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Monday 19 June 2017

High levels of endemism among Galapagos basidiolichens

Published Date
DOI: 10.1007/s13225-017-0380-6


Cite this article as:
Dal Forno, M., Bungartz, F., Yánez-Ayabaca, A. et al. Fungal Diversity (2017). doi:10.1007/s13225-017-0380-6
Author
  • Manuela Dal Forno
  • Frank Bungartz
  • Alba Yánez-Ayabaca
  • Robert Lücking
  • James D. Lawrey
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: AcantholichenCoraCyphellostereum, 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 galapagoensisCyphellostereum unoquinoumDictyonema barbatumD. darwinianumD. ramificans, and D. subobscuratum; and four species have already been described previously, namely Acantholichen galapagoensisCora santacruzensisDictyonema 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.

References
  1. 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.12313CrossRefGoogle Scholar
  2. 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)80360-2CrossRefPubMedGoogle Scholar
  3. Aptroot A (2008) Lichens of St Helena and Ascension Island. Bot J Linn Soc 158:147–171CrossRefGoogle Scholar
  4. Aptroot A, Bungartz F (2007) The lichen genus Ramalina on the Galapagos. The Lichenologist. doi:10.1017/S0024282907006901Google Scholar
  5. Aptroot A, Sparrius LB (2008) Crustose Roccellaceae in the Galapagos Islands, with the new species Schismatomma spierii. Bryol 111(4):659–666CrossRefGoogle Scholar
  6. 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):510–516CrossRefGoogle Scholar
  7. Bensted-Smith H (2002) A biodiversity vision for the Galapagos Islands. Charles Darwin Foundation and World Wildlife Fund, Puerto AyoraGoogle Scholar
  8. Bungartz F (2008) Cyanolichens of the Galapagos Islands–the genera Collema and Leptogium. Sauteria 15:139–158Google Scholar
  9. Bungartz F, Lücking R, Aptroot A (2010) The family Graphidaceae (Ostropales, Lecanoromycetes) in the Galapagos Islands. Nova Hedwig. 90:1–44CrossRefGoogle Scholar
  10. 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:10.1639/0007-2745-116.4.358CrossRefGoogle Scholar
  11. 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.150.1.1CrossRefGoogle Scholar
  12. 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
  13. Bungartz F, Elix JA, Yánez-Ayabaca A, Archer AW (2015) Endemism in the genus Pertusaria (Pertusariales, lichenized Ascomycota) from the Galapagos Islands. Telopea 18:325–369CrossRefGoogle Scholar
  14. Bungartz F, Giralt M, Sheard JW, Elix JA (2016a) The lichen genus Rinodina (Physciaceae, Teloschistales) in the Galapagos Islands, Ecuador. The Bryologist 119:60–93CrossRefGoogle Scholar
  15. 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 48:489–515CrossRefGoogle Scholar
  16. Carlquist S (1974) Island biology. Columbia University Press, New YorkCrossRefGoogle Scholar
  17. 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/gkt1244CrossRefPubMedGoogle Scholar
  18. Cornejo C, Scheidegger C (2016) Cyanobacterial gardens: the liverwort Frullania asagrayana acts as a reservoir of lichen photobionts. Environ Microbiol Rep 8(3):352–357CrossRefPubMedGoogle Scholar
  19. 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/S0024282916000311CrossRefGoogle Scholar
  20. 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.2013.05.006CrossRefPubMedGoogle Scholar
  21. 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:10.3852/15-060CrossRefPubMedGoogle Scholar
  22. 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
  23. Darwin C (1859) On the origins of species by means of natural selection. Murray, LondonGoogle Scholar
  24. Dodge C (1935) Lichenes. HK Svenson: Plants of the Astor Expedition, 1930 (Galápagos and Cocos Islands). Am J Bot 22(2):221
  25. Elix JA, McCarthy PM (1998) Catalogue of the lichens of the smaller Pacific Islands. Bibl Lichenol 70:1–361Google Scholar
  26. Elix JA, McCarthy PM (2008) Checklist of Pacific Island Lichens. Australian Biological Resources Study, Canberra. Version 21 August 2008
  27. Goward T (1994) Living antiquities. Nat Can 1994:14–21Google Scholar
  28. Gradstein SR, Weber WA (1982) Bryogeography of the Galápagos Islands. J Hattori Bot Lab 52:127–152Google Scholar
  29. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  30. Jørgensen PM (1998) Acantholichen pannarioides, a new basidiolichen from South America. The Bryologist 101:444–447CrossRefGoogle Scholar
  31. Katoh K, Toh H (2010) Parallelization of the MAFFT multiple sequence alignment program. Bioinformatics 26:1899–1900CrossRefPubMedPubMedCentralGoogle Scholar
  32. Katoh K, Kuma K, Toh H, Miyata T (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518CrossRefPubMedPubMedCentralGoogle Scholar
  33. Larsson K-H (2007) Re-thinking the classification of corticioid fungi. Mycol Res 111:1040–1063. doi:10.1016/j.mycres.2007.08.001CrossRefPubMedGoogle Scholar
  34. 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 113:1154–1171CrossRefPubMedGoogle Scholar
  35. Linder DH (1934) The Templeton Crocker Expedition of the California Academy of Sciences, 1932. No. 18. Proc Calif Acad Sci Ser IV 21:211–224Google Scholar
  36. Losos JB, Ricklefs RE (2009) Adaptation and diversification on islands. Nature 457:830–836. doi:10.1038/nature07893CrossRefPubMedGoogle Scholar
  37. 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.0800258CrossRefPubMedGoogle Scholar
  38. 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.139.1.1CrossRefGoogle Scholar
  39. Lücking R, Dal-Forno M, Wilk K, Lawrey JD (2013b) Three new species of Dictyonema (lichenized Basidiomycota: Hygrophoraceae) from Bolivia. Acta Nova 6:4–16Google Scholar
  40. 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.1403517111CrossRefPubMedPubMedCentralGoogle Scholar
  41. 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-yCrossRefPubMedGoogle Scholar
  42. 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:10.1639/0007-2745-118.3.293CrossRefGoogle Scholar
  43. 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/s13225-016-0374-9Google Scholar
  44. Mason-Gamer RJ, Kellogg EA (1996) Testing for phylogenetic conflict among molecular data sets in the tribe Triticeae (Gramineae). Syst Biol 45:524–545CrossRefGoogle Scholar
  45. 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
  46. 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 117:119–160CrossRefGoogle Scholar
  47. Moncada B, Bungartz F, Lücking R (2016) The family Lobariaceae in the Galapagos Islands. The 8th IAL Symposium, Helsinki, Finland
  48. 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/gkq443CrossRefPubMedPubMedCentralGoogle Scholar
  49. 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/msq066CrossRefPubMedPubMedCentralGoogle Scholar
  50. Piercey-Normore MD, DePriest PT (2001) Algal switching among lichen symbioses. Am J Bot 88:1490–1498CrossRefPubMedGoogle Scholar
  51. 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:10.1639/0007-2745-117.4.386CrossRefGoogle Scholar
  52. 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.1117018109CrossRefPubMedPubMedCentralGoogle Scholar
  53. Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690CrossRefPubMedGoogle Scholar
  54. Stamatakis A, Ludwig T, Meier H (2005) RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21:456–463CrossRefPubMedGoogle Scholar
  55. Tehler A, Irestedt M, Bungartz F, Wedin M (2009) Evolution and reproduction modes in the Roccella galapagoensis aggregate (Roccellaceae, Arthoniales). Taxon 58:438–456Google Scholar
  56. 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
  57. 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:10.1639/0007-2745-117.4.368CrossRefGoogle Scholar
  58. 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 190–200Google Scholar
  59. Weber WA (1986) The lichen flora of the Galapagos Islands, Ecuador. Mycotaxon 27:451–497Google Scholar
  60. Weber WA (1993) Additions to the Galápagos and Cocos Islands lichen and bryophyte floras. Bryologist 96(3):431–434CrossRefGoogle Scholar
  61. Williamson M (1981) Island populations. Oxford: Oxford University Press xi, 286p.-illus., maps. En Maps, Geog
  62. 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-xCrossRefGoogle Scholar
  63. Yánez A, Ahti T, Bungartz F (2013) The family Cladoniaceae (Lecanorales) in the Galapagos Islands. Phytotaxa 129(1):1–33. doi:10.11646/phytotaxa.129.1.1CrossRefGoogle Scholar

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