Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-22T16:14:37.752Z Has data issue: false hasContentIssue false
  • English
  • Français

Towards an integrative taxonomy of Phyllopsora (Ramalinaceae)

Published online by Cambridge University Press:  21 August 2019

Sonja KISTENICH Open the ORCID record for Sonja KISTENICH [Opens in a new window] ,
Mika BENDIKSBY Open the ORCID record for Mika BENDIKSBY [Opens in a new window] ,
Stefan EKMAN Open the ORCID record for Stefan EKMAN [Opens in a new window] ,
Marcela E. S. CÁCERES ,
Jesús E. HERNÁNDEZ M. Open the ORCID record for Jesús E. HERNÁNDEZ M. [Opens in a new window]  and
Einar TIMDAL
Sonja KISTENICH
Affiliation:
Natural History Museum, University of Oslo, P.O. Box 1172 Blindern, 0318 Oslo, Norway. Email: [email protected]
Mika BENDIKSBY
Affiliation:
Natural History Museum, University of Oslo, P.O. Box 1172 Blindern, 0318 Oslo, Norway. Email: [email protected] NTNU University Museum, Norwegian University of Science and Technology, Erling Skakkes Gate 47, 7012 Trondheim, Norway.
Stefan EKMAN
Affiliation:
Museum of Evolution, Uppsala University, Norbyvägen 16, 75236 Uppsala, Sweden.
Marcela E. S. CÁCERES
Affiliation:
Universidade Federal de Sergipe, Departamento de Biociências, CEP: 49500-000, Itabaiana, SE, Brazil.
Jesús E. HERNÁNDEZ M.
Affiliation:
Instituto Experimental Jardín Botánico, Ave. Salvador Allende, Jardín Botánico de Caracas, Universidad Central de Venezuela, Caracas 1010-A, Venezuela.
Einar TIMDAL
Affiliation:
Natural History Museum, University of Oslo, P.O. Box 1172 Blindern, 0318 Oslo, Norway. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Species identification in the tropical lichen genus Phyllopsora is generally challenging and is based on ascospore morphology, vegetative dispersal units, thallus structure and secondary chemistry. As several type specimens are in poor condition and difficult to interpret, it is often unclear how these old names fit with the currently used taxonomy. In the present study, we aim to identify species boundaries in Phyllopsora s. str. supported by an integrative approach using multiple sources of evidence. We investigated a substantial amount of herbarium as well as freshly collected material and generated mtSSU and ITS sequence data from most of the described species, including several types. Species delimitation analyses are applied on the gene trees using mPTP and we construct a species tree of both markers with *BEAST, facilitating discussion of species delimitation and sister-relationships. Comparing morphology, chemistry and molecular data, we found that the mPTP analyses split established species repeatedly. Based on our integrative results, we exclude nine species from the genus, resurrect one (P. melanoglauca Zahlbr.), reduce two into synonymy with other Phyllopsora species and describe five as new to science: Phyllopsora amazonica Kistenich & Timdal (which shares the secondary chemistry (atranorin and terpenoid pattern) with P. halei chemotype 1, but differs, e.g., in having smaller areolae that are attached to a thinner, white prothallus, and in having more persistently marginate and less convex apothecia), Phyllopsora concinna Kistenich & Timdal (which shares the secondary chemistry (atranorin and parvifoliellin) with P. parvifoliella and P. rappiana, but differs from both in forming larger isidia, having a white prothallus, apothecial margin paler than the disc, and longer and broader ascospores), Phyllopsora furfurella Kistenich & Timdal (which is here segregated from P. furfuracea based on having a white prothallus and in containing skyrin in the hypothecium (K+ red)), Phyllopsora isidosa Kistenich & Timdal (which differs from P. byssiseda in forming a more crustose thallus with more delicate isidia, and from P. isidiotyla in forming somewhat coarser, less branched isidia) and Phyllopsora neotinica Kistenich & Timdal (a neotropical species here segregated from the now exclusively paleotropical P. chodatinica, differing in containing an unknown xanthone (not chodatin)). Lectotypes are designated for Biatora pyrrhomelaena Tuck., Lecidea leucophyllina Nyl., L. pertexta Nyl., and P. brachyspora Müll. Arg. In total, we accept 54 species in the genus Phyllopsora.

Keywords

ITSlichensmolecular phylogenymPTPmtSSUspecies delimitationtropical rainforest
Type
Articles
Information
The Lichenologist , Volume 51 , Issue 4 , July 2019 , pp. 323 - 392
Copyright
Copyright © British Lichen Society 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Altekar, G., Dwarkadas, S., Huelsenbeck, J. P. & Ronquist, F. (2004) Parallel metropolis coupled Markov chain Monte Carlo for Bayesian phylogenetic inference. Bioinformatics 20: 407–415.Google Scholar
Aptroot, A. & Cáceres, M. E. S. (2014) A key to the corticolous microfoliose, foliose and related crustose lichens from Rondônia, Brazil, with the description of four new species. Lichenologist 46: 783–799.Google Scholar
Aptroot, A., Umana, L., Chaves, J. L. & Trest, M. T. (2006) A first assessment of the Ticolichen biodiversity inventory in Costa Rica: three new squamulose genera (Lecanorales: Ramalinaceae and Pilocarpaceae). Journal of the Hattori Botanical Laboratory 100: 617–623.Google Scholar
Aptroot, A., Saipunkaew, W., Sipman, H., Sparrius, L. & Wolseley, P. (2007) New lichens from Thailand, mainly microlichens from Chiang Mai. Fungal Diversity 24: 75–134.Google Scholar
Bouckaert, R., Heled, J., Kühnert, D., Vaughan, T., Wu, C.–H., Xie, D., Suchard, M. A., Rambaut, A. & Drummond, A. J. (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLOS Computational Biology 10: e1003537. doi:10.1371/journal.pcbi.1003537Google Scholar
Brako, L. (1989) Re-evaluation of the genus Phyllopsora with taxonomic notes and introduction of Squamacidia, gen nov. Mycotaxon 35: 1–19.Google Scholar
Brako, L. (1991) Phyllopsora (Bacidiaceae). Flora Neotropica 55: 1–66.Google Scholar
Cáceres, M. E. S. (2007) Corticolous, crustose and microfoliose lichens of northeastern Brazil. Libri Botanici 22: 1–168.Google Scholar
Carstens, B. C., Pelletier, T. A., Reid, N. M. & Satler, J. D. (2013) How to fail at species delimitation. Molecular Ecology 22: 4369–4383. doi:doi:10.1111/mec.12413Google Scholar
Chernomor, O., von Haeseler, A. & Minh, B. Q. (2016) Terrace aware data structure for phylogenomic inference from supermatrices. Systematic Biology 65: 997–1008. doi:10.1093/sysbio/syw037Google Scholar
Clements, F. E. & Shear, C. L. (1931) The Genera of Fungi. New York: H. W. Wilson.Google Scholar
Coppins, B. J. & James, P. (1979) New or interesting British lichens IV. Lichenologist 11: 139–179.Google Scholar
Culberson, C. F. (1972) Improved conditions and new data for identification of lichen products by standardized thin-layer chromatographic method. Journal of Chromatography A 72: 113–125.Google Scholar
Culberson, C. F. & Culberson, W. L. (2001) Future directions in lichen chemistry. Bryologist 104: 230–234.Google Scholar
Culberson, C. F. & Johnson, A. (1976) A standardized two-dimensional thin-layer chromatographic method for lichen products. Journal of Chromatography A 128: 253–259.Google Scholar
Culberson, C. F. & Johnson, A. (1982) Substitution of methyl tert.-butyl ether for diethyl ether in the standardized thin-layer chromatographic method for lichen products. Journal of Chromatography A 238: 483–487.Google Scholar
Culberson, C. F. & Kristinsson, H.–D. (1970) A standardized method for the identification of lichen products. Journal of Chromatography A 46: 85–93.Google Scholar
Drummond, A. J., Ho, S. Y. W., Phillips, M. J. & Rambaut, A. (2006) Relaxed phylogenetics and dating with confidence. PLOS Biology 4: e88. doi:10.1371/journal.pbio.0040088Google Scholar
Elix, J. A. (2006 a) Additional lichen records from Australia 56. Australasian Lichenology 58: 4–13.Google Scholar
Elix, J. A. (2006 b) Additional lichen records from Australia 58. New records from Norfolk Island. Australasian Lichenology 59: 12–15.Google Scholar
Elix, J. A. (2006 c) Five new species of Phyllopsora (lichenized Ascomycota) from Australia. Australasian Lichenology 59: 23–29.Google Scholar
Elix, J. A. (2007) Additional lichen records from Australia 62. Australasian Lichenology 60: 6–12.Google Scholar
Elix, J. A. (2009) Phyllopsoraceae. In Flora of Australia, Volume 57, Lichens 5 (McCarthy, P. M., ed.): 41–59. Canberra and Melbourne: ABRS and CSIRO Publishing.Google Scholar
Eriksson, O. & Hawksworth, D. L. (1986) Notes on Ascomycete systematics. Nos. 1–224. Systema Ascomycetum 5: 113–174.Google Scholar
Flouri, T., Jiao, X., Rannala, B. & Yang, Z. (2018) Species tree inference with BPP using genomic sequences and the multispecies coalescent. Molecular Biology and Evolution 35: 2585–2593. doi:10.1093/molbev/msy147Google Scholar
Galloway, D. J. (1983) New taxa in the New Zealand lichen flora. New Zealand Journal of Botany 21: 191–199. doi: 10.1080/0028825X.1983.10428544Google Scholar
Galloway, D. J. (1985) Flora of New Zealand Lichens. Wellington, New Zealand: PD Hasselberg, Government Printer.Google Scholar
Galloway, D. J. (2007) Flora of New Zealand: Lichens, Including Lichen-Forming and Lichenicolous Fungi Vol. 2. Lincoln, New Zealand: Manaaki Whenua Press, Landcare Research.Google Scholar
Galloway, D. J. & James, P. W. (1985) The Lichen Genus Psoromidium Stirton. Lichenologist 17: 173–188. doi:10.1017/S0024282985000226Google Scholar
Gueidan, C., Aptroot, A., Cáceres, M. E. S. & Binh, N. Q. (2016) Molecular phylogeny of the tropical lichen family Pyrenulaceae: contribution from dried herbarium specimens and FTA card samples. Mycological Progress 15: 7. doi:10.1007/s11557-015-1154-8Google Scholar
Hafellner, J. (1984) Studien in Richtung einer natürlicheren Gliederung der Sammelfamilien Lecanoraceae und Lecideaceae. Beihefte zur Nova Hedwigia 79: 241–371.Google Scholar
Hebert, P. D. N., Cywinska, A., Ball, S. L. & deWaard, J. R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London Series B: Biological Sciences 270: 313–321. doi:10.1098/rspb.2002.2218Google Scholar
Heled, J. & Drummond, A. J. (2010) Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution 27: 570–580. doi:10.1093/molbev/msp274Google Scholar
Hue, A. (1909) Lichenum generis Crocyniae Mass. plerasque species juxta archetypa specimina morphologice et anatomice descripsit. Mémoires de la Société Nationale des Sciences Naturelles et Mathématiques de Cherbourg 37: 223–254.Google Scholar
Hue, A. (1924) Monographia crocyniarum. Bulletin de la Société Botanique de France 71: 311–402.Google Scholar
Jørgensen, P. M. (2003) Conspectus familiae Pannariaceae (Ascomycetes lichenosae). Ilicifolia 4: 1–78.Google Scholar
Jørgensen, P. M. & Andersen, H. L. (2015) The lichen genus Psoromidium (Pannariaceae) re-evaluated, with nomenclatural notes on Degeliella and Psoromaria. Lichenologist 47: 343–348. doi:10.1017/S0024282915000171Google Scholar
Kaasalainen, U., Heinrichs, J., Renner, M. A. M., Hedenäs, L., Schäfer-Verwimp, A., Lee, G. E., Ignatov, M. S., Rikkinen, J. & Schmidt, A. R. (2018) A Caribbean epiphyte community preserved in Miocene Dominican amber. Earth and Environmental Science Transactions of the Royal Society of Edinburgh 107: 321–331. doi:10.1017/S175569101700010XGoogle Scholar
Kalb, K. & Elix, J. (1995) The lichen genus Physcidia. Bibliotheca Lichenologica 57: 265–296.Google Scholar
Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A. & Jermiin, L. S. (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nature Methods 14: 587. doi:10.1038/nmeth.4285Google Scholar
Kapli, P., Lutteropp, S., Zhang, J., Kobert, K., Pavlidis, P., Stamatakis, A. & Flouri, T. (2017) Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo. Bioinformatics 33: 1630–1638. doi:10.1093/bioinformatics/btx025Google Scholar
Katoh, K. & Standley, D. M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. doi:10.1093/molbev/mst010Google Scholar
Kauff, F. & Lutzoni, F. (2002) Phylogeny of the Gyalectales and Ostropales (Ascomycota, Fungi): among and within order relationships based on nuclear ribosomal RNA small and large subunits. Molecular Phylogenetics and Evolution 25: 138–156.Google Scholar
Kistenich, S., Timdal, E., Bendiksby, M. & Ekman, S. (2018 a) Molecular systematics and character evolution in the lichen family Ramalinaceae (Ascomycota: Lecanorales). Taxon 67: 871–904. doi:10.12705/675.1Google Scholar
Kistenich, S., Rikkinen, J., Thüs, H., Vairappan, C., Wolseley, P. A. & Timdal, E. (2018 b) Three new species of Krogia (Ramalinaceae, lichenized Ascomycota) from the Paleotropics. MycoKeys 40: 69–88. doi:10.3897/mycokeys.40.26025Google Scholar
Kistenich, S., Bendiksby, M., Vairappan, C., Weerakoon, G., Wijesundara, S., Wolseley, P. A. & Timdal, E. (2019 a) A regional study of the genus Phyllopsora (Ramalinaceae) in Asia and Melanesia. MycoKeys 53: 23–72. doi: 10.3897/mycokeys.53.33425.Google Scholar
Kistenich, S., Ekman, S., Bendiksby, M. & Timdal, E. (2019 b) Proposal to conserve the name Phyllopsora against Triclinum and Crocynia (Ramalinaceae, lichenized Ascomycota). Taxon (in press).Google Scholar
Kondratyuk, S. Y., Lőkös, L., Halda, J. P., Upreti, D. K., Mishra, G. K., Haji Moniri, M., Farkas, E., Park, J. S., Lee, B. G. & Liu, D. (2016) New and noteworthy lichen-forming and lichenicolous fungi 5. Acta Botanica Hungarica 58: 319–396.Google Scholar
Lakatos, M., Rascher, U. & Büdel, B. (2006) Functional characteristics of corticolous lichens in the understory of a tropical lowland rain forest. New Phytologist 172: 679–695. doi:10.1111/j.1469-8137.2006.01871.xGoogle Scholar
Lamb, I. M. (1963) Index Nominum Lichenum: Inter Annos 1932 et 1960 Divulgatorum. New York: Ronald Press.Google Scholar
Lücking, R., Hodkinson, B. P. & Leavitt, S. D. (2017 a) The 2016 classification of lichenized fungi in the Ascomycota and Basidiomycota – approaching one thousand genera. Bryologist 119: 361–416. doi:10.1639/0007-2745-119.4.361Google Scholar
Lücking, R., Hodkinson, B. P. & Leavitt, S. D. (2017 b) Corrections and amendments to the 2016 classification of lichenized fungi in the Ascomycota and Basidiomycota. Bryologist 120: 58–69. doi:10.1639/0007-2745-120.1.058Google Scholar
Lumbsch, H. T. & Huhndorf, S. M. (2007) Outline of Ascomycota – 2007. Myconet 13: 1–58.Google Scholar
Lumbsch, H. T., Ahti, T., Altermann, S., Amo de Paz, G., Aptroot, A., Arup, U., Bárcenas Peña, A., Bawingan, P. A., Benatti, M. N., Betancourt, L., et al. (2011) One hundred new species of lichenized fungi: a signature of undiscovered global diversity. Phytotaxa 18: 1–127.Google Scholar
McNeill, J. (2014) Holotype specimens and type citations: general issues. Taxon 63: 1112–1113. doi:10.12705/635.7Google Scholar
Menlove, J. E. (1974) Thin-layer chromatography for the identification of lichen substances. British Lichen Society Bulletin 34: 3–5.Google Scholar
Mishra, G. K., Upreti, D. K., Nayaka, S. & Haridas, B. (2011) New taxa and new reports of Phyllopsora (lichenized Ascomycotina) from India. Mycotaxon 115: 29–44.Google Scholar
Müller, J. (1894) Conspectus systematicus specierum lichenum Novae Zelandiae. Bulletin de l'Herbier Boissier 2(App. 1): 1–114.Google Scholar
Nguyen, L.-T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32: 268–274. doi:10.1093/molbev/msu300Google Scholar
Poelt, J. (1973) Appendix A. Classification. In The Lichens (Ahmadjian, V. & Hale, M. E., eds): 599–630. London and New York: Academic Press. doi:10.1016/B978-0-12-044950-7.50008-8Google Scholar
Prosser, S. W., deWaard, J. R., Miller, S. E. & Hebert, P. D. (2016) DNA barcodes from century-old type specimens using next-generation sequencing. Molecular Ecology Resources 16: 487–497.Google Scholar
Rambaut, A., Drummond, A. J., Xie, D., Baele, G. & Suchard, M. A. (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67: 901–904. doi:10.1093/sysbio/syy032Google Scholar
Rannala, B. & Yang, Z. (2013) Improved reversible jump algorithms for Bayesian species delimitation. Genetics 194: 245–253. doi:10.1534/genetics.112.149039Google Scholar
Rannala, B. & Yang, Z. (2017) Efficient Bayesian species tree inference under the multispecies coalescent. Systematic Biology 66: 823–842. doi:10.1093/sysbio/syw119Google Scholar
Riedl, H. (1973) Phyllopsora leprosa, eine neue Flechten-Species aus Surinam. Österreichische Botanische Zeitschrift 121: 145–149. doi:10.1007/bf01373373Google Scholar
Rikkinen, J. & Poinar, G. O. (2008) A new species of Phyllopsora (Lecanorales, lichen-forming Ascomycota) from Dominican amber, with remarks on the fossil history of lichens. Journal of Experimental Botany 59: 1007–1011.Google Scholar
Ronquist, F. & Huelsenbeck, J. P. (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.Google Scholar
Rose, F., Purvis, O. W. & Coppins, B. J. (2009) Phyllopsora Müll. Arg. (1894). In Lichens of Great Britain and Ireland (Smith, C. W., Aptroot, A., Coppins, B. J., Fletcher, A., Gilbert, O. L., James, P. W. & Wolseley, P. A., eds). London: British Lichen Society.Google Scholar
Schneider, G. (1980) Die Flechtengattung Psora sensu Zahlbruckner: versuch einer Gliederung. Bibliotheca Lichenologica 13: 1–291.Google Scholar
Schoch, C. L., Seifert, K. A., Huhndorf, S., Robert, V., Spouge, J. L., Levesque, C. A. & Chen, W. (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences of the United States of America 109: 6241–6246. doi:10.1073/pnas.1117018109Google Scholar
Sequiera, S. & Kumar, M. (2008) Epiphyte host relationship of macrolichens in the tropical wet evergreen forests of Silent Valley National Park, Western Ghats, India. Tropical Ecology 49: 211–224.Google Scholar
Sipman, H. J. M. (2018) Three new lichen species and 48 new records from Vanuatu. Australasian Lichenology 82: 106–129.Google Scholar
Staiger, B., Kalb, K. & Grube, M. (2006) Phylogeny and phenotypic variation in the lichen family Graphidaceae (Ostropomycetidae, Ascomycota). Mycological Research 110: 765–772. doi:10.1016/j.mycres.2006.05.003Google Scholar
Stöver, B. C. & Müller, K. F. (2010) TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics 11: 7. doi:10.1186/1471-2105-11-7Google Scholar
Struck, T. H., Feder, J. L., Bendiksby, M., Birkeland, S., Cerca, J., Gusarov, V. I., Kistenich, S., Larsson, K.-H., Liow, L. H., Nowak, M. D., et al. (2018) Finding evolutionary processes hidden in cryptic species. Trends in Ecology and Evolution 33: 153–163. doi:10.1016/j.tree.2017.11.007Google Scholar
Swinscow, T. D. V. & Krog, H. (1981) The genus Phyllopsora, with a report on East African species. Lichenologist 13: 203–247.Google Scholar
Swinscow, T. D. V. & Krog, H. (1985) Phyllopsora longispora sp. nov. Nordic Journal of Botany 5: 493–495. doi:doi:10.1111/j.1756-1051.1985.tb01682.xGoogle Scholar
Timdal, E. (1986) A revision of Psora (Lecideaceae) in North America. Bryologist 89: 253–275. doi:10.2307/3243197Google Scholar
Timdal, E. (2008) Studies on Phyllopsora (Ramalinaceae) in Peru. Lichenologist 40: 337–362.Google Scholar
Timdal, E. (2011) The lichen genus Phyllopsora (Ramalinaceae) in the West Indies. Bibliotheca Lichenologica 106: 319–351.Google Scholar
Timdal, E. & Krog, H. (2001) Further studies on African species of the lichen genus Phyllopsora (Lecanorales). Mycotaxon 77: 57–90.Google Scholar
Vězda, A. (2003) Lichenes Rariores Exsiccati. Fasciculus 49 (numeris 481–490). Brno: published by the author.Google Scholar
Weerakoon, G., Aptroot, A., Lumbsch, H. T., Wolseley, P. A., Wijeyaratne, S. C. & Gueidan, C. (2012) New molecular data on Pyrenulaceae from Sri Lanka reveal two well-supported groups within this family. Lichenologist 44: 639–647. doi:10.1017/S0024282912000333Google Scholar
Yang, Z. (2015) The BPP program for species tree estimation and species delimitation. Current Zoology 61: 854–865. doi:10.1093/czoolo/61.5.854Google Scholar
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. doi:10.1073/pnas.0913022107Google Scholar
Yang, Z. & Rannala, B. (2014) Unguided species delimitation using DNA sequence data from multiple loci. Molecular Biology and Evolution 31: 3125–3135. doi:10.1093/molbev/msu279Google Scholar
Zahlbruckner, A. (1907) Lichenes (Flechten) B. Spezieller Teil. In Die Natürlichen Pflanzenfamilien, Teil 1 (Engler, A. & Prantl, K., eds): 49–249. Leipzig: Engelmann.Google Scholar
Zahlbruckner, A. (1921–1940) Catalogus Lichenum Universalis Vol. 1–10. Leipzig: Gebrüder Borntraeger.Google Scholar
Zhang, J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29: 2869–2876. doi:10.1093/bioinformatics/btt499Google Scholar
Supplementary material: File

Kistenich et al. supplementary material

Kistenich et al. supplementary material

Download Kistenich et al. supplementary material(File)
File 33.5 KB