Abstract
Colletotrichum is one of the most important plant pathogenic genera that is responsible for numerous diseases which can have a profound impact on the agricultural sector. Species delineation is difficult due to a lack of distinctive phenotypic variation. Therefore, in this study three different genomic approaches based on phylogenetic, evolutionary and coalescent-based methods are applied to establish robust species boundaries. The reliability of five different DNA barcodes was also assessed to provide further insights into species delineation. The ITS region can resolve the placement of taxa up to the species complex level. The GAPDH and TUB2 markers are determined to be the most informative for most complexes. However, no single marker could discriminate between species in all complexes, therefore different molecular approaches based on multi-locus datasets are recommended. This is the first study to provide an estimated divergence time for all species complexes in Colletotrichum. The estimated divergence time for species complexes ranged between 4.8 to 32.2 MYA. Based on the high level of congruent results obtained from the different molecular approaches, a new species complex, the Colletotrichum agaves complex is introduced. This complex consists of five taxa which are characterised by the presence of straight or slightly curved conidia with obtuse apices. This study shows that coalescent approaches and multi-locus phylogeny are crucial to establish species boundaries in Colletotrichum. The taxonomic placement of three singleton taxa Colletotrichum axonopodi, C. cariniferi and C. parallelophorum is revised. We accept 248 species and provide recommendations regarding species boundaries in the graminicola–caudatum complex.
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Arrigoni R, Berumen ML, Chen CA, Terraneo TI, Baird AH, Payri C, Benzoni F (2016) Species delimitation in the reef coral genera Echinophyllia and Oxypora (Scleractinia, Lobophylliidae) with a description of two new species. Mol Phylogenet Evol 105:146–159
Barraclough TG, Birky CW, Burt A (2003) Diversification in sexual and asexual organisms. Evolution 57:2166–2172
Bouckaert R, Vaughan TG, Barido-Sottani J, Duchêne S, Fourment M, Gavryushkina A, Heled J, Jones G, Kühnert D, De Maio N, Matschiner M (2019) BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Comput Biol 15:e1006650
Bramble DM, Lieberman DE (2004) Endurance running and the evolution of Homo. Nature 432:345–352
Braun DR, Aldeias V, Archer W, Arrowsmith JR, Baraki N, Campisano CJ, Deino AL, DiMaggio EN, Dupont-Nivet G, Engda B, Feary DA (2019) Earliest known Oldowan artifacts at >2.58 Ma from Ledi-Geraru, Ethiopia, highlight early technological diversity. PNAS 116:11712–11717
Cai L, Hyde KD, Taylor PWJ, Weir B, Waller JM, Abang MM, Zang JC, Yang YL, Phouliyong S, Prihastuti ZY, Shivas RG, McKenzie EHC, Johnston PR (2009) A polyphasic approach for studying Colletotrichum. Fungal Divers 39:183–204
Cannon PF, Bridge PD, Monte E (2000) Linking the past, present, and future of Colletotrichum systematics. In: Dickman MB, Freeman S, Prusky D (eds) Colletotrichum: host specificity, pathology, and host pathogen interaction. APS Press, Minnesota
Cannon PF, Damm U, Johnston PR, Weir BS (2012) Colletotrichum current status and future directions. Stud Mycol 73:181–213
Cano J, Guarro J, Gené J (2004) Molecular and morphological identification of Colletotrichum species of clinical interest. J Clin Microbiol 42:2450–2454
Carstens BC, Knowles LL (2007) Estimating species phylogeny from gene-tree probabilities despite incomplete lineage sorting: an example from Melanoplus grasshoppers. Syst Biol 56:400–411
Cohen KM, Finney SC, Gibbard PL, Fan JX (2013) The ICS International Chronostratigraphic Chart. Episodes 36:199–204
Coiffard C, Gomez B, Daviero-Gomez V, Dilcher DL (2012) Rise to dominance of angiosperm pioneers in European Cretaceous environments. Proc Natl Acad Sci 109:20955–20959
Corda ACI (1831) Die Pilze Deutschlands. In: Strum J (ed) Deutschlands Flora in Abbildungen nach der Natur mit Beschreibungen. Sturm Nürnberg 3:33–64
Correa C, Vásquez D, Castro-Carrasco C, Zúñiga-Reinoso Á, Ortiz JC, Palma RE (2017) Species delimitation in frogs from South American temperate forests: the case of Eupsophus, a taxonomically complex genus with high phenotypic variation. PLoS ONE 12:e0181026
Crouch JA (2014) Colletotrichum caudatum s.l. is a species complex. IMA Fungus 5:17–30
Crouch JA, Clarke BB, White JF Jr, Hillman BI (2009) Systematic analysis of the falcate-spored graminicolous Colletotrichum and a description of six new species from warm-season grasses. Mycologia 101:717–732
Crous PW, Wingfield MJ, Guarro J, Cheewangkoon R, van der Bank M, Swart WJ, Stchigel AM, Cano-Lira JF, Roux J, Madrid H, Damm U, Wood AR, Shuttleworth LA, Hodges CS, Munster M, de Jesús Y-M, Zúñiga-Estrada L, Cruywagen EM, de Hoog GS, Silvera C, Najafzadeh J, Davison EM, Davison PJ, Barrett MD, Barrett RL, Manamgoda DS, Minnis AM, Kleczewski NM, Flory SL, Castlebury LA, Clay K, Hyde KD, Maússe-Sitoe SN, Chen S, Lechat C, Hairaud M, Lesage-Meessen L, Pawłowska J, Wilk M, Śliwińska-Wyrzychowska A, Mętrak M, Wrzosek M, Pavlic-Zupanc D, Maleme HM, Slippers B, Mac Cormack WP, Archuby DI, Grȕnwald NJ, Telleria MT, Dueñas M, Martin MP, Marincowitz S, de Beer ZW, Perez CA, Gené J, Marin-Felix Y, Groenewald JZ (2013) Fungal Planet description sheets: 154–213. Persoonia 31:188–296
Crous PW, Wingfield MJ, Guarro J, Hernández-Restrepo M, Sutton DA, Acharya K, Barber PA, Boekhout T, Dimitrov RA, Dueñas M, Dutta AK, Gené J, Gouliamova DE, Groenewald M, Lombard L, Morozova OV, Sarkar J, Smith MT, Stchigel AM, Wiederhold NP, Alexandrova AV, Antelmi I, Armengol J, Barnes I, Cano-Lira JF, Castañeda Ruiz RF, Contu M, Courtecuisse PR, da Silveira AL, Decock CA, de Goes A, Edathodu J, Ercole E, Firmino AC, Fourie A, Fournier J, Furtado EL, Geering AD, Gershenzon J, Giraldo A, Gramaje D, Hammerbacher A, He XL, Haryadi D, Khemmuk W, Kovalenko AE, Krawczynski R, Laich F, Lechat C, Lopes UP, Madrid H, Malysheva EF, Marin-Felix Y, Martin MP, Mostert L, Nigro F, Pereira OL, Picillo B, Pinho DB, Popov ES, Rodas Peláez CA, Rooney-Latham S, Sandoval-Denis M, Shivas RG, Silva V, Stoilova-Disheva MM, Telleria MT, Ullah C, Unsicker SB, van der Merwe NA, Vizzini A, Wagner HG, Wong PT, Wood AR, Groenewald JZ (2015) Fungal Planet description sheets: 320–370. Persoonia 34:167–266
Crous PW, Wingfield MJ, Richardson DM, Le Roux JJ, Strasberg D, Edwards J, Roets F, Hubka V, Taylor PW, Heykoop M, Martin MP, Moreno G, Sutton DA, Wiederhold NP, Barnes CW, Carlavilla JR, Gené J, Giraldo A, Guarnaccia V, Guarro J, Hernández-Restrepo M, Kolařik M, Manjón JL, Pascoe IG, Popov ES, Sandoval-Denis M, Woudenberg JH, Acharya K, Alexandrova AV, Alvarado P, Barbosa RN, Baseia IG, Blanchette RA, Boekhout T, Burgess TI, Cano-Lira JF, Čmoková A, Dimitrov RA, Dyakov MY, Dueñas M, Dutta AK, Esteve-Raventós F, Fedosova AG, Fournier J, Gamboa P, Gouliamova DE, Grebenc T, Groenewald M, Hanse B, Hardy GE, Held BW, Jurjević Ž, Kaewgrajang T, Latha KP, Lombard L, Luangsa-Ard JJ, Lysková P, Mallátová N, Manimohan P, Miller AN, Mirabolfathy M, Morozova OV, Obodai M, Oliveira NT, Ordóñez ME, Otto EC, Paloi S, Peterson SW, Phosri C, Roux J, Salazar WA, Sánchez A, Sarria GA, Shin HD, Silva BD, Silva GA, Smith MT, Souza-Motta CM, Stchigel AM, Stoilova-Disheva MM, Sulzbacher MA, Telleria MT, Toapanta C, Traba JM, Valenzuela-Lopez N, Watling R, Groenewald JZ (2016) Fungal Planet description sheets: 400–468. Persoonia 36:316–458
da Silva LL, Moreno HL, Correia HL, Santana MF, de Queiroz MV (2020) Colletotrichum: species complexes, lifestyle, and peculiarities of some sources of genetic variability. Appl Microbiol Biotechnol 104:1891–1904
Damm U, Cannon PF, Woudenberg JH, Johnston PR, Weir BS, Tan YP, Shivas RG, Crous PW (2012a) The Colletotrichum boninense species complex. Stud Mycol 73:1–36
Damm U, Cannon PF, Woudenberg JHC, Crous PW (2012b) The Colletotrichum acutatum species complex. Stud Mycol 73:37–113
Damm U, O’Connell RJ, Groenewald JZ, Crous PW (2014) The Colletotrichum destructivum species complex - hemibiotrophic pathogens of forage and field crops. Stud Mycol 79:49–84
Damm U, Sato T, Alizadeh A, Groenewald JZ, Crous PW (2019) The Colletotrichum dracaenophilum, C. magnum and C. orchidearum species complexes. Stud Mycol 92:1–46
Damm U, Woudenberg JHC, Cannon PF, Crous PW (2009) Colletotrichum species with curved conidia from herbaceous hosts. Fungal Divers 39:45–87
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772
Domínguez-Rodrigo M (2009) Are all Oldowan sites palimpsests? If so, what can they tell us about Hominid carnivory? In: Hovers E, Braun DR (eds) Interdisciplinary approaches to the Oldowan. Springer, Amsterdam
Doyle VP, Oudemans PV, Rehner SA, Litt A (2013) Habitat and host indicate lineage identity in Colletotrichum gloeosporioides sl from wild and agricultural landscapes in North America. PLoS ONE 8:e62394
Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973
Ezard T, Fujisawa T, Barraclough TG (2015) SPLITS: species’ limits by threshold statistics. R package version 1:r45
Farr DF, Aime MC, Rossman AY, Palm ME (2006) Species of Colletotrichum on agavaceae. Mycol Res 110:1395–1408
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
Fujita MK, Leaché AD, Burbrink FT, McGuire JA, Moritz C (2012) Coalescent-based species delimitation in an integrative taxonomy. Trends Ecol Evol 27:480–488
Hacquard S, Kracher B, Hiruma K, Münch PC, Garrido-Oter R, Thon MR, Weimann A, Damm U, Dallery JF, Hainaut M, Henrissat B (2016) Survival trade-offs in plant roots during colonization by closely related beneficial and pathogenic fungi. Nat Commun 7:1–3
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
Hyde KD, Cai L, McKenzie EHC, Yang YL, Zhang JZ, Prihastuti H (2009) Colletotrichum: a catalogue of confusion. Fungal Divers 39:1–17
Hyde KD, Udayanga D, Manamgoda DS, Tedersoo L, Larsson E, Abarenkov K, Bertrand YJK, Oxelman B, Hartmann M, Kauserud H, Ryberg M, Kristiansson E, Nilsson RH (2013) Incorporating molecular data in fungal systematics: a guide for aspiring researchers. Curr Res Environ Appl Mycol 3:1–32
Hyde KD, Nilsson RH, Alias SA, Ariyawansa HA, Blair JE, Cai L, de Cock AWAM, Dissanayake AJ, Glockling SL, Goonasekara ID, Gorczak M, Hahn M, Jayawardena RS, van Kan JAL, Laurence MH, Lévesque CA, Li XH, Liu JK, Maharachchikumbura SSN, Manamgoda DS, Martin FN, McKenzie EHC, McTaggart AR, Mortimer PE, Nair PVR, Pawłowska J, Rintoul TL, Shivas RG, Spies CFJ, Summerell BA, Taylor PWJ, Terhem RB, Udayanga D, Vaghefi N, Walther G, Wilk M, WrzosekM XuJC, Yan JY, Zhou N (2014) One stop shop: backbones trees for important pytopathogenic genera: I. Fungal Divers 67:21–125
Hyde KD, Tennakoon DS, Jeewon R, Bhat DJ, Maharachchikumbura SSN, Rossi W, Leonardi M, Lee HB, Mun HY, Houbraken J, Nguyen TTT, Jeon SJ, Frisvad JC, Dhanushka N, Wanasinghe DN, Luücking R, Aptroot A, Cáceres MES, Karunarathna SC, Hongsanan S, Phookamsak R, de Silva NI, Thambugala KM, Jayawardena RS, Senanayake IC, Boonmee S, Chen J, Luo ZL, Phukhamsakda C, Pereira OL, Abreu VP, Rosado AWC, Bart B, Randrianjohany E, Hofstetter V, Gibertoni TB, da Silva Soares AM, Plautz HL Jr, Sotão HMP, Xavier WKS, Bezerra JDP, de Oliveira TGL, de Souza-Motta CM, Magalhães OMC, Bundhun D, Harishchandra D, Manawasinghe IS, Dong W, Zhang SN, Bao DF, Samarakoon MC, Pem D, Karunarathna A, Lin CG, Yang J, Perera RH, Kumar V, Huang SK, Dayarathne MC, Ekanayaka AH, Jayasiri SC, Xiao YP, Konta S, Niskanen T, Liimatainen K, Dai YC, Ji XH, Tian XM, Mešić A, Singh SK, Phutthacharoen K, Cai L, Sorvongxay T, Thiyagaraja V, Norphanphoun C, Chaiwan N, Lu YZ, Jiang HB, Zhang JF, Abeywickrama PD, Aluthmuhandiram JVS, Brahmanage RS, Zeng M, Chethana T, Wei DP, Réblová M, Fournier J, Nekvindová J et al (2019) Fungal diversity notes 1036–1150: taxonomic and phylogenetic contributions on genera and species of fungal taxa. Fungal Divers 96:1–242
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 (2020a) The numbers of fungi: is the descriptive curve flattening? Fungal Divers 103:219–271
Hyde KD, Norphanphoun C, Maharachchikumbura SSN, Bao DF, Bhat DJ, Boonmee S, Bundhun D, Calabon MS, Chaiwan N, Chen YJ, Chethana KWT, Dai DQ, Dayarathne MC, Devadatha B, Dissanayake AJ, Dissanayake LS, Doilom M, Dong W, Fan XL, Goonasekara ID, Hongsanan S, Huang SK, Jayawardena RS, Jeewon R, Jones EBG, Karunarathna A, Konta S, Kumar V, Lin CG, Liu JK, Liu N, Lu YZ, Luangsa-ard J, Lumyong S, Luo ZL, Marasinghe DS, McKenzie EHC, Niego AGT, Niranjan M, Perera RH, Phukhamsakda C, Rathnayaka AR, Samarakoon MC, Samarakoon SMBC, Sarma VV, Senanayake IC, Shang QJ, Stadler M, Tibpromma S, Wanasinghe DN, Wei DP, Wijayawardene NN, Xiao YP, Xiang MM, Yang J, Zeng XY, Zhang SN (2020b) Refined families of Sordariomycetes. Mycosphere 11:305–1059
Index Fungorum (2020) http://www.indexfungorum.org/names/names.asp
Jayawardena RS, Hyde KD, Damm U, Cai L, Liu M, Li XH, Zhang W, Zhao WS, Yan JY (2016a) Notes on currently accepted species of Colletotrichum. Mycosphere 7:1192–1260
Jayawardena RS, Hyde KD, Jeewon R, Liu XH, Liu M, Yan JY (2016b) Why it is important to correctly name Colletotrichum species? Mycosphere 7:1076–1092
Jayawardena RS, Hyde KD, Chen YJ, Papp V, Palla B, Papp D, Bhunjun CS, Hurdeal VG, Senwanna C, Manawasinghe IS, Harischandra DL, Gautam AK, Avasthi S, Chuankid B, Goonasekara ID, Hongsanan S, Zeng XY, Liyanage KK, Liu N, Karunarathna A, Hapuarachchi KK, Luangharn T, Raspé O, Brahmanage R, Doilom M, Lee HB, Mei L, Jeewon R, Huanraluek N, Chaiwan N, Stadler M, Wang Y (2020) One stop shop IV: taxonomic update with molecular phylogeny for important phytopathogenic genera: 76–100 (2020). Fungal Divers 103:87–218
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
Kar RK, Sharma N, Verma UK (2004) Plant pathogen Protocolletotrichum from a Deccan intertrappean bed (Maastrichtian), India. Cretac Res 25:945–950
Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166
Larsson A (2014) AliView: a fast and lightweight alignment viewer and editor for large datasets. Bioinformatics 30:3276–3278
Lelwala RV, Korhonen PK, Young ND, Scott JB, Ades PK, Gasser RB, Taylor PW (2019) Comparative genome analysis indicates high evolutionary potential of pathogenicity genes in Colletotrichum tanaceti. PLoS ONE 14:e0212248
Lewis JE, Harmand S (2016) An earlier origin for stone tool making: implications for cognitive evolution and the transition to Homo. Philos Trans R Soc Lond B Biol Sci 371:20150233
Liang X, Wang B, Dong Q, Li L, Rollins JA, Zhang R, Sun G (2018) Pathogenic adaptations of Colletotrichum fungi revealed by genome wide gene family evolutionary analyses. PLoS ONE 13:e0196303
Liu F, Weir BS, Damm U, Crous PW, Wang Y, Liu B, Wang M, Zhang M, Cai L (2015) Unravelling Colletotrichum species associated with Camellia: employing ApMat and GS loci to resolve species in the C. gloeosporioides complex. Persoonia 35:63–86
Liu F, Wang M, Damm U, Crous PW, Cai L (2016) Species boundaries in plant pathogenic fungi: a Colletotrichum case study. BMC Evol Biol 16:81
Lücking R, Aime MC, Robbertse B, Miller AN, Ariyawansa HA, Aoki T, Cardinali G, Crous PW, Druzhinina IS, Geiser DM, Hawksworth DL, Hyde KD, Irinyi L, Jeewon R, Johnston PR, Kirk PM, Malosso E, May TW, Meyer W, Öpik M, Robert V, Stadler M, Thines M, Vu D, Yurkov AM, Zhang N, Schoch CL (2020) Unambiguous identification of fungi: where do we stand and how accurate and precise is fungal DNA barcoding? IMA Fungus 11:1–32
Ma X, Nontachaiyapoom S, Jayawardena RS, Hyde KD, Gentekaki E, Zhou S, Qian Y, Wen T, Kang J (2018) Endophytic Colletotrichum species from Dendrobium spp. in China and Northern Thailand. MycoKeys 43:23–57
Maharachchikumbura SSN, Hyde KD, Jones EBG, McKenzie EHC, Bhat JD, Dayarathne MC, Huang SK, Norphanphoun C, Senanayake IC, Perera RH, Shang QJ, Xiao Y, D’souza MJ, Hongsanan S, Jayawardena RS, Daranagama DA, Konta S, Goonasekara ID, Zhuang WY, Jeewon R, Phillips AJL, Abdel-Wahab MA, Al-Sadi AM, Bahkali AH, Boonmee S, Boonyuen N, Cheewangkoon R, Dissanayake AJ, Kang J, Li QR, Liu JK, Liu XZ, Liu ZY, Luangsa-ard JJ, Pang KL, Phookamsak R, Promputtha I, Suetrong S, Stadler M, Wen T, Wijayawardene NN (2016) Families of Sordariomycetes. Fungal Divers 79:1–317
Manamgoda DS, Udayanga D, Cai L, Chukeatirote E, Hyde KD (2013) Endophytic Colletotrichum from tropical grasses with a new species C. endophytica. Fungal Divers 61:107–115
Marin-Felix Y, Groenewald JZ, Cai L, Chen Q, Marincowitz S, Barnes I, Bensch K, Braun U, Camporesi E, Damm U, de Beer ZW, Dissanayake A, Edwards J, Giraldo A, Hernández-Restrepo M, Hyde KD, Jayawardena RS, Lombard L, Luangsa-ard J, McTaggart AR, Rossman AY, Sandoval-Denis M, Shen M, Shivas RG, Tan YP, van der Linde EJ, Wingfield MJ, Wood AR, Zhang JQ, Zhang Y, Crous PW (2017) Genera of phytopathogenic fungi: GOPHY 1. Stud Mycol 86:99–216
Marki PZ, Fjeldså J, Irestedt M, Jønsson KA (2018) Molecular phylogenetics and species limits in a cryptically coloured radiation of Australo-Papuan passerine birds (Pachycephalidae: Colluricincla). Mol Phylogenet Evol 124:100–105
McElwain JC, Punyasena SW (2007) Mass extinction events and the plant fossil record. Trends Ecol Evol 22:548–557
Miller MA, Pfeiffer W, Schwartz T (2017) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In 2010 gateway computing environments workshop (GCE):1–8
Miralles A, Vences M (2013) New metrics for comparison of taxonomies reveal striking discrepancies among species delimitation methods in Madascincus lizards. PLoS ONE 8:e68242
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
Moraga J, Gomes W, Pinedo C, Cantoral JM, Hanso JR, Carbún M, Garriso C, Durán-Patrón R, Collado IG (2019) The current status on secondary metabolites produced by plant pathogenic Colletotrichum species. Phytochem Rev 18:215–239
Nakamura M, Ohzono M, Iwai H, Arai K (2006) Anthracnose of Sansevieria trifasciata caused by Colletotrichum sansevieriae sp. nov. J Gen Plant Pathol 72:253–256
Nieto-Montes de Oca A, Barley AJ, Meza-Lázaro RN, GarcíaVázquez UO, Zamora-Abrego JG, Thomson RC, Leaché AD (2017) Phylogenomics and species delimitation in the knob-scaled lizards of the genus Xenosaurus (Squamata: Xenosauridae) using ddRADseq data reveal a substantial underestimation of diversity. Mol Phylogenet Evol 106:241–253
Nilsson RH, Hyde KD, Pawłowska J, Ryberg M, Tedersoo L, Aas AB, Alias SA, Alves A, Anderson CL, Antonelli A, Arnold AE, Bahnmann B, Bahram M, Bengtsson-Palme J, Berlin A, Branco S, Chomnunti P, Dissanayake A, Drenkhan R, Friberg H, Frøslev TG, Halwachs B, Hartmann M, Henricot B, Jayawardena R, Jumpponen A, Kauserud H, Koskela S, Kulik T, Liimatainen K, Lindahl BD, Lindner D, Liu JK, Maharachchikumbura S, Manamgoda D, Martinsson S, Neves MA, Niskanen T, Nylinder S, Pereira OL, Pinho DB, Porter TM, Queloz V, Riit T, Sánchez-García M, de Sousa F, Stefańczyk E, Tadych M, Takamatsu S, Tian Q, Udayanga D, Unterseher M, Wang Z, Wikee S, Yan J, Larsson E, Larsson KH, Kõljalg U, Abarenkov K (2014) Improving ITS sequence data for identification of plant pathogenic fungi. Fungal Divers 67:11–19
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
Pentinsaari M, Vos R, Mutanen M (2016) Algorithmic single-locus species delimitation: effects of sampling effort, variation and nonmonophyly in four methods and 1870 species of beetles. Mol Ecol Resour 17:393–404
Phillips AJ, Hyde KD, Alves A, Liu JK (2019) Families in Botryosphaeriales: a phylogenetic, morphological and evolutionary perspective. Fungal Divers 94:1–22
Phoulivong S, Cai L, Chen H, McKenzie EHC, Abdelsalam K, Chukeatirote E, Hyde KD (2010) Colletotrichum gloeosporioides is not a common pathogen on tropical fruits. Fungal Divers 44:33–43
Plummer TW (2004) Flaked stones and old bones: biological and cultural evolution at the dawn of technology. Am J Phys Anthropol 125:118–164
Potts R (1991) Why the oldowan? Plio-Pleistocene toolmaking and the transport of resources. J Anthropol Res 47:153–176
Prihastuti H, Cai L, Chen H, McKenzie EHC, Hyde KD (2009b) Characterization of Colletotrichum species associated with coffee berries in Chiang Mai, Thailand. Fungal Divers 39:89–109
R Core Team (2017) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna
Rambaut A (2014) FigTree v1.4. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh http://tree.bio.ed.ac.uk/software/figtree/
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in Bayesian phylogenetics using Tracer 17. Syst Biol 67:901
Rashmi M, Kushveer JS, Sarma VV (2019) A worldwide list of endophytic fungi with notes on ecology and diversity. Mycosphere 10:798–1079
Renner MA, Heslewood MM, Patzak SD, Schäfer-Verwimp A, Heinrichs J (2017) By how much do we underestimate species diversity of liverworts using morphological evidence? An example from Australasian Plagiochila (Plagiochilaceae: Jungermanniopsida). Mol Phylogenet Evol 107:576–593
Ring SJ, Bocherens H, Wings O, Rabi M (2020) Divergent mammalian body size in a stable Eocene greenhouse climate. Sci Rep 10:3987
Rojas EI, Rehner SA, Samuels GJ, Van Bael SA, Herre EA, Cannon P, Chen R, Pang J, Wang R, Zhang Y, Peng YQ, Sha T (2010) Colletotrichum gloeosporioides s.l. associated with Theobroma cacao and other plants in Panama: multilocus phylogenies distinguish pathogen and endophyte clades. Mycologia 102:1318–1338
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Samarakoon MC, Hyde KD, Hongsanan S, McKenzie EH, Ariyawansa HA, Promputtha I, Zeng XY, Tian Q, Liu JKJ (2019) Divergence time calibrations for ancient lineages of Ascomycota classification based on a modern review of estimations. Fungal Divers 96:285–346
Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. PNAS 109:6241–6246
Servis JA, Reid BN, Timmers MA, Stergioula V, Naro-Maciel E (2020) Characterizing coral reef biodiversity: genetic species delimitation in brachyuran crabs of Palmyra Atoll, Central Pacific. Mitochondrial DNA Part A 25:1–2
Sharma G, Pinnaka AK, Shenoy BD (2015) Resolving the Colletotrichum siamense species complex using ApMat marker. Fungal Divers 71:247–264
Shivaprakash MR, Appannanavar SB, Dhaliwal M, Gupta A, Gupta S, Gupta A, Chakrabarti A (2011) Colletotrichum truncatum: an unusual pathogen causing mycotic keratitis and endophthalmitis. J Clin Microbiol 49:2894–2898
Snir A, Nadel D, Groman-Yaroslavski I, Melamed Y, Sternberg M, Bar-Yosef O, Weiss E (2015) The origin of cultivation and proto-weeds, long before Neolithic farming. PLoS ONE 10:e0131422
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313
Swofford DL (2002) PAUP: phylogenetic analysis using parsimony, version 4.0 b10. Sinauer Associates, Sunderland
Tao G, Liu ZY, Liu F, Gao YH, Cai L (2013) Endophytic Colletotrichumspecies from Bletilla ochracea (Orchidaceae), with description of seven new species. Fungal Divers 61:139–164
Udayanga D, Manamgoda DS, Liu X-Z, Chukeatirote E, Hyde KD (2013) What are the common anthracnose pathogens of tropical fruits? Fungal Divers 61:165–179
Vajda V, McLoughlin S (2004) Fungal proliferation at the Cretaceous-Tertiary boundary. Science 303:1489
Weir B, Johnston PR, Damm U (2012) The Colletotrichum gloeosporioides species complex. Stud Mycol 73:115–180
Wilf P, Johnson KR (2004) Land plant extinction at the end of the Cretaceous: a quantitative analysis of the North Dakota megafloral record. Paleobiology 30:347–368
Xing Y, Onstein RE, Carter RJ, Stadler T, Peter Linder H (2014) Fossils and a large molecular phylogeny show that the evolution of species richness, generic diversity, and turnover rates are disconnected. Evolution 68:2821–2832
Zhang J, Kapli P, Pavlidis P, Stamatakis A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29:2869–2876
Acknowledgements
We would like to thank the Thailand Research Fund, grant RDG6130001 entitled “Impact of climate change on fungal diversity and biogeography in the Greater Mekong Subregion”. Kevin D Hyde thanks Chiang Mai University for the award of a Visiting Professor. Dr Rajesh Jeewon would like to acknowledge the support from University of Mauritius and the Mauritius Research and Innovative Council (MRC/RUN/1705). RS Jayawardena thanks the National Research Council of Thailand, grant for new researcher NRCT5-TRG630010-01, entitled “Biodiversity, taxonomy, phylogeny and evolution of Colletotrichum in northern Thailand”.
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Bhunjun, C.S., Phukhamsakda, C., Jayawardena, R.S. et al. Investigating species boundaries in Colletotrichum. Fungal Diversity 107, 107–127 (2021). https://doi.org/10.1007/s13225-021-00471-z
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DOI: https://doi.org/10.1007/s13225-021-00471-z