Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-23T05:45:31.627Z Has data issue: false hasContentIssue false
  • English
  • Français

A molecular phylogenetic evaluation of the Ramalina siliquosa complex, with notes on species circumscription and relationships within Ramalina

Published online by Cambridge University Press:  03 June 2020

Scott LaGreca Open the ORCID record for Scott LaGreca [Opens in a new window] ,
H. Thorsten Lumbsch ,
Martin Kukwa Open the ORCID record for Martin Kukwa [Opens in a new window] ,
Xinli Wei ,
Jeong Eun Han ,
Kwang Hee Moon ,
Hiroyuki Kashiwadani ,
André Aptroot  and
Steven D. Leavitt
Scott LaGreca*
Affiliation:
Department of Biology, Box 90338, 137 Biological Sciences Building, 130 Science Drive, Duke University, Durham, NC27708-0338, USA
H. Thorsten Lumbsch
Affiliation:
Science & Education, The Field Museum, 1400 S. Lake Shore Drive, Chicago, IL60605, USA
Martin Kukwa
Affiliation:
Department of Plant Taxonomy and Nature Conservation, Faculty of Biology, University of Gdańsk, Wita Stwosza 59, PL-80-308 Gdańsk, Poland
Xinli Wei
Affiliation:
State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101, China
Jeong Eun Han
Affiliation:
National Institute of Biological Resources, Hwangyeong-ro 42, Seo-gu, Incheon22689, Republic of Korea
Kwang Hee Moon
Affiliation:
National Institute of Biological Resources, Hwangyeong-ro 42, Seo-gu, Incheon22689, Republic of Korea
Hiroyuki Kashiwadani
Affiliation:
National Museum of Nature and Science, 4-1-1, Amakubo, Tsukuba-shi, Ibaraki 305-0005, Japan
André Aptroot
Affiliation:
Laboratório de Botânica/Liquenologia, Central de Ciências Biológicas e da Saúde, Universidade Federal de Mato Grosso, Caixa Postal 549, CEP 79070-900, Campo Grande, Mato Grosso do Sul, Brazil
Steven D. Leavitt
Affiliation:
Department of Biology & M. L. Bean Life Science Museum, Brigham Young University, 4102 Life Science Building, Provo, UT84602, USA
*
Author for correspondence: Scott LaGreca. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Lichens of the Ramalina siliquosa complex dominate seashore cliffs in Europe and South-East Asia, but their taxonomy has been vigorously debated for over a century. On many cliffs, they exhibit a bewildering zonation of chemotypes that resembles the classic zonation of organisms that occupy the littoral zone below. Do the chemotypes represent separate species, or infraspecific variation? To better understand the systematics of this group, sequences from four genetic loci (ITS, IGS, RPB1 and RPB2) were obtained for 59 samples from Denmark, France, Iceland, Norway, UK, Japan and Korea, including all major chemotypes. Maximum likelihood analysis of these sequences, together with sequences from 36 other Ramalina species, reveals that the complex comprises two distinct phylogenetic lineages, each including multiple chemotypes. These two putative species-level lineages correspond to the currently accepted taxa R. cuspidata and R. siliquosa. There is no evidence that these two taxa are phylogenetic sister species. Consequently, the explanation of this chemotype complex as an example of ‘sibling speciation’ is rejected. Specimens traditionally called ‘R. siliquosa’ from South-East Asia form a third clade, identified here as R. semicuspidata, with an additional, divaricatic acid chemotype. Other results include a robustly supported clade of Ramalina species that produce medullary depsides and depsidones; this clade includes another well-supported clade of south-eastern United States coastal plain and tropical Ramalina species. By contrast, large, strap-shaped Ramalina species that lack medullary depsides and depsidones occur in separate lineages. In addition, close relationships between the following groups of species are indicated: R. farinacea with R. subfarinacea; R. fraxinea with R. leptocarpha, R. menziesii and R. subleptocarpha; R. sinensis with R. unifolia. Furthermore, a new, variolaric acid-only chemotype is reported for R. farinacea, and a new, acid-deficient chemotype is reported for a more broadly circumscribed R. culbersoniorum.

Keywords

LecanoromyceteslichensphylogenyRamalinaceaesystematicstaxonomy
Type
Standard Papers
Information
The Lichenologist , Volume 52 , Issue 3 , May 2020 , pp. 197 - 211
Copyright
Copyright © British Lichen Society 2020

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

Altschul, SF, Madden, TL, Schäffer, AA, Zhang, J, Zhang, Z, Miller, W and Lipman, DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.CrossRefGoogle ScholarPubMed
Alvarez, J, Paz-Bermúdez, G and Sánchez-Biezma, MJ (2001) Estudio quimiotaxonómico del género Ramalina Ach. (Lecanorales, Ascomycotina) en Galicia (NW de España). Cryptogamie Mycologie 22, 271–287.CrossRefGoogle Scholar
Argüello, A, Del-Prado, R, Cubas, P and Crespo, A (2007) Parmelina quercina (Parmeliaceae, Lecanorales) includes four phylogenetically supported morphospecies. Biological Journal of the Linnean Society 91, 455–467.CrossRefGoogle Scholar
Armaleo, D and Clerc, P (1995) A rapid and inexpensive method for the purification of DNA from lichens and their symbionts. Lichenologist 27, 207–213.CrossRefGoogle Scholar
Armaleo, D, Zhang, Y and Cheung, S (2008) Light might regulate divergently depside and depsidone accumulation in the lichen Parmotrema hypotropum by affecting thallus temperature and water potential. Mycologia 100, 565–576.CrossRefGoogle ScholarPubMed
Armaleo, D, Sun, X and Culberson, C (2011) Insights from the first putative biosynthetic gene cluster for a lichen depside and depsidone. Mycologia 103, 741–754.CrossRefGoogle ScholarPubMed
Baloch, E and Grube, M (2009) Pronounced genetic diversity in tropical epiphyllous lichen fungi. Molecular Ecology 18, 2185–2197.CrossRefGoogle ScholarPubMed
Bhattacharya, D, Lutzoni, F, Reeb, V, Simon, D, Nason, J and Fernandez, F (2000) Widespread occurrence of spliceosomal introns in the rDNA genes of ascomycetes. Molecular Biology and Evolution 17, 1971–1984.CrossRefGoogle ScholarPubMed
Bickford, D, Lohman, DJ, Sodhi, NS, Ng, PK, Meier, R, Winker, K, Ingram, KK and Das, I (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution 22, 148–155.CrossRefGoogle ScholarPubMed
Bowler, PA and Rundel, PW (1978) The Ramalina farinacea complex in North America: chemical, ecological and morphological variation. Bryologist 81, 386–403.CrossRefGoogle Scholar
Brodo, IM (1986) Interpreting chemical variation in lichens for systematic purposes. Bryologist 89, 132–138.CrossRefGoogle Scholar
Bryant, JP, Chapin, FS III and Klein, DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40, 357–368.CrossRefGoogle Scholar
Bu'Lock, JD (1961) Intermediary metabolism and antibiotic synthesis. Advances in Applied Microbiology 3, 293–342.CrossRefGoogle ScholarPubMed
Buschbom, J and Mueller, GM (2006) Testing ‘species pair’ hypotheses: evolutionary processes in the lichen-forming species complex Porpidia flavocoerulescens and Porpidia melinodes. Molecular Biology and Evolution 23, 574–586.CrossRefGoogle Scholar
Calvelo, S and Liberatore, S (2002) Catálogo de los liquenes de la Argentina [Checklist of Argentinian Lichens]. Kurtziana 29, 7–170.Google Scholar
Carbone, I and Kohn, LM (1999) A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91, 553–556.CrossRefGoogle Scholar
Chu, FJ, Seaward, MRD and Hodgkiss, IJ (2000) Effects of wave exposure and aspect on Hong Kong supralittoral lichens. Lichenologist 32, 155–170.CrossRefGoogle Scholar
CNALH (2019) Consortium of North American Lichen Herbaria. [WWW resource] URL http://lichenportal.org/portal/ [Accessed 3 December 2019].Google Scholar
Crespo, A, Ferencova, Z, Pérez-Ortega, S, Elix, JA and Divakar, PK (2010) Austroparmelina, a new Australasian lineage in parmelioid lichens (Parmeliaceae, Ascomycota). Systematics and Biodiversity 8, 209–221.CrossRefGoogle Scholar
Culberson, CF and Ammann, K (1979) Standardmethode zur Dünnschichtchromatographie von Flechtensubstanzen. Herzogia 5, 1–24.Google Scholar
Culberson, CF and Armaleo, D (1992) Induction of a complete secondary-product pathway in a cultured lichen fungus. Experimental Mycology 16, 52–63.CrossRefGoogle 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 128, 253–259.CrossRefGoogle Scholar
Culberson, CF, Culberson, WL and Johnson, A (1990) The Ramalina americana complex (Ascomycotina, Ramalinaceae): chemical and geographic correlations. Bryologist 93, 167–186.CrossRefGoogle Scholar
Culberson, WL (1966) Chimie et taxonomie des lichens du groupe Ramalina farinacea en Europe. Revue Bryologique et Lichénologique 34, 841–851.Google Scholar
Culberson, WL (1967) Analysis of chemical and morphological variation in the Ramalina siliquosa species complex. Brittonia 19, 333–352.CrossRefGoogle Scholar
Culberson, WL (1969 a) The use of chemistry in the systematics of the lichens. Taxon 18, 152–166.CrossRefGoogle Scholar
Culberson, WL (1969 b) The behavior of the species of the Ramalina siliquosa group in Portugal. Österreichische Botanische Zeitschrift 116, 85–94.CrossRefGoogle Scholar
Culberson, WL (1970) Ramalina siliquosa discovered in Japan. Journal of Japanese Botany 45, 295–296.Google Scholar
Culberson, WL (1973) The Parmelia perforata group: niche characteristics of chemical races, speciation by parallel evolution, and a new taxonomy. Bryologist 76, 20–29.CrossRefGoogle Scholar
Culberson, WL (1986) Chemistry and sibling speciation in the lichen-forming fungi: ecological and biological considerations. Bryologist 89, 123–131.CrossRefGoogle Scholar
Culberson, WL and Culberson, CF (1967) Habitat selection by chemically differentiated races of lichens. Science 158, 1195–1197.CrossRefGoogle ScholarPubMed
Culberson, WL and Culberson, CF (1970) A phylogenetic view of chemical evolution in the lichens. Bryologist 73, 1–31.CrossRefGoogle Scholar
Culberson, WL and Culberson, CF (1973) Parallel evolution in lichen-forming fungi. Science 180, 196–198.CrossRefGoogle Scholar
Culberson, WL and Culberson, CF (1977) Chemosyndromic variation in lichens. Systematic Botany 1, 325–339.CrossRefGoogle Scholar
Culberson, WL, Culberson, CF and Johnson, A (1977) Correlations between secondary-product chemistry and ecogeography in the Ramalina siliquosa group (lichens). Plant Systematics and Evolution 127, 191–200.CrossRefGoogle Scholar
Culberson, WL, Culberson, CF and Johnson, A (1993) Speciation in lichens of the Ramalina siliquosa complex (Ascomycotina, Ramalinaceae): gene flow and reproductive isolation. American Journal of Botany 80, 1472–1481.CrossRefGoogle Scholar
de Paz, GA, Cubas, P, Crespo, A, Elix, JA and Lumbsch, HT (2012) Transoceanic dispersal and subsequent diversification on separate continents shaped diversity of the Xanthoparmelia pulla group (Ascomycota). PLoS ONE 7, e39683.CrossRefGoogle Scholar
Del-Prado, R, Divakar, PK, Lumbsch, HT and Crespo, AM (2016) Hidden genetic diversity in an asexually reproducing lichen forming fungal group. PLoS ONE 11, e0161031.CrossRefGoogle Scholar
DePriest, PT (1994) Variation in the Cladonia chlorophaea complex II: ribosomal DNA variation in a Southern Appalachian population. Bryologist 97, 117–126.CrossRefGoogle Scholar
DePriest, PT (1995) Phylogenetic analyses of the variable ribosomal DNA of the Cladonia chlorophaea complex. Cryptogamic Botany 5, 60–70.Google Scholar
DePriest, PT and Been, MD (1992) Numerous Group I introns with variable distributions in the ribosomal DNA of a lichen fungus. Journal of Molecular Biology 228, 315–321.CrossRefGoogle Scholar
Divakar, PK, Leavitt, SD, Molina, MC, Del-Prado, R, Lumbsch, HT and Crespo, A (2015) A DNA barcoding approach for identification of hidden diversity in Parmeliaceae (Ascomycota): Parmelia sensu stricto as a case study. Botanical Journal of the Linnean Society 180, 21–29.CrossRefGoogle Scholar
Dolnik, C, Beck, A and Zarabska, D (2010) Distinction of Cladonia rei and C. subulata based on molecular, chemical and morphological characteristics. Lichenologist 42, 373–386.CrossRefGoogle Scholar
Drummond, AJ and Rambaut, A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.CrossRefGoogle ScholarPubMed
Drummond, AJ, Ho, SYW, Phillips, MJ and Rambaut, A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biology 4, e88.CrossRefGoogle Scholar
Elix, JA and Stocker-Wörgötter, E (2008) Biochemistry and secondary metabolites. In Nash, TH III (ed.), Lichen Biology. Cambridge: Cambridge University Press, pp. 104–133.CrossRefGoogle Scholar
Esslinger, TL (2019) A cumulative checklist for the lichen-forming, lichenicolous and allied fungi of the continental United States and Canada, version 23. Opuscula Philolichenum 18, 102–378.Google Scholar
Farrell, TM (1991) Models and mechanisms of succession: an example from a rocky intertidal community. Ecological Monographs 61, 95–113.CrossRefGoogle Scholar
Figueira, R, Pacheco, AMG, Sousa, AJ and Catarino, F (1999 a) Biological monitoring of airborne salinity through epiphytic lichens. Revista Biologia (Lisboa) 17, 3–12.Google Scholar
Figueira, R, Pacheco, AMG, Sousa, AJ and Catarino, F (1999 b) Variability of sea-salt deposition assessed by lichen monitoring in the south-west Portuguese coast. In Brebbia, CA, Jacobson, M and Power, H (eds), Air Pollution VII. Billerica, Massachusetts: WIT Press, pp. 599–607.Google Scholar
Fink, B (1935) The Lichen Flora of the United States. Ann Arbor: University of Michigan Press.CrossRefGoogle Scholar
Fox, EM and Howlett, BJ (2008) Secondary metabolism: regulation and role in fungal biology. Current Opinion in Microbiology 11, 481–487.CrossRefGoogle ScholarPubMed
Futuyma, DJ and Kirkpatrick, M (2017) Evolutionary Biology, Fourth Edition. New York: Oxford University Press.Google Scholar
Gardes, M and Bruns, TD (1993) ITS primers with enhanced specificity for basidiomycetes – application to the identification of mycorrhizae and rusts. Molecular Ecology 2, 113–118.CrossRefGoogle ScholarPubMed
Gargas, A, DePriest, PT and Taylor, JW (1995) Positions of multiple insertions in SSU rDNA of lichen-forming fungi. Molecular Biology and Evolution 12, 208–218.Google ScholarPubMed
Gasparyan, A, Sipman, HJM and Lücking, R (2017) Ramalina europaea and R. labiosorediata, two new species of the R. pollinaria group (Ascomycota: Ramalinaceae), and new typifications for Lichen pollinarius and L. squarrosus. Lichenologist 49, 301–319.CrossRefGoogle Scholar
Gerlach, ADCL, Toprak, Z, Naciri, Y, Caviró, EA, de Silveira, RMB and Clerc, P (2019) New insights into the Usnea cornuta aggregate (Parmeliaceae, lichenized Ascomycota): molecular analysis reveals high genetic diversity correlated with chemistry. Molecular Phylogenetics and Evolution 131, 125–137.CrossRefGoogle ScholarPubMed
Gjelstrup, P and Søchting, U (1979) Cryptostigmatid mites (Acarina) associated with Ramalina siliquosa (Lichenes) on Bornholm in the Baltic. Pedobiologia 19, 237–245.Google Scholar
Grant, V (1981) Plant Speciation, Second Edition. New York: Columbia University Press.CrossRefGoogle Scholar
Grewe, F, Lagostina, E, Wu, H, Printzen, C and Lumbsch, HT (2018) Population genomic analyses of RAD sequences resolves the phylogenetic relationship of the lichen-forming fungal species Usnea antarctica and Usnea aurantiacoatra. MycoKeys 49, 91–113.CrossRefGoogle Scholar
Groner, U and LaGreca, S (1997) The ‘Mediterranean’ Ramalina panizzei north of the Alps: morphological, chemical, and rDNA sequence data. Lichenologist 29, 441–454.CrossRefGoogle Scholar
Grube, M and Kantvilas, G (2006) Siphula represents a remarkable case of morphological convergence in sterile lichens. Lichenologist 38, 241–249.CrossRefGoogle Scholar
Gumboski, EL, Eliasaro, S, Scur, MC, Lorenz-Lemke, AP and Borges da Silveira, RM (2018) A new riparian species of Ramalina (Ramalinaceae) from Brazil, with a key to neotropical saxicolous species. Lichenologist 50, 541–553.CrossRefGoogle Scholar
Gutiérrez, G, Blanco, O, Divakar, PK, Lumbsch, HT and Crespo, A (2007) Patterns of Group I intron presence in nuclear SSU rDNA of the lichen family Parmeliaceae. Journal of Molecular Evolution 64, 181–195.CrossRefGoogle Scholar
Hamada, N (1981) The effect of temperature on the content of the medullary depsidone salazinic acid in Ramalina siliquosa (lichens). Canadian Journal of Botany 60, 383–385.CrossRefGoogle Scholar
Hamada, N (1985) Distribution of the Ramalina siliquosa complex (lichens) having depsidone-negative ramuli. Journal of Japanese Botany 60, 8–15.Google Scholar
Hawksworth, DL (1968) A note on the chemical strains of the lichen Ramalina subfarinacea. Botaniska Notiser 121, 317–320.Google Scholar
Hayward, GC, Blanchon, DJ and Lumbsch, HT (2014) Molecular data support Ramalina ovalis as a distinct lineage (Ramalinaceae, Ascomycota). Lichenologist 46, 553–561.CrossRefGoogle Scholar
Heled, J and Drummond, AJ (2010) Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution 27, 570–580.CrossRefGoogle ScholarPubMed
Hodkinson, BP and Lendemer, JC (2011) Molecular analyses reveal semi-cryptic species in Xanthoparmelia tasmanica. Bibliotheca Lichenologica 106, 108–119.Google Scholar
Howe, RH Jr (1912) Classification de la Famille des Usneaceae dans l'Amerique du Nord. Ph.D. thesis, Université de Paris.Google Scholar
Howe, RH Jr (1913) North American species of the genus Ramalina. Part II. Bryologist 16, 81–89.CrossRefGoogle Scholar
Hyvärinen, M, Walter, B and Koopmann, R (2002) Secondary metabolites in Cladina stellaris in relation to reindeer grazing and thallus nutrient content. Oikos 96, 273–280.CrossRefGoogle Scholar
Joneson, S (2003) Studies in Ramalina (Ascomycotina, Lecanorales) with emphasis on the R. almquistii species complex. M.Sc. thesis, University of Washington.Google Scholar
Kashiwadani, H (1992) Ramalina siliquosa (Huds.) A. L. Sm. and R. subbreviuscula Asha. in Japan. Memoirs of the National Science Museum (Tokyo) 25, 63–69.Google Scholar
Katoh, K and Standley, DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.CrossRefGoogle ScholarPubMed
Krog, H and James, PW (1977) The genus Ramalina in Fennoscandia and the British Isles. Norwegian Journal of Botany 24, 15–43.Google Scholar
LaGreca, SA (1997) The systematics and evolution of the lichen genus Ramalina with an emphasis on the R. americana chemotype complex. Ph.D. thesis, Duke University.Google Scholar
LaGreca, S (1999) A phylogenetic evaluation of the Ramalina americana chemotype complex (lichenized Ascomycota, Ramalinaceae) based on rDNA ITS sequence data. Bryologist 102, 602–618.CrossRefGoogle Scholar
LaGreca, S and Lumbsch, HT (2001) No evidence from rDNA ITS sequence data for a placement of Ramalinora in the Ramalinaceae. Lichenologist 33, 172–176.CrossRefGoogle Scholar
Lane, DJ, Pace, B, Olsen, GJ, Stahl, DA, Sogin, ML and Pace, NR (1985) Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proceedings of the National Academy of Sciences of the United States of America 82, 6955–6959.CrossRefGoogle ScholarPubMed
Laundon, JR (1966) Hudson's Lichen siliquosus from Wiltshire. Lichenologist 3, 236–241.CrossRefGoogle Scholar
Leavitt, SD, Divakar, PK, Ohmura, Y, Wang, L-S, Esslinger, TL and Lumbsch, HT (2015) Who's getting around? Assessing species diversity and phylogeography in the widely distributed lichen-forming fungal genus Montanelia (Parmeliaceae, Ascomycota). Molecular Phylogenetics and Evolution 90, 85–96.CrossRefGoogle Scholar
Leavitt, SD, Esslinger, TL, Divakar, PK, Crespo, A and Lumbsch, HT (2016) Hidden diversity before our eyes: delimiting and describing cryptic lichen-forming fungal species in camouflage lichens (Parmeliaceae, Ascomycota). Fungal Biology 120, 1374–1391.CrossRefGoogle Scholar
Leavitt, SD, Westberg, M, Nelsen, MP, Elix, JA, Timdal, E, Sohrabi, M, St. Clair, LL, Williams, L, Wedin, M and Lumbsch, HT (2018) Multiple, distinct intercontinental lineages but isolation of Australian populations in a cosmopolitan lichen-forming fungal taxon, Psora decipiens (Psoraceae, Ascomycota). Frontiers in Microbiology 9, 283.CrossRefGoogle Scholar
Lee, Y-H and Lin, C-P (2012) Pleistocene speciation with and without gene flow in Euphaea damselflies of subtropical and tropical East Asian islands. Molecular Ecology 21, 3739–3756.CrossRefGoogle ScholarPubMed
Lendemer, JC (2012) A tale of two species: molecular data reveal the chemotypes of Lepraria normandinoides (Stereocaulaceae) to be two sympatric species. Journal of the Torrey Botanical Society 139, 118–130.CrossRefGoogle Scholar
Lewis, JR (1964) The Ecology of Rocky Shores. London: English University Press.Google Scholar
Liu, YJ, Whelen, S and Hall, BD (1999) Phylogenetic relationships among ascomycetes: evidence from an RNA polymerase II subunit. Molecular Biology and Evolution 16, 1799–1808.CrossRefGoogle Scholar
Lohtander, K, Källersjö, M and Tehler, A (1998) Dispersal strategies in Roccellina capensis (Arthoniales). Lichenologist 30, 341–350.CrossRefGoogle Scholar
Lumbsch, HT (1998) Taxonomic use of metabolic data in lichen-forming fungi. In Frisvad, JC, Bridge, PD and Arora, DK (eds), Chemical Fungal Taxonomy. New York: Marcel Dekker, pp. 345–387.Google Scholar
Lynge, B (1940) Lichens from Iceland collected by Norwegian botanists in 1937 and 1938. I. Macrolichens. Skrifter utgitt av det Norske videnskaps-akademi i Oslo I: Matematisk-naturvidenskabelig klasse 1940, 1–56.Google Scholar
Marsh, J (1996) A cladistic classification of the lichen family Ramalinaceae (lichenized Ascomycotina) using morphological and molecular data. Ph.D. thesis, University of Arizona.Google Scholar
Matheny, PB, Liu, YJ, Ammirati, JF and Hall, BD (2002) Using RPB1 sequences to improve phylogenetic inference among mushrooms (Inocybe, Agaricales). American Journal of Botany 89, 688–698.CrossRefGoogle Scholar
Mattsson, JE (1990) The combination of protein characters and secondary-product biogenesis as a taxonomic tool in lichen systematics. In Abstracts of the Fourth International Mycological Congress, 28 August–3 September 1990, Regensburg, Germany, p. 332.Google Scholar
Mattsson, JE and Kärnefelt, I (1986) Protein banding patterns in the Ramalina siliquosa group. Lichenologist 18, 231–240.CrossRefGoogle Scholar
Mayr, E (1970) Populations, Species and Evolution: an Abridgment of Animal Species and Evolution. Cambridge: Belknap Press.Google Scholar
Miadlikowska, J, Kauff, F, Högnabba, F, Oliver, JC, Molnár, K, Fraker, E, Gaya, E, Hafellner, J, Hofstetter, V, Gueidan, C, et al. (2014) A multigene phylogenetic synthesis for the class Lecanoromycetes (Ascomycota): 1307 fungi representing 1139 infrageneric taxa, 317 genera and 66 families. Molecular Phylogenetics and Evolution 79, 132–168.CrossRefGoogle ScholarPubMed
Miller, MA, Pfeiffer, W and Schwartz, T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE), 14 November 2010, New Orleans, Louisiana, pp. 1–8.Google Scholar
Mishler, BD (1996) Individuality, pluralism, and the phylogenetic species concept. In Brandon, RN (ed.), Studies in Philosophy and Biology: Concepts and Methods in Evolutionary Biology. New York: Cambridge University Press, pp. 106–160.Google Scholar
Moon, KH (2013) Lichen-forming and Lichenicolous Fungi of Korea. Incheon, South Korea: National Institute of Biological Resources.Google Scholar
Moore, PG and Seed, R (1986) The Ecology of Rocky Coasts. New York: Columbia University Press.Google Scholar
Muggia, L, Grube, M and Tretiach, M (2008) Genetic diversity and photobiont associations in selected taxa of the Tephromela atra group (Lecanorales, lichenised Ascomycota). Mycological Progress 7, 147–160.CrossRefGoogle Scholar
Myllys, L, Lohtander, K and Tehler, A (2001) β-tubulin, ITS and group I intron sequences challenge the species pair concept in Physcia aipolia and P. caesia. Mycologia 93, 335–343.Google Scholar
Nevo, E (2001) Evolution of genome-phenome diversity under environmental stress. Proceedings of the National Academy of Sciences of the United States of America 98, 6233–6240.CrossRefGoogle ScholarPubMed
Nimis, PL (2016) The Lichens of Italy. A Second Annotated Catalogue. Trieste: Università Degli Studi Di Trieste.Google Scholar
Nylander, W (1870) Recognitio monographica Ramalinarum. Bulletin de la Société Linnéenne de Normandie, sér. 2 4, 101–181.Google Scholar
Nylander, W (1890) Lichenes Japoniae. Accedunt Observationibus Lichenes Insulae Labuan. Paris: P. Schmidt.Google Scholar
Ohmura, Y, Moon, KH and Kashiwadani, H (2008) Morphology and molecular phylogeny of Ramalina pollinaria, R. sekika and R. yasudae (Ramalinaceae, lichenized Ascomycotina). Journal of Japanese Botany 83, 156–164.Google Scholar
Otálora, MA, Martínez, I, Aragón, G and Molina, MC (2010) Phylogeography and divergence date estimates of a lichen species complex with a disjunct distribution pattern. American Journal of Botany 97, 216–223.CrossRefGoogle ScholarPubMed
Parrot, D, Jan, S, Baert, N, Guyot, S and Tomasi, S (2013) Comparative metabolite profiling and chemical study of Ramalina siliquosa complex using LC-ESI-MS/MS approach. Phytochemistry 89, 114–124.CrossRefGoogle ScholarPubMed
Peksa, O and Škaloud, P (2011) Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae). Molecular Ecology 20, 3936–3948.CrossRefGoogle Scholar
Pérez-Vargas, I and Pérez-Ortega, S (2014) A new endemic Ramalina species from the Canary Islands (Ascomycota, Lecanorales). Phytotaxa 159, 269–278.CrossRefGoogle Scholar
Posada, D (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.CrossRefGoogle ScholarPubMed
Prata, EMB, Sass, C, Rodrigues, DP, Domingos, FMCB, Specht, CD, Damasco, G, Ribas, CC, Fine, PVA and Vicentini, A (2018) Towards integrative taxonomy in Neotropical botany: disentangling the Pagamea guianensis species complex (Rubiaceae). Botanical Journal of the Linnean Society 188, 213–231.CrossRefGoogle Scholar
Rambaut, A and Drummond, AJ (2003) Tracer v1.6. [WWW resource] URL http://beast.bio.ed.ac.uk/TracerGoogle Scholar
Rambaut, A and Drummond, AJ (2009) TreeAnnotator v1.8.3. [WWW resource] URL http://beast.bio.ed.ac.uk/Google Scholar
Ranković, B (ed.) (2015) Lichen Secondary Metabolites: Bioactive Properties and Pharmaceutical Potential. Cham, Switzerland: Springer International Publishing.Google Scholar
Räsänen, V (1940) Lichenes ab A. Yasuda et aliis in Japonia collecti (I). Journal of Japanese Botany 16, 82–98.Google Scholar
Rogers, RW (1989) Chemical variation and the species concept in lichenized ascomycetes. Botanical Journal of the Linnean Society 101, 229–239.CrossRefGoogle Scholar
Rohland, N, Reich, D, Mallick, S, Meyer, M, Green, RE, Georgiadis, NJ, Roca, AL and Hofreiter, M (2010) Genomic DNA sequences from mastodon and woolly mammoth reveal deep speciation of forest and savanna elephants. PLoS Biology 8(12), e1000564.CrossRefGoogle ScholarPubMed
Rundel, PW and Bowler, PA (1976) Ramalina leptocarpha and R. subleptocarpha: a fertile-sorediate species pair. Bryologist 79, 364–369.CrossRefGoogle Scholar
Sarver, SK and Foltz, DW (1993) Genetic population structure of a species complex of blue mussels (Mytilus spp.). Marine Biology 117, 105–112.CrossRefGoogle Scholar
Schneider, K, Resl, P and Spribille, T (2016) Escape from the cryptic species trap: lichen evolution on both sides of a cyanobacterial acquisition event. Molecular Ecology 25, 3453–3468.CrossRefGoogle ScholarPubMed
Sela, I, Ashkenazy, H, Katoh, K and Pupko, T (2015) GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Research 43, W7–W14.CrossRefGoogle ScholarPubMed
Sérusiaux, E, van den Boom, P and Ertz, D (2010) A two-gene phylogeny shows the lichen genus Niebla (Lecanorales) is endemic to the New World and does not occur in Macaronesia nor in the Mediterranean basin. Fungal Biology 114, 528–537.CrossRefGoogle Scholar
Sheard, JW (1978 a) The taxonomy of the Ramalina siliquosa species aggregate (lichenized ascomycetes). Canadian Journal of Botany 56, 916–938.CrossRefGoogle Scholar
Sheard, JW (1978 b) The comparative ecology and distribution and within-species variation of the lichenized Ascomycetes Ramalina cuspidata and R. siliquosa in the British Isles. Canadian Journal of Botany 56, 939–952.CrossRefGoogle Scholar
Sheard, JW and James, PW (1976) Typification of the taxa belonging to the R. siliquosa aggregate. Lichenologist 8, 35–46.CrossRefGoogle Scholar
Singh, G, Dal Grande, F, Divakar, PK, Otte, J, Leavitt, SD, Szczepanska, K, Crespo, A, Rico, VJ, Aptroot, A, Cáceres, MES, et al. (2015) Coalescent-based species delimitation approach uncovers high cryptic diversity in the cosmopolitan lichen-forming fungal genus Protoparmelia (Lecanorales, Ascomycota). PLoS ONE 10, e0124625.CrossRefGoogle Scholar
Smith, CW, Aptroot, A, Coppins, BJ, Fletcher, A, Gilbert, OL, James, PW and Wolseley, PA (eds) (2009) The Lichens of Great Britain and Ireland. London: British Lichen Society.Google Scholar
Søchting, U (1976) The Ramalina siliquosa aggregate on the Danish island of Bornholm. Særtryk af Botanisk Tidsskrift 71, 87–94.Google Scholar
Spribille, T, Tuovinen, V, Resl, P, Vanderpool, D, Wolinski, H, Aime, MC, Schneider, K, Stabentheiner, E, Toome-Heller, M, Thor, G, et al. (2016) Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353, 488–492.CrossRefGoogle ScholarPubMed
Stamatakis, A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313.CrossRefGoogle ScholarPubMed
Stenroos, S, Velmala, S, Pykälä, J and Ahti, T (eds) (2016) Lichens of Finland. Norrlinia 30, 1–896.Google Scholar
Steyskal, GC (1972) The meaning of the term ‘sibling species’. Systematic Zoology 21, 446.CrossRefGoogle Scholar
Stiller, JW and Hall, BD (1997) The origin of red algae: implications for plastid evolution. Proceedings of the National Academy of Sciences of the United States of America 94, 4520–4525.CrossRefGoogle ScholarPubMed
Stocker-Wörgötter, E (2001) Experimental studies of the lichen symbiosis: DNA-analyses, differentiation and secondary chemistry of selected mycobionts, artificial resynthesis of two- and tripartite symbioses. Symbiosis 30, 207–227.Google Scholar
Stocker-Wörgötter, E, Elix, JA and Grube, M (2004) Secondary chemistry of lichen-forming fungi: chemosyndromic variation and DNA-analyses of cultures and chemotypes in the Ramalina farinacea complex. Bryologist 107, 152–162.CrossRefGoogle Scholar
Struck, TH, Feder, JL, Bendiksby, M, Birkeland, S, Cerca, J, Gusarov, VI, Kistenich, S, Larsson, K-H, Liow, LH, Nowak, MD, et al. (2017) Finding evolutionary processes hidden in cryptic species. Trends in Ecology and Evolution 33, 153–163.CrossRefGoogle ScholarPubMed
Tehler, A (1982) The species pair concept in lichenology. Taxon 31, 708–717.CrossRefGoogle Scholar
Thomson, JW (1990) Ramalina unifolia sp. nov. from North America. Bryologist 93, 341–342.CrossRefGoogle Scholar
Timsina, BA, Stocker-Wörgötter, E and Piercey-Normore, MD (2012) Monophyly of some North American species of Ramalina and inferred polyketide synthase gene function. Botany 90, 1295–1307.CrossRefGoogle Scholar
Timsina, BA, Sorensen, JL, Weihrauch, D and Piercey-Normore, MD (2013) Effect of aposymbiotic conditions on colony growth and secondary metabolite production in the lichen-forming fungus Ramalina dilacerata. Fungal Biology 117, 731–743.CrossRefGoogle ScholarPubMed
Underwood, AJ and Jernakoff, P (1984) The effects of tidal height, wave-exposure, seasonality and rock-pools on grazing and the distribution of intertidal macroalgae in New South Wales. Journal of Experimental Marine Biology and Ecology 75, 71–96.CrossRefGoogle Scholar
White, TJ, Bruns, T, Lee, S and Taylor, JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In Innis, MA, Gelfand, DH, Sninsky, JJ and White, TJ (eds), PCR Protocols: A Guide to Methods and Applications. San Diego: Academic Press, pp. 315–322.Google Scholar
Widhelm, TJ, Egan, RS, Bertoletti, FR, Asztalos, MJ, Kraichak, E, Leavitt, SD and Lumbsch, HT (2016) Picking holes in traditional species delimitations: an integrative taxonomic reassessment of the Parmotrema perforatum group (Parmeliaceae, Ascomycota). Botanical Journal of the Linnean Society 182, 868–884.CrossRefGoogle Scholar
Yamamoto, Y, Takahagi, T, Sato, F, Kinoshita, Y, Nakashima, H and Yoshimura, I (2001) Screening of halophilic or salt tolerant lichen mycobionts cultured on sodium chloride enriched media. Journal of the Hattori Botanical Laboratory 90, 307–314.Google Scholar
Zedda, L (2002) The epiphytic lichens on Quercus in Sardinia (Italy) and their value as ecological indicators. Englera 24, 1–457.Google Scholar
Zeigler, DD (2014) Evolution: Components and Mechanisms. New York: Elsevier Publishing.CrossRefGoogle Scholar
Zopf, W (1906) Biologische und morphologische Beobachtungen an Flechten. II. Berichte der Deutschen Botanischen Gesellschaft 24, 574–580.Google Scholar
Supplementary material: File

LaGreca et al. Supplementary materials

Download LaGreca et al. Supplementary materials(File)
File 31.3 KB
Supplementary material: File

LaGreca et al. Supplementary materials

Download LaGreca et al. Supplementary materials(File)
File 38.4 KB
Supplementary material: File

LaGreca et al. Supplementary materials

Download LaGreca et al. Supplementary materials(File)
File 317.8 KB
Supplementary material: Image

LaGreca et al. Supplementary materials

Download LaGreca et al. Supplementary materials(Image)
Image 2.2 MB