Integrating coalescent and phylogenetic approaches to delimit species in the lichen photobiont Trebouxia

Molecular Phylogenetics and Evolution

Volumn 76, Issue 1, 2014, Pages 202-210

  Sadowska Deś, Anna D ^a,b   Dal Grande, Francesco ^b   Lumbsch, H Thorsten ^c   Beck, Andreas ^d,e   Otte, Jürgen ^b   Hur, Jae Seoun ^f   Kim, Jung A ^f   Schmitt, Imke ^a,b  

^a GOETHE UNIVERSITY   (Germany)

^b BIODIVERSITY AND CLIMATE RESEARCH CENTRE BIK F   (Germany)

^c FIELD MUSEUM OF NATURAL HISTORY   (United States)

^d BAVARIAN NATURAL HISTORY COLLECTIONS   (Germany)

^e UNIVERSITY OF MUNICH   (Germany)

^f Sunchon National University   (South Korea)

Author keywords

Cryptic species; Environmental specialization; Lasallia pustulata; Photobiont sharing; Terrestrial green algae

Indexed keywords

ASEXUAL REPRODUCTION; CLASSIFICATION; DNA SEQUENCE; GENETIC VARIABILITY; GENETICS; GREEN ALGA; LICHEN (ORGANISM); PHYLOGENY; PHYSIOLOGY;

CHLOROPHYTA; GENETIC VARIATION; LICHENS; PHYLOGENY; REPRODUCTION, ASEXUAL; SEQUENCE ANALYSIS, DNA;

EID: 84898623609     PISSN: 10557903     EISSN: 10959513     Source Type: Journal    
DOI: 10.1016/j.ympev.2014.03.020     Document Type: Article

References (107)

1. Ahmadjian V. Coevolution in Lichens. Ann. N. Y. Acad. Sci. 1987, 503:307-315.
2. Avise J.C., Ball R.M. Principles of genealogical concordance in species concepts and biological taxonomy. Oxf. Surv. Evol. Biol. 1990, 7:45-67.
3. Bálint M., Domisch S., Engelhardt C.H.M., Haase P., Lehrian S., Sauer J., Theissinger K., Pauls S.U., Nowak C. Cryptic biodiversity loss linked to global climate change. Nat. Clim. Change 2011, 1:313-318.
4. Barraclough T.G., Birky C.W., Burt A. Diversification in sexual and asexual organisms. Evolution 2003, 57:2166-2172.
5. Baum, D.A., Shaw, K.L., 1995. Genealogical perspectives on the species problem. In: Hoch, P.C., Stephenson A.G. (Eds.), Experimental and Molecular Approaches to Plant Biosystematics. Missouri Botanical Garden, St. Louis, pp. 289-303.
6. Beck A. Photobiont inventory of a lichen community growing on heavy-metal-rich rock. Lichenologist 1999, 31:501-510.
7. Beck A., Mayr C. Nitrogen and carbon isotope variability in the green-algal lichen Xanthoria parietina and their implications on mycobiont-photobiont interactions. Ecol. Evol. 2012, 2:3132-3144.
8. Beck A., Friedl T., Rambold G. Selectivity of photobiont choice in a defined lichen community: inferences from cultural and molecular studies. New Phytol. 1998, 139:709-720.
9. Beck A., Kasalicky T., Rambold G. Myco-photobiontal selection in a Mediterranean cryptogam community with Fulgensia fulgida. New Phytol. 2002, 153:317-326.
10. Bickford D., Lohman D.J., Sodhi N.S., Ng P.K.L., Meier R., Winker K., Ingram K.K., Das I. Cryptic species as a window on diversity and conservation. Trends Ecol. Evol. 2007, 22:148-155.
11. Blaha J., Baloch E., Grube M. High photobiont diversity associated with the euryoecious lichen-forming ascomycete Lecanora rupicola (Lecanoraceae, Ascomycota). Biol. J. Linn. Soc. 2006, 88:283-293.
12. Campbell V., Legendre P., Lapointe F.J. The performance of the Congruence Among Distance Matrices (CADM) test in phylogenetic analysis. BMC Evol. Biol. 2011, 11:64.
13. Carstens B.C., Dewey T.A. Species delimitation using a Combined Coalescent and Information-Theoretic approach: an example from North American Myotis bats. Syst. Biol. 2010, 59:400-414.
14. Carstens B.C., Pelletier T.A., Reid N.M., Satler J.D. How to fail at species delimitation. Mol. Ecol. 2013, 22:4369-4383.
15. Casano L.M., del Campo E.M., García-Breijo F.J., Reig-Armiñana J., Gasulla F., del Hoyo A., Guéra A., Barreno E. Two Trebouxia algae with different physiological performances are ever-present in lichen thalli of Ramalina farinacea. Coexistence versus competition?. Environ. Microbiol. 2011, 13:806-818.
16. Crespo A., Lumbsch H.T. Cryptic species in lichen-forming fungi. IMA Fungus: Glob. Mycol. J. 2010, 1:167-170.
17. Crespo A., Perez-Ortega S. Cryptic species and species pairs in lichens: a discussion on the relationship between molecular phylogenies and morphological characters. An. Jard. Bot. Madr. 2009, 66:71-81.
18. Cubero O.F., Crespo A. Isolation of nucleic acids from lichens. Protocols in Lichenology 2002, 381-391. Springer, Berlin. I.C. Kranner, R.P. Beckett, A.K. Varma (Eds.).
19. Dal Grande F., Widmer I., Wagner H.H., Scheidegger C. Vertical and horizontal photobiont transmission within populations of a lichen symbiosis. Mol. Ecol. 2012, 21:3159-3172.
20. Dal Grande F., Alors D., Divakar P.K., Bálint M., Crespo A., Schmitt I. Insights into intrathalline genetic diversity of the cosmopolitan lichen symbiotic green alga Trebouxia decolorans Ahmadjian using microsatellite markers. Mol. Phylogenet. Evol. 2014, 72:54-60.
21. Dal Grande F., Beck A., Cornejo C., Singh G., Cheenacharoen S., Nelsen M.P., Scheidegger C. Molecular phylogeny and symbiotic selectivity of the green algal genus Dictyochloropsis s.l. (Trebouxiophyceae): a polyphyletic and widespread group forming photobiont-mediated guilds in the lichen family Lobariaceae. New Phytol. 2014, 202:455-470. 10.1111/nph.12678.
22. Darriba D., Taboada G.L., Doallo R., Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 2012, 9:772.
23. Del Campo E.M., Catalá S., Gimeno J., del Hoyo A., Martínez-Alberola F., Casano L.M., Grube M., Barreno E. The genetic structure of the cosmopolitan three-partner lichen Ramalina farinacea evidences the concerted diversification of symbionts. FEMS Microbiol. Ecol. 2013, 83:310-323.
24. Dettman J., Jacobson D.J., Taylor J.W. A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Evol. Int. J. Org. Evol. 2003, 57:2703-2720.
25. Dettman J., Anderson J.B., Kohn L.M. Divergent adaptation promotes reproductive isolation among experimental populations of the filamentous fungus Neurospora. BMC Evol. Biol. 2008, 8:35.
26. Doering M., Piercey-Normore M.D. Genetically divergent algae shape an epiphyticlichen community on Jack Pine in Manitoba. Lichenologist 2009, 41:69-80.
27. Drummond, A.J., Ashton, B., Buxton, S., Cheung, M., 2011. Geneious v5.4. <>. http://www.geneious.com/.
28. Drummond A.J., Suchard M.A., Xie D., Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 2012, 29:1969-1973.
29. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
30. Esselstyn J.A., Evans B.J., Sedlock J.L., Anwarali Khan F.A., Heaney L.R. Single-locus species delimitation: a test of the mixed Yule-coalescent model, with an empirical application to Philippine round-leaf bats. Proc. Biol. Sci. 2012, 279:3678-3686.
31. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985, 39:783.
32. Fernandez-Mendoza, Domaschke S., Gracía M.A., Jordan P., Martín M.P., Printzen C. Population structure of mycobionts and photobionts of the widespread lichen Cetraria aculeata. Mol. Ecol. 2011, 20:1208-1232.
33. Friedl T. Thallus development and phycobionts of the parasitic lichen Diploschistes muscorum. Lichenologist 1987, 19:183-191.
34. Friedl T., Büdel B. Photobionts. Lichen Biology 2008, 9-26. Cambridge University Press, Cambridge, UK. third ed. T.H. Nash (Ed.).
35. Fujisawa T., Barraclough T.G. Delimiting species using single-locus data and the generalized mixed Yule coalescent approach: a revised method and evaluation on simulated datasets. Syst. Biol. 2013, 62:707-724.
36. Gärtner G. Die Gattung Trebouxia Puymaly (Chlorellales, Chlorophyceae). Arch. Hydrobiol. Suppl. Algol. Stud. 1985, 41:495-548.
37. Grube, M., Muggia, L., 2010. Identifying Algal Symbionts in Lichen Symbioses. EUT Edizioni Università di Trieste.
38. Grube M., Spribille T. Exploring symbiont management in lichens. Mol. Ecol. 2012, 21:3098-3099.
39. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003, 52:696-704.
40. Haffner, P., 1982. Landschaftsschutzgebiet Saarschleife: Vegetationskarte mit Erläuterungen. Institut für Landeskunde im Saarland.
41. Hamilton C.A., Formanowicz D.R., Bond J.E. Species delimitation and phylogeography of Aphonopelma hentzi (Araneae, Mygalomorphae, Theraphosidae): cryptic diversity in North American tarantulas. PLoS One 2011, 6:e26207.
42. Harrington R.C., Near T.J. Phylogenetic and coalescent strategies of species delimitation in snubnose darters (Percidae: Etheostoma). Syst. Biol. 2012, 61:63-79.
43. Hausdorf B., Hennig C. Species delimitation using dominant and codominant multilocus markers. Syst. Biol. 2010, 59:491-503.
44. Hebert P.D.N., Penton E.H., Burns J.M., Janzen D.H., Hallwachs W. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc. Natl. Acad. Sci. USA 2004, 101:14812-14817.
45. Heled J., Drummond A.J. Bayesian inference of species trees from multilocus data. Mol. Biol. Evol. 2010, 27:570-580.
46. Helms, G., 2003. Taxonomy and Symbiosis in Associations of Physciaceae and Trebouxia. Unpublished PhD Thesis, Georg-August Universität, Göttingen.
47. Hickerson M.J., Meyer C.P., Moritz C. DNA barcoding will often fail to discover new animal species over broad parameter space. Syst. Biol. 2006, 55:729-739.
48. Hudson R.R., Coyne J.A. Mathematical consequences of the genealogical species concept. Evol. Int. J. Org. Evol. 2002, 56:1557-1565.
49. Huelsenbeck J.P., Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics Oxf. Engl. 2001, 17:754-755.
50. Huelsenbeck J.P., Andolfatto P., Huelsenbeck E.T. Structurama: bayesian inference of population structure. Evol. Bioinformatics Online 2011, 7:55-59.
51. John V. Verbreitungstypen von Flechten im Saarland - eine Orientierungshilfe für die Raumbewertung. Abh. Delattinia 1986, 15:1-170.
52. Knowles L.L., Carstens B.C. Delimiting species without monophyletic gene trees. Syst. Biol. 2007, 56:887-895.
53. Kroken S., Taylor J.W. Principles of genealogical concordance in species concepts and biological taxonomy. Oxf. Surv. Evol. Biol. 1990, 45-67.
54. Kroken S., Taylor J.W. Outcrossing and recombination in the lichenized fungus Letharia. Fungal Genet. Biol. 2001, 34:83-92.
55. Kubatko L.S., Carstens B.C., Knowles L.L. STEM: species tree estimation using maximum likelihood for gene trees under coalescence. Bioinformatics 2009, 25:971-973.
56. Leavitt S.D., Johnson L., St.Clair L.L. Species delimitation and evolution in morphologically and chemically diverse communities of the lichen-forming genus Xanthoparmelia (Parmeliaceae, Ascomycota) in western North America. Am. J. Bot. 2011, 98:175-188.
57. Leavitt S.D., Esslinger T.L., Lumbsch H.T. Neogene-dominated diversification in neotropical montane lichens: dating divergence events in the lichen-forming fungal genus Oropogon (Parmeliaceae). Am. J. Bot. 2012, 99:1764-1777.
58. Leavitt S., Fernández-Mendoza F., Pérez-Ortega S., Sohrabi M., Divakar P., Lumbsch T., Clair L.S. DNA barcode identification of lichen-forming fungal species in the Rhizoplaca melanophthalma species-complex (Lecanorales, Lecanoraceae), including five new species. MycoKeys 2013, 7:1-22.
59. Legendre P., Lapointe F.J. Assessing congruence among distance matrices: single-Malt Scotch Whiskies Revisited. Aust. N. Z. J. Stat. 2004, 46:615-629.
60. Leliaert, F., Verbruggen, H., Vanormelingen, P., Steen, F., Lopez-Bautista, J.M., Zuccarello, G.C., De Clerck, O., 2014. DNA-based species delimitation in algae. J. Phycol. (in press).
61. Lumbsch H.T., Leavitt S.D. Goodbye morphology? A paradigm shift in the delimitation of species in lichenized fungi. Fungal Divers. 2011, 50:59-72.
62. Macedo M.F., Miller A.Z., Dionísio A., Saiz-Jimenez C. Biodiversity of cyanobacteria and green algae on monuments in the Mediterranean Basin: an overview. Microbiol. Read. Engl. 2009, 155:3476-3490.
63. Meyer, D., Zeileis, A., Hornik, K., Friendly, M., 2011. vcd: Visualizing Categorical Data. <>. http://www.cran.r.
64. Monaghan M.T., Wild R., Elliot M., Fujisawa T., Balke M., Inward D.J.G., Lees D.C., Ranaivosolo R., Eggleton P., Barraclough T.G., Vogler A.P. Accelerated species inventory on Madagascar using coalescent-based models of species delineation. Syst. Biol. 2009, 58:298-311.
65. Morariu, V., Srinivasan, B.V., Raykar, V.C., Duraiswami, R., Davis, L., 2009. Automatic online tuning for fast Gaussian summation. In: Koller, D., Schuurmans, D., Bengio, Y., Bottou, L. (Eds.), Adv. Neural Inf. Process. Syst., vol. 21, pp. 1113-1120.
66. Muggia L., Zellnig G., Rabensteiner J., Grube M. Morphological and phylogenetic study of algal partners associated with the lichen-forming fungus Tephromela atra from the Mediterranean region. Symbiosis 2010, 51:149-160.
67. Muggia L., Vancurova L., Škaloud P., Peksa O., Wedin M., Grube M. The symbiotic playground of lichen thalli - a highly flexible photobiont association in rock-inhabiting lichens. FEMS Microbiol. Ecol. 2013, 85:313-323.
68. Nelsen M.P., Gargas A. Symbiont flexibility in Thamnolia vermicularis (Pertusariales: Icmadophilaceae). Bryologist 2009, 112:404-417.
69. Nelsen M.P., Plata E.R., Andrew C.J., Lücking R., Lumbsch H.T. Phylogenetic diversity of Trentepohlialean algae associated with lichen-forming fungi. J. Phycol. 2011, 47:282-290.
70. Ohmura Y., Kawachi M., Kasai F., Watanabe M.M., Takeshita S. Genetic combinations of symbionts in a vegetatively reproducing lichen, Parmotrema tinctorum, based on ITS rDNA sequences. Bryologist 2006, 109:43-59.
71. O'Meara B.C. New heuristic methods for joint species delimitation and species tree inference. Syst. Biol. 2010, 59:59-73.
72. Opanowicz M., Grube M. Photobiont genetic variation in Flavocetraria nivalis from Poland (Parmeliaceae, lichenized Ascomycota). Lichenologist 2004, 36:125-131.
73. Parnmen S., Rangsiruji A., Mongkolsuk P., Boonpragob K., Nutakki A., Lumbsch H.T. Using phylogenetic and coalescent methods to understand the species diversity in the Cladia aggregata complex (Ascomycota, Lecanorales). PLoS One 2012, 7:e52245.
74. Pauls S.U., Nowak C., Bálint M., Pfenninger M. The impact of global climate change on genetic diversity within populations and species. Mol. Ecol. 2013, 22:925-946.
75. Payo D.A., Leliaert F., Verbruggen H., D'Hondt S., Calumpong H.P., De Clerck O. Extensive cryptic species diversity and fine-scale endemism in the marine red alga Portieria in the Philippines. Proc. R. Soc. B 2013, 280:20122660.
76. Peksa O., Škaloud P. Do photobionts influence the ecology of lichens? A case study of environmental preferences in symbiotic green alga Asterochloris (Trebouxiophyceae). Mol. Ecol. 2011, 20:3936-3948.
77. Piercey-Normore M.D. The lichen-forming ascomycete Evernia mesomorpha associates with multiple genotypes of Trebouxia jamesii. New Phytol. 2006, 169:331-344.
78. Piercey-Normore M.D. Vegetatively reproducing fungi in three genera of the Parmeliaceae share divergent algal partners. Bryologist 2009, 112:773-785.
79. Pons J., Barraclough T.G., Gomez-Zurita J., Cardoso A., Duran D.P., Hazell S., Kamoun S., Sumlin W.D., Vogler A.P. Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst. Biol. 2006, 55:595-609.
80. Posada D. JModelTest: phylogenetic model averaging. Mol. Biol. Evol. 2008, 25:1253-1256.
81. Puillandre N., Modica M.V., Zhang Y., Sirovich L., Boisselier M.C., Cruaud C., Holford M., Samadi S. Large-scale species delimitation method for hyperdiverse groups. Mol. Ecol. 2012, 21:2671-2691.
82. Queiroz K.D. Species concepts and species delimitation. Syst. Biol. 2007, 56:879-886.
83. Rambold G., Triebel D. The inter-Lecanoralean associations. Bibl. Lichenol. 1992, 4:1-201.
84. Rikkinen J. Lichen guilds share related cyanobacterial symbionts. Science 2002, 297:357.
85. Romeike J., Friedl T., Helms G., Ott S. Genetic diversity of algal and fungal partners in four species of Umbilicaria (lichenized Ascomycetes) along a transect of the Antarctic Peninsula. Mol. Biol. Evol. 2002, 19:1209-1217.
86. Ruprecht U., Brunauer G., Printzen C. Genetic diversity of photobionts in Antarctic lecideoid lichens from an ecological view point. Lichenologist 2012, 44:661-678.
87. Sadowska-Deś A.D., Bálint M., Otte J., Schmitt I. Assessing intraspecific diversity in a lichen-forming fungus and its green algal symbiont: evaluation of eight molecular markers. Fungal Ecol. 2013, 6:141-151.
88. Sanders W.B. Observing microscopic phases of lichen life cycles on transparent substrata placed in situ. Lichenologist 2005, 37:373-382.
89. Sanders W.B., Lücking R. Reproductive strategies, relichenization and thallus development observed in situ in leaf-dwelling lichen communities. New Phytol. 2002, 155:425-435.
90. Sanderson M.J. Estimating absolute rates of molecular evolution and divergence times: a penalized likelihood approach. Mol. Biol. Evol. 2002, 19:101-109.
91. Škaloud P., Peksa O. Evolutionary inferences based on nrITS rDNA and actin sequences reveal extensive diversity of the common lichen alga Asterochloris (Trebouxiophyceae, Chlorophyta). Mol. Phylogenet. Evol. 2010, 54:36-46.
92. Souffreau C., Vanormelingen P., Van de Vijver B., Isheva T., Verleyen E., Sabbe K., Vyverman W. Molecular evidence for distinct Antarctic lineages in the cosmopolitan terrestrial diatoms Pinnularia borealis and Hantzschia amphioxys. Protist 2013, 164:101-115.
93. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics Oxf. Engl. 2006, 22:2688-2690.
94. Taylor J.W., Jacobson D.J., Kroken S., Kasuga T., Geiser D.M., Hibbett D.S., Fisher M.C. Phylogenetic species recognition and species concepts in fungi. Fungal Genet. Biol. 2000, 31:21-32.
95. Thorne J.L., Kishino H. Divergence time and evolutionary rate estimation with multilocus data. Syst. Biol. 2002, 51:689-702.
96. Tschermak-Woess E. New and known taxa of Chlorella (Chlorophyceae): occurrence as lichen phycobionts and observations on living dictyosomes. Plant Syst. Evol. 1988, 159:123-139.
97. van Oppen M.J.H., Klerk H., Olsen J.L., Stam W.T. Hidden diversity in marine algae: some examples of genetic variation below the species level. J. Mar. Biol. Assoc. UK 1996, 76:239-242.
98. Vargas R., Beck A. Photobiont selectivity and specificity in Caloplaca species in a fog-induced community in the Atacama Desert, northern Chile. Fungal Biol. 2012, 116:665-676.
99. Verbruggen H. Morphological complexity, plasticity, and species diagnosability in the application of old species names in DNA-based taxonomies. J. Phycol. 2014, 50:26-31.
100. Verbruggen H., Vlaeminck C., Sauvage T., Sherwood A.R., Leliaert F., De Clerck O. Phylogenetic analysis of Pseudochlorodesmis strains reveals cryptic diversity above the family level in the siphonous green algae (Bryopsidales, Chlorophyta). J. Phycol. 2009, 45:726-731.
101. Welton L.J., Siler C.D., Oaks J.R., Diesmos A.C., Brown R.M. Multilocus phylogeny and Bayesian estimates of species boundaries reveal hidden evolutionary relationships and cryptic diversity in Southeast Asian monitor lizards. Mol. Ecol. 2013, 22:3495-3510.
102. Werth S., Sork V.L. Local genetic structure in a North American epiphytic lichen, Ramalina menziesii (Ramalinaceae). Am. J. Bot. 2008, 95:568-576.
103. Werth S., Sork V.L. Identity and genetic structure of the photobiont of the epiphytic lichen Ramalina menziesii on three oak species in southern California. Am. J. Bot. 2010, 97:821-830.
104. Wiens J.J., Penkrot T.A. Delimiting species using DNA and morphological variation and discordant species limits in spiny lizards (Sceloporus). Syst. Biol. 2002, 51:69-91.
105. Wirtz N., Lumbsch H.T., Green T.G.A., Türk R., Pintado A., Sancho L., Schroeter B. Lichen fungi have low cyanobiont selectivity in maritime Antarctica. New Phytol. 2003, 160:177-183.
106. Wornik S., Grube M. Joint dispersal does not imply maintenance of partnerships in lichen symbioses. Microb. Ecol. 2010, 59:150-157.
107. Yahr R., Vilgalys R., DePriest P.T. Geographic variation in algal partners of Cladonia subtenuis (Cladoniaceae) highlights the dynamic nature of a lichen symbiosis. New Phytol. 2006, 171:847-860.