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Published: 2024-07-18
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Ophiocordyceps taiwanensis sp. nov. (Ophiocordycipitaceae, Hypocreales) on Odontotermes formosanus (Termitidae, Blattodea)

Department of Entomology and Plant Pathology, Faculty of Agriculture, Chiang Mai University, Chiang Mai 50200, Thailand
Kaohsiung Nature Observation Society, Kaohsiung City, Taiwan
Department of Entomology and Plant Pathology, Faculty of Agriculture, Chiang Mai University, Chiang Mai 50200, Thailand
Department of Plant Pathology, National Chung Hsing University, Taichung, 402202, Taiwan
Department of Entomology, National Chung Hsing University, Taichung, 402202, Taiwan, i-Center for Advanced Science and Technology, National Chung Hsing University, Taichung, 402202, Taiwan
Department of Entomology and Plant Pathology, Faculty of Agriculture, Chiang Mai University, Chiang Mai 50200, Thailand, Office of Research Administration, Chiang Mai University, Chiang Mai 50200, Thailand
Fungi 1 new taxon Cordycepioideus Entomophagous Phylogeny Taxonomy

Abstract

Ophiocordyceps species are found worldwide, with their greatest diversity occurring in tropical and subtropical regions, particularly in Southeast Asia. In June 2020, during a study conducted in Taiwan, stromata associated with dead termite alates (or winged termites) (Odontotermes formosanus) were collected and characterized. This study identified a unique sexual morph, Ophiocordyceps taiwanensis sp. nov., distinguished by its asci and ascospore morphology compared to the majority of Ophiocordyceps species. Our new collection exhibits similarities to O. bispora (≡ Cordycepioideus bisporus), particularly in having asci with two ascospores. However, it differs in the shape of its perithecia, which are subglobose to ovoid, and in possessing smaller, aseptate ascospores. Phylogenetic analysis using various gene combinations in both preliminary and final LSU-ITS-SSU-TEF1-RPB2 sequence alignments revealed that our new isolates form a clade closely related to O. bispora KVL 606, supported by 88% MP/100% ML/1.00 PP BI statistical support. Based on its distinct morphology and phylogenetic placement, we propose O. taiwanensis as a new species, representing the first recorded instance of an Ophiocordyceps species associated with termites in Taiwan.

References

  1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. (1990) Basic local alignment search tool. Journal of Molecular Biology 215: 403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
  2. Araújo, J.P.M., Evans, H.C., Fernandes, I.O., Ishler, M.J. & Hughes, D.P. (2020) Zombie-ant fungi cross continents: II. Myrmecophilous hymenostilboid species and a novel zombie lineage. Mycologia 112: 1138–1170. https://doi.org/10.1080/00275514.2020.1822093
  3. Araújo, J.P.M., Evans, H.C., Geiser, D.M., Mackay, W.P. & Hughes, D.P. (2015) Unravelling the diversity behind the Ophiocordyceps unilateralis (Ophiocordycipitaceae) complex: Three new species of zombie-ant fungi from the Brazilian Amazon. Phytotaxa 220 (3): 224. https://doi.org/10.11646/phytotaxa.220.3.2
  4. Araújo, J.P.M. & Hughes, D.P. (2016) Diversity of Entomopathogenic Fungi. Advances in Genetics, Elsevier, pp. 1–39. https://doi.org/10.1016/bs.adgen.2016.01.001
  5. Araújo, J.P.M., Moriguchi, G.M., Uchiyama, S., Kinjo, N. & Matsuura, Y. (2021) Ophiocordyceps salganeicola, a parasite of social cockroaches in Japan and insights into the evolution of other closely-related Blattodea-associated lineages. IMA Fungus 12: 3. https://doi.org/10.1186/s43008-020-00053-9
  6. Ashrafi, S., Stadler, M., Dababat, A.A., Richert-Pöggeler, K.R., Finckh, M.R. & Maier, W. (2017) Monocillium gamsii sp. nov. and Monocillium bulbillosum: two nematode-associated fungi parasitising the eggs of Heterodera filipjevi. MycoKeys 27: 21–38. https://doi.org/10.3897/mycokeys.27.21254
  7. Ban, S., Sakane, T. & Nakagiri, A. (2015) Three new species of Ophiocordyceps and overview of anamorph types in the genus and the family Ophiocordyceptaceae. Mycological Progress 14: 1017. https://doi.org/10.1007/s11557-014-1017-8
  8. Blackwell, M. & Gilbertson, R.L. (1981) Cordycepioideus Octosporus, A termite suspected pathogen from Jalisco, Mexico. Mycologia 73: 358–362. https://doi.org/10.1080/00275514.1981.12021355
  9. Blackwell, M. & Gilbertson, R.L. (1984) New information on Cordycepioideus bisporus and Cordycepioideus octosporus. Mycologia 76: 763–765. https://doi.org/10.1080/00275514.1984.12023912
  10. Chaverri, P., Salgado, C., Hirooka, Y., Rossman, A.Y. & Samuels, G.J. (2011) Delimitation of Neonectria and Cylindrocarpon (Nectriaceae, Hypocreales, Ascomycota) and related genera with cylindrocarpon-like anamorphs. Studies in Mycology 68: 57–78. https://doi.org/10.3114/sim.2011.68.03
  11. Chethana, K.W.T., Manawasinghe, I.S., Hurdeal, V.G., Bhunjun, C.S., Appadoo, M.A., Gentekaki, E., Raspé, O., Promputtha, I., Hyde, K.D. (2021) What are fungal species and how to delineate them? Fungal Diversity 109: 1–25. https://doi.org/10.1007/s13225-021-00483-9
  12. Crous, P.W., Wingfield, M.J., Guarro, J., Cheewangkoon, R., van der Bank, M., Swart, W.J., Stchigel, A.M., Cano-Lira, J.F., Roux, J., Madrid, H., Damm, U., Wood, A.R., Shuttleworth, L.A., Hodges, C.S., Munster, M., de Jesús Yáñez-Morales, M., Zúñiga-Estrada, L., Cruywagen, E.M., De Hoog, G.S., Silvera, C., Najafzadeh, J., Davison, E.M., Davison, P.J.N., Barrett, M.D., Barrett, R.L., Manamgoda, D.S., Minnis, A.M., Kleczewski, N.M., Flory, S.L., Castlebury, L.A., Clay, K., Hyde, K.D., Maússe-Sitoe, S.N.D., Chen, S., Lechat, C., Hairaud, M., Lesage-Meessen, L., Pawłowska, J., Wilk, M., Śliwińska-Wyrzychowska, A., Mętrak, M., Wrzosek, M., Pavlic-Zupanc, D., Maleme, H.M., Slippers, B., Mac Cormack, W.P., Archuby, D.I., Grünwald, N.J., Tellería, M.T., Dueñas, M., Martín, M.P., Marincowitz, S., de Beer, Z.W., Perez, C.A., Gené, J., Marin-Felix, Y. & Groenewald, J.Z. (2013) Fungal Planet Description Sheets: 154–213. Persoonia—Molecular Phylogeny and Evolution of Fungi 31: 188–296. https://doi.org/10.3767/003158513X675925
  13. Currie, C.R., Wong, B., Stuart, A.E., Schultz, T.R., Rehner, S.A., Mueller, U.G., Sung, G.-H., Spatafora, J.W. & Straus, N.A. (2003) Ancient tripartite coevolution in the attine ant-microbe symbiosis. Science 299: 386–388. https://doi.org/10.1126/science.1078155
  14. Fan, Q., Wang, Y.-B., Zhang, G.-D., Tang, D.-X. & Yu, H. (2021) Multigene phylogeny and morphology of Ophiocordyceps alboperitheciata sp. nov., a new entomopathogenic fungus attacking lepidopteran larva from Yunnan, China. Mycobiology 49: 133–141. https://doi.org/10.1080/12298093.2021.1903130
  15. Fan, Q., Yang, T., Li, H., Wang, X.-M., Liao, H.-F., Shen, P.-H., Yang, Z.-L., Zeng, W.-B. & Wang, Y.-B. (2024) Molecular phylogeny and morphology reveal two new entomopathogenic species of Ophiocordyceps (Ophiocordycipitaceae, Hypocreales) parasitic on termites from China. MycoKeys 103: 1–24. https://doi.org/10.3897/mycokeys.103.116153
  16. Glenn, A.E., Bacon, C.W., Price, R. & Hanlin, R.T. (1996) Molecular phylogeny of Acremonium and its taxonomic implications. Mycologia 88: 369–383. https://doi.org/10.1080/00275514.1996.12026664
  17. Grum-Grzhimaylo, A.A., Debets, A.J.M., Van Diepeningen, A.D., Georgieva, M.L. & Bilanenko, E.N. (2013) Sodiomyces alkalinus, a new holomorphic alkaliphilic ascomycete within the Plectosphaerellaceae. Persoonia—Molecular Phylogeny and Evolution of Fungi 31: 147–158. https://doi.org/10.3767/003158513X673080
  18. Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95–98.
  19. Hirooka, Y., Kobayashi, T., Ono, T., Rossman, A.Y. & Chaverri, P. (2010) Verrucostoma, a new genus in the Bionectriaceae from the Bonin Islands, Japan. Mycologia 102: 418–429. https://doi.org/10.3852/09-137
  20. Hou, L.W., Giraldo, A., Groenewald, J.Z., Rämä, T., Summerbell, R.C., Huang, G.Z., Cai, L. & Crous, P.W. (2023) Redisposition of acremonium-like fungi in Hypocreales. Studies in Mycology 105: 23–203. https://doi.org/10.3114/sim.2023.105.02
  21. Hyde, K.D., Norphanphoun, C., Maharachchikumbura, S.S.N., Bhat, D.J., Jones, E.B.G., Bundhun, D., Chen, Y.J., Bao, D.F., Boonmee, S., Calabon, M.S., Chaiwan, N., Chethana, K.W.T., Dai, D.Q., Dayarathne, M.C., Devadatha, B., Dissanayake, A.J., Dissanayake, L.S., Doilom, M., Dong, W., Fan, X.L., Goonasekara, I.D., Hongsanan, S., Huang, S.K., Jayawardena, R.S., Jeewon, R., Karunarathna, A., Konta, S., Kumar, V., Lin, C.G., Liu, J.K., Liu, N.G., Luangsa-ard, J., Lumyong, S., Luo, Z.L., Marasinghe, D.S., McKenzie, E.H.C., Niego, A.G.T., Niranjan, M., Perera, R.H., Phukhamsakda, C., Rathnayaka, A.R., Samarakoon, M.C., Samarakoon, S.M.B.C., Sarma, V.V., Senanayake, I.C., Shang, Q.J., Stadler, M., Tibpromma, S., Wanasinghe, D.N., Wei, D.P., Wijayawardene, N.N., Xiao, Y.P., Yang, J., Zeng, X.Y., Zhang, S.N. & Xiang, M.M. (2020) Refined families of Sordariomycetes. Mycosphere 11: 305–1059. https://doi.org/10.5943/mycosphere/11/1/7
  22. Hyde, K.D., Tennakoon, D.S., Jeewon, R., Bhat, D.J., Maharachchikumbura, S.S.N., Rossi, W., Leonardi, M., Lee, H.B., Mun, H.Y., Houbraken, J., Nguyen, T.T.T., Jeon, S.J., Frisvad, J.C., Wanasinghe, D.N., Lücking, R., Aptroot, A., Cáceres, M.E.S., Karunarathna, S.C., Hongsanan, S., Phookamsak, R., de Silva, N.I., Thambugala, K.M., Jayawardena, R.S., Senanayake, I.C., Boonmee, S., Chen, J., Luo, Z.-L., Phukhamsakda, C., Pereira, O.L., Abreu, V.P., Rosado, A.W.C., Bart, B., Randrianjohany, E., Hofstetter, V., Gibertoni, T.B., Soares, A.M. da S., Plautz, H.L., Sotão, H.M.P., Xavier, W.K.S., Bezerra, J.D.P., de Oliveira, T.G.L., de Souza-Motta, C.M., Magalhães, O.M.C., Bundhun, D., Harishchandra, D., Manawasinghe, I.S., Dong, W., Zhang, S.-N., Bao, D.-F., Samarakoon, M.C., Pem, D., Karunarathna, A., Lin, C.-G., Yang, J., Perera, R.H., Kumar, V., Huang, S.-K., Dayarathne, M.C., Ekanayaka, A.H., Jayasiri, S.C., Xiao, Y., Konta, S., Niskanen, T., Liimatainen, K., Dai, Y.-C., Ji, X.-H., Tian, X.-M., Mešić, A., Singh, S.K., Phutthacharoen, K., Cai, L., Sorvongxay, T., Thiyagaraja, V., Norphanphoun, C., Chaiwan, N., Lu, Y.-Z., Jiang, H.-B., Zhang, J.-F., Abeywickrama, P.D., Aluthmuhandiram, J.V.S., Brahmanage, R.S., Zeng, M., Chethana, T., Wei, D., Réblová, M., Fournier, J., Nekvindová, J., do Nascimento Barbosa, R., dos Santos, J.E.F., de Oliveira, N.T., Li, G.-J., Ertz, D., Shang, Q.-J., Phillips, A.J.L., Kuo, C.-H., Camporesi, E., Bulgakov, T.S., Lumyong, S., Jones, E.B.G., Chomnunti, P., Gentekaki, E., Bungartz, F., Zeng, X.-Y., Fryar, S., Tkalčec, Z., Liang, J., Li, G., Wen, T.-C., Singh, P.N., Gafforov, Y., Promputtha, I., Yasanthika, E., Goonasekara, I.D., Zhao, R.-L., Zhao, Q., Kirk, P.M., Liu, J.-K., Yan, J., Mortimer, P.E., Xu, J. & Doilom, M. (2019) Fungal diversity notes 1036–1150: taxonomic and phylogenetic contributions on genera and species of fungal taxa. Fungal Diversity 96: 1–242. https://doi.org/10.1007/s13225-019-00429-2
  23. Jaklitsch, W.M. & Voglmayr, H. (2011) Stromatonectria gen. nov. and notes on Myrmaeciella. Mycologia 103: 431–440. https://doi.org/10.3852/10-240
  24. Jayasiri, S.C., Hyde, K.D., Ariyawansa, H.A., Bhat, J., Buyck, B., Cai, L., Dai, Y.-C., Abd-Elsalam, K.A., Ertz, D., Hidayat, I., Jeewon, R., Jones, E.B.G., Bahkali, A.H., Karunarathna, S.C., Liu, J.-K., Luangsa-ard, J.J., Lumbsch, H.T., Maharachchikumbura, S.S.N., McKenzie, E.H.C., Moncalvo, J.-M., Ghobad-Nejhad, M., Nilsson, H., Pang, K.-L., Pereira, O.L., Phillips, A.J.L., Raspé, O., Rollins, A.W., Romero, A.I., Etayo, J., Selçuk, F., Stephenson, S.L., Suetrong, S., Taylor, J.E., Tsui, C.K.M., Vizzini, A., Abdel-Wahab, M.A., Wen, T.-C., Boonmee, S., Dai, D.Q., Daranagama, D.A., Dissanayake, A.J., Ekanayaka, A.H., Fryar, S.C., Hongsanan, S., Jayawardena, R.S., Li, W.-J., Perera, R.H., Phookamsak, R., de Silva, N.I., Thambugala, K.M., Tian, Q., Wijayawardene, N.N., Zhao, R.-L., Zhao, Q., Kang, J.-C. & Promputtha, I. (2015) The Faces of Fungi database: fungal names linked with morphology, phylogeny and human impacts. Fungal Diversity 74: 3–18. https://doi.org/10.1007/s13225-015-0351-8
  25. Johnson, D., Sung, G.-H., Hywel-Jones, N.L., Luangsa-Ard, J.J., Bischoff, J.F., Kepler, R.M. & Spatafora, J.W. (2009) Systematics and evolution of the genus Torrubiella (Hypocreales, Ascomycota). Mycological Research 113: 279–289. https://doi.org/10.1016/j.mycres.2008.09.008
  26. Kanzaki, N., Liang, W.-R., Chiu, C.-I., Yang, C.-T., Hsueh, Y.-P. & Li, H.-F. (2019) Nematode-free agricultural system of a fungus-growing termite. Scientific Reports 9: 8917. https://doi.org/10.1038/s41598-019-44993-8
  27. Kepler, R., Ban, S., Nakagiri, A., Bischoff, J., Hywel-Jones, N., Owensby, C.A. & Spatafora, J.W. (2013) The phylogenetic placement of hypocrealean insect pathogens in the genus Polycephalomyces: An application of One Fungus One Name. Fungal Biology 117: 611–622. https://doi.org/10.1016/j.funbio.2013.06.002
  28. Kepler, R.M., Humber, R.A., Bischoff, J.F. & Rehner, S.A. (2014) Clarification of generic and species boundaries for Metarhizium and related fungi through multigene phylogenetics. Mycologia 106: 811–829. https://doi.org/10.3852/13-319
  29. Kepler, R.M., Sung, G.-H., Ban, S., Nakagiri, A., Chen, M.-J., Huang, B., Li, Z. & Spatafora, J.W. (2012) New teleomorph combinations in the entomopathogenic genus Metacordyceps. Mycologia 104: 182–197. https://doi.org/10.3852/11-070
  30. Khonsanit, A., Luangsa-ard, J.J., Thanakitpipattana, D., Kobmoo, N. & Piasai, O. (2019) Cryptic species within Ophiocordyceps myrmecophila complex on formicine ants from Thailand. Mycological Progress 18: 147–161. https://doi.org/10.1007/s11557-018-1412-7
  31. Kishino, H. & Hasegawa, M. (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. Journal of Molecular Evolution 29: 170–179. https://doi.org/10.1007/BF02100115
  32. Lechat, C., Fournier, J. & Moreau, P.-A. (2016) Xanthonectria, a new genus for the nectrioid fungus Nectria pseudopeziza. Ascomycete.org 8: 172–178. https://doi.org/10.25664/ART-0185
  33. Lin, C.-G., Chen, Y., McKenzie, E.H.C., Bhat, D.J., Ariyawansa, H.A., Hyde, K.D. & Wang, Y. (2016) The genus Fusariella. Mycological Progress 15: 1313–1326. https://doi.org/10.1007/s11557-016-1246-0
  34. Lombard, L., Van Der Merwe, N.A., Groenewald, J.Z. & Crous, P.W. (2015) Generic concepts in Nectriaceae. Studies in Mycology 80: 189–245. https://doi.org/10.1016/j.simyco.2014.12.002
  35. Luangsa-ard, J., Tasanathai, K., Thanakitpipattana, D., Khonsanit, A. & Stadler, M. (2018) Novel and interesting Ophiocordyceps spp. (Ophiocordycipitaceae, Hypocreales) with superficial perithecia from Thailand. Studies in Mycology 89: 125–142. https://doi.org/10.1016/j.simyco.2018.02.001
  36. Luangsa-Ard, J.J., Hywel-Jones, N.L., Manoch, L. & Samson, R.A. (2005) On the relationships of Paecilomyces sect. Isarioidea species. Mycological Research 109: 581–589. https://doi.org/10.1017/S0953756205002741
  37. Luangsa-ard, J.J., Ridkaew, R., Mongkolsamrit, S., Tasanathai, K. & Hywel-Jones, N.L. (2010) Ophiocordyceps barnesii and its relationship to other melolonthid pathogens with dark stromata. Fungal Biology 114: 739–745. https://doi.org/10.1016/j.funbio.2010.06.007
  38. Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. 2010 Gateway Computing Environments Workshop (GCE), IEEE, pp. 1–8.
  39. Montalva, C., Silva, J.J., Rocha, L.F.N., Luz, C. & Humber, R.A. (2019) Characterization of Tolypocladium cylindrosporum (Hypocreales, Ophiocordycipitaceae) isolates from Brazil and their efficacy against Aedes aegypti (Diptera, Culicidae). Journal of Applied Microbiology 126: 266–276. https://doi.org/10.1111/jam.14093
  40. Otani, S., Challinor, V.L., Kreuzenbeck, N.B., Kildgaard, S., Krath Christensen, S., Larsen, L.L.M., Aanen, D.K., Rasmussen, S.A., Beemelmanns, C. & Poulsen, M. (2019) Disease-free monoculture farming by fungus-growing termites. Scientific Reports 9: 8819. https://doi.org/10.1038/s41598-019-45364-z
  41. Park, M.-J., Hong, S.-B. & Shin, H.-D. (2016) Lecanicillium uredinophilum sp. nov. associated with rust fungi from Korea. Mycotaxon 130: 997–1005. https://doi.org/10.5248/130.997
  42. Peng, X.-C., Wen, T.-C., Wei, D.-P., Liao, Y.-H., Wang, Y., Zhang, X., Wang, G.-Y., Zhou, Y., Tangtrakulwanich, K. & Liang, J.-D. (2024) Two new species and one new combination of Ophiocordyceps (Hypocreales, Ophiocordycipitaceae) in Guizhou. MycoKeys 102: 245–266. https://doi.org/10.3897/mycokeys.102.113351
  43. Penzig, O. & Saccardo, P.A. (1904) Icones fungorum javanicorum. E.J. Brill, Leiden, 285 pp. https://doi.org/10.5962/bhl.title.17234
  44. Perera, R.H., Hyde, K.D., Jones, E.B.G., Maharachchikumbura, S.S.N., Bundhun, D., Camporesi, E., Akulov, A., Liu, J.K. & Liu, Z.Y. (2023) Profile of Bionectriaceae, Calcarisporiaceae, Hypocreaceae, Nectriaceae, Tilachlidiaceae, Ijuhyaceae fam. nov., Stromatonectriaceae fam. nov. and Xanthonectriaceae fam. nov. Fungal Diversity 118: 95–271. https://doi.org/10.1007/s13225-022-00512-1
  45. Quandt, C.A., Kepler, R.M., Gams, W., Araújo, J.P.M., Ban, S., Evans, H.C., Hughes, D., Humber, R., Hywel-Jones, N., Li, Z., Luangsa-ard, J.J., Rehner, S.A., Sanjuan, T., Sato, H., Shrestha, B., Sung, G.-H., Yao, Y.-J., Zare, R. & Spatafora, J.W. (2014) Phylogenetic-based nomenclatural proposals for Ophiocordycipitaceae (Hypocreales) with new combinations in Tolypocladium. IMA Fungus 5: 121–134. https://doi.org/10.5598/imafungus.2014.05.01.12
  46. Rambaut, A. (2012) FigTree v. 1.4.0. Available from: http://tree.bio.ed.ac.uk/software/figtree/ (accessed 18 July 2024)
  47. Rehner, S.A., Minnis, A.M., Sung, G.-H., Luangsa-ard, J.J., Devotto, L. & Humber, R.A. (2011) Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia 103: 1055–1073. https://doi.org/10.3852/10-302
  48. Rehner, S.A. & Samuels, G.J. (1995) Molecular systematics of the Hypocreales: a teleomorph gene phylogeny and the status of their anamorphs. Canadian Journal of Botany 73: 816–823. https://doi.org/10.1139/b95-327
  49. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542. https://doi.org/10.1093/sysbio/sys029
  50. Rossman, A.Y., Farr, D.F., Platas, G. & Newcombe, G. (2008) Hydropisphaera fungicola. Fungal Planet 24: 1–2.
  51. Samarakoon, M.C., Hyde, K.D., Maharachchikumbura, S.S.N., Stadler, M., Gareth Jones, E.B., Promputtha, I., Suwannarach, N., Camporesi, E., Bulgakov, T.S. & Liu, J.-K. (2022) Taxonomy, phylogeny, molecular dating and ancestral state reconstruction of Xylariomycetidae (Sordariomycetes). Fungal Diversity 112: 1–88. https://doi.org/10.1007/s13225-021-00495-5
  52. Sanjuan, T.I., Franco-Molano, A.E., Kepler, R.M., Spatafora, J.W., Tabima, J., Vasco-Palacios, A.M. & Restrepo, S. (2015) Five new species of entomopathogenic fungi from the Amazon and evolution of neotropical Ophiocordyceps. Fungal Biology 119: 901–916. https://doi.org/10.1016/j.funbio.2015.06.010
  53. Schoch, C.L., Seifert, K.A., Huhndorf, S., Robert, V., Spouge, J.L., Levesque, C.A., Chen, W., Fungal Barcoding Consortium, Fungal Barcoding Consortium Author List, Bolchacova, E., Voigt, K., Crous, P.W., Miller, A.N., Wingfield, M.J., Aime, M.C., An, K.-D., Bai, F.-Y., Barreto, R.W., Begerow, D., Bergeron, M.-J., Blackwell, M., Boekhout, T., Bogale, M., Boonyuen, N., Burgaz, A.R., Buyck, B., Cai, L., Cai, Q., Cardinali, G., Chaverri, P., Coppins, B.J., Crespo, A., Cubas, P., Cummings, C., Damm, U., De Beer, Z.W., De Hoog, G.S., Del-Prado, R., Dentinger, B., Diéguez-Uribeondo, J., Divakar, P.K., Douglas, B., Dueñas, M., Duong, T.A., Eberhardt, U., Edwards, J.E., Elshahed, M.S., Fliegerova, K., Furtado, M., García, M.A., Ge, Z.-W., Griffith, G.W., Griffiths, K., Groenewald, J.Z., Groenewald, M., Grube, M., Gryzenhout, M., Guo, L.-D., Hagen, F., Hambleton, S., Hamelin, R.C., Hansen, K., Harrold, P., Heller, G., Herrera, C., Hirayama, K., Hirooka, Y., Ho, H.-M., Hoffmann, K., Hofstetter, V., Högnabba, F., Hollingsworth, P.M., Hong, S.-B., Hosaka, K., Houbraken, J., Hughes, K., Huhtinen, S., Hyde, K.D., James, T., Johnson, E.M., Johnson, J.E., Johnston, P.R., Jones, E.B.G., Kelly, L.J., Kirk, P.M., Knapp, D.G., Kõljalg, U., Kovács, G.M., Kurtzman, C.P., Landvik, S., Leavitt, S.D., Liggenstoffer, A.S., Liimatainen, K., Lombard, L., Luangsa-ard, J.J., Lumbsch, H.T., Maganti, H., Maharachchikumbura, S.S.N., Martin, M.P., May, T.W., McTaggart, A.R., Methven, A.S., Meyer, W., Moncalvo, J.-M., Mongkolsamrit, S., Nagy, L.G., Nilsson, R.H., Niskanen, T., Nyilasi, I., Okada, G., Okane, I., Olariaga, I., Otte, J., Papp, T., Park, D., Petkovits, T., Pino-Bodas, R., Quaedvlieg, W., Raja, H.A., Redecker, D., Rintoul, T.L., Ruibal, C., Sarmiento-Ramírez, J.M., Schmitt, I., Schüßler, A., Shearer, C., Sotome, K., Stefani, F.O.P., Stenroos, S., Stielow, B., Stockinger, H., Suetrong, S., Suh, S.-O., Sung, G.-H., Suzuki, M., Tanaka, K., Tedersoo, L., Telleria, M.T., Tretter, E., Untereiner, W.A., Urbina, H., Vágvölgyi, C., Vialle, A., Vu, T.D., Walther, G., Wang, Q.-M., Wang, Y., Weir, B.S., Weiß, M., White, M.M., Xu, J., Yahr, R., Yang, Z.L., Yurkov, A., Zamora, J.-C., Zhang, N., Zhuang, W.-Y. & Schindel, D. (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences 109: 6241–6246. https://doi.org/10.1073/pnas.1117018109
  54. Sigler, L., Gibas, C.F.C., Kokotovic, B. & Bertelsen, M.F. (2010) disseminated mycosis in veiled chameleons (Chamaeleo calyptratus) caused by Chamaeleomyces granulomatis, a new fungus related to Paecilomyces viridis. Journal of Clinical Microbiology 48: 3182–3192. https://doi.org/10.1128/JCM.01079-10
  55. Simmons, D.R., Kepler, R.M., Renner, S.A. & Groden, E. (2015a) Phylogeny of Hirsutella species (Ophiocordycipitaceae) from the USA: remedying the paucity of Hirsutella sequence data. IMA Fungus 6: 345–356. https://doi.org/10.5598/imafungus.2015.06.02.06
  56. Simmons, D.R., Lund, J., Levitsky, T. & Groden, E. (2015b) Ophiocordyceps myrmicarum, a new species infecting invasive Myrmica rubra in Maine. Journal of Invertebrate Pathology 125: 23–30. https://doi.org/10.1016/j.jip.2014.12.010
  57. Spatafora, J.W., Quandt, C.A., Kepler, R.M., Sung, G.-H., Shrestha, B., Hywel-Jones, N.L. & Luangsa-ard, J.J. (2015) New 1F1N species combinations in Ophiocordycipitaceae (Hypocreales). IMA Fungus 6: 357–362. https://doi.org/10.5598/imafungus.2015.06.02.07
  58. Spatafora, J.W., Sung, G. ‐H., Sung, J. ‐M., Hywel‐Jones, N.L. & White, J.F. (2007) Phylogenetic evidence for an animal pathogen origin of ergot and the grass endophytes. Molecular Ecology 16: 1701–1711. https://doi.org/10.1111/j.1365-294X.2007.03225.x
  59. Spatafora, J.W., Sung, G.-H., Johnson, D., Hesse, C., O’Rourke, B., Serdani, M., Spotts, R., Lutzoni, F., Hofstetter, V., Miadlikowska, J., Reeb, V., Gueidan, C., Fraker, E., Lumbsch, T., Lucking, R., Schmitt, I., Hosaka, K., Aptroot, A., Roux, C., Miller, A.N., Geiser, D.M., Hafellner, J., Hestmark, G., Arnold, A.E., Budel, B., Rauhut, A., Hewitt, D., Untereiner, W.A., Cole, M.S., Scheidegger, C., Schultz, M., Sipman, H. & Schoch, C.L. (2006) A five-gene phylogeny of Pezizomycotina. Mycologia 98: 1018–1028. https://doi.org/10.3852/mycologia.98.6.1018
  60. Stifler, C.B. (1941) A new genus of Hypocreales. Mycologia 33: 82–86. https://doi.org/10.1080/00275514.1941.12020795
  61. Suh, S.-O., Spatafora, J.W., Ochiel, G.R.S., Evans, H.C. & Blackwell, M. (1998) Molecular phylogenetic study of a termite pathogen Cordycepioideus bisporus. Mycologia 90: 611–617. https://doi.org/10.1080/00275514.1998.12026950
  62. Sung, G.-H., Hywel-Jones, N.L., Sung, J.-M., Luangsa-ard, J.J., Shrestha, B. & Spatafora, J.W. (2007a) Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Studies in Mycology 57: 5–59. https://doi.org/10.3114/sim.2007.57.01
  63. Sung, G.-H., Spatafora, J.W., Zare, R., Hodge, K.T. & Gams, W. (2001) A revision of Verticillium sect. Prostrata. II. Phylogenetic analyses of SSU and LSU nuclear rDNA sequences from anamorphs and teleomorphs of the Clavicipitaceae. Nova Hedwigia 72: 311–328. https://doi.org/10.1127/nova.hedwigia/72/2001/311
  64. Sung, G.-H., Sung, J.-M., Hywel-Jones, N.L. & Spatafora, J.W. (2007b) A multi-gene phylogeny of Clavicipitaceae (Ascomycota, Fungi): Identification of localized incongruence using a combinational bootstrap approach. Molecular Phylogenetics and Evolution 44: 1204–1223. https://doi.org/10.1016/j.ympev.2007.03.011
  65. Swofford, D.L. (2002) PAUP* Version 4.0 b10. Phylogenetic Analysis Using Parsimony (* and Other Methods). Sinauer, Sunderland
  66. Tang, D., Zhu, J., Luo, L., Hou, D., Wang, Z., Yang, S. & Yu, H. (2022) Ophiocordyceps ovatospora sp. nov. (Ophiocordycipitaceae, Hypocreales), pathogenic on termites from China. Phytotaxa 574 (1): 105–117. https://doi.org/10.11646/phytotaxa.574.1.8
  67. Tasanathai, K., Khonsanit, A., Noisripoom, W., Kobmoo, N. & Luangsa-ard, J. (2022) Hidden species behind Ophiocordyceps (Ophiocordycipitaceae, Hypocreales) on termites: four new species from Thailand. Mycological Progress 21: 86. https://doi.org/10.1007/s11557-022-01837-6
  68. Tasanathai, K., Noisripoom, W., Chaitika, T., Khonsanit, A., Hasin, S. & Luangsa-ard, J. (2019) Phylogenetic and morphological classification of Ophiocordyceps species on termites from Thailand. MycoKeys 56: 101–129. https://doi.org/10.3897/mycokeys.56.37636
  69. Tibpromma, S., Hyde, K.D., McKenzie, E.H.C., Bhat, D.J., Phillips, A.J.L., Wanasinghe, D.N., Samarakoon, M.C., Jayawardena, R.S., Dissanayake, A.J., Tennakoon, D.S., Doilom, M., Phookamsak, R., Tang, A.M.C., Xu, J., Mortimer, P.E., Promputtha, I., Maharachchikumbura, S.S.N., Khan, S. & Karunarathna, S.C. (2018) Fungal diversity notes 840–928: micro-fungi associated with Pandanaceae. Fungal Diversity 93. https://doi.org/10.1007/s13225-018-0408-6
  70. Trifinopoulos, J., Nguyen, L.-T., von Haeseler, A. & Minh, B.Q. (2016) W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Research 44: W232–W235. https://doi.org/10.1093/nar/gkw256
  71. Vilgalys, R. & Hester, M. (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. Journal of Bacteriology 172: 4238–4246. https://doi.org/10.1128/JB.172.8.4238-4246.1990
  72. Vu, D., Groenewald, M., de Vries, M., Gehrmann, T., Stielow, B., Eberhardt, U., Al-Hatmi, A., Groenewald, J.Z., Cardinali, G., Houbraken, J., Boekhout, T., Crous, P.W., Robert, V. & Verkley, G.J.M. (2019) Large-scale generation and analysis of filamentous fungal DNA barcodes boosts coverage for kingdom fungi and reveals thresholds for fungal species and higher taxon delimitation. Studies in Mycology 92: 135–154. https://doi.org/10.1016/j.simyco.2018.05.001
  73. Wang, X.W., Houbraken, J., Groenewald, J.Z., Meijer, M., Andersen, B., Nielsen, K.F., Crous, P.W. & Samson, R.A. (2016a) Diversity and taxonomy of Chaetomium and chaetomium-like fungi from indoor environments. Studies in Mycology 84: 145–224. https://doi.org/10.1016/j.simyco.2016.11.005
  74. Wang, X.W., Lombard, L., Groenewald, J.Z., Li, J., Videira, S.I.R., Samson, R.A., Liu, X.Z. & Crous, P.W. (2016b) Phylogenetic reassessment of the Chaetomium globosum species complex. Persoonia—Molecular Phylogeny and Evolution of Fungi 36: 83–133. https://doi.org/10.3767/003158516X689657
  75. Wei, D., Gentekaki, E., Wanasinghe, D., Tang, S. & Hyde, K. (2022) Diversity, molecular dating and ancestral characters state reconstruction of entomopathogenic fungi in Hypocreales. Mycosphere 13: 281–351. https://doi.org/10.5943/mycosphere/si/1f/8
  76. Wijayawardene, N.N., Hyde, K.D., Dai, D.Q., Sánchez-García, M., Goto, B.T., Saxena, R.K., Erdoğdu, M., Selçuk, F., Rajeshkumar, K.C., Aptroot, A., Błaszkowski, J., Boonyuen, N., da Silva, G.A., de Souza, F.A., Dong, W., Ertz, D., Haelewaters, D., Jones, E.B.G., Karunarathna, S.C., Kirk, P.M., Kukwa, M., Kumla, J., Leontyev, D.V., Lumbsch, H.T., Maharachchikumbura, S.S.N., Marguno, F., Martínez-Rodríguez, P., Mešić, A., Monteiro, J.S., Oehl, F., Pawłowska, J., Pem, D., Pfliegler, W.P., Phillips, A.J.L., Pošta, A., He, M.Q., Li, J.X., Raza, M., Sruthi, O.P., Suetrong, S., Suwannarach, N., Tedersoo, L., Thiyagaraja, V., Tibpromma, S., Tkalčec, Z., Tokarev, Y.S., Wanasinghe, D.N., Wijesundara, D.S.A., Wimalaseana, S.D.M.K., Madrid, H., Zhang, G.Q., Gao, Y., Sánchez-Castro, I., Tang, L.Z., Stadler, M., Yurkov, A. & Thines, M. (2022) Outline of fungi and fungus-like taxa—2021. Mycosphere 13: 53–453. https://doi.org/10.5962/bhl.title.17234
  77. White, T.J., Bruns, T., Lee, S. & Taylor, J. (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols. Elsevier, pp. 315–322.
  78. Wilson, M., Barden, P. & Ware, J. (2021) A review of ectoparasitic fungi associated with termites. Annals of the Entomological Society of America 114: 373–396. https://doi.org/10.1093/aesa/saab001
  79. Xiao, Y.-P., Hongsanan, S., Hyde, K.D., Brooks, S., Xie, N., Long, F.-Y. & Wen, T.-C. (2019) Two new entomopathogenic species of Ophiocordyceps in Thailand. MycoKeys 47: 53–74. https://doi.org/10.3897/mycokeys.47.29898
  80. Xiao, Y.-P., Wang, Y.B., Hyde, K.D., Eleni, G., Sun, J., Yang, Y., Meng, J., Yu, H. & Wen, T.-C. (2023) Polycephalomycetaceae, a new family of clavicipitoid fungi segregates from Ophiocordycipitaceae. Fungal Diversity 120: 1–76. https://doi.org/10.1007/s13225-023-00517-4
  81. Xu, Z.-H., Tran, N.-L., Wang, Y., Zhang, G.-D., Dao, V.-M., Nguyen, T.-T., Wang, Y.-B. & Yu, H. (2022) Phylogeny and morphology of Ophiocordyceps puluongensis sp. nov. (Ophiocordycipitaceae, Hypocreales), a new fungal pathogen on termites from Vietnam. Journal of Invertebrate Pathology 192: 107771. https://doi.org/10.1016/j.jip.2022.107771
  82. Yamamoto, K., Sugawa, G., Takeda, K. & Degawa, Y. (2022) Tolypocladium bacillisporum (Ophiocordycipitaceae): A new parasite of Elaphomyces from Japan. Truffology 5: 15–21.
  83. Yu, Y., Hou, S.-Y., Sun, Z.-L., Zhang, M.-Y., Zhang, T.-Y. & Zhang, Y.-X. (2018) Drechmeria panacis sp. nov., an endophyte isolated from Panax notoginseng. International Journal of Systematic and Evolutionary Microbiology 68: 3255–3259. https://doi.org/10.1099/ijsem.0.002971
  84. Zare, R., Gams, W. & Culham, A. (2000) A revision of Verticillium sect. Prostrata I. Phylogenetic studies using ITS sequences. Nova Hedwigia 71: 465–480. https://doi.org/10.1127/nova/71/2000/465
  85. Zhuang, W.-Y. & Zeng, Z.Q. (2017) Cocoonihabitus sinensis gen. et sp. nov. on remaining leaf veins of cocoons in a new family Cocoonihabitaceae fam. nov. of Hypocreales. Mycosystema 36: 1591–1598. https://doi.org/10.13346/j.mycosystema.170176
  86. Zou, X., Zhou, J.-X., Liang, Z.-Q. & Han, Y.-F. (2016) Hirsutella shennongjiaensis, a new entomopathogenic species infecting Earwig (Dermaptera). Mycosystema 35: 1070–1079. https://doi.org/10.13346/j.mycosystema.160077