Abstract
Biodiversity loss from disturbances caused by human activities means that species are disappearing at an ever increasing rate. The high number of species that have yet to be described have generated extreme crisis to the taxonomist. Therefore, more than in any other era, effective ways to discover and delimitate species are needed. This paper reviews the historically foremost approaches used to delimit species in Ascomycota, the most speciose phylum of Fungi. These include morphological, biological, and phylogenetic species concepts. We argue that a single property to delineate species boundaries has various defects and each species concept comes with its own advantages and disadvantages. Recently the rate of species discovery has increased because of the advancement of phylogenetic approaches. However, traditional phylogenetic methods with few gene regions lack species-level resolution, and do not allow unambiguous conclusions. We detail the processes that affect gene tree heterogeneity, which acts as barriers to delimiting species boundaries in classical low-rank phylogenies. So far, limited insights were given to the DNA-based methodologies to establish well-supported boundaries among fungal species. In addition to reviewing concepts and methodologies used to delimit species, we present a case study. We applied different species delimitation methods to understand species boundaries in the plant pathogenic and cryptic genus Phyllosticta (Dothideomycetes, Botryosphaeriales). Several DNA-based methods over-split the taxa while in some methods several taxa fall into a single species. These problems can be resolved by using multiple loci and coalescence-based methods. Further, we discuss integrative approaches that are crucial for understanding species boundaries within Ascomycota and provide several examples for ideal and pragmatic approaches of species delimitation.
Similar content being viewed by others
References
Achari SR, Kaur J, Dinh Q, Mann R, Sawbridge T, Summerell BA, Edwards J (2020) Phylogenetic relationship between Australian Fusarium oxysporum isolates and resolving the species complex using the multispecies coalescent model. BMC Genom 21:1–20
Aguileta G, Marthey S, Chiapello H, Lebrun MH, Rodolphe F, Fournier E, Gendrault-Jacquemard A, Giraud T (2008) Assessing the performance of single-copy genes for recovering robust phylogenies. Syst Biol 57:613–627
Aime MC, Miller AN, Aoki T, Bensch K, Cai L, Crous PW, Hawksworth DL, Hyde KD, Kirk PM, Lücking R, May TW, Malosso E, Redhead SA, Rossman AY, Stadler M, Thines M, Yurkov AM, Zhang N, Schoch CL (2021) How to publish a new fungal species, or name, version 3.0. IMA Fungus 12:11
Ané C (2010) BUCKy: gene tree/species tree reconciliation with Bayesian concordance analysis. Bioinformatics 26:2910–2911
Ansari MA, Butt TM (2011) Effects of successive subculturing on stability, virulence, conidial yield, germination and shelf-life of entomopathogenic fungi. J App Microbiol 110:1460–1469
Aoki T, O’Donnell K, Geiser DM (2014) Systematics of key phytopathogenic Fusarium species: current status and future challenges. J Gen Plant Pathol 80:189–201
Araújo JP, Evans HC, Kepler R, Hughes DP (2018) Zombie-ant fungi across continents: 15 new species and new combinations within Ophiocordyceps. I. Myrmecophilous hirsutelloid species. Stud Mycol 90:119–160
Arnold AE, Maynard Z, Gilbert GS (2001) Fungal endophytes in dicotyledonous neotropical trees: patterns of abundance and diversity. Mycol Res 105:1502–1507
Avise JC, Johns GC (1999) Proposal for a standardized temporal scheme of biological classification for extant species. PNAS 96:7358–7363
Baayen R, Bonants P, Verkley G, Carroll GC, Van Der Aa HA, de Weerdt M, van Brouwershaven IR, Schutte GC, Maccheroni W Jr, de Blanco CG, Azevedo JL (2002) Nonpathogenic isolates of the citrus black spot fungus, Guignardia citricarpa, identified as a cosmopolitan endophyte of woody plants, G. mangiferae (Phyllosticta capitalensis). Phytopathology 92:464–477
Becker K, Stadler M (2021) Recent progress in biodiversity research on the Xylariales and their secondary metabolism. J Antibiot 74:1–23
Beimforde C, Feldberg K, Nylinder S, Rikkinen J, Tuovila H, Dörfelt H, Gube M, Jackson DJ, Reitner J, Seyfullah LJ, Schmidt AR (2014) Estimating the phanerozoic history of the Ascomycota lineages: combining fossil and molecular data. Mol Phylogenet Evol 78:386–398
Bengtsson-Palme J, Ryberg M, Hartmann M, Branco S, Wang Z, Godhe A, De Wit P, Sánchez-García M, Ebersberger I, de Sousa F, Amend AS, Jumpponen A, Unterseher M, Kristiansson E, Abarenkov K, Bertrand YJK, Sanli K, Eriksson KM, Vik U, Veldre V, Nilsson RH, Bunce M (2013) Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol Evol 4:914–919
Benkert D (2011) Lamprospora bavarica and L. esterlechnerae (Pezizales), zwei neue Arten aus dem Nationalpark Bayerischer Wald (Deutschland, Bayern). Z Mycol 77:149–155
Berbee ML, Taylor JW (1993) Dating the evolutionary radiations of the true fungi. Can J Bot 71:1114–1127
Bhunjun CS, Phukhamsakda C, Jayawardena RS, Jeewon R, Promputtha I, Hyde KD (2021) Investigating species boundaries in Colletotrichum. Fungal Divers 107:107–127
Boehm EWA, Mugambi GK, Miller AN, Huhndorf SM, Marincowitz S, Spatafora JW, Schoch CL (2009) A molecular phylogenetic reappraisal of the Hysteriaceae, Mytilinidiaceae and Gloniaceae (Pleosporomycetidae, Dothideomycetes) with keys to world species. Stud Mycol 64:49–83
Boluda CG, Rico VJ, Divakar PK, Nadyeina O, Myllys L, McMullin RT, Zamora JC, Scheidegger C, Hawksworth DL (2019) Evaluating methodologies for species delimitation: the mismatch between phenotypes and genotypes in lichenized fungi (Bryoria sect. Implexae, Parmeliaceae). Persoonia 42:75–100
Borman AM, Johnson EM (2020) Name changes for fungi of medical importance, 2018 to 2019. J Clin Microbiol 59:e01811-e1820
Bouckaert R, Vaughan TG, Barido-Sottani J, Duchêne S, Fourment M, Gavryushkina A, Heled J, Jones G, Kühnert D, De Maio N, Matschiner M, Mendes FK, Müller NF, Ogilvie HA, du Plessis L, Popinga A, Rambaut A, Rasmussen D, Siveroni I, Suchard MA, Wu C-H, Xie D, Zhang C, Stadler T, Drummond AJ (2019) BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLOS Comput Biol 15(4):e1006650
Brasier C (2000) The rise of the hybrid fungi. Nature 405:134–135
Braun U, Dick MA (2002) Leaf spot diseases of eucalypts in New Zealand caused by Pseudocercospora species. N Z J Sci 32:221–234
Brookfield J (2011) Coalescence: the sharing of ancestry of alleles. eLS. https://doi.org/10.1002/9780470015902.a0001775.pub2
Bruns TD, White TJ, Taylor JW (1991) Fungal molecular systematics. Annu Rev Ecol Syst 22:525–564
Bustamante DE, Oliva M, Leiva S, Mendoza JE, Bobadilla L, Angulo G, Calderon MS (2019) Phylogeny and species delimitations in the entomopathogenic genus Beauveria (Hypocreales, Ascomycota), including the description of B. peruviensis sp. nov. MycoKeys 58:47–68
Carlile M, Watkinson SC, Gooday GW (1994) The fungi, first edit. Academic Press, New York
Carstens BC, Pelletier TA, Reid NM, Satler JD (2013) How to fail at species delimitation. Mol Ecol 22:4369–4383
Chan JZ, Halachev MR, Loman NJ, Constantinidou C, Pallen MJ (2012) Defining bacterial species in the genomic era: insights from the genus Acinetobacter. BMC Microbiol 12:302
Cheek M, Nic Lughadha E, Kirk P, Lindon H, Carretero J, Looney B, Douglas B, Haelewaters D, Gaya E, Llewellyn T, Ainsworth AM (2020) New scientific discoveries: plants and fungi. Plants People Planet 2:371–388
Chethana TKW, Manawasinghe IS, Hurdeal VG, Bhunjun CS, Appadoo MA, Gentekaki E, Raspé O, Promputtha I, Hyde KD (2021) What are fungal species and how to delineate them? Fungal Divers (in press)
Chung Y, Ane C (2011) Comparing two Bayesian methods for gene tree/species tree reconstruction: simulations with incomplete lineage sorting and horizontal gene transfer. Syst Biol 60:261–275
Cissé OH, Ma L, Khil PP, Dekker JP, Kutty G, Bishop L, Liu Y, Deng X, Hauser PM, Pagni M, Hirsch V (2018) Comparative population genomics analysis of the mammalian fungal pathogen Pneumocystis. Mbio 9:e00381-e418
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659
Cottrell TE, Riddick EW (2012) Limited transmission of the ectoparasitic fungus Hesperomyces virescens between lady beetles. Psyche 2012. Article ID 814378
Cracraft J (2000) Species concepts in theoretical and applied biology: a systematic debate with consequences. Pages 3-14 in species concept and phylogenetic theory: a debate (Q. D. Wheeler, and R. Meier, eds.). Colombia University Press, New York
Cronquist A (1978) Once again, what is a species? In: Knutson LV (ed) Bio systematics in agriculture. Alleheld Osmun, Montclair
Crous PW, Lombard L, Sandoval-Denis M et al (2021a) Fusarium: more than a node or a foot-shaped basal cell. Stud Mycol. https://doi.org/10.1016/j.simyco.2021.100116
Crous PW, Rossman AY, Aime C, Allen C, Burgess T, Groenewald JZ, Castlebury L (2021b) Names of phytopathogenic fungi: a practical guide. Phytopathology. https://doi.org/10.1094/PHYTO-11-20-0512-PER
Crowther TW, Maynard DS, Crowther TR, Peccia J, Smith JR, Bradford MA (2014) Untangling the fungal niche: the trait-based approach. Front Microbiol 5:579
De Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886
Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430
Dettman JR, Jacobson DJ, Taylor JW (2003) A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Evolution 57:2703–2720
Devanadera BEA (2011) Molecular identification of Mycelia sterilia by analysis of the internal transcribed spacer (ITS) region DNA sequences and screening for protease and xylanase activities. University Library, University of the Philippines at Los Baños, Los Baños
Dobzhansky T (1935) A critique of the species concept in biology. Philos Sci 2:344–355
Dobzhansky T (1937) Genetics and the origin of species. Columbia University Press, New York
Drenth A, McTaggart AR, Wingfield BD (2019) Fungal clones win the battle, but recombination wins the war. IMA Fungus 10:18
Dupuis JR, Roe AD, Sperling FA (2012) Multi-locus species delimitation in closely related animals and fungi: one marker is not enough. Mol Ecol 18:4422–4436
Dyer PS, O’Gorman CM (2011) A fungal sexual revolution: Aspergillus and Penicillium show the way. Curr Opin Microbiol 14:649–654
Ezard T, Fujisawa T, Barraclough T (2017) splits: SPecies' LImits by Threshold Statistics. R package version 1.0-19/r52. https://R-Forge.R-project.org/projects/splits/
Ezra D, Hess W, Strobel GA (2004) New endophytic isolates of Muscodor albus, a volatile-antibiotic-producing fungus. Microbiol 150:4023–4031
Flouri T, Jiao X, Rannala B, Yang Z (2018) Species Tree Inference with BPP using genomic sequences and the multispecies coalescent. Mol Biol Evol 35:2585–2593
Fones HN, Bebber DP, Chaloner TM, Kay WT, Steinberg G, Gurr SJ (2020) Threats to global food security from emerging fungal and oomycete crop pathogens. Nat Food 1:332–342
Frisvad JC, Andersen B, Thrane U (2008) The use of secondary metabolite profiling in chemotaxonomy of filamentous fungi. Mycol Res 112:231–240
Fryar SC, Haelewaters D, Catcheside DE (2019) Annabella australiensis gen. & sp. nov. (Helotiales, Cordieritidaceae) from South Australian mangroves. Mycol Prog 18:973–981
Fujisawa T, Barraclough TG (2013) Delimiting species using single-locus data and the generalized mixed Yule coalescent approach: a revised method and evaluation on simulated data sets. Syst Biol 62:707–724
Garcia JF, Lawrence DP, Morales-Cruz A, Travadon R, Minio A, Hernandez-Martinez R, Rolshausen PE, Baumgartner K, Cantu D (2021) Phylogenomics of plant-associated Botryosphaeriaceae species. Front Microbiol 12:587
Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318
Geiser DM, Aoki T, Bacon CW, Baker SE, Bhattacharyya MK, Brandt ME, Brown DW, Burgess LW, Chulze S, Coleman JJ, Correll JC (2013) One fungus, one name: defining the genus Fusarium in a scientifically robust way that preserves longstanding use. Phytopathol 103:400–408
Geiser DM, Al-Hatmi A, Aoki T et al (2020) Phylogenomic analysis of a 55.1 kb 19-gene dataset resolves a monophyletic Fusarium that includes the Fusarium solani species complex. Phytopathol. https://doi.org/10.1094/PHYTO-08-20-0330-LE
Giordano L, Sillo F, Garbelotto M, Gonthier P (2018) Mitonuclear interactions may contribute to fitness of fungal hybrids. Sci Rep 8:1–7
Giraud T, Refrégier G, Le Gac M, de Vienne DM, Hood ME (2008) Speciation in fungi. Fungal Genet Biol 45:791–802
Gladieux P, Condon B, Ravel S, Soanes D, Maciel JL, Nhani A, Chen L, Terauchi R, Lebrun MH, Tharreau D, Mitchell T (2018) Gene flow between divergent cereal-and grass-specific lineages of the rice blast fungus Magnaporthe oryzae. Mbio 9(1):e01219-17
Glienke C, Pereira O, Stringari D, Fabris J, Kava-Cordeiro V, GalliTerasawa L, Cunnington J, Shivas RG, Groenewald JZ, Crous PW (2011) Endophytic and pathogenic Phyllosticta species, with reference to those associated with Citrus Black Spot. Persoonia 26:47–56
Gnavi G, Ercole E, Panno L, Vizzini A, Varese GC (2014) Dothideomycetes and Leotiomycetes sterile mycelia isolated from the Italian seagrass Posidonia oceanica based on rDNA data. Springerplus 3:508
Goldstein PZ, Desalle R, Amato G, Vogler AP (2000) Conservation genetics at the species boundary. Conserv Biol 14:120–131
González MC, Anaya AL, Glenn AE, Macías-Rubalcava ML, Hernández-Bautista BE, Hanlin RT (2009) Muscodor yucatanensis, a new endophytic ascomycete from Mexican chakah, Bursera simaruba. Mycotaxon 110:363–372
Gostinčar C (2020) Towards genomic criteria for delineating fungal species. J Fungi 6:246
Groenewald JZ, Nakashima C, Nishikawa J, Shin HD, Park JH, Jama AN, Groenewald M, Braun U, Crous PW (2013) Species concepts in Cercospora: spotting the weeds among the roses. Stud Mycol 75:115–170
Grünwald NJ, McDonald BA, Milgroom MG (2016) Population genomics of fungal and oomycete pathogens. Annu Rev Phytopathol 54:323–346
Guého E, Leclerc MC, de Hoog GS, Dupont B (1997) Molecular taxonomy and epidemiology of Blastomyces and Histoplasma species. Mycoses 40:69–81
Gueidan C, Roux C, Lutzoni F (2007) Using a multigene phylogenetic analysis to assess generic delineation and character evolution in Verrucariaceae (Verrucariales, Ascomycota). Mycol Res 111:1145–1168
Guicking D, Lawson R, Joger U, Wink M (2006) Evolution and phylogeny of the genus Natrix (Serpentes: Colubridae). Biol J Linn Soc 87:127–143
Guo LD, Hyde KD, Liew ECY (2000) Identification of endophytic fungi from Livistona chinensis based on morphology and rDNA sequences. New Phytol 147:617–630
Guzow-Krzemińska B, Flakus A, Kosecka M, Jabłońska A, Rodriguez-Flakus P, Kukwa M (2019) New species and records of lichens from Bolivia. Phytotaxa 397:257–279
Haelewaters D, De Kesel A (2020) Checklist of thallus-forming Laboulbeniomycetes from Belgium and the Netherlands, including Hesperomyces halyziae and Laboulbenia quarantenae spp. nov. MycoKeys 71:23–86
Haelewaters D, Pfister DH (2019) Morphological species of Gloeandromyces (Ascomycota, Laboulbeniales) evaluated using single-locus species delimitation methods. Fungal Syst Evol 3:19–33
Haelewaters D, Comont RF, Zhao SY, Pfister DH (2014) Hesperomyces virescens (Fungi, Ascomycota, Laboulbeniales) attacking Harmonia axyridis (Coleoptera, Coccinellidae) in its native range. Chin Sci Bull 59:528–532
Haelewaters D, Zhao SY, Clusella-Trullas S, Cottrell TE, De Kesel A, Fiedler L, Herz A, Hesketh H, Hui C, Kleespies RG, Losey JE, Minnaar IA, Murray KM, Nedvěd O, Pfliegler WP, Raak-van den Berg CL, Riddick EW, Shapiro-Ilan DI, Smyth RR, Steenberg T, van Wielink PS, Viglášová S, Zhao Z, Ceryngier P, Roy HE (2017) Parasites of Harmonia axyridis: current research and perspectives. Biocontrol 62:355–371
Haelewaters D, De Kesel A, Pfister DH (2018) Integrative taxonomy reveals hidden species within a common fungal parasite of ladybirds. Sci Rep 8:15966
Haelewaters D, Dima B, Abdel-Hafiz BII, Abdel-Wahab MA, Abul-Ezz SR, Acar I, Aguirre-Acosta E, Aime MC, Aldemir S, Ali M, Ayala-Vásquez O, Bakhit MS, Bashir H, Battistin E, Bendiksen E, Castro-Rivera R, Çolak ÖF, De Kesel A, de la Fuente JI, Dizkırıcı A, Hussain S, Jansen GM, Kaygusuz O, Khalid AN, Khan J, Kiyashko AA, Larsson E, Martínez-González CR, Morozova OV, Niazi AR, Noordeloos ME, Pham THG, Popov ES, Psurtseva NV, Schoutteten N, Sher H, Türkekul İ, Verbeken A, Ahmad H, Afshan NS, Christe P, Fiaz M, Glaizot O, Liu J, Majeed J, Markotter W, Nagy A, Nawaz H, Papp V, Péter Á, Pfliegler WP, Qasim T, Riaz M, Sándor AD, Szentiványi T, Voglmayr H, Yousaf N, Krisai-Greilhuber I (2020a) Fungal systematics and evolution: FUSE 6. Sydowia 72:231–356
Haelewaters D, Hiller T, Kemp EA, van Wielink PS, Shapiro-Ilan DI, Aime MC, Nedvěd O, Pfister DH, Cottrell TE (2020b) Mortality of native and invasive ladybirds co-infected by ectoparasitic and entomopathogenic fungi. PeerJ 8:e10110
Haelewaters D, Okrasińska A, Gorczak M, Pfister DH (2020c) Draft genome sequence of the globally distributed cockroach-infecting fungus Herpomyces periplanetae strain D. Haelew. 1187d. Microbiol Res Announc 9:e01458-e1519
Haelewaters D, Blackwell M, Pfister DH (2021) Laboulbeniomycetes: intimate fungal associates of arthropods. Ann Rev Entomol 66:257–276
Hage C, Azar M, Bahr N, Loyd J, Wheat L (2015) Histoplasmosis: up-to-date evidence-based approach to diagnosis and management. Semin Respir Crit Care Med 36:729–745
Hahn MW, Nakhleh L (2016) Irrational exuberance for resolved species trees. Evolution 70:7–17
Han KH, Lee DB, Kim JH, Kim MS, Han KY, Kim WS, Park YS, Kim HB, Han DM (2003) Environmental factors affecting development of Aspergillus nidulans. J Microbiol 41:34–40
Hardoim PR, Van Overbeek LS, Berg G, Pirttilä AM, Compant S, Campisano A, Döring M, Sessitsch A (2015) The hidden world within plants: ecological and evolutionary considerations for defining functioning of microbial endophytes. Microbiol Mol Biol Rev 79:293–320
Haridas S, Albert R, Binder M, Bloem J, LaButti K, Salamov A, Andreopoulos B, Baker SE, Barry K, Bills G, Bluhm BH, Cannon C, Castanera R, Culley DE, Daum C, Ezra D, Gonzalez JB, Henrissat B, Kuo A, Liang C, Lipzen A, Lutzoni F, Magnuson J, Mondo SJ, Nolan M, Ohm RA, Pangilinan J, Park HJ, Ramirez L, Alfaro M, Sun H, Tritt A, Yoshinaga Y, Zwiers LH, Turgeon BG, Goodwin SB, Spatafora JW, Crous PW, Grigoriev IV (2020) 101 Dothideomycetes genomes: a test case for predicting lifestyles and emergence of pathogens. Stud Mycol 96:141–153
Harrington TC, Rizzo DM (1999) Defining species in the fungi. In: Worrall JJ (ed) Structure and dynamics of fungal populations. Population and community biology series, vol 25. Springer, Dordrecht
Hart MW, Sunday J (2007) Things fall apart: biological species form unconnected parsimony networks. Biol Lett 3:509–512
Hawksworth DL (1991) The fungal dimension of biodiversity: magnitude, significance, and conservation. Mycol Res 95:641–655
Hawksworth DL (2001) The magnitude of fungal diversity: the 1· 5 million species estimate revisited. Mycol Res 105:1422–1432
Hawksworth DL, Lücking R (2017) Fungal diversity revisited: 2.2 to 3.8 million species. Microbiol Spec 5:1–17
Hawksworth DL, Kirk PM, Sutton B, Pegler D (1996) Ainsworth and Bisby’s dictionary of the fungi, 8th edn. CABI, Wallingford
Hawksworth DL, McNeill J, de Beer W et al (2013) Names of fungal species with the same epithet applied to different morphs: how to treat them. IMA Fungus 4:53–56
Hawksworth DL, Hibbett DS, Kirk PM, Lücking R (2016) (308–310) Proposals to permit DNA sequence data to serve as types of names of fungi. Taxon 65:899–900
Helaly SE, Thongbai B, Stadler M (2018) Diversity of biologically active secondary metabolites from endophytic and saprotrophic fungi of the ascomycete order Xylariales. Nat Prod Rep 35:992–1014
Hittinger CT, Rokas A, Bai FY, Boekhout T, Goncalves P, Jeffries TW, Kominek J, Lachance MA, Libkind D, Rosa CA, Sampaio JP (2015) Genomics and the making of yeast biodiversity. Curr Opin Genet Dev 35:100–109
Hoang DT, Vinh LS, Flouri T, Stamatakis A, von Haeseler A, Minh BQ (2018) MPBoot: fast phylogenetic maximum parsimony tree inference and bootstrap approximation. BMC Evol Biol 18:11
Hongsanan S, Jeewon R, Purahong W, Xie N et al (2018) Can we use environmental DNA as holotypes? Fungal Divers 92:1–30
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755
Hyde KD, Cai L, McKenzi EHC, Yang YL, Zhang JZ, Prihastuti H (2009) Colletotrichum: a catalogue of confusion. Fungal Divers 39:1–17
Hyde KD, Maharachchikumbura SSN, Hongsanan S et al (2017) The ranking of fungi: a tribute to David L. Hawksworth on his 70th birthday. Fungal Divers 84:1–23
Hyde KD, Chaiwan N, Norphanphoun C, Boonmee S, Camporesi E, Chethana KWT, Dayarathne MC et al (2018) Mycosphere notes 169–224. Mycosphere 9:271–430
Hyde KD, Xu JC, Rapior S, Jeewon R, Lumyong S, Niego AGT, Abeywickrama PD, Aluthmuhandiram JVS, Brahamanage RS, Brooks S, Chaiyasen A, Chethana KWT, Chomnunti P, Chepkirui C, Chuankid B, de Silva NI, Doilom M, Faulds C, Gentekaki E, Gopalan V, Kakumyan P, Harishchandra D, Hemachandran H, Hongsanan S, Karunarathna A, Karunarathna SC, Khan S, Kumla J, Jayawardena RS, Liu JK, Liu N, Luangharn T, Macabeo APG, Marasinghe DS, Meeks D, Mortimer PE, Mueller P, Nadir S, Nataraja KN, Nontachaiyapoom S, O’Brien M, Penkhrue W, Phukhamsakda C, Ramanan US, Rathnayaka AR, Sadaba RB, Sandargo B, Samarakoon BC, Tennakoon DS, Siva R, Sriprom W, Suryanarayanan TS, Sujarit K, Suwannarach N, Suwunwong T, Thongbai B, Thongklang N, Wei DP, Wijesinghe SN, Winiski J, Yan J, Yasanthika E, Stadler M (2019) The amazing potential of fungi: 50 ways we can exploit fungi industrially. Fungal Divers 97:1–136
Hyde KD, Jeewon R, Chen YJ, Bhunjun CS, Calabon MS, Jiang HB, Lin CG, Norphanphoun C, Sysouphanthong P, Pem D, Tibpromma S, Zhang Q, Doilom M, Jayawardena RS, Liu JK, Maharachchikumbura SSN, Phukhamsakda C, Phookamsak R, Al-Sadi AM, Thongklang N, Wang Y, Gafforov Y, Jones EBG, Lumyong S (2020) The numbers of fungi: is the descriptive curve flattening? Fungal Divers 103:219–271
James TY, Stajich JE, Hittinger CT, Rokas A (2020) Toward a fully resolved fungal tree of life. Annu Rev Microbiol 74:291–313
Jayawardena RS, Hyde KD, Jeewon R, Ghobad-Nejhad M, Wanasinghe DN, Liu N, Phillips AJL, Oliveira-Filho JRC, da Silva GA, Gibertoni TB, Abeywikrama P, Carris LM, Chethana KWT, Dissanayake AJ, Hongsanan S, Jayasiri SC, McTaggart AR, Perera RH, Phutthacharoen K, Savchenko KG, Shivas RG, Thongklang N, Dong W, Wei D, Wijayawardena NN, Kang JC (2019) One stop shop II: taxonomic update with molecular phylogeny for important phytopathogenic genera: 26–50. Fungal Divers 94:41–129
Jones G (2017) Algorithmic improvements to species delimitation and phylogeny estimation under the multispecies coalescent. J Math Biol 74:447–467
Jones G, Aydin Z, Oxelman B (2014) DISSECT: an assignment-free Bayesian discovery method for species delimitation under the multispecies coalescent. Bioinformatics 31:991–998
Kanz B, von Brackel W, Cezanne R, Eichler M, Hohmann ML, Teuber D, Printzen C (2015) DNA barcodes for the distinction of reindeer lichens: a case study using Cladonia rangiferina and C. stygia. Herzogia 28:445–464
Kanzi AM, Trollip C, Wingfield MJ, Barnes I, Van der Nest MA, Wingfield BD (2020) Phylogenomic incongruence in Ceratocystis: a clue to speciation? BMC Genom 21:362
Kapli P, Lutteropp S, Zhang J, Kobert K, Pavlidis P, Stamatakis A, Flouri T (2017) Multi-rate Poisson tree processes for single-locus species delimitation under maximum likelihood and Markov chain Monte Carlo. Bioinformatics 33:1630–1638
Kasuga T, White TJ, Koenig G, Mcewen J, Restrepo A, Castañeda E, Da Silva LC, Heins-Vaccari EM, De Freitas RS, Zancopé-Oliveira RM, Qin Z (2003) Phylogeography of the fungal pathogen Histoplasma capsulatum. Mol Ecol 12:3383–3401
Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166
Keuler R, Garretson A, Saunders T, Erickson RJ, Andre NS, Grewe F, Smith H, Lumbsch HT, Huang JP, Clair LL, Leavitt SD (2020) Genome-scale data reveal the role of hybridization in lichen-forming fungi. Sci Rep 10:1497
Khan FK, Kluting K, Tångrot J, Urbina H, Ammunet T, Sahraei SE, Rydén M, Ryberg M, Rosling A (2020) Naming the untouchable –environmental sequences and niche partitioning as taxonomical evidence in fungi. IMA Fungus 11:23
Kim M, Oh H-S, Park S-C, Chun J (2014) Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64:346–351
Kjaerbolling I, Vesth T, Frisvad JC, Nybo JL, Theobald S, Kildgaard S, Petersen TI, Kuo A, Sato A, Lyhne EK, Kogle ME, Wiebenga A, Kun RS, Lubbers RJM, Makela MR, Barry K, Chovatia M, Clum A, Daum C, Haridas S, He G, LaButti K, Lipzen A, Mondo S, Pangilinan J, Riley R, Salamov A, Simmons BA, Magnuson JK, Henrissat B, Mortensen UH, Larsen TO, de Vries RP, Grigoriev IV, Machida M, Baker SE, Andersen MR (2020) A comparative genomics study of 23 Aspergillus species from section Flavi. Nat Commun 11:1106
Knapp DG, Kovács GM, Zajta E, Groenewald JZ, Crous PW (2015) Dark septate endophytic pleosporalean genera from semiarid areas. Persoonia 35:87–100
Kobmoo N, Mongkolsamrit S, Arnamnart N, Luangsa-Ard JJ, Giraud T (2019) Population genomics revealed cryptic species within host-specific zombie-ant fungi (Ophiocordyceps unilateralis). Mol Phylogenet Evol 140:106580
Kohn LM (2005) Mechanisms of fungal speciation. Annu Rev Phytopathol 43:279–308
Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A (2019) RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35:4453–4455
Kück U, Pöggeler S (2009) Cryptic sex in fungi. Fungal Biol Rev 23:86–90
Lacap DC, Hyde KD, Liew ECY (2003) An evaluation of the fungal ‘morphotype’ concept based on ribosomal DNA sequences. Fungal Divers 12:53–66
Lambert C, Wendt L, Hladki AI et al (2019) Hypomontagnella (Hypoxylaceae): a new genus segregated from Hypoxylon by a polyphasic taxonomic approach. Mycol Prog 18:187–201
Lanfear R, Calcott B, Ho SYW, Guindon S (2012) PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29:1695–1701
Lawrence DP, Rotondo F, Gannibal PB (2016) Biodiversity and taxonomy of the pleomorphic genus Alternaria. Mycol Prog 15:1–22
Leavitt SD, Johnson L, St. Clair LL (2011) 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 98:175–188
Leavitt SD, Moreau CS, Lumbsch HT (2015) The dynamic discipline of species delimitation: progress toward effectively recognizing species boundaries in natural populations. In: Recent advances in lichenology. Springer, New Delhi
Lee SC, Ni M, Li W, Shertz C, Heitman J (2010) The evolution of sex: a perspective from the fungal kingdom. Microbiol Mol Biol Rev 74:298–340
Letunic I, Bork P (2019) Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 47(W1):W256–W259
Liu L, Yu L, Pearl DK, Edwards SV (2009) Estimating species phylogenies using coalescence times among sequences. Syst Biol 58:468–477
Liu F, Wang M, Damm U, Crous PW, Cai L (2016) Species boundaries in plant pathogenic fungi: a Colletotrichum case study. BMC Evol Biol 16:1–4
Liu J-K, Hyde KD, Jeewon R et al (2017) Ranking higher taxa using divergence times: a case study in Dothideomycetes. Fungal Divers 84:75–99
Lombard L, van der Merwe NA, Groenewald JZ, Crous PW (2015) Generic concepts in Nectriaceae. Stud Mycol 80:189–245
Lücking R, Hawksworth DL (2018) Formal description of sequence-based voucherless Fungi: promises and pitfalls, and how to resolve them. IMA Fungus 9:143–165
Lücking R, Aime MC, Robbertse B et al (2020) Unambiguous identification of fungi: where do we stand and how accurate and precise is fungal DNA barcoding? IMA Fungus 11:14
Lumbsch HT, Leavitt SD (2011) Goodbye morphology? A paradigm shift in the delimitation of species in lichenized fungi. Fungal Divers 50:59–72
Maharachchikumbura SSN, Guo LD, Chukeatirote E, Hyde KD (2014) Improving the backbone tree for the genus Pestalotiopsis; addition of P. steyaertii and P. magna sp. nov. Mycol Prog 13:617–624
Maharachchikumbura SSN, Larignon P, Hyde KD, Al-Sadi AM, Liu ZY (2016) Characterization of Neopestalotiopsis, Pestalotiopsis and Truncatella species associated with grapevine trunk diseases in France. Phytopathol Mediterr 55:380–390
Maharachchikumbura SSN, Wanasinghe DN, Cheewangkoon R, Al-Sadi AM (2021) Uncovering the hidden taxonomic diversity of fungi in Oman. Fungal Divers 106:229–268
Mallet J (1995) A species definition for the modern synthesis. Trends Ecol Evol 10:294–299
Manamgoda DS, Rossman AY, Castlebury LA, Crous PW, Madrid H, Chukeatirote E, Hyde KD (2014) The genus Bipolaris. Stud Mycol 79:221–288
Matute DR, Sepulveda VE (2019) Fungal species boundaries in the genomics era. Fungal Genet Biol 131:103249
Mayr E (1940) Speciation phenomena in birds. Am Nat 74(752):249–278
Mayr E (1942) Systematics and the origin of species. Columbia University Press, New York
Mayr E (1999) Systematics and the origin of species, from the viewpoint of a zoologist. Harvard University Press, Cambridge
Mays HL, McKay BD, Tietze DT et al (2015) A multilocus molecular phylogeny for the avian genus Liocichla (Passeriformes: Leiothrichidae: Liocichla). Avian Res 6:17
McDonald J (2015) Morphological and molecular systematics of Resupinatus (Basidiomycota). The University of Western Ontario, London
McMullin RT, Lendemer JC, Braid HE, Newmaster SG (2016) Molecular insights into the lichen genus Alectoria (Parmeliaceae) in North America. Botany 94:165–175
McNeill J, Barrie FR, Buck WR, Demoulin V, Greuter W, Hawksworth DL, Herendeen PS, Knapp S, Marhold K, Prado J, Prud’homme van Reine WF, Smith GF, Wiersema JH, Turland NJ (2012) International code of nomenclature for algae, fungi, and plants (Melbourne Code). Koeltz Scientific Books, Königstein
Meshram V (2017) Muscodor camphora, a new endophytic species from Cinnamomum camphora. Mycosphere 8:568–582
Mirarab S, Warnow T (2015) ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics 31:i44–i52
Monaghan MT, Wild R, Elliot M, Fujisawa T, Balke M, Inward DJ, 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 58:298–311
Mortimer PE, Jeewon R, Xu J-C, Lumyong S, Wanasinghe DN (2021) Morpho-phylo taxonomy of novel dothideomycetous fungi associated with dead woody twigs in Yunnan province China. Front Microbiol 12:654683
Myllys L, Velmala S, Holien H, Halonen P, Li-Song WA, Goward T (2011) Phylogeny of the genus Bryoria. Lichenologist 43:617–638
Naciri Y, Linder HP (2015) Species delimitation and relationships: the dance of the seven veils. Taxon 64:3–16
Naik BS (2009) Taxonomic placement for mycelia sterilia in endophytic fungal research: a molecular approach. Curr Sci 97:1276–1277
Nalim FA, Samuels GJ, Wijesundera RL, Geiser DM (2011) New species from the Fusarium solani species complex derived from perithecia and soil in the Old World tropics. Mycologia 103:1302–1330
Naranjo-Ortiz MA, Gabaldón T (2019) Fungal evolution: major ecological adaptations and evolutionary transitions. Biol Rev 94:1443–1476
Nevalainen H, Peterson R (2014) Making recombinant proteins in filamentous fungi-are we expecting too much? Front Microbiol 5:75
Norphanphoun C, Hongsanan S, Gentekaki E, Chen YJ, Kuo CH, Hyde KD (2020) Differentiation of species complexes in Phyllosticta enables better species resolution. Mycosphere 11:2542–2628
Nosratabadi M, Kordbacheh P, Kachuei R, Safara M, Rezaie S, Afshari MA, Jafari H (2017) Isolation and identification of non-pathogenic and pathogenic fungi from the soil of Greater Tunb, Abu-Musa and Sirri Islands, Persian Gulf, Iran. J Appl Biotechnol Rep 4:713–718
Noumeur SR, Teponno RB, Helaly SE et al (2020) Diketopiperazines from Batnamyces globulariicola, gen. & sp. nov.(Chaetomiaceae), a fungus associated with roots of the medicinal plant Globularia alypum in Algeria. Mycol Prog 19:589–603
Ntana F, Mortensen UH, Sarazin C, Figge R (2020) Aspergillus: a powerful protein production platform. Catalysts 10:1064
O’Donnell K, Sutton DA, Fothergill A, McCarthy D, Rinaldi MG, Brandt ME, Zhang N, Geiser DM (2008) Molecular phylogenetic diversity; multilocus haplotype nomenclature, and in vitro antifungal resistance within the Fusarium solani species complex. J Clin Microbiol 46:2477–2490
O’Donnell K, Rooney AP, Proctor RH, Brown DW, McCormick SP, Ward TJ, Frandsen RJ, Lysøe E, Rehner SA, Aoki T, Robert VA et al (2013) Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria. Fungal Genet Biol 52:20–31
O’Donnell K, Al-Hatmi AM, Aoki T, Brankovics B, Cano-Lira JF, Coleman JJ, de Hoog GS, Di Pietro A, Frandsen RJN, Geiser DM et al (2020) No to Neocosmospora: phylogenomic and practical reasons for continued inclusion of the Fusarium solani species complex in the genus Fusarium. mSphere 5:e810–20
Olarte RA, Menke J, Zhang Y, Sullivan S, Slot JC, Huang Y, Badalamenti JP, Quandt AC, Spatafora JW, Bushley KE (2019) Chromosome rearrangements shape the diversification of secondary metabolism in the cyclosporin producing fungus Tolypocladium inflatum. BMC Genom 20:1–23
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:e52245
Pažoutová S, Follert S, Bitzer J, Keck M, Surup F, Šrůtka P, Holuša J, Stadler M (2013) A new endophytic insect-associated Daldinia species, recognised from a comparison of secondary metabolite profiles and molecular phylogeny. Fungal Divers 60:107–123
Peberdy JF (1980) Sexual reproduction in fungi. In: Developmental microbiology. Springer, Boston
Pérez-Ortega S, Garrido-Benavent I, Grube M, Olmo R, de los Ríos A (2016) Hidden diversity of marine borderline lichens and a new order of fungi: Collemopsidiales (Dothideomyceta). Fungal Divers 80:285–300
Persoon CH (1818) Traite sur les champignons comestibles, contenant l’undication des especes nuisible precede d’une introduction a l’historie des Champignons–Paris
Peter J, De Chiara M, Friedrich A, Yue JX, Pflieger D, Bergstrom A, Sigwalt A, Barre B, Freel K, Llored A, Cruaud C, Labadie K, Aury JM, Istace B, Lebrigand K, Barbry P, Engelen S, Lemainque A, Wincker P, Liti G, Schacherer J (2018) Genome evolution across 1,011 Saccharomyces cerevisiae isolates. Nature 556:339–344
Pitt JI (1979) The genus Penicillium and its teleomorphic states Eupenicillium and Talaromyces. Academic Press, London
Pizarro D, Divakar PD, Grewe F et al (2018) Phylogenomic analysis of 2556 single-copy protein-coding genes resolves most evolutionary relationships for the major clades in the most diverse group of lichen-forming fungi. Fungal Divers 92:31–41
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 55:595–609
Pore RS, Tsao GC, Plunkett OA (1965) A new species of Arthroderma established according to biological species concepts. Mycologia 57:969–973
Powell JR, Monaghan MT, Öpik M, Rillig MC (2011) Evolutionary criteria outperform operational approaches in producing ecologically relevant fungal species inventories. Mol Ecol 20:655–666
Prieto M, Baloch E, Tehler A, Wedin M (2013) Mazaedium evolution in the Ascomycota (Fungi) and the classification of mazaediate groups of formerly unclear relationship. Cladistics 29:296–308
Puillandre N, Lambert A, Brouillet S, Achaz G (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Mol Ecol 21:1864–1877
Qiu H, Cai G, Luo J, Bhattacharya D, Zhang N (2016) Extensive horizontal gene transfers between plant pathogenic fungi. BMC Biol 14:41
Qu J, Zhou Y, Yu J, Zhang J, Han Y, Zou X (2018) Estimated divergence times of Hirsutella (asexual morphs) in Ophiocordyceps provides insight into evolution of phialide structure. BMC Evol Biol 18:111
Quaedvlieg W, Kema GHJ, Groenewald JZ et al (2011) Zymoseptoria gen. nov.: a new genus to accommodate Septoria-like species occurring on graminicolous hosts. Persoonia 26:57–69
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67:901–904
Rannala B, Yang Z (2003) Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci. Genetics 164:1645–1656
Rehner SA, Minnis AM, Sung GH, Luangsa-ard JJ, Devotto L, Humber RA (2011) Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia 103:1055–1073
Ren R, Sun Y, Zhao Y, Geiser D, Ma H, Zhou X (2016) Phylogenetic resolution of deep eukaryotic and fungal relationships using highly conserved low-copy nuclear genes. Genome Biol Evol 8:2683–2701
Reynolds DR (1993) The fungal holomorph: An overview. In: Reynolds DR, Taylor JW (eds) The fungal holomorph: mitotic, meiotic and pleomorphic speciation in fungal systematics. CAB International, Wallingford, pp 15–25
Rodriguez RJ, White JF Jr, Arnold AE, Redman AR (2009) Fungal endophytes: diversity and functional roles. New Phytol 182:314–330
Rossman AY, Crous PW, Hyde KD, Hawksworth DL, Aptroot A, Bezerra JL, Bhat JD, Boehm E, Braun U, Boonmee S, Camporesi E (2015) Recommended names for pleomorphic genera in Dothideomycetes. IMA Fungus 6:507–523
Roy HE, Brown PMJ, Adriaens T, Berkvens N, Borges I, Clusella-Trullas S, Comont RF, De Clercq P, Eschen R, Estoup A, Evans EW, Facon B, Gardiner MM, Gil A, Grez AA, Guillemaud T, Haelewaters D, Herz A, Honek A, Howe AG, Hui C, Hutchison WD, Kenis M, Koch RL, Kulfan J, Lawson Handley L, Lombaert E, Loomans A, Losey J, Lukashuk AO, Maes D, Magro A, Murray KM, San Martin G, Martinkova Z, Minnaar I, Nedvěd O, Orlova-Bienkowskaja MJ, Rabitsch W, Ravn HP, Rondoni G, Rorke SL, Ryndevich SK, Saethre M-G, Sloggett JJ, Soares AO, Stals R, Tinsley MC, Vandereycken A, van Wielink P, Viglášová S, Zach P, Zaviezo T, Zhao Z (2016) The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol Invasions 18:997–1044
Ryan M, Bridge P, Smith D, Jeffries P (2002) Phenotypic degeneration occurs during sector formation in Metarhizium anisopliae. J Appl Microbiol 93:163–168
Ryberg M, Nilsson RH (2018) New light on names and naming of dark taxa. MycoKeys 30:31–39
Samarakoon MC, Hyde KD, Promputtha I, Hongsanan S et al (2016) Evolution of Xylariomycetidae (Ascomycota: Sordariomycetes). Mycosphere 7:1746–1761
Samarakoon MC, Thongbai B, Hyde KD et al (2020) Elucidation of the life cycle of the endophytic genus Muscodor and its transfer to Induratia in Induratiaceae fam. nov., based on a polyphasic taxonomic approach. Fungal Divers 101:177–210
Sandargo B, Chepkirui C, Cheng T, Chaverra-Munoz L, Thongbai B, Stadler M, Hüttel S (2019) Biological and chemical diversity go hand in hand: Basidomycota as source of new pharmaceuticals and agrochemicals. Biotechnol Adv 37(6):107344
Sandoval-Denis M, Crous PW (2018) Removing chaos from confusion: assigning names to common human and animal pathogens in Neocosmospora. Persoonia 41:109–129
Sandoval-Denis M, Lombard L, Crous PW (2019) Back to the roots: a reappraisal of 1238 Neocosmospora. Persoonia 43:90–185
Santos L, Alves A, Alves R (2017) Evaluating multi-locus phylogenies for species boundaries determination in the genus Diaporthe. PeerJ 5:3120
Schardl CL, Craven KD (2003) Interspecific hybridization in plant-associated fungi and oomycetes: a review. Mol Ecol 12:2861–2873
Schroers HJ, Samuels GJ, Zhang N, Short DP, Juba J, Geiser DM (2016) Epitypification of Fusisporium (Fusarium) solani and its assignment to a common phylogenetic species in the Fusarium solani species complex. Mycologia 108:806–819
Senanayake IC, Rathnayake AR, Marasinghe DS, Calabon MS, Gentekaki E, Lee HB, Hurdeal VG, Pem D, Dissanayake LS, Wijesinghe SN, Bundhun D, Nguyen TT, Goonasekara ID, Abeywickrama PD, Bhunjun CS, Jayawardena RS, Wanasinghe DN, Jeewon R, Bhat DJ, Xiang MM (2020) Morphological approaches in studying fungi: collection, examination, isolation, sporulation and preservation. Mycosphere 11:2678–2754
Seppey M, Manni M, Zdobnov EM (2019) BUSCO: assessing genome assembly and annotation completeness. Methods Mol Biol 1962:227–245
Sepúlveda VE, Márquez R, Turissini DA, Goldman WE, Matute DR (2017) Genome sequences reveal cryptic speciation in the human pathogen Histoplasma capsulatum. Mbio 8(6):e01339-e11317
Shear CL, Dodge BO (1927) Life histories and heterothallism of the red bread-mold fungi of the Monilia sitophila group. US Government Printing Office, pp 1019–1042
Shen XX, Opulente DA, Kominek J, Zhou X, Steenwyk JL, Buh KV, Haase MAB, Wisecaver JH, Wang M, Doering DT, Boudouris JT, Schneider RM, Langdon QK, Ohkuma M, Endoh R, Takashima M, Manabe RI, Cadez N, Libkind D, Rosa CA, DeVirgilio J, Hulfachor AB, Groenewald M, Kurtzman CP, Hittinger CT, Rokas A (2018) Tempo and mode of genome evolution in the budding yeast Subphylum. Cell 175:1533-1545.e20
Shen XX, Steenwyk JL, LaBella AL, Opulente DA, Zhou X, Kominek J, Li Y, Groenewald M, Hittinger CT, Rokas A (2020) Genome-scale phylogeny and contrasting modes of genome evolution in the fungal phylum Ascomycota. Sci Adv 6(45):eabd0079
Shivas RG, Cai L (2012) Cryptic fungal species unmasked. Microbiol Aust 33:36–37
Shoemaker RA, Babcock CE (1989) Phaeosphaeria. Can J Bot 67:1500–1599
Short DPG, O’Donnell K, Thrane U, Nielsen KF, Zhang N, Juba JH, Geiser DM (2013) Phylogenetic relationships among members of the Fusarium solani species complex in human infections and the descriptions of F. keratoplasticum sp. nov. and F. petroliphilum stat. nov. Fungal Genet Biol 53:59–70
Skrede I, Carlsen T, Schumacher T (2017) A synopsis of the saddle fungi (Helvella: Ascomycota) in Europe–species delimitation, taxonomy and typification. Persoonia 39:201–253
Sochorová Z, Döbbeler P, Sochor M, van Rooy J (2019) Octospora conidiophora (Pyronemataceae)—a new species from South Africa and the first report of anamorph in bryophilous Pezizales. MycoKeys 54:49–76
Springer MS, Gatesy J (2016) The gene tree delusion. Mol Phylogenet Evol 94:1–33
Steenkamp ET, Wingfield MJ, McTaggart AR, Wingfield BD (2018) Fungal species and their boundaries matter–definitions, mechanisms and practical implications. Fungal Biol Rev 32:104–116
Stewart JE, Timmer LW, Lawrence CB, Pryor BM, Peever TL (2014) Discord between morphological and phylogenetic species boundaries: incomplete lineage sorting and recombination results in fuzzy species boundaries in an asexual fungal pathogen. BMC Evol Biol 14:1–4
Strobel GA, Dirkse E, Sears J, Markworth C (2001) Volatile antimicrobials from Muscodor albus, a novel endophytic fungus. Microbiology 147:2943–2950
Stukenbrock EH (2016) The role of hybridization in the evolution and emergence of new fungal plant pathogens. Phytopathology 106:104–112
Suwannarach N, Kumla J, Bussaban B et al (2013) Molecular and morphological evidence support four new species in the genus Muscodor from northern Thailand. Ann Microbiol 63:1341–1351
Talbot PHB (1971) Fungi with a sterile mycelium or conidia: Eumycota subdivision Deuteromycotina. In: Principles of fungal taxonomy. Macmillan Education UK, London
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 31:21–32
Taylor DL, Hollingsworth TN, McFarland JW, Lennon NJ, Nusbaum C, Ruess RW (2014) A first comprehensive census of fungi in soil reveals both hyperdiversity and fine-scale niche partitioning. Ecol Monogr 84:3–20
Teixeira MD, Patané JS, Taylor ML, Gómez BL, Theodoro RC, de Hoog S, Engelthaler DM, Zancopé-Oliveira RM, Felipe MS, Barker BM (2016) Worldwide phylogenetic distributions and population dynamics of the genus Histoplasma. PLoS Negl Trop Dis 10(6):e0004732
Thines M, Crous PW, Aime MC, Aoki T, Cai L, Hyde KD, Miller AN, Zhang N, Stadler M (2018) Ten reasons why a sequence-based nomenclature is not useful for fungi anytime soon. IMA Fungus 9:177–183
Thiyagaraja V, Lücking R, Ertz D, Karunarathna SC, Wanasinghe DN, Lumyong S, Hyde KD (2021) The evolution of life modes in Stictidaceae, with three novel taxa. J Fungi 7:105
Thorp James H, Christopher Rogers D (eds) (2015) Thorp and Covich’s freshwater invertebrates. Elsevier, London
Udayanga D, Castlebury LA, Rossman AY, Chukeatirote E, Hyde KD (2014) Insights into the genus Diaporthe: phylogenetic species delimitation in the D. eres species complex. Fungal Divers 67:203–229
Vandepol N, Liber J, Desirò A, Na H, Kennedy M, Barry K, Grigoriev IV, Miller AN, O’Donnell K, Stajich JE, Bonito G (2020) Resolving the Mortierellaceae phylogeny through synthesis of multi-gene phylogenetics and phylogenomics. Fungal Divers 104:267–289
Wallen RM, Perlin MH (2018) An overview of the function and maintenance of sexual reproduction in dikaryotic fungi. Front Microbiol 9:503
Wanasinghe DN, Jones EG, Camporesi E, Boonmee S, Ariyawansa HA, Wijayawardene NN, Mortimer PE, Xu J, Yang JB, Hyde KD (2014) An exciting novel member of Lentitheciaceae in Italy from Clematis vitalba. Cryptogam Mycol 35:323–337
Wang Z, Li N, Li J, Dunlap JC, Trail F, Townsend JP (2016) The fast-evolving phy-2 gene modulates sexual development in response to light in the model fungus Neurospora crassa. Mbio 7:e02148
Wang M, Liu B, Ruan R, Zeng Y, Luo J, Li H (2020) Genomic sequencing of Phyllosticta citriasiana provides insight into its conservation and diversification with two closely related Phyllosticta species associated with Citrus. Front Microbial 10:2979
Wibberg D, Stadler M, Lambert C, Bunk B, Spröer C, Rückert C, Kalinowski J, Cox RJ, Kuhnert E (2020) High quality genome sequences of thirteen Hypoxylaceae (Ascomycota) strengthen the phylogenetic family backbone and enable the discovery of new taxa. Fungal Divers 106:7–28
Wikee S, Lombard L, Crous PW, Nakashima C, Motohashi K, Chukeatirote E, Alias SA, McKenzie EHC, Hyde KD (2013) Phyllosticta capitalensis, a widespread endophyte of plants. Fungal Divers 60:91–105
Winston JE (1999) Describing species: practical taxonomic procedure for biologists. Columbia University Press, New York
Wolfe KH (2015) Origin of the yeast whole-genome duplication. PLoS Biol 13(8):e1002221
Worapong J, Strobel G, Ford E et al (2001) Muscodor albus anam. gen. et sp nov., an endophyte from Cinnamomum zeylanicum. Mycotaxon 79:67–79
Worrall JJ (ed) (1999) Structure and dynamics of fungal populations, vol 25. Springer, Berlin
Wu B, Hussain M, Zhang W, Stadler M, Liu X, Xiang M (2019) Current insights into fungal species diversity and perspective on naming the environmental DNA sequences of fungi. Mycology 10:127–140
Xu J (2020) Fungal species concepts in the genomics era. Genome 63:459–468
Yang Z (2015) The BPP program for species tree estimation and species delimitation. Curr Zool 61:854–865
Yang J, Maharachchikumbura SSN, Liu JK, Hyde KD, Jones EG, Al-Sadi AM, Liu ZY (2017) Pseudostanjehughesia aquitropica gen. et sp. nov. and Sporidesmium sensu lato species from freshwater habitats. Mycol Prog 17:591–616
Yu G (2020) Using ggtree to visualize data on tree-like structures. Curr Protoc Bioinform 69:96
Zajc J, Zalar P, Gunde-Cimerman N (2017) Yeasts in hypersaline habitats. Yeasts in natural ecosystems: diversity 2017. Springer, Cham, pp 293–329
Zamora JC, Svensson M, Kirschner R, Olariaga I, Ryman S, Parra LA, Geml J, Rosling A, Adamčík S, Ahti T, Aime MC et al (2018) Considerations and consequences of allowing DNA sequence data as types of fungal taxa. IMA Fungus 9:167–175
Zhang N, O’Donnell K, Sutton DA, Nalim FA, Summerbell RC, Padhye AA, Geiser DM (2006) Members of the Fusarium solani species complex that cause infections in both humans and plants are common in the environment. J Clin Microbiol 44:2186–2190
Zhang J, Kapli P, Pavlidis P, Stamatakis A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29:2869–2876
Zhang H, Dong W, Hyde KD, Maharachchikumbura SSN, Hongsanan S, Bhat DJ, Al-Sadi AM, Zhang D (2017) Towards a natural classification of Annulatascaceae-like taxa: introducing Atractosporales ord. nov. and six new families. Fungal Divers 85:75–110
Zhang L, Fasoyin OE, Molnár I, Xu Y (2020) Secondary metabolites from hypocrealean entomopathogenic fungi: novel bioactive compounds. Nat Prod Rep 37(9):1181–1206
Zhao R-L, Zhou J-L, Chen J et al (2016) Towards standardizing taxonomic ranks using divergence times—a case study for reconstruction of the Agaricus taxonomic system. Fungal Divers 78:239–292
Acknowledgements
Danny Haelewaters is supported by the Research Foundation – Flanders (junior postdoctoral fellowship 1206620N). Dhanushka Wanasinghe thanks the CAS President’s International Fellowship Initiative (PIFI) for funding his postdoctoral research (number 2021FYB0005), the Postdoctoral Fund from Human Resources and Social Security Bureau of Yunnan Province.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest.
Additional information
Handling Editor: Chayanard Phukhamsakda.
Supplementary Information
Below is the link to the electronic supplementary material.
13225_2021_486_MOESM1_ESM.pdf
Supplementary file1 (PDF 721 kb) Supplementary Fig. 1. Color strips represent the species delimitation results from 5 methods, ABGD, bPTP, GMYC, mPTP, TCS based 5 single loci and combined sequences, respectively. Different symbols represent each complex. White means missing data. The number of defined species from different methods, number of reported species and percentages of recovered taxonomic species (Number of defined species/number of reported species * 100%) were displayed on the top.
Rights and permissions
About this article
Cite this article
Maharachchikumbura, S.S.N., Chen, Y., Ariyawansa, H.A. et al. Integrative approaches for species delimitation in Ascomycota. Fungal Diversity 109, 155–179 (2021). https://doi.org/10.1007/s13225-021-00486-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13225-021-00486-6