Abstract
Teloschistaceae is one of the largest lichen-forming fungal lineages, with more than one thousand species worldwide distributed, including areas with extreme environmental conditions, such as Antarctica. Two species of this family, Austroplaca hookeri and Rusavskia elegans were investigated with molecular, morphological, and anatomical data to understand their diversity patterns in maritime Antarctica. These species can be confounded in a superficial identification due to their apparent similarities in color, shape, size, and dispersal mode (spores). Sampling area included the King George Island (South Shetland Islands), James Ross Island, and the Antarctica Peninsula. New nuITS sequences revealed low divergence in A. hookeri (haplotypes with a maximum divergence of 0.8%) and high phylogenetic diversity in R. elegans (haplotypes with up to 5.5% of divergence distributed in three different lineages). The same pattern was found examining the morphological and anatomical features, with phenotypic uniformity in A. hookeri and several variations among the R. elegans specimens (such as the presence and location of the isidioid structures, the margin of the hymenial disc, and the parahimenial tissue thickness). The phenotypic variability found in R. elegans is not linked to the different nuITS lineages or to the geographic origin of the specimens analyzed. These patterns probably reflect the unique evolutionary history of each species and their different pathways in the colonization of Antarctica.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aptroot A, Cáceres M (2016) Two new lecanoroid Caloplaca (Teloschistaceae) species from gneiss inselbergs in equatorial Brazil, with a key to tropical lecanoroid species of Caloplaca s. lat. Lichenol 48:201–207. https://doi.org/10.1017/S0024282916000049
Arup U, Søchting U, Froden U (2013) A new taxonomy of the family Teloschistaceae. Nord J Bot 31:16–83. https://doi.org/10.1111/j.1756-1051.2013.00062.x
Beck A, Bechteler J, Casanova-Katny A, Dzhilyanova I (2019) The pioneer lichen Placopsis in maritime Antarctica: genetic diversity of their mycobionts and green algal symbionts, and their correlation with deglaciation time. Symbiosis 79:1–24. https://doi.org/10.1007/s13199-019-00624-4
Brandt A, De Vera J, Onofri S, Ott S (2015) Viability of the lichen Xanthoria elegans and its symbionts after 18 months of space exposure and simulated mars conditions on the ISS. Int J Astrobiol 14:411–425. https://doi.org/10.1017/S1473550414000214
Buschbom J (2007) Migration between continents: geographical structure and long-distance gene flow in Porpidia flavicunda (lichen-forming Ascomycota). Mol Ecol 16:1835–1846. https://doi.org/10.1111/j.1365-294X.2007.03258.x
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109
Domaschke S, Fernández-Mendoza F, García MA, Martín M, Printzen C (2012) Low genetic diversity in Antarctic populations of the lichenforming ascomycete Cetraria aculeata and its photobiont. Polar Res 31:17353–17366
Dyer PS, Murtagh GJ (2001) Variation in the ribosomal ITS-sequence of the lichens Buellia Frigida and Xanthoria elegans from the Vestfold Hills, Eastern Antarctica. Lichenologist 33(02):151–159. https://doi.org/10.1006/lich.2000.0306
Fries TM (1860) Lichenes Arctoi Europae Groenlandiaeque Hactenus cogniti. Upsaliae
Fryday AM, Orange A, Ahti T, Øvstedal DO, Crabtree DE (2019) An annotated checklist of lichen-forming and lichenicolous fungi reported from the Falkland Islands (Islas Malvinas). Glalia 8:1–100
Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x
Garrido-Benavent I, los Ríos A, Fernández-Mendoza F, Pérez-Ortega S (2017) No need for stepping stones: direct, joint dispersal of the lichen-forming fungus Mastodia tessellata (Ascomycota) and its photobiont explains their bipolar distribution. J Biogeogr 45:213–224. https://doi.org/10.1111/jbi.13105
Garrido-Benavent I, Pérez-Ortega S, de los Ríos A, Mayhofer H, Fernández-Mendoza F (2021) Neogene speciation and pleistocene expansion of the genus Pseudophebe (Parmeliaceae, lichenized fungi) involving multiple colonizations of Antarctica. Mol Phylogenet Evol 155:107020. https://doi.org/10.1016/j.ympev.2020.107020
Gaya E, Hognabba F, Holguin Á, Molnar K, Fernández-Brime S, Stenroos S, Arup U, Søchting U, Boom VD, Lücking R, Sipman HJM (2012) Implementing a cumulative supermatrix approach for a comprehensive phylogenetic study of the Teloschistales (Pezizomycotina, Ascomycota). Mol Phylogenet Evol 63:374–387. https://doi.org/10.1016/j.ympev.2012.01.012
Gaya E, Fernández-Brime S, Vargas R, Lachlan RF, Gueidan C, Ramírez-Mejía M, Lutzoni F (2015) The adaptive radiation of lichen-forming Teloschistaceae is associated with sunscreening pigments and a bark-to-rock substrate shift. Proc Natl Acad Sci USA 112:11600–11605. https://doi.org/10.1073/pnas.1507072112
Jones TC, Hogg ID, Wilkins RJ, Green TGA (2015) Microsatellite analyses of the Antarctic endemic lichen Buellia frigida Darb. (Physciaceae) suggest limited dispersal and the presence of glacial refugia in the Ross Sea region. Polar Biol 38:941–949. https://doi.org/10.1007/s00300-015-1652-9
Joshi Y, Bisht K, Upadhyay S (2019) Higher growth rates of saxicolous lichens in alpine regions of Western Himalaya—a consequence of warming climate? ENVIS Bull Himal Ecol 27:69–72
Katoh K, Misawa K, Kuma K, Miyata T (2002) Mafft: a novel method for rapid multiple sequence alignment based on fast fourier transform. Nucleics Acids Res 30:3059–3066. https://doi.org/10.1093/nar/gkf436
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Kitaura MJ, Scur MC, Spielmann AA, Lorenz-Lemke AP (2018) A revision of Leptogium (Collemataceae, lichenized Ascomycota) from Antarctica with a key to species. Lichenol 50:467–485. https://doi.org/10.1017/S0024282918000269
Kondratyuk SY, Kim JA, Yu NH, Jeong MH, Jang SH, Kondratiuk AS, Zarei-Darki B, Hur JS (2015) Zeroviella, a new genus of xanthorioid lichens (Teloschistaceae, Ascomycota) proved by three gene phylogeny. Ukr Bot J 72:574–584. https://doi.org/10.15407/ukrbotj72.06.574
Kraichak E, Divakar PK, Crespo A, Leavitt SD, Nelsen MP, Lücking R, Lumbsch HT (2015) A tale of two hyper-diversities: diversification dynamics of the two largest families of lichenized fungi. Sci Rep 5:10028. https://doi.org/10.1038/srep10028
Lagostina E, Andreev M, Dal Grande F, Grewe F, Lorenz A, Lumbsch HT, Rozzi R, Ruprecht U, Sancho LP, Søchting U, Scur MC, Wirtz N, Printzen C (2021) Effects of dispersal strategy and migration history on genetic diversity and population structure of Antarctic lichens. J Biogeogr 00:1–19. https://doi.org/10.1111/jbi.14101
Láska K, Barták M, Hájek J, Prosek P, Bohuslavová O (2011) Climatic and ecological characteristics of deglaciated area of James Ross Island, Antarctica, with a special respect to vegetation cover. Czech Polar Rep 1:49–62. https://doi.org/10.5817/CPR2011-1-5
Lättman H, Lindlom L, Mattsson JE, Milberg P, Skage M, Ekman S (2009) Estimating the dispersal capacity of the rare lichen Cliostomum corrugatum. Biol Conserv 142:1870–1878. https://doi.org/10.1016/j.biocon.2009.03.026
Leavitt SD, Esslinger TL, Divakar PK, Crespo A, Lumbsch HT (2016) Hidden diversity before our eyes: delimiting and describing cryptic lichen-forming fungal species in camouflage lichens (Parmeliaceae, Ascomycota). Fungal Biol 120:1374–1391. https://doi.org/10.1016/j.funbio.2016.06.001
Lindblom L (1997) The genus Xanthoria (fr.) Th.fr. in North America. J Hattori Bot Lab 83:75–172. https://doi.org/10.18968/jhbl.83.0_75
Lindblom L, Ekman S (2007) New evidence corroborates population differentiation in Xanthoria parietina. Lichenol 39:259–271. https://doi.org/10.1017/S0024282907006780
Lindblom L, Ekman S (2012) RAPDs distinguish the lichens Xanthoria aureola and X. parietina in a mixed seashore rock population. Nova Hedwig 94:279–285. https://doi.org/10.1127/0029-5035/2012/0009
Link HF (1791) Botanische Bemerkungen. In: Link HF (ed) Annalen der Naturgeschichte, Verlag Johann Christian Dieterich, Göttingen, pp 27–38
Lücking R, Hodkinson BP, Leavitt SD (2017) Corrections and amendments to the classification of lichenized fungi in the Ascomycota and Basidiomycota. Bryol 120:58–69. https://doi.org/10.1639/0007-2745-120.1.058
Lücking R, Aime MC, Robbertse B, Miller AN, Ariyawansa HA, Aoki T, Cardinali G, Crous PW, Druzhinina IS, Geiser DM, Hawksworth DL, Hyde KD, Irinyi L, Jeewon R, Johnston PR, Kirk PM, Malosso E, May TW, Meyer W, Öpik M, Robert V, Stadler M, Thines M, Vu D, Yurkov AM, Zhang N, Schoch CL (2020) Unambiguous identification of fungi: where do we stand and how accurate and precise is fungal DNA barcoding? IMA Fungus 11:14. https://doi.org/10.1186/s43008-020-00033-z
Lücking R, Moncada B, Soto-Medina E, Simijaca D, Sipman HJM (2021) Actualización nomenclatural y taxonómica del Catálogo de Líquenes de Colombia. RACCEFYN 45(174):147–189. https://doi.org/10.18257/raccefyn.1266
Mark K, Laanisto L, Bueno CG, Niinemets Ü, Keller C, Scheidegger C (2020) Contrasting co-occurrence patterns of photobiont and cystobasidiomycete yeast associated with common epiphytic lichen species. New Phytol 227:1362–1375. https://doi.org/10.1111/nph.16475
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. Gateway Computing Environments Workshop (GCE), New Orleans, LA, pp 1–8
Muñoz J, Felicisimo M, Cabezas F, Burgaz AR, Martínez I (2004) Wind as a long-distance dispersal vehicle in the southern Hemisphere. Science 304:1144–1147. https://doi.org/10.1126/science.1095210
Murtagh GJ, Dyer PS, Furneaux PA, Crittender PD (2002) Molecular and physiological diversity in the bipolar lichen-forming fungus Xanthoria elegans. Mycol Res 106:1277–1286. https://doi.org/10.1017/S0953756202006615
Olech M (2004) Lichens of king George Island, Antarctica. Jagiellonian University, Kraków
Øvstedal DO, Lewis-Smith R (2001) Lichens of Antarctica and South Georgia: a guide to their identification and ecology. Cambridge University Press, Cambridge
Pérez-Ortega S, Fernández-Mendoza F, Raggio J, Vivas M, Ascaso C, Sancho LG, Printzen C, de Los RA (2012) Extreme phenotypic variation in Cetraria aculeata (lichenized Ascomycota): adaptation or incidental modification? Ann Bot 109:1133–1148. https://doi.org/10.1093/aob/mcs042
Poelt J (1969) Bestimmungsschlüssel europäischer Flechten.—Verlag von J. Cramer, Lehre
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarisation in Bayesian phylogenetics using tracer 1.7. Syst Biol 67(5):901–904. https://doi.org/10.1093/sysbio/syy032
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Scherrer S, Honegger R (2003) Inter- and intraspecific variation of homologous hydrophobin (H1) gene sequences among Xanthoria spp. (lichen-forming Ascomycete). New Phytol 158:375–389. https://doi.org/10.1046/j.1469-8137.2003.00740.x
Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for fungi. Proc Natl Acad Sci USA 109:6241–6246. https://doi.org/10.1073/pnas.1117018109
Søchting U, Castello M (2012) The polar lichens Caloplaca darbishirei and C. soropelta highlight the direction of bipolar migration. Pol Biol 35:1143–1149. https://doi.org/10.1007/s00300-012-1161-z
Søchting U, Øvstedal DO, Sancho LG (2004) The lichens of Hurd Peninsula, Livingston Island, South Shetlands, Antarctica. Bibl Lichenol 88:607–658
Spielmann AA, Pereira AB (2012) Lichens on the maritime Antarctica (a small field guide to some common species). Glalia 4(3):01–28
Spribille T, Tuovinen V, Resl P, Vanderpool D, Wolinski H, Aime MC, Schneider K, Stanbentheiner E, Toome-Heller M, Thor G, Mayrhofer H, Johannesson H, McCutheon JP (2016) Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353:488–492. https://doi.org/10.1126/science.aaf8287
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Vondrák J, Frolov I, Davydov EA, Yakovchenko L, Malíček J, Svoboda S, Kubásek J (2019) The lichen family Teloschistaceae in the Altai-Sayan region (Central Asia). Phytotaxa 396:1. https://doi.org/10.11646/phytotaxa.396.1.1
Werth S, Wagner HH, Gugerli I, Holdrerer R, Csencsics D, Kalwij JM, Scheidegger C (2006) Quantifying dispersal and establishment limitation in a population of an epiphytic lichen. Ecology 87:2037–2046. https://doi.org/10.1890/0012-9658(2006)87[2037:QDAELI]2.0.CO;2
White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. New York Academic Press, New York, pp 315–322
Wilk K, Pabijan M, Saługa M, Gaya E, Lücking R (2021) Phylogenetic revision of South American Teloschistaceae (lichenized Ascomycota, Teloschistales) reveals three new genera and species. Mycologia 113:278–299. https://doi.org/10.1080/00275514.2020.1830672
Acknowledgements
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001. It was also supported by the Brazilian “Evolution and Dispersal of Antarctic Bipolar Species of Mosses and Lichens” project (MCTI/CNPq/FNDCT—Ação Transversal n° 64/2013). M.C. Scur and M. J. Kitaura would like to thank the CAPES for Scholarships of Institutional Scholarship Program and National Postdoctoral Program levels. M.J. Kitaura also want to thank the Fundação de Apoio ao Desenvolvimento do Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul to Postdoctoral scholarship of the Chamada Fundect/CNPq No. 04/2019—PDCTR. We also want to thank the Helsinki Herbarium that generously sent the isoneotype material and the Instituto Antártico Argentino for the logistic support during the fieldwork on James Ross Island.
Author information
Authors and Affiliations
Contributions
AAS designed and coordinated the project. MCS, JBP and MJK conducted experiments. MSC, MJK, and APL analyzed data. MCS, MJK and APL wrote the manuscript. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there are no conflicts of interest at any level for the publication of this study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Scur, M.C., Kitaura, M.J., de Paula, J.B. et al. Contrasting variation patterns in Austroplaca hookeri and Rusavskia elegans (Teloschistaceae, lichenized Ascomycota) in maritime Antarctica. Polar Biol 45, 101–111 (2022). https://doi.org/10.1007/s00300-021-02976-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-021-02976-4