Abstract
This study is a re-assessment of basidiolichen diversity in the Galapagos Islands. We present a molecular phylogenetic analysis, based on 92 specimens from Galapagos, using two nuclear ribosomal DNA markers (ITS and nuLSU). We also re-examined the morphology and anatomy of all sequenced material. The molecular results confirm our previous assessment that all Galapagos basidiolichens belong to the Dictyonema clade, which in Galapagos is represented by four genera: Acantholichen, Cora, Cyphellostereum, and Dictyonema. Most species previously reported from Galapagos in these genera were at the time believed to represent widely distributed taxa. This conclusion, however, has changed with the inclusion of molecular data. Although almost the same number of species is distinguished, the phylogenetic data now suggest that all are restricted to the Galapagos Islands. Among them, six species are proposed here as new to science, namely Cora galapagoensis, Cyphellostereum unoquinoum, Dictyonema barbatum, D. darwinianum, D. ramificans, and D. subobscuratum; and four species have already been described previously, namely Acantholichen galapagoensis, Cora santacruzensis, Dictyonema pectinatum, and D. galapagoense, here recombined as Cyphellostereum galapagoense. Our analysis is set on a very broad phylogenetic framework, which includes a large number of specimens (N = 826) mainly from Central and South America, and therefore strongly suggests an unusually high level of endemism previously not recognized. This analysis also shows that the closest relatives of half of the basidiolichens now found in Galapagos are from mainland Ecuador, implying that they reached the islands through the shortest route, with all species arriving on the islands through independent colonization events.
Similar content being viewed by others
References
Ali JR, Aitchison JC (2014) Exploring the combined role of eustasy and oceanic island thermal subsidence in shaping biodiversity on the Galápagos. J Biogeogr 41:1227–1241. doi:10.1111/jbi.12313
Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410. doi:10.1016/S0022-2836(05)80360-2
Aptroot A (2008) Lichens of St Helena and Ascension Island. Bot J Linn Soc 158:147–171
Aptroot A, Bungartz F (2007) The lichen genus Ramalina on the Galapagos. The Lichenologist. doi:10.1017/S0024282907006901
Aptroot A, Sparrius LB (2008) Crustose Roccellaceae in the Galapagos Islands, with the new species Schismatomma spierii. Bryol 111(4):659–666
Aptroot A, Sparrius LB, LaGreca S, Bungartz F (2008) Angiactis, a new crustose lichen genus in the Roccellaceae, with species from Bermuda, the Galapagos Islands and Australia. The Bryologist 111(3):510–516
Bensted-Smith H (2002) A biodiversity vision for the Galapagos Islands. Charles Darwin Foundation and World Wildlife Fund, Puerto Ayora
Bungartz F (2008) Cyanolichens of the Galapagos Islands–the genera Collema and Leptogium. Sauteria 15:139–158
Bungartz F, Lücking R, Aptroot A (2010) The family Graphidaceae (Ostropales, Lecanoromycetes) in the Galapagos Islands. Nova Hedwig. 90:1–44
Bungartz F, Benatti MN, Spielmann AA (2013a) The genus Bulbothrix (Parmeliaceae, Lecanoromycetes) in the Galapagos Islands: a case study of superficially similar, but overlooked macrolichens. The Bryologist 116:358–372. doi:10.1639/0007-2745-116.4.358
Bungartz F, Hillmann G, Kalb K, Elix JA (2013b) Leprose and leproid lichens of the Galapagos, with a particular focus on Lepraria (Stereocaulaceae) and Septotrapelia (Pilocarpaceae). Phytotaxa 150:1. doi:10.11646/phytotaxa.150.1.1
Bungartz F, Ziemmeck F, Yánez Ayabaca A, Nugra F, Aptroot A (2013) CDF checklist of Galapagos lichenized fungi [FCD Lista de especies de Hongos liquenizados Galápagos]. In: Bungartz F, Herrera H, Jaramillo P, Tirado N, Jiménez-Uzcátegui G, Ruiz D, Guézou A, Ziemmeck F (eds) Charles Darwin Foundation Galapagos species checklist [Lista de Especies de Galápagos de la Fundación Charles Darwin]. Charles Darwin Foundation/Fundación Charles Darwin, Puerto Ayora, Galapagos. http://www.darwinfoundation.org/datazone/checklists/true-fungi/lichens/. http://www.darwinfoundation.org/datazone/checklists/media/lists/download/2013Dec03_Bungartz_et_al_Galapagos_Lichens_Checklist.pdf. Accessed 03 Dec 2013
Bungartz F, Elix JA, Yánez-Ayabaca A, Archer AW (2015) Endemism in the genus Pertusaria (Pertusariales, lichenized Ascomycota) from the Galapagos Islands. Telopea 18:325–369
Bungartz F, Giralt M, Sheard JW, Elix JA (2016a) The lichen genus Rinodina (Physciaceae, Teloschistales) in the Galapagos Islands, Ecuador. The Bryologist 119:60–93
Bungartz F, Klaus K, Giralt M et al (2016b) New and overlooked species from the Galapagos Islands: the generic concept of Diploicia reassessed. The Lichenologist 48:489–515
Carlquist S (1974) Island biology. Columbia University Press, New York
Cole JR, Wang Q, Fish JA et al (2014) Ribosomal database project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42:D633–D642. doi:10.1093/nar/gkt1244
Cornejo C, Scheidegger C (2016) Cyanobacterial gardens: the liverwort Frullania asagrayana acts as a reservoir of lichen photobionts. Environ Microbiol Rep 8(3):352–357
Cornejo C, Nelson PR, Stepanchikova I et al (2016) Contrasting pattern of photobiont diversity in the Atlantic and Pacific populations of Erioderma pedicellatum (Pannariaceae). The Lichenologist 48:275–291. doi:10.1017/S0024282916000311
Dal-Forno M, Lawrey JD, Sikaroodi M et al (2013) Starting from scratch: evolution of the lichen thallus in the basidiolichen Dictyonema (Agaricales: Hygrophoraceae). Fungal Biol 117:584–598. doi:10.1016/j.funbio.2013.05.006
Dal-Forno M, Lücking R, Bungartz F et al (2016a) From one to six: unrecognized species diversity in the genus Acantholichen P. M. Jørg. (lichenized Basidiomycota: Hygrophoraceae). Mycologia 108:38–55. doi:10.3852/15-060
Dal-Forno M, Lücking R, Sikaroodi M et al (2016b) Photobiont diversity in cyanolichens of the Dictyonema clade (Hygrophoraceae: Basidiomycota). In: The 8th IAL Symposium, Helsinki, Finland
Darwin C (1859) On the origins of species by means of natural selection. Murray, London
Dodge C (1935) Lichenes. HK Svenson: Plants of the Astor Expedition, 1930 (Galápagos and Cocos Islands). Am J Bot 22(2):221
Elix JA, McCarthy PM (1998) Catalogue of the lichens of the smaller Pacific Islands. Bibl Lichenol 70:1–361
Elix JA, McCarthy PM (2008) Checklist of Pacific Island Lichens. Australian Biological Resources Study, Canberra. Version 21 August 2008
Goward T (1994) Living antiquities. Nat Can 1994:14–21
Gradstein SR, Weber WA (1982) Bryogeography of the Galápagos Islands. J Hattori Bot Lab 52:127–152
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Jørgensen PM (1998) Acantholichen pannarioides, a new basidiolichen from South America. The Bryologist 101:444–447
Katoh K, Toh H (2010) Parallelization of the MAFFT multiple sequence alignment program. Bioinformatics 26:1899–1900
Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518
Larsson K-H (2007) Re-thinking the classification of corticioid fungi. Mycol Res 111:1040–1063. doi:10.1016/j.mycres.2007.08.001
Lawrey JD, Lücking R, Sipman HJM, Chaves JL, Redhead SA, Bungartz F, Sikaroodi M, Gillevet PM (2009) High concentration of basidiolichens in a single family of agaricoid mushrooms (Basidiomycota: Agaricales: Hygrophoraceae). Mycol Res 113:1154–1171
Linder DH (1934) The Templeton Crocker Expedition of the California Academy of Sciences, 1932. No. 18. Proc Calif Acad Sci Ser IV 21:211–224
Losos JB, Ricklefs RE (2009) Adaptation and diversification on islands. Nature 457:830–836. doi:10.1038/nature07893
Lücking R, Lawrey JD, Sikaroodi M et al (2009) Do lichens domesticate photobionts like farmers domesticate crops? Evidence from a previously unrecognized lineage of filamentous cyanobacteria. Am J Bot 96:1409–1418. doi:10.3732/ajb.0800258
Lücking R, Dal-Forno M, Lawrey JD et al (2013a) Ten new species of lichenized Basidiomycota in the genera Dictyonema and Cora (Agaricales: Hygrophoraceae), with a key to all accepted genera and species in the Dictyonema clade. Phytotaxa 139:1. doi:10.11646/phytotaxa.139.1.1
Lücking R, Dal-Forno M, Wilk K, Lawrey JD (2013b) Three new species of Dictyonema (lichenized Basidiomycota: Hygrophoraceae) from Bolivia. Acta Nova 6:4–16
Lücking R, Dal-Forno M, Sikaroodi M et al (2014a) A single macrolichen constitutes hundreds of unrecognized species. Proc Natl Acad Sci 111:11091–11096. doi:10.1073/pnas.1403517111
Lücking R, Lawrey JD, Gillevet PM et al (2014b) Multiple ITS Haplotypes in the Genome of the Lichenized Basidiomycete Cora inversa (Hygrophoraceae): Fact or Artifact? J Mol Evol 78:148–162. doi:10.1007/s00239-013-9603-y
Lücking R, Caceres MES, Silva NG, Alves RJV (2015) The genus Cora in the South Atlantic and the Mascarenes: two novel taxa and inferred biogeographic relationships. Bryol 118(3):293–303. doi:10.1639/0007-2745-118.3.293
Lücking R, Forno MD, Moncada B et al (2016) Turbo-taxonomy to assemble a megadiverse lichen genus: seventy new species of Cora (Basidiomycota: Agaricales: Hygrophoraceae), honouring David Leslie Hawksworth’s seventieth birthday. Fungal Divers. doi:10.1007/s13225-016-0374-9
Mason-Gamer RJ, Kellogg EA (1996) Testing for phylogenetic conflict among molecular data sets in the tribe Triticeae (Gramineae). Syst Biol 45:524–545
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Gateway Computing Environments Workshop (GCE), 2010. IEEE, pp 1–8
Moncada B, Reidy B, Lücking R (2014) A phylogenetic revision of Hawaiian Pseudocyphellaria sensu lato (lichenized Ascomycota: Lobariaceae) reveals eight new species and a high degree of inferred endemism. Bryol 117:119–160
Moncada B, Bungartz F, Lücking R (2016) The family Lobariaceae in the Galapagos Islands. The 8th IAL Symposium, Helsinki, Finland
Penn O, Privman E, Ashkenazy H et al (2010a) GUIDANCE: a web server for assessing alignment confidence scores. Nucleic Acids Res 38:W23–W28. doi:10.1093/nar/gkq443
Penn O, Privman E, Landan G et al (2010b) An alignment confidence score capturing robustness to guide tree uncertainty. Mol Biol Evol 27:1759–1767. doi:10.1093/molbev/msq066
Piercey-Normore MD, DePriest PT (2001) Algal switching among lichen symbioses. Am J Bot 88:1490–1498
Schmull M, Dal-Forno M, Lücking R et al (2014) Dictyonema huaorani (Agaricales: Hygrophoraceae), a new lichenized basidiomycete from Amazonian Ecuador with presumed hallucinogenic properties. Bryol 117:386–394. doi:10.1639/0007-2745-117.4.386
Schoch CL, Seifert KA, Huhndorf S et al (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci 109:6241–6246. doi:10.1073/pnas.1117018109
Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690
Stamatakis A, Ludwig T, Meier H (2005) RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21:456–463
Tehler A, Irestedt M, Bungartz F, Wedin M (2009) Evolution and reproduction modes in the Roccella galapagoensis aggregate (Roccellaceae, Arthoniales). Taxon 58:438–456
Tye A, Snell H, Peck S, Adsersen H (2002) Outstanding terrestrial features of the Galapagos archipelago. Biodivers Vis Galapagos Isl Charles Darwin Found World Wildl Fund Puerto Ayora 25–35
Vargas LY, Moncada B, Lücking R (2014) Five new species of Cora and Dictyonema (Basidiomycota: Hygrophoraceae) from Colombia: chipping away at cataloging hundreds of unrecognized taxa. The Bryologist 117:368–378. doi:10.1639/0007-2745-117.4.368
Weber WA (1966) Lichenology and bryology in the Galapagos Islands, with check lists of the lichens and bryophytes thus far reported. In: Bowman RI (ed) The Galapagos. University of California Press, Berkeley, pp 190–200
Weber WA (1986) The lichen flora of the Galapagos Islands, Ecuador. Mycotaxon 27:451–497
Weber WA (1993) Additions to the Galápagos and Cocos Islands lichen and bryophyte floras. Bryologist 96(3):431–434
Williamson M (1981) Island populations. Oxford: Oxford University Press xi, 286p.-illus., maps. En Maps, Geog
Yánez A, Dal-Forno M, Bungartz F et al (2012) A first assessment of Galapagos basidiolichens. Fungal Divers 52:225–244. doi:10.1007/s13225-011-0133-x
Yánez A, Ahti T, Bungartz F (2013) The family Cladoniaceae (Lecanorales) in the Galapagos Islands. Phytotaxa 129(1):1–33. doi:10.11646/phytotaxa.129.1.1
Acknowledgements
Authors want to thank National Science Foundation for financial support through a Division of Environmental Biology grant (DEB 0841405, PI: J. Lawrey; CoPIs: R. Lücking, P. Gillevet) and a Postdoctoral Research Fellowship in Biology (PRFB 1609022, PI: M. Dal Forno). Authors also thank all colleagues around the world who have contributed valuable Dictyonema s.l. collections over many years so a broad phylogenetic study could be done. Masoumeh Sikaroodi and Patrick Gillevet are thanked for their help and support in the molecular laboratory. Taxonomic research on Galapagos species, with the goal of establishing the first IUCN red list of endemic Galapagos lichens, is supported by the Mohamed bin Zayed Species Conservation Fund, Project 152510692. We are very grateful to the Charles Darwin Foundation, especially its executive director Arturo Izurieta and science coordinator José Marin, for their continued support of the Galapagos Lichen Inventory. For research and collection permits we are especially indebted to the Galapagos National Park, particularly Washington Tapia and Galo Quedaza, and, more recently, Jorge Carrion and Daniel Lara. The lichen inventory is part of the Census of Galapagos Biodiversity by Charles Darwin Foundation (donors cited at http://www.darwinfoundation.org/datazone/checklists/). This publication is contribution number 2159 of the Charles Darwin Foundation for the Galapagos Islands. Lastly, authors would like to thank managing editor Jian-Kui Liu and two anonymous reviewers for their contributions to improve this paper.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Fig. 1
Phylogeny (ITS) of Cora obtained under ML. Branches are thickened for all bootstrap (BS) values ≥70. Placement of Galapagos species are in bold (PDF 601 kb)
Supplementary Fig. 2
Phylogeny (ITS) of Dictyonema obtained under ML. Branches are thickened for all bootstrap (BS) values ≥70. Placement of Galapagos species are in bold (PDF 301 kb)
Rights and permissions
About this article
Cite this article
Dal Forno, M., Bungartz, F., Yánez-Ayabaca, A. et al. High levels of endemism among Galapagos basidiolichens. Fungal Diversity 85, 45–73 (2017). https://doi.org/10.1007/s13225-017-0380-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13225-017-0380-6