we there yet?): a system for graphical exploration of MCMC convergence in Bayesian phylogenetics. Bioinformatics, 24, 581–583.PubMedCrossRefGoogle Scholar
  59. O’Donnell, K., Ward, T. J., Geiser, D. M., Kistler, H. C., & Aoki, T. (2004). Genealogical concordance between the mating type locus and seven other nuclear genes support formal recognition of nine phylogenetically distinct species within the Fusarium graminearum clade. Fungal Genetics and Biology, 41, 600–623.PubMedCrossRefGoogle Scholar
  60. Ohmura, Y. (2001). Taxonomic study of the genus Usnea (lichenized Ascomycetes) in Japan and Taiwan. Journal of the Hattori Botanical Laboratory, 90, 1–96.Google Scholar
  61. Ott, S., Brinkmann, M., Wirtz, N., & Lumbsch, H. T. (2004). Mitochondrial and nuclear ribosomal DNA data do not support the separation of the Antarctic lichens Umbilicaria kappenii and Umbilicaria antarctica as distinct species. The Lichenologist, 36, 227–234.CrossRefGoogle Scholar
  62. Øvstedal, D. O., & Lewis Smith, R. I. (2001). Lichens of Antarctica and South Georgia: A guide to their identification and ecology. Studies in Polar Research. Cambridge: Cambridge University Press.Google Scholar
  63. Pfenninger, M., & Posada, D. (2002). Phylogeographic history of the land snail Candidula unifasciata (Helicellinae, Stylommatophora): fragmentation, corridor migration, and secondary contact. Evolution, 56, 1776–1788.PubMedGoogle Scholar
  64. Poelt, J. (1970). Das Konzept der Artenpaare bei den Flechten. Vorträge aus dem Gesamtgebiet der Botanik, Neue Folge [Deutsche Botanische Gesellschaft], 4, 187–198.Google Scholar
  65. Poelt, J. (1972). Die taxonomische Behandlung von Artenpaaren bei den Flechten. Botaniska Notiser, 125, 77–81.Google Scholar
  66. Pons, J., Barraclough, T. G., Gómez-Zurita, J., Cardoso, A., Duran, D. P., Hazell, S., Kamoun, S., Sumlin, W. D., & Vogler, A. P. (2006). Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology, 55, 595–609.PubMedCrossRefGoogle Scholar
  67. Posada, D., & Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817–818.PubMedCrossRefGoogle Scholar
  68. Posada, D., & Crandall, K. A. (2001). Selecting the best-fit model of nucleotide substitution. Systematic Biology, 50, 580–601.PubMedCrossRefGoogle Scholar
  69. Printzen, C., Ekman, S., & Tønsberg, T. (2003). Phylogeography of Cavernularia hultenii: evidence of slow genetic drift in a widely disjunct lichen. Molecular Ecology, 12, 1473–1486.PubMedCrossRefGoogle Scholar
  70. Rieseberg, L. H., & Brouillet, L. (1994). Are many plant-species paraphyletic? Taxon, 43, 21–32.CrossRefGoogle Scholar
  71. Rodriguez, F., Oliver, J. L., Marin, A., & Medina, J. R. (1990). The general stochastic-model of nucleotide substitution. Journal of Theoretical Biology, 142, 485–501.PubMedCrossRefGoogle Scholar
  72. Seymour, F. A., Crittenden, P. D., Dickinson, M. J., Paoletti, M., Montiel, D., Cho, L., & Dyer, P. S. (2005). Breeding systems in the lichen-forming fungal genus Cladonia. Fungal Genetics and Biology, 42, 554–563.PubMedCrossRefGoogle Scholar
  73. Seymour, F. A., Crittenden, P. D., Wirtz, N., Øvstedal, D. O., Dyer, P. S., & Lumbsch, H. T. (2007). Phylogenetic and morphological analysis of Antarctic lichen-forming Usnea species in the group Neuropogon. Antarctic Science, 19, 71–82.CrossRefGoogle Scholar
  74. Soltis, P. S., & Soltis, D. E. (2009). The role of hybridization in plant speciation. Annual Review of Plant Biology, 60, 561–588.PubMedCrossRefGoogle Scholar
  75. Soltis, D. E., Soltis, P. S., Schemske, D. W., Hancock, J. F., Thompson, J. N., Husband, B. C., & Judd, W. S. (2007). Autopolyploidy in angiosperms: have we grossly underestimated the number of species? Taxon, 56, 13–30.Google Scholar
  76. Syring, J., Farrell, K., Businsky, R., Cronn, R., & Liston, A. (2007). Widespread genealogical nonmonophyly in species of Pinus subgenus Strobus. Systematic Biology, 56, 163–181.PubMedCrossRefGoogle Scholar
  77. Taylor, J. W., Jacobson, D. J., Kroken, S., Kasuga, T., Geiser, D. M., Hibbett, D. S., & Fisher, M. C. (2000). Phylogenetic species recognition and species concepts in fungi. Fungal Genetics and Biology, 31, 21–32.PubMedCrossRefGoogle Scholar
  78. Templeton, A. R. (1989). The meaning of species and speciation: A genetic perspective. In D. Otte & J. A. Endler (Eds.), Speciation and its consequences (pp. 3–27). Sunderland: Sinauer Associates.Google Scholar
  79. Templeton, A. R. (2001). Using phylogeographic analyses of gene trees to test species status and processes. Molecular Ecology, 10, 779–791.PubMedCrossRefGoogle Scholar
  80. Templeton, A. R., & Sing, C. F. (1993). A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. 4. Nested analyses with cladogram uncertainty and recombination. Genetics, 134, 659–669.PubMedGoogle Scholar
  81. Templeton, A. R., Boerwinkle, E., & Sing, C. F. (1987). A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. 1. Basic theory and an analysis of alcohol-dehydrogenase activity in Drosophila. Genetics, 117, 343–351.PubMedGoogle Scholar
  82. Templeton, A. R., Crandall, K. A., & Sing, C. F. (1992). A cladistic analysis of phenotypic association with haplotypes inferred from restriction endonuclease mapping and DNA-sequence data. 3. Cladogram estimation. Genetics, 132, 619–633.PubMedGoogle Scholar
  83. Thompson, J. D., Higgins, D. G., & Gibson, T. J. (1994). CLUSTAL-W - improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680.PubMedCrossRefGoogle Scholar
  84. Tuffley, C., & Steel, M. (1998). Modeling the covarion hypothesis of nucleotide substitution. Mathematical Biosciences, 147, 63–91.PubMedCrossRefGoogle Scholar
  85. Walker, F. J. (1985). The lichen genus Usnea subgenus Neuropogon. Bulletin of the British Museum, 13, 1–130. (Natural History), Botany series.Google Scholar
  86. Watterson, G. A. (1975). On the number of segregating sites in genetical models without recombination. Theoretical Population Biology, 7, 256–276.PubMedCrossRefGoogle Scholar
  87. Wirtz, N., Printzen, C., Sancho, L. G., & Lumbsch, H. T. (2006). The phylogeny and classification of Neuropogon and Usnea (Parmeliaceae, Ascomycota) revisited. Taxon, 55, 367–376.CrossRefGoogle Scholar
  88. Wirtz, N., Printzen, C., & Lumbsch, H. T. (2008). The delimitation of Antarctic and bipolar species of neuropogonoid Usnea (Ascomycota, Lecanorales): a cohesion approach of species recognition for the Usnea perpusilla complex. Mycological Research, 112, 472–484.PubMedCrossRefGoogle Scholar
  89. Yang, Z., & Rannala, B. (2010). Bayesian species delimitation using multilocus sequence data. Proceedings of the National Academy of Sciences of the United States of America, 107, 9264–9269.PubMedCrossRefGoogle Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2011

Authors and Affiliations

  • Nora Wirtz
    • 1
    • 4
  • Christian Printzen
    • 2
    • 3
  • H. Thorsten Lumbsch
    • 1
    Email author
  1. 1.Department of BotanyThe Field MuseumChicagoUSA
  2. 2.Abteilung Botanik und Molekulare EvolutionsforschungForschungsinstitut SenckenbergFrankfurt/MainGermany
  3. 3.Biodiversität und Klima ForschungszentrumFrankfurt/MainGermany
  4. 4.11 Grosvenor MountLeedsUK

Personalised recommendations