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Is asexual reproduction an evolutionary dead end in lichens?

Published online by Cambridge University Press:  27 September 2016

Erin A. TRIPP*
Affiliation:
Department of Ecology & Evolutionary Biology, University of Colorado, Boulder, CO 80309, USA; Museum of Natural History, University of Colorado, Boulder, CO 80309, USA

Abstract

Classical hypotheses in lichenology predict pairs of species in which sexual lineages are ancestral and long-lived evolutionarily and that these give rise to derived, evolutionarily transient asexual lineages. Extensive phylogenetic information generated over the last 20 years regarding relationships within and among various groups of lichens makes possible an investigation of polarity and lability in reproductive mode across diverse clades. To test the long-held hypothesis of asexual reproduction as an evolutionary dead end in lichens, existing phylogenetic data from 23 studies were utilized to reconstruct gains and losses of sexual and asexual reproduction in a model-based statistical framework. Summed across all studies, between 26–44 origins of asexual reproduction from sexual ancestors (forward transitions) and 14–25 origins of sexual reproduction from asexual ancestors (reverse transitions) were identified. However, the higher number of gains of asexual reproduction was concentrated in a relatively low number of clades (e.g. Dirina). The greater number of forward compared to reverse transitions is consistent with dogma in both lichenology and evolutionary biology, but nonetheless this study documents numerous reverse transitions, suggesting that asexual lineages represent a source for evolutionary innovation.

Type
Articles
Copyright
© British Lichen Society, 2016 

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References

Alors, D., Lumbsch, H. T., Divakar, P. K., Leavitt, S. D. & Crespo, A. (2016) An integrative approach for understanding diversity in the Punctelia rudecta species complex (Parmeliaceae, Ascomycota). PLoS ONE doi.org/10.1371/journal.pone.0146537 Google Scholar
Altermann, S., Leavitt, S. D., Goward, T., Nelsen, M. P. & Lumbsch, H. T. (2014) How do you solve a problem like Letharia? A new look at cryptic species in lichen-forming fungi using Bayesian clustering and SNPs from multilocus sequence data. PLoS ONE 9: e97556.CrossRefGoogle Scholar
Arnold, E. A., Miadlikowska, J., Higgins, K. L., Sarvate, S. D., Gugger, P., Way, A., Hofstetter, V., Kauff, F. & Lutzoni, F. (2009) A phylogenetic estimation of trophic transition networks for ascomycetous fungi: are lichens cradles of symbiotrophic fungal diversification? Systematic Biology 58: 283297.CrossRefGoogle ScholarPubMed
Asplen, M. K., Whitfield, J. B., De Boer, J. G. & Heimpel, G. E. (2009) Ancestral state reconstruction analysis of hymenopteran sex determination mechanisms. Journal of Evolutionary Biology 22: 17621769.CrossRefGoogle ScholarPubMed
Bowler, P. A. & Rundel, P. W. (1975) Reproductive strategies in lichens. Botanical Journal of the Linnean Society 70: 325340.Google Scholar
Brady, S. G., Litman, J. R. & Danforth, B. N. (2011) Rooting phylogenies using gene duplications: an empirical example from the bees (Apoidea). Molecular Phylogenetics and Evolution 60: 295304.CrossRefGoogle ScholarPubMed
Brodo, I. M. & Lendemer, J. C. (2012) On the perplexing variability of reproductive modes in the genus Ochrolechia: notes on O. africana and O. arborea in eastern North America. Opuscula Philolichenum 11: 120134.Google Scholar
Burt, A., Carter, D. A., Koenig, G. L., White, T. J. & Taylor, J. W. (1996) Molecular markers reveal cryptic sex in the human pathogen Coccidioides immitis . Proceedings of the National Academy of Sciences of the United States of America 93: 770773.Google Scholar
Buschbom, J. & Barker, D. (2006) Evolutionary history of vegetative reproduction in Porpidia s.l. (lichen-forming Ascomycota). Systematic Biology 55: 471484.Google Scholar
Buschbom, J. & Mueller, G. M. (2005) Testing “species-pair” hypotheses: evolutionary processes in the lichen-forming species complex Porpidia flavocoerulescens and Porpidia melinodes . Molecular Biology and Evolution 23: 574586.Google Scholar
Carroll, S. B. (2008) Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134: 2536.CrossRefGoogle Scholar
Case, A. L., Graham, S. W., Macfarlane, T. D. & Barrett, S. C. H. (2008) A phylogenetic study of evolutionary transitions in sexual systems in Australasian Wurmbea (Colchicaceae). International Journal of Plant Sciences 169: 141156.CrossRefGoogle Scholar
Castagnone-Sereno, P. & Danchin, E. G. J. (2014) Parasitic success without sex – the nematode experience. Journal of Evolutionary Biology 27: 13231333.Google Scholar
Charlesworth, D. (2006) Evolution of plant breeding systems. Current Biology 16: R726R735.CrossRefGoogle ScholarPubMed
Clutterbuck, A. J. (1996) Parasexual recombination in fungi. Journal of Genetics 75: 281286.Google Scholar
Collin, R. & Miglietta, M. P. (2008) Reversing opinions on Dollo’s Law. Trends in Ecology and Evolution 23: 602609.Google Scholar
Coppin, E., Debuchy, R., Arnaise, S. & Picard, M. (1997) Mating types and sexual development in filamentous ascomycetes. Microbiology and Molecular Biology Reviews 61: 411428.Google Scholar
Cornejo, C. & Scheidegger, C. (2015) Multi-gene phylogeny of the genus Lobaria: evidence of species-pair and allopatric cryptic speciation in East Asia. American Journal of Botany 102: 20582073.Google Scholar
Cornejo, C., Chabanenko, S. & Scheidegger, C. (2009) Phylogenetic analysis indicates transitions from vegetative to sexual reproduction in the Lobaria retigera group (Lecanoromycetidae, Ascomycota). Lichenologist 41: 275284.CrossRefGoogle Scholar
Crespo, A., Divakar, P. K., Argüello, A., Gasca, C. & Hawksworth, D. L. (2004) Molecular studies on Punctelia species of the Iberian Peninsula, with an emphasis on specimens newly colonizing Madrid. Lichenologist 36: 299308.CrossRefGoogle Scholar
Crespo, A., Ferencova, Z., Pérez-Ortega, S., Elix, J. A. & Divakar, P. K. (2010) Austroparmelina, a new Australasian lineage in parmelioid lichens (Parmeliaceae, Ascomycota). Systematics and Biodiversity 8: 209221.CrossRefGoogle Scholar
Cusimano, N. & Renner, S. S. (2014) Ultrametric trees or phylograms for ancestral state reconstruction: does it matter? Taxon 63: 721726.Google Scholar
Dacks, J. & Roger, A. J. (1999) The first sexual lineage and the relevance of facultative sex. Journal of Molecular Evolution 48: 779783.Google Scholar
Dal Grande, F., Widmer, I., Wagner, H. H. & Scheidegger, C. (2012) Vertical and horizontal photobiont transmission within populations of a lichen symbiosis. Molecular Ecology 21: 31593172.Google Scholar
Del-Prado, R., Blanco, O., Lumbsch, H. T., Divakar, P. K., Elix, J. A., Molina, M. C. & Crespo, A. (2013) Molecular phylogeny and historical biogeography of the lichen-forming fungal genus Flavoparmelia (Ascomycota: Parmeliaceae). Taxon 62: 928939.Google Scholar
Denison, W. C. (2003) Apothecia and ascospores of Lobaria oregana and Lobaria pulmonaria investigated. Mycologia 95: 513518.Google Scholar
Divakar, P. K., Lumbsch, H. T., Ferencova, Z., Del Prado, R. & Crespo, A. (2010) Remotrachyna, a newly recognized tropical lineage of lichens in the Hypotrachyna clade (Parmeliaceae, Ascomycota), originated in the Indian subcontinent. American Journal of Botany 97: 579590.CrossRefGoogle ScholarPubMed
Du Rietz, G. E. (1924) Die Soredien und Isidien der Flechten. Svensk Botanisk Tidskrift 18: 371396.Google Scholar
Duchêne, S. & Lanfear, R. (2015) Phylogenetic uncertainty can bias the number of evolutionary transitions estimated from ancestral state reconstruction methods. Journal of Experimental Zoology (Molecular Development and Evolution) 324: 517524.Google Scholar
Ekman, S. & Blaalid, R. (2011) The devil in the details: interactions between the branch-length prior and likelihood model affect node support and branch lengths in the phylogeny of the Psoraceae . Systematic Biology 60: 541561.Google Scholar
Ekman, S., Andersen, H. L. & Wedin, M. (2008) The limitations of ancestral state reconstruction and the evolution of the ascus in the Lecanorales (lichenized Ascomycota). Systematic Biology 57: 141156.Google Scholar
Ekman, S., Wedin, M., Lindblom, L. & Jørgensen, P. M. (2014) Extended phylogeny and a revised generic classification of the Pannariaceae (Peltigerales, Ascomycota). Lichenologist 46: 627656.Google Scholar
Esslinger, T. L. (2015) A cumulative checklist for the lichen-forming, lichenicolous and allied fungi of the continental United States and Canada. North Dakota State University: http://www.ndsu.edu/pubweb/~esslinge/chcklst/chcklst7.hmt (first posted 1 December 1997, most recent version (#20) 19 April 2015), Fargo, North Dakota.Google Scholar
Felsenstein, J. (2012) A comparative method for both discrete and continuous characters using the threshold model. American Naturalist 179: 145156.Google Scholar
Ferrer, M. M. & Good-Avila, S. V. (2007) Macrophylogenetic analyses of the gain and loss of self-incompatibility in the Asteraceae . New Phytologist 173: 401414.CrossRefGoogle ScholarPubMed
Fisher, R. A. (1941) Average excess and average effect of a gene substitution. Annals of Eugenics 11: 5363.Google Scholar
Frank, S. A. (2010) Somatic evolutionary genomics: mutations during development cause highly variable genetic mosaicism with risk of cancer and neurodegeneration. Proceedings of the National Academy of Sciences of the United States of America 107: 17251730.Google Scholar
Gaya, E., Navarro-Rosinés, P., Llimona, X., Hladun, N. & Lutzoni, F. (2008) Phylogenetic reassessment of the Teloschistaceae (lichen-forming Ascomycota, Lecanoromycetes). Mycological Research 112: 528546.Google Scholar
Gaya, E., Redelings, B. D., Navarro-Rosinés, P., Llimona, X., De Cáceres, M. & Lutzoni, F. (2011) Align or not to align? Resolving species complexes within the Caloplaca saxicola group as a case study. Mycologia 103: 361378.Google Scholar
Geiser, D. M., Pitt, J. I. & Taylor, J. W. (1998) Cryptic speciation and recombination in the aflatoxin-producing fungus Aspergillus flavus . Proceedings of the National Academy of Sciences of the United States of America 95: 388393.CrossRefGoogle ScholarPubMed
Gioti, A., Stajich, J. E. & Johannesson, H. (2013) Neurospora and the dead-end hypothesis: genomic consequences of selfing in the model genus. Evolution 67: 36003616.Google Scholar
Gomez-Mestre, I., Pyron, R. A. & Wiens, J. J. (2012) Phylogenetic analyses reveal unexpected patterns in the evolution of reproductive modes in frogs. Evolution 66: 36873700.CrossRefGoogle ScholarPubMed
Goodwillie, C. (1997) The genetic control of self-incompatibility in Linanthus parviflorus (Polemoniaceae). Heredity 79: 424432.CrossRefGoogle Scholar
Goodwillie, C., Kalisz, S. & Eckert, C. G. (2005) The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annual Review of Ecology, Evolution, and Systematics 36: 4779.Google Scholar
Grant, V. (1958) The regulation of recombination in plants. In Cold Spring Harbor Symposia on Quantitative Biology. Exchange of Genetic Material: Mechanisms and Consequences, Vol. 23 (C. Madden, ed.): 337363. Cold Spring Harbor, New York: Long Island Biological Association.Google Scholar
Hale, M. E. (1976) A monograph of the lichen genus Bulbothrix Hale (Parmeliaceae). Smithsonian Contributions to Botany 32: 132.Google Scholar
Hawksworth, D. L. (2001) The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycological Research 105: 14221432.Google Scholar
Hespeels, B., Flot, J. F., Derzelle, A. & Van Doninck, K. (2014) Evidence for ancient horizontal gene acquisitions in bdelloid rotifers of the genus Adineta . In Evolutionary Biology: Genome Evolution, Speciation, Coevolution and Origin of Life (P. Pontarotti, ed.): 207225. Cham, Switzerland: Springer International Publishing.Google Scholar
Hestmark, G. (1991) Teleomorph-anamorph relationships in Umbilicaria I. Making the connections. Lichenologist 23: 343359.CrossRefGoogle Scholar
Hestmark, G. (1992) Sex, size, competition and escape – strategies of reproduction and dispersal in Lasallia pustulata (Umbilicariaceae, Ascomycetes). Oecologia 92: 305312.Google Scholar
Hestmark, G., Miadlikowska, J., Kauff, F., Fraker, E., Molnar, K. & Lutzoni, F. (2011) Single origin and subsequent diversification of central Andean endemic Umbilicaria species. Mycologia 103: 4556.Google Scholar
Honegger, R. (1997) Metabolic interactions at the mycobiont-photobiont interface in lichens. In The Mycota V. Plant Relationships (G. C. Carroll & P. Tudzynski, eds): 209221. Berlin: Springer.CrossRefGoogle Scholar
Honegger, R. (1984) Ultrastructural studies on conidiomata, conidiophores, and conidiogenous cells in six lichen-forming Ascomycetes. Canadian Journal of Botany 62: 20812093.Google Scholar
Honegger, R., Zippler, U., Gansner, H. & Scherrer, S. (2004) Mating systems in the genus Xanthoria (lichen-forming ascomycetes). Mycological Research 108: 480488.Google Scholar
Howe, N. M. & Lendemer, J. C. (2010) The recovery of a simplified lichen community at the Palmerton Zinc Smelter after 34 years. Bibliotheca Lichenologica 106: 120136.Google Scholar
Igic, B., Bohs, L. & Kohn, J. R. (2006) Ancient polymorphism reveals unidirectional breeding system shifts. Proceedings of the National Academy of Sciences of the United States of America 103: 13591363.Google Scholar
Jaklitsch, W., Baral, H.O., Lücking, R., Lumbsch, H. T. & Frey, W. (2016) Syllabus of Plant Families - A. Engler’s Syllabus der Pflanzenfamilia Part 1/2: Ascomycota. Stuttgart: Gebrüder Borntraeger.Google Scholar
Judson, O. P. & Normark, B. B. (1996) Ancient asexual scandals. Trends in Ecology and Evolution 11: 4146.Google Scholar
Karron, J. D., Ivey, C. T., Mitchell, R. J., Whitehead, M. R., Peakall, R. & Case, A. L. (2012) New perspectives on the evolution of plant mating systems. Annals of Botany 109: 493503.Google Scholar
Kerr, A. M., Baird, A. H. & Hughes, T. P. (2011) Correlated evolution of sex and reproductive mode in corals (Anthozoa: Scleractinia). Proceedings of the Royal Society of London, Series B 278: 7581.Google Scholar
King, B. & Lee, M. S. Y. (2015) Ancestral state reconstruction, rate heterogeneity, and the evolution of reptile viviparity. Systematic Biology 64: 532544.Google Scholar
Kroken, S. & Taylor, J. W. (2001 a) Outcrossing and recombination in the lichenized fungus Letharia. Fungal Genetics and Biology 34: 8392.Google Scholar
Kroken, S. & Taylor, J. W. (2001 b) A gene genealogical approach to recognize phylogenetic species boundaries in the lichenized fungus Letharia . Mycologia 93: 3853.Google Scholar
Leavitt, S. D., Lumbsch, H. T. & St. Clair, L. L. (2013) Contrasting demographic histories of two species in the lichen-forming fungal genus Xanthomendoza (Teloschistaceae, Ascomycota). Bryologist 116: 337349.CrossRefGoogle Scholar
Leavitt, S. D., Divakar, P. K., Ohmura, Y., Wang, L. S., Esslinger, T. L. & Lumbsch, H. T. (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: 8596.Google Scholar
LeBlanc, F. & De Sloover, J. (1970) Relation between industrialization and the distribution and growth of epiphytic lichens and mosses in Montreal. Canadian Journal of Botany 48: 14851496.Google Scholar
Lendemer, J. C. (2013) A monograph of the crustose members of the genus Lepraria Ach. s. str. (Stereocaulaceae, lichenized Ascomycetes) in North America north of Mexico. Opuscula Philolichenum 13: 36141.Google Scholar
Lendemer, J. C. & Harris, R. C. (2014) Studies in lichens and lichenicolous fungi - no. 18: resolution of three names introduced by Degelius and Magnusson based on material from the Great Smoky Mountains. Castanea 79: 106117.Google Scholar
Lendemer, J. C. & Hodkinson, B. P. (2013) A radical shift in the taxonomy of Lepraria s.l.: molecular and morphological studies shed new light on the evolution of asexuality and lichen growth form diversification. Mycologica 105: 9941018.Google Scholar
Lendemer, J. C., Allen, J. L. & Noell, N. (2015) The Parmotrema acid test: a look at species delineation in the P. perforatum group 40 y later. Mycologia 107: 11201129.Google Scholar
Litsios, G. & Salamin, N. (2012) Effects of phylogenetic signal on ancestral state reconstruction. Systematic Biology 61: 533538.Google Scholar
Maynard Smith, J. (1978) The Evolution of Sex. Cambridge: Cambridge University Press.Google Scholar
Miadlikowska, J., Schoch, C. L., Kageyama, S. A., Molnar, K., Lutzoni, F. & McCune, B. (2011) Hypogymnia phylogeny, including Cavernularia, reveals biogeographic structure. Bryologist 113: 392400.CrossRefGoogle Scholar
Miadlikowska, J., Kauff, F., Högnabba, F., Oliver, J. C., Molnár, K., Fraker, E., Gaya, E., Hafellner, J., Hofstetter, V., Gueidan, C., et al. (2014) Multigene phylogenetic synthesis for the class Lecanoromycetes (Ascomycota): 1307 fungi representing 1139 infrageneric taxa, 312 genera and 66 families. Molecular Phylogenetics and Evolution 79: 132168.Google Scholar
Moncada, B., Lücking, R. & Betancourt-Macuase, L. (2013) Phylogeny of the Lobariaceae (lichenized Ascomycota: Peltigerales), with a reappraisal of the genus Lobariella . Lichenologist 45: 203263.Google Scholar
Naesborg, R. R., Ekman, S. & Tibell, L. (2007) Molecular phylogeny of the genus Lecania (Ramalinaceae, lichenized Ascomycota). Mycological Research 111: 581591.CrossRefGoogle Scholar
Neiman, M., Meirmans, S. & Meirmans, P. G. (2009) What can asexual lineage age tell us about the maintenance of sex? Annals of the New York Academy of Sciences 1168: 185200.CrossRefGoogle ScholarPubMed
Nelsen, M. P., Lücking, R., Grube, M., Mbatchou, J. S., Muggia, L., Plata, E. R. & Lumbsch, H. T. (2009) Unravelling the phylogenetic relationships of lichenised fungi in Dothideomyceta. Studies in Mycology 64: 135144.Google Scholar
Normark, B. B., Judson, O. P. & Moran, N. A. (2003) Genomic signatures of ancient asexual lineages. Biological Journal of the Linnean Society 79: 6984.Google Scholar
Oliveira, R. C., Oi, C. A., do Nascimento, M. M. C., Vollet-Neto, A., Alves, D. A., Campos, M. C., Nascimento, F. & Wenseleers, T. (2015) The origin and evolution of queen and fertility signals in corbiculate bees. BMC Evolutionary Biology 15: 254.Google Scholar
O’Meara, B. C. (2012) Evolutionary inference from phylogenies: a review of methods. Annual Reviews in Ecology, Evolution, and Systematics 43: 267285.Google Scholar
Osborn, H. F. (1902) Homoplasy as a law of latent or potential homology. American Naturalist 36: 259271.Google Scholar
Pagel, M. (1999) The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Systematic Biology 48: 612622.Google Scholar
Pérez-Ortega, S., Spribille, T., Palice, Z., Elix, J. A. & Printzen, C. (2010) A molecular phylogeny of the Lecanora varia group, including a new species from western North America. Mycological Progress 9: 523535.Google Scholar
Pierre-Olivier, C. (2012) The evolution of plant mating system: is it time for a synthesis? In Studies in Population Genetics (M. C. Fusté, ed.): 17–38. Rijeka, Croatia: InTech.Google Scholar
Pino-Bodas, R., Burgaz, A. R., Martín, M. P., Ahti, T., Stenroos, S., Wedin, M. & Lumbsch, H. T. (2015) The phenotypic features used for distinguishing species within the Cladonia furcata complex are highly homoplasious. Lichenologist 47: 287303.Google Scholar
Poelt, J. (1965) Über einige Artengruppen de Flechtengattungen Caloplaca und Fulgensia . Mitteilungen der Botanischen Staatssammlung München 5: 571607.Google Scholar
Poelt, J. (1970) Das Konzept der Artenpaare bei den Flechten. Vorträge aus dem Gesamtgebiet der Botanik, Neue Folge 4: 187198.Google Scholar
Poulíčková, A., Sato, S., Evans, K. M., Chepurnov, V. A. & Mann, D. G. (2014) Repeated evolution of uniparental reproduction in Sellaphora (Baccilariophyceae). European Journal of Phycology 50: 6279.Google Scholar
Printzen, C. (2014) A molecular phylogeny of the lichen genus Biatora including some morphologically similar species. Lichenologist 46: 441453.CrossRefGoogle Scholar
Ramesh, M. A., Malik, S. B. & Logsdon, J. M. (2005) A phylogenomic inventory of meiotic genes; evidence for sex in Giardia and an early eukaryotic origin of meiosis. Current Biology 15: 185191.Google Scholar
Redecker, D. (2002) New views on fungal evolution based on DNA markers and the fossil record. Research in Microbiology 153: 125130.Google Scholar
Rydholm, C., Dyer, P. S. & Lutzoni, F. (2007) DNA sequence characterization and molecular evolution of MAT1 and MAT2 mating-type loci of the self-compatible ascomycete mold Neosartorya fischeri . Eukaryotic Cell 6: 868874.Google Scholar
Saag, L., Saag, A. & Randlane, T. (2009) World survey of the genus Lepraria (Stereocaulaeae, lichenized Ascomycota). Lichenologist 41: 2560.Google Scholar
Saag, L., Mark, K., Saag, A. & Randlane, T. (2014) Species delimitation in the lichenized fungal genus Vulpicida (Parmeliaceae, Ascomycota) using gene concatenation and coalescent-based species tree approaches. American Journal of Botany 101: 21692182.Google Scholar
Salisbury, B. A. & Kim, J. (2001) Ancestral state estimation and taxon sampling density. Systematic Biology 50: 557564.Google Scholar
Sanders, W. B. (2014) Complete life cycle of the lichen fungus Calopadia puiggarii (Pilocarpaceae, Ascomycetes) documented in situ: propagule dispersal, establishment of symbiosis, thallus development, and formation of sexual and asexual reproductive structures. American Journal of Botany 101: 18361848.Google Scholar
Savíc, S., Tibell, L., Gueidan, C. & Lutzoni, F. (2008) Molecular phylogeny and systematics of Polyblastia (Verrucariaceae, Eurotiomycetes) and allied genera. Mycological Research 112: 13071318.CrossRefGoogle ScholarPubMed
Scherrer, S., Zippler, U. & Honegger, R. (2005) Characterisation of the mating-type locus in the genus Xanthoria (lichen-forming ascomycetes, Lecanoromycetes). Fungal Genetics and Biology 42: 976988.CrossRefGoogle ScholarPubMed
Sheard, J. W. (2010) Lichen Genus Rinodina (Ach.) Gray (Lecanorales, Physciaceae) in North America, North of Mexico. Ottawa: NRC Research Press.Google Scholar
Shuker, D. M. & Simmons, L. W. (2014) The Evolution of Insect Mating Systems. Oxford: Oxford University Press.Google Scholar
Singh, G., Dal Grande, F., Cornejo, C., Schmitt, I. & Scheidegger, C. (2012) Genetic basis of self-incompatibility in the lichen-forming fungus Lobaria pulmonaria and skewed frequency distribution of mating-type idiomorphs: implications for conservation. PLoS ONE 7: e51402.Google Scholar
Singh, G., Dal Grande, F., Divakar, P. K., Otte, J., Leavitt, S. D., Szczepanska, K., Crespo, A., Rico, V., Aptroot, A., Cáceres, M. E. S., 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.Google Scholar
Stebbins, G. L. (1957) Self fertilization and population variability in the higher plants. American Naturalist 91: 337354.Google Scholar
Takebayashi, N. & Morrell, P. L. (2001) Is self-fertilization an evolutionary dead end? Revisiting an old hypothesis with genetic theories and a macroevolutionary approach. American Journal of Botany 88: 11431150.Google Scholar
Tehler, A. (1982) The species pair concept in lichenology. Taxon 31: 708714.Google Scholar
Tehler, A., Irestedt, M., Bungartz, F. & Wedin, M. (2009) Evolution and reproduction modes in the Roccella galapagoensis aggregate (Roccellaceae, Arthoniales). Taxon 58: 438456.Google Scholar
Tehler, A., Ertz, D. & Irestedt, M. (2013) The genus Dirina (Roccellaceae, Arthoniales) revisited. Lichenologist 45: 427476.Google Scholar
Timdal, E. (1991) A monograph of the genus Toninia (Lecideaceae, Ascomycetes). Opera Botanica 110: 1137.Google Scholar
Tripp, E. A. & Manos, P. S. (2008) Is floral specialization an evolutionary dead-end? Pollination system transitions in Ruellia (Acanthaceae). Evolution 62: 17121737.Google Scholar
Tripp, E. A., Lendemer, J. C., Barberán, A., Dunn, R. R. & Fierer, N. (2016) Biodiversity gradients in obligate symbiotic organisms: exploring the diversity and traits of lichen propagules across the United States. Journal of Biogeography (published online 17 March 2016, DOI: 10.1111/jbi.12746).Google Scholar
Van der Niet, T., Peakall, R. & Johnson, S. D. (2014) Pollinator-driven ecological speciation in plants: new evidence and future perspectives. Annals of Botany 113: 199212.Google Scholar
Wiens, J. J., Kuczynski, C. A., Duellman, W. E. & Reeder, T. W. (2007) Loss and re-evolution of complex life cycles in marsupial frogs: does ancestral trait reconstruction mislead? Evolution 61: 18861899.Google Scholar
Wootton, R. J. & Smith, C. (2014) Reproductive Biology of Teleost Fishes. Oxford: Wiley Blackwell.Google Scholar
Yong, E. (2012) Tree’s leaves genetically different from its roots. Nature News doi:10.1038/nature.2012.11156 Google Scholar
Zoller, S., Lutzoni, F. & Scheidegger, C. (1999) Genetic variation within and among populations of the threatened lichen Lobaria pulmonaria in Switzerland and implications for its conservation. Molecular Ecology 8: 20492059.Google Scholar
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