Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-23T03:59:15.411Z Has data issue: false hasContentIssue false

Usnea dasopoga (Ach.) Nyl. and U. barbata (L.) F. H. Wigg. (Ascomycetes, Parmeliaceae) are two different species: a plea for reliable identifications in molecular studies

Published online by Cambridge University Press:  26 May 2021

Philippe Clerc*
Affiliation:
Conservatoire et Jardin botaniques de la Ville de Genève, Case postale 71, CH-1292Chambésy/GE, Switzerland
Yamama Naciri
Affiliation:
Conservatoire et Jardin botaniques de la Ville de Genève, Case postale 71, CH-1292Chambésy/GE, Switzerland Plant Systematics and Biodiversity Laboratory, Department of Botany and Plant Biology, University of Geneva, Case postale 71, CH-1292Chambésy/GE, Switzerland
*
Author for correspondence: Philippe Clerc. E-mail: [email protected]

Abstract

Using molecular data to delimit species or reconstruct their evolutionary history is now widely used across all organisms. However, such analyses can suffer from poor or false specimen identifications leading to incorrect conclusions. Here we show that the use of misidentified specimens in a phylogenetic framework resulted in questionable conclusions in a previously published study (Mark et al. 2016). Using morphological, chemical and statistical analyses on the specimens used in that study, we found support for Usnea barbata and U. dasopoga being morphologically and anatomically distinct species with separate clusters in the molecular phylogeny. Furthermore, our revision of specimen identifications refutes the synonymization of U. substerilis with U. lapponica. In conclusion, we discuss the issue of correct identification of voucher specimens in DNA databases and conclude with some general suggestions to avoid false specimen identifications in phylogenetic studies.

Type
Standard Papers
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of the British Lichen Society

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

Articus, K, Mattsson, JE, Tibell, L, Grube, M and Wedin, M (2002) Ribosomal DNA and β-tubulin data do not support the separation of the lichens Usnea florida and U. subfloridana as distinct species. Mycological Research 106, 412418.CrossRefGoogle Scholar
Benjamini, Y and Yekutieli, D (2001) The control of false discovery rate dependency. Annals of Statistics 29, 11651188.CrossRefGoogle Scholar
Bidartondo, MI, Bruns, TD, Blackwell, M, Edwards, I, Taylor, AFS, Horton, T, Zhang, N, Koljalg, U, May, G, Kuyper, TW, et al. (2008) Preserving accuracy in GenBank. Science 319, 1616.CrossRefGoogle ScholarPubMed
Bridge, PD, Roberts, PJ, Spooner, BM and Panchal, G (2003) On the unreliability of published DNA sequences. New Phytologist 160, 4348.CrossRefGoogle ScholarPubMed
Bungartz, F, Truong, C, Herrera-Campos, M and Clerc, P (2018) The genus Usnea (Parmeliaceae, Lecanoromycetes) in the Galapagos Islands. Herzogia 31, 571629.Google Scholar
Buyck, B (1999) Taxonomists are an endangered species in Europe. Nature 401, 321.CrossRefGoogle ScholarPubMed
Clerc, P (1987) Systematics of the Usnea fragilescens aggregate and its distribution in Scandinavia. Nordic Journal of Botany 7, 479495.CrossRefGoogle Scholar
Clerc, P (1997) Notes on the genus Usnea Dill. ex Adanson. Lichenologist 29, 209215.CrossRefGoogle Scholar
Clerc, P (1998) Species concepts in the genus Usnea (lichenized Ascomycetes). Lichenologist 30, 321340.CrossRefGoogle Scholar
Clerc, P (2004) Notes on the genus Usnea Adanson. II. Bibliotheca Lichenologica 88, 8990.Google Scholar
Clerc, P (2006) Synopsis of Usnea (lichenized Ascomycetes) from the Azores with additional information on the species in Macaronesia. Lichenologist 38, 191212.CrossRefGoogle Scholar
Clerc, P (2007) Usnea. In Nash, TH III, Gries, C and Bungartz, F (eds), Lichen Flora of the Greater Sonoran Desert Region, Vol. 3. Tempe, Arizona: Lichens Unlimited, Arizona State University, pp. 302335.Google Scholar
Clerc, P (2011 a) Notes on the genus Usnea Adanson (lichenized Ascomycota). III. Bibliotheca Lichenologica 106, 4151.Google Scholar
Clerc, P (2011 b) Usnea. In Thell, A and Moberg, R (eds), Nordic Lichen Flora. Volume 4: Parmeliaceae. Uppsala: Nordic Lichen Society, Uppsala University, pp. 107127.Google Scholar
Clerc, P (2016) Notes on the genus Usnea Adanson (lichenized Ascomycota). IV. Herzogia 29, 403411.CrossRefGoogle Scholar
Clerc, P and Herrera-Campos, M (1997) Saxicolous species of Usnea subgenus Usnea (lichenized Ascomycetes) in North America. Bryologist 100, 281301.CrossRefGoogle Scholar
Clerc, P and Otte, V (2018) Usnea viktoriana (Ascomycota, Parmeliaceae), a new European taxon of the Usnea barbata-dasopoga group, with a key to the shrubby-subpendulous sorediate Usnea species in Europe. Lichenologist 50, 513527.CrossRefGoogle Scholar
Culberson, CF and Ammann, K (1979) Standardmethode zur Dünnschichtchromatographie von Flechtensubstanzen. Herzogia 5, 124.Google Scholar
Culberson, CF and 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 238, 483487.CrossRefGoogle Scholar
Gerlach A da, CL, Clerc, P and da Silveira, RMB (2017) Taxonomy of the corticolous, shrubby, esorediate, neotropical species of Usnea Adans. (Parmeliaceae) with an emphasis on southern Brazil. Lichenologist 49, 199238.CrossRefGoogle Scholar
Gerlach A da, CL, Zeynep, T, Naciri, Y, Araujo Caviro, E, da Silveira, RMB and Clerc, P (2018) New insights into the Usnea cornuta aggregate (Parmeliaceae, lichenized Ascomycota): molecular analysis reveals high genetic diversity correlated with chemistry. Molecular Phylogenetics and Evolution 131, 125137.CrossRefGoogle Scholar
Halonen, P (2000) Usnea pacificana, sp. nov. and U. wasmuthii (lichenized Ascomycetes) in Pacific North America. Bryologist 103, 3843.CrossRefGoogle Scholar
Halonen, P, Clerc, P, Goward, T, Brodo, IM and Wulff, K (1998) Synopsis of the genus Usnea (lichenized Ascomycetes) in British Columbia, Canada. Bryologist 101, 3660.CrossRefGoogle Scholar
Herrera-Campos, M and Clerc, P (1998) Pendulous species of Usnea from the temperate forests of Mexico. Bryologist 101, 303329.CrossRefGoogle Scholar
Hofstetter, V, Buyck, B, Eyssartier, G, Schnee, S and Gindro, K (2019) The unbearable lightness of sequenced-based identification. Fungal Diversity 96, 243284.CrossRefGoogle Scholar
Kang, S, Mansfield, MA, Park, B, Geiser, DM, Ivors, KL, Coffey, MD, Grünwald, NJ, Martin, FN, Lévesque, A and Blair, JE (2010) The promise and pitfalls of sequence-based identification of plant-pathogenic fungi and oomycetes. Phytopathology 100, 732737.CrossRefGoogle ScholarPubMed
Kelly, LJ, Hollingsworth, PM, Coppins, BJ, Ellis, CJ, Harrold, P, Tosh, J and Yahr, R (2011) DNA barcoding of lichenized fungi demonstrates high identification success in a floristic context. New Phytologist 191, 288300.CrossRefGoogle Scholar
Kirk, PM, Cannon, PF, Minter, DW and Stalpers, JA (2008) Ainsworth & Bisby's Dictionary of the Fungi, 10th edition. Wallingford: CAB International.CrossRefGoogle Scholar
Ko, TW, Stephenson, SL, Bahkali, AH and Hyde, KD (2011) From morphology to molecular biology: can we use sequence data to identify fungal endophytes? Fungal Diversity 50, 113120.CrossRefGoogle Scholar
Mark, K, Saag, L, Leavitt, SD, Will-Wolf, S, Nelsen, MP, Tõrra, T, Saag, A, Randlane, T and Lumbsch, HT (2016) Evaluation of traditionally circumscribed species of the lichen-forming genus Usnea, section Usnea (Parmeliaceae, Ascomycota) using a six-locus dataset. Organisms Diversity and Evolution 16, 497524.CrossRefGoogle Scholar
Naciri, Y and Linder, HP (2015) Species delimitation and relationships: the dance of the seven veils. Taxon 64, 316.CrossRefGoogle Scholar
Nilsson, RH, Ryberg, M, Kristiansson, E, Abarenkov, K, Larsson, K-H and Kõljalg, U (2006) Taxonomic reliability of DNA sequences in public sequence databases: a fungal perspective. PLoS ONE 1, 14.CrossRefGoogle ScholarPubMed
Ohmura, Y (2001) Taxonomic study of the genus Usnea (lichenized Ascomycetes) in Japan and Taiwan. Journal of the Hattori Botanical Laboratory 90, 196.Google Scholar
Ohmura, Y and Onimaru, K (2010) Materials for the distribution of lichens in Japan (16). Usnea filipendula Stirt. Journal of Japanese Botany 85, 190192.Google Scholar
Ohmura, Y, Skirina, I and Skirin, F (2017) Contribution to the knowledge of the genus Usnea (Parmeliaceae, Ascomycota) in southern Far East Russia. Bulletin of the National Museum of Nature and Science 43, 110.Google Scholar
Poelt, J (1970) Das Konzept der Artenpaare bei den Flechten. Deutsche Botanische Gesellschaft, Neue Folge 4, 187198.Google Scholar
R Development Core Team (2016) R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. [WWW resource] URL https://www.r-project.org/Google Scholar
Saag, L, Tõrra, T, Saag, A, Del Prado, R, Randlane, T (2011) Phylogenetic relations of European shrubby taxa of the genus Usnea. Lichenologist 43, 427444.CrossRefGoogle Scholar
Stevens, GN (1990) Usnea himantodes Stirton and its synonyms. Lichenologist 22, 409412.CrossRefGoogle Scholar
Stevens, GN (1999) A revision of the lichen family Usneaceae in Australia. Bibliotheca Lichenologica 72, 1128.Google Scholar
Swinscow, TDV and Krog, H (1978) Pendulous species of Usnea in South Africa. Norwegian Journal of Botany 25, 221241.Google Scholar
Swinscow, TDV and Krog, H (1979) The fruticose species of Usnea subgenus Usnea in East Africa. Lichenologist 11, 207252.CrossRefGoogle Scholar
Thell, A, Crespo, A, Divakar, PK, Kärnefelt, I, Leavitt, SD, Lumbsch, HT and Seaward, MRD (2012) A review of lichen family Parmeliaceae – history, phylogeny and current taxonomy. Nordic Journal of Botany 30, 641664.CrossRefGoogle Scholar
Truong, C and Clerc, P (2012) The lichen genus Usnea (Parmeliaceae) in tropical South America: species with a pigmented medulla, reacting C+ yellow. Lichenologist 44, 625637.CrossRefGoogle Scholar
Truong, C and Clerc, P (2013) Eumitrioid Usnea species (Parmeliaceae, lichenized Ascomycota) in tropical South America and the Galapagos. Lichenologist 45, 383395.CrossRefGoogle Scholar
Truong, C and Clerc, P (2016) New species and new records in the genus Usnea (Parmeliaceae, lichenized Ascomycota) from tropical South America. Lichenologist 48, 7193.CrossRefGoogle Scholar
Truong, C, Bungartz, F and Clerc, P (2011) The lichen genus Usnea (Parmeliaceae) in the tropical Andes and the Galapagos: species with a red-orange cortical or subcortical pigmentation. Bryologist 114, 504525.CrossRefGoogle Scholar
Truong, C, Rodriguez, JM and Clerc, P (2013) Pendulous Usnea species (Parmeliaceae, lichenized Ascomycota) in tropical South America and the Galapagos. Lichenologist 45, 139.Google Scholar
Vainio, E (1925) Enumeratio Usnearum in Fennia collectarum. Meddelanden af Societas pro Fauna et Flora Fennica 48, 172174.Google Scholar
van den Boom, PPG, Clerc, P and Ertz, D (2015) New records of lichens and lichenicolous fungi from La Gomera (Canary Islands), including the new species: Usnea boomiana P. Clerc. Candollea 70, 165177.CrossRefGoogle Scholar
Venables, WN and Ripley, BD (2002) Modern Applied Statistics with S, 4th edition. New York: Springer.CrossRefGoogle Scholar
Vilgalys, R (2003) Taxonomic misidentification in public DNA databases. New Phytologist 160, 34.CrossRefGoogle ScholarPubMed
Weihs, C, Ligges, U, Luebke, K and Raabe, N (2005) klaR analyzing German business cycles. In Baier, D, Decker, R and Schmidt-Thieme, L (eds), Data Analysis and Decision Support. Berlin: Springer-Verlag, pp. 335343.CrossRefGoogle Scholar
Wirtz, N, Printzen, C, Sancho, LG and Lumbsch, HT (2006) The phylogeny and classification of Neuropogon and Usnea (Parmeliaceae, Ascomycota) revisited. Taxon 55, 367376.CrossRefGoogle Scholar
Wirtz, N, Printzen, C and Lumbsch, HT (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, 472484.CrossRefGoogle ScholarPubMed
Zhao, JD, Hsu, LW and Sun, ZM (1975) Species novae Usneae Sinicae. Acta Phytotaxa Sinica 13, 90107.Google Scholar