Advertisement

The Dynamic Discipline of Species Delimitation: Progress Toward Effectively Recognizing Species Boundaries in Natural Populations

  • Steven D. Leavitt
  • Corrie S. Moreau
  • H. Thorsten Lumbsch

Abstract

Species represent a fundamental unit in evolutionary biology and provide a valuable context for organizing, evaluating, and communicating important biological concepts and principles. Empirical species delimitation is a dynamic discipline, with ongoing methodological and bioinformatical developments. Novel analytical methods, increasing availability of genetic/genomic data, increasing computational power, reassessments of morphological and chemical characters, and improved availability of distributional and ecological records offer exciting avenues for empirically exploring species delimitation and evolutionary relationships among species-level lineages. In this chapter, we aim to contribute a contemporary perspective on delimiting species, including a brief discussion on species concepts and practical direction for empirical species delimitation studies. Using lichen-forming fungi as an example, we illustrate the importance and difficulties in documenting and describing species-level biodiversity.

Keywords

Barcoding Coalescence DNA taxonomy Fungi Gene tree Genomics Lichens Species circumscription Species concept Species tree 

Notes

Acknowledgments

We are indebted to various colleagues for valuable, thought-provoking discussion, notably Matthew Nelsen (University of Chicago), Ana Crespo (Universidad Complutense de Madrid), Pradeep Divakar (Universidad Complutense de Madrid), Beckett Sterner (The Field Museum), and Joyce Havstad (The Field Museum). We also thank anonymous reviewers who provided valuable comments that improved this chapter. Support by the US National Science Foundation is gratefully acknowledged (“Hidden diversity in parmelioid lichens,” DEB-0949147).

References

  1. Ahti T, Hawksworth DL (2005) Xanthoparmelia stenophylla, the correct name for X. somloënsis, one of the most widespread usnic acid containing species of the genus. The Lichenologist 37(4):363–366. doi: 10.1017/S0024282905015197 Google Scholar
  2. Altermann S, Leavitt SD, Goward T, Nelsen MP, Lumbsch HT (2014) How do you solve a problem like Letharia? A new look at cryptic species in lichen-forming fungi using Bayesian clustering and SNPSs from multilocus sequence data. PLoS ONE 9(5):e97556. doi: 10.1371/journal.pone.0097556
  3. Amo de Paz G, Cubas P, Crespo A, Elix JA, Lumbsch HT (2012) Transoceanic dispersal and subsequent diversification on separate continents shaped diversity of the Xanthoparmelia pulla group (Ascomycota). PLoS ONE 7(6):e39683. doi: 10.1371/journal.pone.0039683 PubMedGoogle Scholar
  4. Argüello A, Del Prado R, Cubas P, Crespo A (2007) Parmelina quercina (Parmeliaceae, Lecanorales) includes four phylogenetically supported morphospecies. Biol J Linn Soc 91(3):455–467. doi: 10.1111/j.1095-8312.2007.00810.x Google Scholar
  5. Arup U, Berlin ES (2011) A taxonomic study of Melanelixia fuliginosa in Europe. The Lichenologist 43(02):89–97. doi: 10.1017/S0024282910000678 Google Scholar
  6. Arup U, Grube M (2000) Is Rhizoplaca (Lecanorales, lichenized Ascomycota) a monophyletic genus? Can J Bot 78(3):318–327. doi: 10.1139/b00-006 Google Scholar
  7. Avise J, Ball R (1990) Principles of genealogical concordance in species concepts and biological taxonomy. Oxf Surv Evol Biol 7:45–67Google Scholar
  8. Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, Selker EU, Cresko WA, Johnson EA (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3(10):e3376. doi: 10.1371/journal.pone.0003376 PubMedCentralPubMedGoogle Scholar
  9. Baum DA, Shaw KL (1995) Genealogical perspectives on the species problem. In: Hoch PC, Stephenson AG (eds) Experimental and molecular approaches to plant biosystematics. Missouri Botanical Garden, St. Louis, pp 289–303Google Scholar
  10. Beaumont MA, Nielsen R, Robert C, Hey J, Gaggiotti O, Knowles L, Estoup A, Panchal M, Corander J, Hickerson M, Sisson SA, Fagundes N, Chikhi L, Beerli P, Vitalis R, Cornuet J-M, Huelsenbeck J, Foll M, Yang Z, Rousset F, Balding D, Excoffier L (2010) In defence of model-based inference in phylogeography. Mol Ecol 19(3):436–446. doi: 10.1111/j.1365-294X.2009.04515.x Google Scholar
  11. Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22(3):148–155. doi: 10.1016/j.tree.2006.11.004 PubMedGoogle Scholar
  12. Bonan GB, Shugart HH (1989) Environmental factors and ecological processes in boreal forests. Annu Rev Ecol Syst 20(1989):1–28Google Scholar
  13. Bond J, Stockman A (2008) An integrative method for delimiting cohesion species: finding the population-species interface in a group of Californian trapdoor spiders with extreme genetic divergence and geographic structuring. Syst Biol 57(4):628–646. doi: 10.1080/10635150802302443 PubMedGoogle Scholar
  14. Brodo IM (1978) Changing concepts regarding chemical diversity in lichens. The Lichenologist 10(1):1–11. doi: 10.1017/S0024282978000031 Google Scholar
  15. Brodo IM (1986) Interpreting chemical variation in lichens for systematic purposes. The Bryologist 89(2):132–138Google Scholar
  16. Caley MJ, Fisher R, Mengersen K (2014) Global species richness estimates have not converged. Trends Ecol Evol 29(4):187–188. doi: 10.1016/j.tree.2014.02.002 PubMedGoogle Scholar
  17. Camargo A, Sites JW (2013) Species delimitation: a decade after the Renaissance. In: Pavlinov I (ed) The species problem—ongoing issues. InTech. doi: 10.5772/52664
  18. Camargo A, Morando M, Avila LJ, Sites JW (2012) Species delimitation with ABC and other coalescent-based methods: a test of accuracy with simulations and an empirical example with lizards of the Liolaemus darwinii complex (Squamata: Liolaemidae). Evolution 66(9):2834–2849. doi: 10.1111/j.1558-5646.2012.01640.x PubMedGoogle Scholar
  19. Carstens BC, Dewey TA (2010) Species delimitation using a combined coalescent and information-theoretic approach: an example from North American Myotis bats. Syst Biol 59(4):400–414. doi: 10.1093/sysbio/syq024 PubMedCentralPubMedGoogle Scholar
  20. Carstens BC, Pelletier TA, Reid NM, Satler JD (2013) How to fail at species delimitation. Mol Ecol 22(17):4369–4383. doi: 10.1111/mec.12413 PubMedGoogle Scholar
  21. Corander J, Marttinen P (2006) Bayesian identification of admixture events using multi-locus molecular markers. Mol Ecol 15(10):2833–2843. doi: 10.1111/j.1365-294X.2006.02994.x PubMedGoogle Scholar
  22. Corander J, Waldmann P, Marttinen P, Sillanpaa M (2004) BAPS 2: enhanced possibilities for the analysis of genetic population structure. Bioinformatics 20(15):2363–2369. doi: 10.1093/bioinformatics/bth250 PubMedGoogle Scholar
  23. Corander J, Marttinen P, Mantyniemi S (2006) Bayesian identification of stock mixtures from molecular marker data. Fish Bull 104:550–558Google Scholar
  24. Corander J, Marttinen P, Siren J, Tang J (2008) Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinf 9(1):539. doi: 10.1186/1471-2105-9-539 Google Scholar
  25. Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, SunderlandGoogle Scholar
  26. Cracraft J (1983) Species concepts and speciation analysis. Curr Ornithol 1:159–187Google Scholar
  27. Crespo A, Lumbsch HT (2010) Cryptic species in lichen-forming fungi. IMA Fungus 1:167–170. doi: 10.5598/imafungus.2010.01.02.09 PubMedCentralPubMedGoogle Scholar
  28. Crespo A, Pérez-Ortega S (2009) Cryptic species and species pairs in lichens: a discussion on the relationship between molecular phylogenies and morphological characters. Anales del Jardin Botanico de Madrid 66(S1):71–81. doi: 10.3989/ajbm.2225 Google Scholar
  29. Crespo A, Kauff F, Divakar PK, del Prado R, Perez-Ortega S, Amo de Paz G, Ferencova Z, Blanco O, Roca-Valiente B, Nunez-Zapata J, Cubas P, Arguello A, Elix JA, Esslinger TL, Hawksworth DL, Millanes A, Molina MC, Wedin M, Ahti T, Aptroot A, et al (2010) Phylogenetic generic classification of parmelioid lichens (Parmeliaceae, Ascomycota) based on molecular, morphological and chemical evidence. Taxon 59(6):1735–1753Google Scholar
  30. Culberson WL (1969) The use of chemistry in the systematics of the lichens. Taxon 18:498–505Google Scholar
  31. Culberson WL (1970) Chemosystematics and ecology of lichen-forming fungi. Annu Rev Ecol Syst 1:153–170Google Scholar
  32. Culberson CF, Culberson WL (1976) Chemosyndromic variation in lichens. Syst Bot 1:325–339Google Scholar
  33. Darwin C (1859) On the origin of species by means of natural selection or the preservation of favoured races in the struggle for life. J. Murray, LondonGoogle Scholar
  34. Dayrat B (2005) Towards integrative taxonomy. Biol J Linn Soc 85(3):407–415. doi: 10.1111/j.1095-8312.2005.00503.x Google Scholar
  35. de Queiroz K (1998) The general lineage concept of species, species criteria, and the process of speciation: a conceptual unification and terminological recommendations. In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, Oxford, pp 57–75Google Scholar
  36. de Queiroz K (1999) The general lineage concept of species and the defining properties of the species category. In: Wilson RA (ed) Species: new interdisciplinary essays. MIT Press, Cambridge, pp 49–89Google Scholar
  37. de Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56(6):879–886. doi: 10.1080/10635150701701083 PubMedGoogle Scholar
  38. de Queiroz A, Donoghue MJ, Kim J (1995) Separate versus combined analysis of phylogenetic evidence. Annu Rev Ecol Syst 26(1):657–681. doi: 10.1146/annurev.es.26.110195.003301 Google Scholar
  39. Degnan J, Rosenberg N (2006) Discordance of species trees with their most likely gene trees. PLoS Genet 2(5):e68. doi: 10.1371/journal.pgen.0020068 PubMedCentralPubMedGoogle Scholar
  40. Degnan JH, Rosenberg NA (2009) Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends Ecol Evol 24(6):332–340. doi:http://dx.doi.org/10.1016/j.tree.2009.01.009
  41. Del-Prado R, Cubas P, Lumbsch HT, Divakar PK, Blanco O, de Paz GA, Molina MC, Crespo A (2010) Genetic distances within and among species in monophyletic lineages of Parmeliaceae (Ascomycota) as a tool for taxon delimitation. Mol Phylogenet Evol 56(1):125–133. doi: 10.1016/j.ympev.2010.04.014 PubMedGoogle Scholar
  42. Del-Prado R, Divakar PK, Crespo A (2011) Using genetic distances in addition to ITS molecular phylogeny to identify potential species in the Parmotrema reticulatum complex: a case study. The Lichenologist 43(06):569–583. doi: 10.1017/S0024282911000582 Google Scholar
  43. Del-Prado R, Blanco O, Lumbsch HT, Divakar PK, Elix JA, Molina MC, Crespo A (2013) Molecular phylogeny and historical biogeography of the lichen-forming fungal genus Flavoparmelia (Ascomycota: Parmeliaceae). Taxon 62(5):928–939. doi: 10.12705/625.22 Google Scholar
  44. Dettman J, Jacobson D, Taylor J (2003a) A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Evolution 57(12):2703–2720. doi: 10.1111/j.0014-3820.2003.tb01514.x PubMedGoogle Scholar
  45. Dettman JR, Jacobson DJ, Turner E, Pringle A, Taylor JW (2003b) Reproductive isolation and phylogenetic divergence in Neurospora: comparing methods of species recognition in a model eukaryote. Evolution 57(12):2721. doi: 10.1554/03-074 PubMedGoogle Scholar
  46. Devkota S, Cornejo C, Werth S, Chaudhary RP, Scheidegger C (2014) Characterization of microsatellite loci in the Himalayan lichen fungus Lobaria pindarensis (Lobariaceae). Appl Plant Sci 2(5):1300101. doi: 10.3732/apps.1300101 Google Scholar
  47. Divakar PK, Molina MC, Lumbsch HT, Crespo A (2005) Parmelia barrenoae, a new lichen species related to Parmelia sulcata (Parmeliaceae) based on molecular and morphological data. The Lichenologist 37(01):37–46. doi: 10.1017/S0024282904014641 Google Scholar
  48. Divakar PK, Amo De paz G, del Prado R, Esslinger TL, Crespo A (2007) Upper cortex anatomy corroborates phylogenetic hypothesis in species of Physconia (Ascomycota, Lecanoromycetes). Mycol Res 111(11):1311–1320. doi: 10.1016/j.mycres.2007.08.009
  49. Divakar PK, Figueras G, Hladun N, Crespo A (2010) Molecular phylogenetic studies reveal an undescribed species within the North American concept of Melanelixia glabra (Parmeliaceae). Fungal Divers 42(1):47–55. doi: 10.1007/s13225-010-0027-3 Google Scholar
  50. Donoghue MJ, Gauthier A (2004) Implementing the phylocode. Trends Ecol Evol 19(6):281–282. doi: 10.1016/j.tree.2004.04.004 PubMedGoogle Scholar
  51. Eaton DAR, Ree RH (2013) Inferring phylogeny and introgression using RADseq data: an example from flowering plants (Pedicularis: Orobanchaceae). Syst Biol 62(5):689–706. doi: 10.1093/sysbio/syt032 PubMedCentralPubMedGoogle Scholar
  52. Edwards SV (2009) Is a new and general theory of molecular systematics emerging? Evolution 63(1):1–19. doi: 10.1111/j.1558-5646.2008.00549.x PubMedGoogle Scholar
  53. Edwards DL, Knowles LL (2014) Species detection and individual assignment in species delimitation: can integrative data increase efficacy? Proc R Soc B: Biol Sci 281(1777). doi: 10.1098/rspb.2013.2765
  54. Egan RS (1986) Correlations and non-correlations of chemical variation patterns with lichen morphology and geography. The Bryologist 89:99–110Google Scholar
  55. Elix JA, Corush J, Lumbsch HT (2009) Triterpene chemosyndromes and subtle morphological characters characterise lineages in the Physcia aipolia group in Australia (Ascomycota). Syst Biodivers 7(04):479–487. doi: 10.1017/S1477200009990223 Google Scholar
  56. Emerson KJ, Merz CR, Catchen JM, Hohenlohe PA, Cresko WA, Bradshaw WE, Holzapfel CM (2010) Resolving postglacial phylogeography using high-throughput sequencing. Proc Natl Acad Sci 107(37):16196–16200. doi: 10.1073/pnas.1006538107 PubMedCentralPubMedGoogle Scholar
  57. Ence DD, Carstens BC (2011) SpedeSTEM: a rapid and accurate method for species delimitation. Mol Ecol Resour 11(3):473–480. doi: 10.1111/j.1755-0998.2010.02947.x PubMedGoogle Scholar
  58. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620. doi: 10.1111/j.1365-294X.2005.02553.x PubMedGoogle Scholar
  59. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164(4):1567–1587. doi: 10.1111/j.1471-8286.2007.01758.x PubMedCentralPubMedGoogle Scholar
  60. Fan HH, Kubatko LS (2011) Estimating species trees using approximate Bayesian computation. Mol Phylogenet Evol 59(2):354–363. doi: 10.1016/j.ympev.2011.02.019 PubMedGoogle Scholar
  61. Fernández-Mendoza F, Printzen C (2013) Pleistocene expansion of the bipolar lichen Cetraria aculeata into the Southern hemisphere. Mol Ecol 22(7):1961–1983. doi: 10.1111/mec.12210 PubMedGoogle Scholar
  62. Fernández-Mendoza F, Domaschke S, García MA, Jordan P, Martin MP, Printzen C (2011) Population structure of mycobionts and photobionts of the widespread lichen Cetraria aculeata. Mol Ecol 20(6):1208–1232. doi: 10.1111/j.1365-294X.2010.04993.x PubMedGoogle Scholar
  63. Fraley C, Raftery A (2007) Model-based methods of classification: Using the mclust software in chemometrics. J Stat Softw 18:i06 [Available online at http://www.doaj.org/doaj?func=abstract&id=218544]
  64. Fujisawa T, Barraclough TG (2013) Delimiting species using single-locus data and the generalized mixed yule coalescent (GMYC) approach: a revised method and evaluation on simulated datasets. Syst Biol 62(5):707–724. doi: 10.1093/sysbio/syt033 PubMedCentralPubMedGoogle Scholar
  65. Fujita MK, Leaché AD, Burbrink FT, McGuire JA, Moritz C (2012) Coalescent-based species delimitation in an integrative taxonomy. Trends Ecol Evol 27(9):480–488. doi: 10.1016/j.tree.2012.04.012 PubMedGoogle Scholar
  66. Gatesy J, O’Grady P, Baker RH (1999) Corroboration among data sets in simultaneous analysis: hidden support for phylogenetic relationships among higher level Artiodactyl taxa. Cladistics 15(3):271–313. doi: 10.1111/j.1096-0031.1999.tb00268.x Google Scholar
  67. Gladieux P, Ropars J, Badouin H, Branca A, Aguileta G, de Vienne DM, Rodríguez de la Vega RC, Branco S, Giraud T (2014) Fungal evolutionary genomics provides insight into the mechanisms of adaptive divergence in eukaryotes. Mol Ecol 23(4):753–773. doi: 10.1111/mec.12631
  68. Goffinet B, Miadlikowska J, Goward T (2003) Phylogenetic inferences based on nrDNA sequences support five morphospecies within the Peltigera didactyla complex (Lichenized Ascomycota). The Bryologist 106(3):349–364. doi: 10.1639/01 Google Scholar
  69. Gowan SP (1986) Evolution of secondary natural products in the genus Porpidia (Ascomycata, Porpidiaceae). Am J Bot 73:606Google Scholar
  70. Griffin PC, Hoffmann AA (2014) Limited genetic divergence among Australian alpine Poa tussock grasses coupled with regional structuring points to ongoing gene flow and taxonomic challenges. Ann Bot. doi: 10.1093/aob/mcu017
  71. Grube M, Hawksworth DL (2007) Trouble with lichen: the re-evaluation and re-interpretation of thallus form and fruit body types in the molecular era. Mycol Res 111(9):1116–1132. doi: 10.1016/j.mycres.2007.04.008 PubMedGoogle Scholar
  72. Gueidan C, Savi S, Thues H, Roux C, Keller C, Tibell L, Prieto M, Heimarsson S, Breuss O, Orange A, Froberg L, Wynns AA, Navarro-Rosines P, Krzewicka B, Pykaelae J, Grube M, Lutzoni F (2009) Generic classification of the Verrucariaceae (Ascomycota) based on molecular and morphological evidence: recent progress and remaining challenges. Taxon 58(1):184–208Google Scholar
  73. Guillot G, Mortier F, Estoup A (2005) Geneland: a computer package for landscape genetics. Mol Ecol Notes 5(3):712–715. doi: 10.1111/j.1471-8286.2005.01031.x Google Scholar
  74. Guillot G, Renaud S, Ledevin R, Michaux J, Claude J (2012) A unifying model for the analysis of phenotypic, genetic, and geographic data. Syst Biol 61(6):897–911. doi: 10.1093/sysbio/sys038 PubMedGoogle Scholar
  75. Guisan A, Thuiller W (2005) Predicting species distribution: offering more than simple habitat models. Ecol Lett 8(9):993–1009. doi: 10.1111/j.1461-0248.2005.00792.x Google Scholar
  76. Hale ME (1990) A synopsis of the lichen genus Xanthoparmelia (Vainio) Hale (Ascomycotina, Parmeliaceae). Smithsonian Institution Press, Washington, DCGoogle Scholar
  77. Hamilton CA, Hendrixson BE, Brewer MS, Bond JE (2014) An evaluation of sampling effects on multiple DNA barcoding methods leads to an integrative approach for delimiting species: a case study of the North American tarantula genus Aphonopelma (Araneae, Mygalomorphae, Theraphosidae). Mol Phylogenet Evol 71:79–93. doi: 10.1016/j.ympev.2013.11.007 PubMedGoogle Scholar
  78. Hausdorf B (2011) Progress toward a general species concept. Evolution 65(4):923–931. doi: 10.1111/j.1558-5646.2011.01231.x PubMedGoogle Scholar
  79. Hausdorf B, Hennig C (2010) Species delimitation using dominant and codominant multilocus markers. Syst Biol 59(5):491–503. doi: 10.1093/sysbio/syq039 PubMedGoogle Scholar
  80. Hawksworth DL (1976) Lichen chemotaxonomy. In: Bailey RH (ed) Lichenology: progress and problems. Academic, London, pp 139–184Google Scholar
  81. Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc Lond B Biol Sci 270(1512):313–321. doi: 10.1098/rspb.2002.2218 Google Scholar
  82. Hebert PDN, Stoeckle MY, Zemlak TS, Francis CM (2004) Identification of birds through DNA barcodes. PLoS Biol 2(10):e312. doi: 10.1371/journal.pbio.0020312 PubMedCentralPubMedGoogle Scholar
  83. Heled J, Drummond AJ (2010) Bayesian inference of species trees from multilocus data. Mol Biol Evol 27(3):570–580. doi: 10.1093/molbev/msp274 PubMedCentralPubMedGoogle Scholar
  84. Hey J (2006) On the failure of modern species concepts. Trends Ecol Evol 21(8):447–450. doi: 10.1016/j.tree.2006.05.011 PubMedGoogle Scholar
  85. Hibbett DS, Ohman A, Glotzer D, Nuhn M, Kirk P, Nilsson RH (2011) Progress in molecular and morphological taxon discovery in Fungi and options for formal classification on environmental sequences. Fungal Biol Rev 25:38–47. doi: 10.1016/j.fbr.2011.01.001 Google Scholar
  86. Högnabba F, Wedin M (2003) Molecular phylogeny of the Sphaerophorus globosus species complex. Cladistics 19(3):224–232. doi: 10.1111/j.1096-0031.2003.tb00365.x Google Scholar
  87. Hudson RR, Coyne JA (2002) Mathematical consequences of the genealogical species concept. Evolution 56(8):1557. doi: 10.1111/j.0014-3820.2002.tb01467.x PubMedGoogle Scholar
  88. Huelsenbeck JP, Andolfatto P, Huelsenbeck ET (2011) Structurama: Bayesian inference of population structure. Evol Bioinf Online 7(2011):55–59. doi: 10.4137/EBO.S6761 Google Scholar
  89. Jones G, Oxelman B (2014) DISSECT: an assignment-free Bayesian discovery method for species delimitation under the multispecies coalescent. Bioinformatics. doi: 10.1101/003178
  90. Kekkonen M, Hebert PD (2014) DNA barcode-based delineation of putative species: efficient start for taxonomic workflows. Mol Ecol Res. doi: 10.1111/1755-0998.12233
  91. Kelly LJ, Hollingsworth PM, Coppins BJ, Ellis CJ, Harrold P, Tosh J, Yahr R (2011) DNA barcoding of lichenized fungi demonstrates high identification success in a floristic context. New Phytol 191(1):288–300. doi: 10.1111/j.1469-8137.2011.03677.x PubMedGoogle Scholar
  92. Kiss L (2012) Limits of nuclear ribosomal DNA internal transcribed spacer (ITS) sequences as species barcodes for fungi. Proc Natl Acad Sci 109(27):E1811–E1811. doi: 10.1073/pnas.1207143109 PubMedCentralPubMedGoogle Scholar
  93. Kluge AG (1989) A concern for evidence and a phylogenetic hypothesis for relationships among Epicrates (Boidae, Serpentes). Syst Zool 38(1):7–25. doi: 10.1093/sysbio/38.1.7 Google Scholar
  94. Knowles LL, Carstens BC (2007) Delimiting species without monophyletic gene trees. Syst Biol 56(6):887–895. doi: 10.1080/10635150701701091 PubMedGoogle Scholar
  95. Kroken S, Taylor JW (2001) A gene genealogical approach to recognize phylogenetic species boundaries in the lichenized fungus Letharia. Mycologia 93(1):38–53Google Scholar
  96. Kubatko LS, Degnan JH (2007) Inconsistency of phylogenetic estimates from concatenated data under coalescence. Syst Biol 56(1):17–24. doi: 10.1080/10635150601146041 PubMedGoogle Scholar
  97. Latch EK, Dharmarajan G, Glaubitz JC, Rhodes OE Jr (2006) Relative performance of Bayesian clustering software for inferring population substructure and individual assignments at low levels of population differentiation. Conserv Genet 7(2):295–302. doi: 10.1007/s10592-005-9098-1 Google Scholar
  98. Lawrey JD (1986) Biological role of lichen substances. The Bryologist 89(2):111–122Google Scholar
  99. Le Gac M, Hood ME, Fournier E, Giraud T (2007) Phylogenetic evidence of host-specific cryptic species in the anther smut fungus. Evolution 61(1):15–26. doi: 10.1111/j.1558-5646.2007.00002.x PubMedGoogle Scholar
  100. Leaché AD (2009) Species tree discordance traces to phylogeographic clade boundaries in North American fence lizards (Sceloporus). Syst Biol 58(6):547–559. doi: 10.1093/sysbio/syp057 PubMedGoogle Scholar
  101. Leaché AD, Fujita MK (2010) Bayesian species delimitation in West African forest geckos (Hemidactylus fasciatus). Proc R Soc B: Biol Sci 277:3071–3077. doi: 10.1098/rspb.2010.0662 Google Scholar
  102. Leaché AD, Koo M, Spencer C, Papenfuss T, Fisher R, McGuire J (2009) Quantifying ecological, morphological, and genetic variation to delimit species in the coast horned lizard species complex (Phrynosoma). Proc Natl Acad Sci USA 106:12418–12423. doi: 10.1073/pnas.0906380106 PubMedCentralPubMedGoogle Scholar
  103. Leaché AD, Fujita MK, Minin VN, Bouckaert RR (2014) Species delimitation using genome-wide SNP data. Systematic Biology. doi: 10.1093/sysbio/syu018
  104. Leavitt SD, Fankhauser JD, Leavitt DH, Porter LD, Johnson LA, St. Clair LL (2011a) Complex patterns of speciation in cosmopolitan “rock posy” lichens—discovering and delimiting cryptic fungal species in the lichen-forming Rhizoplaca melanophthalma species-complex (Lecanoraceae, Ascomycota). Mol Phylogenet Evolu 59(3):587–602. doi: 10.1016/j.ympev.2011.03.020
  105. Leavitt SD, Johnson L, St. Clair LL (2011b) 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 98 (2):175–188. doi: 10.3732/ajb.1000230
  106. Leavitt SD, Johnson LA, Goward T, St. Clair LL (2011c) Species delimitation in taxonomically difficult lichen-forming fungi: an example from morphologically and chemically diverse Xanthoparmelia (Parmeliaceae) in North America. Mol Phylogen Evol 60(3):317–332. doi: 10.1016/j.ympev.2011.05.012
  107. Leavitt S, Esslinger T, Divakar P, Lumbsch H (2012a) Miocene and Pliocene dominated diversification of the lichen-forming fungal genus Melanohalea (Parmeliaceae, Ascomycota) and Pleistocene population expansions. BMC Evol Biol 12(1):176. doi: 10.1186/1471-2148-12-176 PubMedCentralPubMedGoogle Scholar
  108. Leavitt SD, Esslinger TL, Divakar PK, Lumbsch HT (2012b) Miocene divergence, phenotypically cryptic lineages, and contrasting distribution patterns in common lichen-forming fungi (Ascomycota: Parmeliaceae). Biol J Linn Soc 1007:920–937. doi: 10.1111/j.1095-8312.2012.01978.x Google Scholar
  109. Leavitt SD, Esslinger TL, Lumbsch HT (2012c) Neogene-dominated diversification in neotropical montane lichens: dating divergence events in the lichen-forming fungal genus Oropogon (Parmeliaceae). Am J Bot 99(11):1764–1777. doi: 10.3732/ajb.1200146 PubMedGoogle Scholar
  110. Leavitt SD, Esslinger TL, Nelsen MP, Lumbsch HT (2013a) Further species diversity in Neotropical Oropogon (Lecanoromycetes: Parmeliaceae) in Central America. The Lichenologist 45(04):553–564. doi: 10.1017/S0024282913000212 Google Scholar
  111. Leavitt SD, Esslinger TL, Spribille T, Divakar PK, Lumbsch HT (2013b) Multilocus phylogeny of the lichen-forming fungal genus Melanohalea (Parmeliaceae, Ascomycota): insights on diversity, distributions, and a comparison of species tree and concatenated topologies. Mol Phylogenet Evol 66(2013):138–152. doi: 10.1016/j.ympev.2012.09.013 PubMedGoogle Scholar
  112. Leavitt SD, Fernández-Mendoza F, Pérez-Ortega S, Sohrabi M, Divakar PK, Lumbsch HT, St. Clair LL (2013c) DNA barcode identification of lichen-forming fungal species in the Rhizoplaca melanophthalma species-complex (Lecanorales, Lecanoraceae), including five new species. MycoKeys 7:1–22. doi: 10.3897/mycokeys.7.4508
  113. Leavitt SD, Fernández-Mendoza F, Pérez-Ortega S, Sohrabi M, Divakar PK, Vondrák J, Thorsten Lumbsch H, Clair LLS (2013d) Local representation of global diversity in a cosmopolitan lichen-forming fungal species complex (Rhizoplaca, Ascomycota). J Biogeogr 40(9):1792–1806. doi: 10.1111/jbi.12118
  114. Leavitt SD, Lumbsch HT, Stenroos S, St. Clair LL (2013e) Pleistocene speciation in North American lichenized fungi and the impact of alternative species circumscriptions and rates of molecular evolution on divergence estimates. PLoS ONE 8(12):e85240. doi: 10.1371/journal.pone.0085240
  115. Leavitt SD, Esslinger TL, Hansen ES, Divakar PK, Crespo A, Loomis BF, Lumbsch HT (2014) DNA barcoding of brown Parmeliae (Parmeliaceae) species: a molecular approach for accurate specimen identification, emphasizing species in Greenland. Organ Divers Evol 14(1):11–20. doi: 10.1007/s13127-013-0147-1 Google Scholar
  116. Leliaert F, Verbruggen H, Vanormelingen P, Steen F, Lopez-Bautista JM, Zuccarello GC, De Clerck O (2014) DNA-based species delimitation in algae. Eur J Phycol 49(2). doi: 10.1080/09670262.2014.904524
  117. Leuckert C (1985) Probleme der Flechten-Chemotaxonomie—Stoffkombinationen und ihre taxonomische Wertung. Ber Deut Bot Ges 98:401–408Google Scholar
  118. Lewis ZA, Shiver AL, Stiffler N, Miller MR, Johnson EA, Selker EU (2007) High-density detection of restriction-site-associated DNA markers for rapid mapping of mutated loci in Neurospora. Genetics 177(2):1163–1171. doi: 10.1534/genetics.107.078147 PubMedCentralPubMedGoogle Scholar
  119. Lindblom L, Søchting U (2008) Taxonomic revision of Xanthomendoza borealis and Xanthoria mawsonii (Lecanoromycetes, Ascomycota). The Lichenologist 40(05):399–409. doi: 10.1017/S0024282908007937 Google Scholar
  120. Lohtander K, Källersjö M, Roland M, Tehler A (2000) The family physciaceae in fennoscandia: phylogeny inferred from its sequences. Mycologia 92(4):728–735Google Scholar
  121. Longton RE (1997) The role of bryophytes and lichens in polar ecosystems. In: Woodin SJ, Marquiss M (eds) Ecology of Arctic Environments. Blackwell Science, Oxford, pp 69–96 (Special publication No. 13)Google Scholar
  122. Lücking R (2012) Predicting species richness in tropical lichenized fungi with ‘modular’ combinations of character states. Biodiver Conserv 21(9):2341–2360. doi: 10.1007/s10531-011-0217-7 Google Scholar
  123. Lücking R, del Prado R, Lumbsch HT, Will-Wolf S, Aptroot A, Sipman HJM, Umana L, Chaves JL (2008) Phytogenetic patterns of morphological and chemical characters and reproductive mode in the Heterodermia obscurata group in Costa Rica (Ascomycota, Physciaceae). Syst Biodivers 6(1):31–41. doi: 10.1017/S1477200007002629 Google Scholar
  124. Lumbsch HT (1994) Die Lecanora subfusca-Gruppe in Australasien. J Hattori Bot Lab 77:1–175Google Scholar
  125. Lumbsch HT (1998a) Taxonomic use of metabolic data in lichen-forming fungi. In: Frisvad JC, Bridge PD, Arora DK (eds) Chemical Fungal Taxonomy. Marcel Dekker, New York, pp 345–387Google Scholar
  126. Lumbsch HT (1998b) The use of metabolic data in lichenology at the species and subspecific levels. The Lichenologist 30(4–5):357–367. doi: 10.1017/S0024282992000380 Google Scholar
  127. Lumbsch HT (2002) Analysis of phenolic products in lichens for identification and taxonomy. Protocols in lichenology. Culturing, biochemistry, ecophysiology and use in biomonitoring. Springer, BerlinGoogle Scholar
  128. Lumbsch HT, Leavitt SD (2011) Goodbye morphology? A paradigm shift in the delimitation of species in lichenized fungi. Fungal Divers 50(1):59–72. doi: 10.1007/s13225-011-0123-z Google Scholar
  129. Lumbsch HT, Ahti T, Altermann S, Amo de Paz G, Aptroot A, Arup U, Barcenas Peña A, Bawingan PA, Benatti MN, Betancourt L, Björk CR, Boonpragob K, Brand M, Bungartz F, Caceres MES, Candan M, Chaves JL, Clerc P, Common R, Coppins BJ, Crespo A, Dal Forno M, Divakar PK, Duya MV, Elix JA, Elvebakk A, Fankhauser J, Farkas E, Ferraro LI, Fischer E, Galloway DJ, Gaya E, Giralt M, Goward T, Grube M, Hafellner J, Hernandez JE, Herrera-Campos MA, Kalb K, Kärnefelt I, Kantvilas G, Killmann D, Kirika P, Knudesn K, Komposch H, Kondratyuk S, Lawrey JD, Mangold A, Marcelli MP, McCune BP, Michlig A, Miranda Gonzalez R, Moncada B, Naikatini A, Nelsen MP, Øvstedal DO, Palice Z, Papong K, Parnmen S, Pérez-Ortega S, Printzen C, Rico VJ, Rivas Plata E, Robayo J, Rosabal D, Ruprecht U, Salazar Allen N, Sancho L, Santos de Jesus L, Santos Vieira T, Schultz M, Seaward MRD, Sérusiaux E, Schmitt I, Sipman HJM, Sohrabi M, Søchting U, Søgaard MZ, Sparrius LB, Spielmann A, Spribille T, Sutjaritturakan J, Thammathaworn A, Thell A, Thor G, Thüs H, Timdal E, Truong C, Türk R, Umaña Tenorio L, Upreti D, van den Boom P, Vivas Rebuelta M, Wedin M, Will-Wolf S, Wirth V, Wirtz N, Yahr R, Yeshitela K, Ziemmeck F, Wheeler T, Lücking R (2011) One hundred new species of lichenized fungi: a signature of undiscovered global diversity. Phytotaxa 18:1–127Google Scholar
  130. Mark K, Saag L, Saag A, Thell A, Randlane T (2012) Testing morphology-based delimitation of Vulpicida juniperinus and V. tubulosus (Parmeliaceae) using three molecular markers. The Lichenologist 44(06):757–772. doi: 10.1017/S0024282912000448 Google Scholar
  131. Martín MP, LaGreca S, Lumbsch HT (2003) Molecular phylogeny of Diploschistes inferred from ITS sequence data. The Lichenologist 35(01):27–32. doi: 10.1006/lich.2002.0427 Google Scholar
  132. Masters BC, Fan V, Ross HA (2011) Species delimitation—a geneious plugin for the exploration of species boundaries. Mol Ecol Res 11(1):154–157. doi: 10.1111/j.1755-0998.2010.02896.x Google Scholar
  133. Mayden RL (1997) A hierarchy of species concepts: the denouement in the saga of the species problem. In: Claridge MF, Dawah HA, Wilson MR (eds) Species: the units of biodiversity. Chapman & Hall, London, pp 381–424Google Scholar
  134. Mayr E (1963) Animal species and evolution. Harvard University Press, CambridgeGoogle Scholar
  135. Mayr E (1970) Populations, species, and evolution. Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  136. McCune B (2000) Lichen communities as indicators of forest health. The Bryologist 103(2):353–356. doi: 10.1639/0007-2745(2000)103[0353:LCAIOF]2.0.CO;2 Google Scholar
  137. McCune B, Printzen C (2011) Distribution and climatic niches of the Lecanora varia group in western U.S.A. Bibliotheca Lichenologica 106:225–234Google Scholar
  138. McDonald T, Miadlikowska J, Lutzoni F (2003) The lichen genus Sticta in the Great Smoky Mountains: a phylogenetic study of morphological, chemical, and molecular data. The Bryologist 106(1):61–79. doi: 10.1639/0007-2745(2003)106[0061:TLGSIT]2.0.CO;2 Google Scholar
  139. McKay BD, Mays HL, Wu Y, Li H, Yao C-T, Nishiumi I, Zou F (2013) An empirical comparison of character-based and coalescent-based approaches to species delimitation in a young avian complex. Mol Ecol 22(19):4943–4957. doi: 10.1111/mec.12446
  140. Miller MR, Dunham JP, Amores A, Cresko WA, Johnson EA (2007) Rapid and cost-effective polymorphism identification and genotyping using restriction site associated DNA (RAD) markers. Genome Res 17(2):240–248. doi: 10.1101/gr.5681207 PubMedCentralPubMedGoogle Scholar
  141. Miralles A, Vences M (2013) New metrics for comparison of taxonomies reveal striking discrepancies among species delimitation methods in Madascincus lizards. PLoS ONE 8(7):e68242. doi: 10.1371/journal.pone.0068242 PubMedCentralPubMedGoogle Scholar
  142. Mishler BD, Brandon RN (1987) Individuality, pluralism, and the phylogenetic species concept. Biol Philos 2:397Google Scholar
  143. Molina M, Crespo A, Blanco O, Lumbsch HT, Hawksworth DL (2004) Phylogenetic relationships and species concepts in Parmelia s. str. (Parmeliaceae) inferred from nuclear ITS rDNA and β-tubulin sequences. The Lichenologist 36(01):37–54. doi: 10.1017/S0024282904013933
  144. Molina M, Del-Prado R, Divakar P, Sánchez-Mata D, Crespo A (2011) Another example of cryptic diversity in lichen-forming fungi: the new species Parmelia mayi (Ascomycota: Parmeliaceae). Organ Divers Evol 11(5):331–342. doi: 10.1007/s13127-011-0060-4 Google Scholar
  145. Monaghan MT, Wild R, Elliot M, Fujisawa T, Balke M, Inward DJG, Lees DC, Ranaivosolo R, Eggleton P, Barraclough TG, Vogler AP (2009) Accelerated species inventory on Madagascar using coalescent-based models of species delineation. Syst Biol 58(3):298–311. doi: 10.1093/sysbio/syp027 PubMedGoogle Scholar
  146. Moncada B, Reidy B, Lücking R (2014) A phylogenetic revision of Hawaiian Pseudocyphellaria (lichenized Ascomycota: Lobariaceae) reveals eight new species and a high degree of inferred endemism. The Bryologist 117(2):119–160. doi: http://dx.doi.org/10.1639/0007-2745-117.2.119
  147. Moreau CS (2009) Inferring ant evolution in the age of molecular data. Myrmecological New 12:201Google Scholar
  148. Muggia L, Grube M, Tretiach M (2008) A combined molecular and morphological approach to species delimitation in black-fruited, endolithic Caloplaca: high genetic and low morphological diversity. Mycol Res 112(1):36–49. doi: 10.1016/j.mycres.2007.02.001 PubMedGoogle Scholar
  149. Muggia L, Pérez-Ortega S, Fryday A, Spribille T, Grube M (2014) Global assessment of genetic variation and phenotypic plasticity in the lichen-forming species Tephromela atra. Fungal Divers 64(1):233–251. doi: 10.1007/s13225-013-0271-4 Google Scholar
  150. Nash TH, Zavada M (1977) Population studies among Sonoran Desert species of Parmelia subg. Xanthoparmelia (Parmeliaceae). Am J Bot 64(6):664–669Google Scholar
  151. Nylander W (1866a) Circa novum in studio Lichenum criterium chemicum. Flora 49:198–201Google Scholar
  152. Nylander W (1866b) Hypochlorite of lime and hydrate of potash. Two new criteria for the study of lichens (Tanslated and communicated by the Rev. W. A. Leighton). Bot J Linn Soc 9:358–365Google Scholar
  153. O’Brien HE, Miadlikowska J, Lutzoni F (2009) Assessing reproductive isolation in highly diverse communities of the lichen-forming fugnal genus Peltigera. Evolution 63(8):2076–2086. doi: 10.1111/j.1558-5646.2009.00685.x PubMedGoogle Scholar
  154. O’Meara BC (2010) New heuristic methods for joint species delimitation and species tree inference. Syst Biol 59(1):59–73. doi: 10.1093/sysbio/syp077 PubMedGoogle Scholar
  155. O’Neill EM, Schwartz R, Bullock CT, Williams JS, Shaffer HB, Aguilar-Miguel X, Parra-Olea G, Weisrock DW (2013) Parallel tagged amplicon sequencing reveals major lineages and phylogenetic structure in the North American tiger salamander (Ambystoma tigrinum) species complex. Mol Ecol 22(1):111–129. doi: 10.1111/mec.12049 PubMedGoogle Scholar
  156. Orock EA, Leavitt SD, Fonge BA, St. Clair LL, Lumbsch HT (2012) DNA-based identification of lichen-forming fungi: Can publicly available sequence databases aid in lichen diversity inventories of Mount Cameroon (West Africa)? The Lichenologist 44(6):833–839. doi: 10.1017/S0024282912000424
  157. Otálora MAG, Martínez I, Aragón G, Molina MC (2010) Phylogeography and divergence date estimates of a lichen species complex with a disjunct distribution pattern. Am J Bot 97(2):216–223. doi: 10.3732/ajb.0900064 PubMedGoogle Scholar
  158. Padial J, Castroviejo-Fisher S, Kohler J, Vila C, Chaparro J, De la Riva I (2009) Deciphering the products of evolution at the species level: the need for an integrative taxonomy. Zoolog Scr 38(4):431–447. doi: 10.1111/j.1463-6409.2008.00381.x Google Scholar
  159. Padial J, Miralles A, De la Riva I, Vences M (2010) The integrative future of taxonomy. Front Zoo 7(1):16. doi: 10.1186/1742-9994-7-16 Google Scholar
  160. Papong K, Lücking R, Thammathaworn A, Boonpragob K (2009) Four new taxa of Chroodiscus (thelotremoid Graphidaceae) from Southeast Asia. The Bryologist 112(1):152–163. doi: 10.1639/0007-2745-112.1.152 Google Scholar
  161. Park S-Y, Choi J, Kim JA, Jeong M-H, Kim S, Lee Y-H, Hur J-S (2013a) Draft genome sequence of Cladonia macilenta KoLRI003786, a lichen-forming fungus producing biruloquinone. Genome Announcements 1(5):e00695-13. doi: 10.1128/genomeA.00695-13 PubMedCentralPubMedGoogle Scholar
  162. Park S-Y, Choi J, Kim JA, Yu N-H, Kim S, Kondratyuk SY, Lee Y-H, Hur J-S (2013b) Draft genome sequence of lichen-forming fungus Caloplaca flavorubescens Strain KoLRI002931. Genome Announcements 1(4):e00678-13. doi: 10.1128/genomeA.00678-13 PubMedCentralPubMedGoogle Scholar
  163. Park S-Y, Choi J, Lee G-W, Kim JA, Oh S-O, Jeong M-H, Yu N-H, Kim S, Lee Y-H, Hur J-S (2014) Draft genome sequence of lichen-forming fungus Cladonia metacorallifera Strain KoLRI002260. Genome Announcements 2(1):e01065-13. doi: 10.1128/genomeA.01065-13 PubMedCentralPubMedGoogle Scholar
  164. Parnmen S, Rangsiruji A, Mongkolsuk P, Boonpragob K, Nutakki A, Lumbsch HT (2012) Using phylogenetic and coalescent methods to understand the species diversity in the Cladia aggregata complex (Ascomycota, Lecanorales). PLoS ONE 7(12):e52245. doi: 10.1371/journal.pone.0052245 PubMedCentralPubMedGoogle Scholar
  165. Pérez-Ortega S, Fernández-Mendoza F, Raggio J, Vivas M, Ascaso C, Sancho LG, Printzen C, de los Ríos A (2012) Extreme phenotypic variation in Cetraria aculeata (lichenized Ascomycota): adaptation or incidental modification? Ann Bot 109(6):1133–1148. doi: 10.1093/aob/mcs042
  166. Pino-Bodas R, Burgaz A, Martín M, Lumbsch HT (2011) Phenotypical plasticity and homoplasy complicate species delimitation in the Cladonia gracilis group (Cladoniaceae, Ascomycota). Organ Divers Evol 11(5):343–355. doi: 10.1007/s13127-011-0062-2 Google Scholar
  167. Pino-Bodas R, Burgaz AR, Martin MP, Lumbsch HT (2012a) Species delimitations in the Cladonia cariosa group (Cladoniaceae, Ascomycota). The Lichenologist 44(01):121–135. doi: 10.1017/S002428291100065X Google Scholar
  168. Pino-Bodas R, Martín M, Burgaz A (2012b) Cladonia subturgida and C. iberica (Cladoniaceae) form a single, morphologically and chemically polymorphic species. Mycol Prog 11(1):269–278. doi: 10.1007/s11557-011-0746-1 Google Scholar
  169. Pino-Bodas R, Ahti T, Stenroos S, Martín MP, Burgaz AR (2013a) Multilocus approach to species recognition in the Cladonia humilis complex (Cladoniaceae, Ascomycota). Am J Bot 100(4):664–678. doi: 10.3732/ajb.1200162 PubMedGoogle Scholar
  170. Pino-Bodas R, Martín AP, Burgaz AR, Lumbsch HT (2013b) Species delimitation in Cladonia (Ascomycota): a challenge to the DNA barcoding philosophy. Mol Ecol Resour 13(6):1058–1068. doi: 10.1111/1755-0998.12086 PubMedGoogle Scholar
  171. Pons J, Barraclough TG, Gomez-Zurita J, Cardoso A, Duran DP, Hazell S, Kamoun S, Sumlin WD, Vogler AP (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol 55(4):595–609. doi: 10.1080/10635150600852011 PubMedGoogle Scholar
  172. Porada P, Weber B, Elbert W, Pöschl U, Kleidon A (2014) Estimating impacts of lichens and bryophytes on global biogeochemical cycles. Global Biogeochem Cycles 28(2):71–85. doi: 10.1002/2013GB004705 Google Scholar
  173. Pringle A, Baker DM, Platt JL, Wares JP, Latgé JP, Taylor JW (2005) Cryptic speciation in the cosmopolitan and clonal human pathogenic fungus Aspergillus fumigatus. Evolution 59(9):1886–1899. doi: 10.1554/04-241.1 PubMedGoogle Scholar
  174. Printzen C (2009) Lichen systematics: the role of morphological and molecular data to reconstruct phylogenetic relationships. Progress in botany, vol 71. Springer, Berlin, pp 233–275Google Scholar
  175. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959PubMedCentralPubMedGoogle Scholar
  176. Puillandre N, Lambert A, Brouillet S, Achaz G (2012) ABGD, automatic barcode gap discovery for primary species delimitation. Mol Ecol 21(8):1864–1877. doi: 10.1111/j.1365-294X.2011.05239.x PubMedGoogle Scholar
  177. Rannala B, Yang Z (2003) Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci. Genetics 164:1645–1656PubMedCentralPubMedGoogle Scholar
  178. Raxworthy CJ, Ingram CM, Rabibisoa N, Pearson RG (2007) Applications of ecological niche modeling for species delimitation: a review and empirical evaluation using day geckos (Phelsuma) from Madagascar. Syst Biol 56(6):907–923. doi: 10.1080/10635150701775111 PubMedGoogle Scholar
  179. Ray J (1686) Historia planarum, vol 1. Clark, LondonGoogle Scholar
  180. Reese Næsborg R, Ekman S, Tibell L (2007) Molecular phylogeny of the genus Lecania (Ramalinaceae, lichenized Ascomycota). Mycol Res 111(5):581–591. doi: 10.1016/j.mycres.2007.03.001 PubMedGoogle Scholar
  181. Reid N, Carstens B (2012) Phylogenetic estimation error can decrease the accuracy of species delimitation: a Bayesian implementation of the general mixed Yule-coalescent model. BMC Evol Biol 12(1):196. doi: 10.1186/1471-2148-12-196 PubMedCentralPubMedGoogle Scholar
  182. Rissler L, Apodaca J (2007) Adding more ecology into species delimitation: ecological niche models and phylogeography help define cryptic species in the Black Salamander (Aneides flavipunctatus). Syst Biol 56:924–942. doi: 10.1080/10635150701703063 PubMedGoogle Scholar
  183. Rivas Plata E, Lücking R (2013) High diversity of Graphidaceae (lichenized Ascomycota: Ostropales) in Amazonian Perú. Fungal Divers 58(1):13–32. doi: 10.1007/s13225-012-0172-y Google Scholar
  184. Rivas Plata E, Lumbsch HT (2011) Parallel evolution and phenotypic divergence in lichenized fungi: a case study in the lichen-forming fungal family Graphidaceae (Ascomycota: Lecanoromycetes: Ostropales). Mol Phylogenet Evol 61(1):45–63. doi: 10.1016/j.ympev.2011.04.025 PubMedGoogle Scholar
  185. Rogers RW (1989) Chemical variation and the species concept in lichenized ascomycetes. Bot J Linn Soc 101:229–239Google Scholar
  186. Ross HA (2014) The incidence of species-level paraphyly in animals: a re-assessment. Mol Phylogenet Evol 76:10–17. doi: 10.1016/j.ympev.2014.02.021 PubMedGoogle Scholar
  187. Ross KG, Gotzek D, Ascunce MS, Shoemaker DD (2010) Species delimitation: a case study in a problematic ant taxon. Syst Biol 59(2):162–184. doi: 10.1093/sysbio/syp089 PubMedGoogle Scholar
  188. Rubin BER, Ree RH, Moreau CS (2012) Inferring phylogenies from RAD sequence data. PLoS ONE 7(4):e33394. doi: 10.1371/journal.pone.0033394 PubMedCentralPubMedGoogle Scholar
  189. Rubinoff D (2006) Utility of mitochondrial DNA barcodes in species conservation. Conserv Biol 20(4):1026–1033. doi: 10.1111/j.1523-1739.2006.00372.x PubMedGoogle Scholar
  190. Ruiz-Sanchez E, Sosa V (2010) Delimiting species boundaries within the Neotropical bamboo Otatea (Poaceae: Bambusoideae) using molecular, morphological and ecological data. Mol Phylogenet Evol 54(2):344–356. doi: 10.1016/j.ympev.2009.10.035 PubMedGoogle Scholar
  191. Ruprecht U, Lumbsch HT, Brunauer G, Green TGA, Türk R (2010) Diversity of Lecidea (Lecideaceae, Ascomycota) species revealed by molecular data and morphological characters. Antarctic Sci 22 (Special Issue 06):727–741. doi: 10.1017/S0954102010000477
  192. Salicini I, Ibáñez C, Juste J (2011) Multilocus phylogeny and species delimitation within the Natterer’s bat species complex in the Western Palearctic. Mol Phylogenet Evol 61(3):888–898. doi: 10.1016/j.ympev.2011.08.010 PubMedGoogle Scholar
  193. Satler JD, Carstens BC, Hedin M (2013) Multilocus species delimitation in a complex of morphologically conserved trapdoor spiders (Mygalomorphae, Antrodiaetidae, Aliatypus). Syst Biol 62(6):805–823. doi: 10.1093/sysbio/syt041 PubMedGoogle Scholar
  194. Schlick-Steiner BC, Steiner FM, Seifert B, Stauffer C, Christian E, Crozier RH (2010) Integrative taxonomy: a multisource approach to exploring biodiversity. Annu Rev Entomol 55(1):421–438. doi: 10.1146/annurev-ento-112408-085432 PubMedGoogle Scholar
  195. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Fungal Barcoding Consortium (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci 109(16):6241–6246. doi: 10.1073/pnas.1117018109
  196. Sérusiaux E, Villarreal AJC, Wheeler T, Goffinet B (2011) Recent origin, active speciation and dispersal for the lichen genus Nephroma (Peltigerales) in Macaronesia. J Biogeogr 38(6):1138–1151. doi: 10.1111/j.1365-2699.2010.02469.x Google Scholar
  197. Shrestha G, Peterson SL, St. Clair LL (2012) Predicting the distribution of the air pollution sensitive lichen species Usnea hirta. The Lichenologist 44(04):511–521. doi: 10.1017/S0024282912000060
  198. Simpson GG (1951) The species concept. Evolution 5:285–298Google Scholar
  199. Sites JW, Marshall JC (2003) Delimiting species: a renaissance issue in systematic biology. Trends Ecol Evol 18:462–470. doi: 10.1016/S0169-5347(03)00184-8 Google Scholar
  200. Sites JW, Marshall JC (2004) Operational criteria for delimiting species. Annu Rev Ecol Evol Syst 35(1):199–227. doi: 10.1146/annurev.ecolsys.35.112202.130128 Google Scholar
  201. Šlapeta J, López-García P, Moreira D (2006) Global dispersal and ancient cryptic species in the smallest marine eukaryotes. Mol Biol Evol 23(1):23–29. doi: 10.1093/molbev/msj001 PubMedGoogle Scholar
  202. Spribille T, Klug B, Mayrhofer H (2011) A phylogenetic analysis of the boreal lichen Mycoblastus sanguinarius (Mycoblastaceae, lichenized Ascomycota) reveals cryptic clades correlated with fatty acid profiles. Mol Phylogenet Evol 59(3):603–614. doi: 10.1016/j.ympev.2011.03.021 PubMedCentralPubMedGoogle Scholar
  203. Stenroos SK, DePriest PT (1998) SSU rDNA phylogeny of cladoniiform lichens. Am J Bot 85(11):1548–1559PubMedGoogle Scholar
  204. Talavera G, Dincă V, Vila R (2013) Factors affecting species delimitations with the GMYC model: insights from a butterfly survey. Methods Ecol Evol 4(12):1101–1110. doi: 10.1111/2041-210X.12107 Google Scholar
  205. Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS, Fisher MC (2000) Phylogenetic species recognition and species concepts in fungi. Fungal Genet Biol 31(1):21–32. doi: 10.1006/fgbi.2000.1228 PubMedGoogle Scholar
  206. Tewksbury J, Anderson JGT, Bakker JD, Billo TJ, Dunwiddie PW, Groom MJ, Hampton SE, Herman SG, Levey DJ, Machnicki NJ, del Rio CM, Power ME, Rowell K, Salomon AK, Stacey L, Trombulak SC, Wheeler TA (2014) Natural history’s place in science and society. BioScience. doi: 10.1093/biosci/biu032
  207. Thell A, Högnabba F, Elix JA, Feuerer T, Kärnefelt I, Myllys L, Randlane T, Saag A, Stenroos S, Ahti T, Seaward MRD (2009) Phylogeny of the cetrarioid core (Parmeliaceae) based on five genetic markers. The Lichenologist 41(05):489–511. doi: 10.1017/S0024282909990090
  208. Velmala S, Myllys L, Halonen P, Goward T, Ahti T (2009) Molecular data show that Bryoria fremontii and B. tortuosa (Parmeliaceae) are conspecific. The Lichenologist 41(03):231–242. doi: 10.1017/S0024282909008573 Google Scholar
  209. Vondrák J, Říha P, Arup U, Søchting U (2009) The taxonomy of the Caloplaca citrina group (Teloschistaceae) in the Black Sea region; with contributions to the cryptic species concept in lichenology. The Lichenologist 41(06):571–604. doi: 10.1017/S0024282909008317 Google Scholar
  210. Wagner CE, Keller I, Wittwer S, Selz OM, Mwaiko S, Greuter L, Sivasundar A, Seehausen O (2013) Genome-wide RAD sequence data provide unprecedented resolution of species boundaries and relationships in the Lake Victoria cichlid adaptive radiation. Mol Ecol 22(3):787–798. doi: 10.1111/mec.12023 PubMedGoogle Scholar
  211. Wang Y-Y, Liu B, Zhang X-Y, Zhou Q-M, Zhang T, Li H, Yu Y-F, Zhang X-L, Hao X-Y, Wang M, Wang L, Wei J-C (2014) Genome characteristics reveal the impact of lichenization on lichen-forming fungus Endocarpon pusillum Hedwig (Verrucariales, Ascomycota). BMC Genom 15(1):34. doi: 10.1186/1471-2164-15-34 Google Scholar
  212. Wedin M, Westberg M, Crewe AT, Tehler A, Purvis OW (2009) Species delimitation and evolution of metal bioaccumulation in the lichenized Acarospora smaragdula (Ascomycota, Fungi) complex. Cladistics 25(2):161–172. doi: 10.1111/j.1096-0031.2009.00240.x Google Scholar
  213. Weisrock DW, Rasoloarison RM, Fiorentino I, Ralison JM, Goodman SM, Kappeler PM, Yoder AD (2010) Delimiting species without nuclear monophyly in Madagascar’s mouse lemurs. PLoS ONE 5(3):e9883. doi: 10.1371/journal.pone.0009883 PubMedCentralPubMedGoogle Scholar
  214. Werth S, Cornejo C, Scheidegger C (2013) Characterization of microsatellite loci in the lichen fungus Lobaria pulmonaria (Lobariaceae). Appl Plant Sci 1(2):1200290. doi: 10.3732/apps.1200290 Google Scholar
  215. Westberg M, Arup U, Kärnefelt I (2007) Phylogenetic studies in the Candelariaceae (lichenized Ascomycota) based on nuclear ITS DNA sequence data. Mycol Res 111(11):1277–1284. doi: 10.1017/S0953756204002102 PubMedGoogle Scholar
  216. Wiemers M, Fiedler K (2007) Does the DNA barcoding gap exist?—A case study in blue butterflies (Lepidoptera: Lycaenidae). Front Zoo 4(1):8. doi: 10.1186/1742-9994-4-8 Google Scholar
  217. Wiens JJ (1998) Combining data sets with different phylogenetic histories. Syst Biol 4:568–581. doi: 10.1080/106351598260581
  218. Wiens JJ, Penkrot T (2002) Delimiting species using DNA and morphological variation and discordant species limits in spiny lizards (Sceloporus). Syst Biol 51:69–91. doi: 10.1080/106351502753475880 PubMedGoogle Scholar
  219. Wiens JJ, Servedio MR (2000) Species delimitation in systematics: inferring diagnostic differences between species. Proc R Soc Lond B Biol Sci 267(1444):631–636. doi: 10.1098/rspb.2000.1049 Google Scholar
  220. Will KW, Mishler BD, Wheeler QD (2005) The perils of DNA barcoding and the need for integrative taxonomy. Syst Biol 54(5):844–851. doi: 10.1080/10635150500354878 PubMedGoogle Scholar
  221. Wirtz N, Printzen C, Lumbsch HT (2012) Using haplotype networks, estimation of gene flow and phenotypic characters to understand species delimitation in fungi of a predominantly Antarctic Usnea group (Ascomycota, Parmeliaceae). Organ Divers Evol 12(1):17–37. doi: 10.1007/s13127-011-0066-y Google Scholar
  222. Yang Z, Rannala B (2010) Bayesian species delimitation using multilocus sequence data. Proc Natl Acad Sci 107(20):9264–9269. doi: 10.1073/pnas.0913022107 PubMedCentralPubMedGoogle Scholar
  223. Yeates DK, Seago A, Nelson L, Cameron SL, Joseph LEO, Trueman JWH (2011) Integrative taxonomy, or iterative taxonomy? Syst Entomol 36(2):209–217. doi: 10.1111/j.1365-3113.2010.00558.x Google Scholar
  224. Zhang C, Zhang D-X, Zhu T, Yang Z (2011) Evaluation of a Bayesian coalescent method of species delimitation. Syst Biol 60(6):747–761. doi: 10.1093/sysbio/syr071 PubMedGoogle Scholar
  225. Zhang J, Kapli P, Pavlidis P, Stamatakis A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29(22):2869–2876. doi: 10.1093/bioinformatics/btt499

Copyright information

© Springer India 2015

Authors and Affiliations

  • Steven D. Leavitt
    • 1
    • 2
  • Corrie S. Moreau
    • 2
  • H. Thorsten Lumbsch
    • 2
  1. 1.Committee on Evolutionary BiologyUniversity of ChicagoChicagoUSA
  2. 2.Department of Science and EducationField Museum of Natural HistoryChicagoUSA

Personalised recommendations