Zombie-ant fungi cross continents: II. Myrmecophilous hymenostilboid species and a novel zombie lineage

LITERATURE CITED

• Andersen SB, Gerritsma S, Yusah KM, Mayntz D, Hywel-Jones NL, Billen J, Boomsma JJ, Hughes DP. 2009. The life of a dead ant: the expression of an adaptive extended phenotype. American Naturalist 174:424–433.
   PubMed Web of Science ®Google Scholar
• Araújo JPM, Evans HC, Geiser DM, Mackay WP, Hughes DP. 2015. Unravelling the diversity behind the Ophiocordyceps unilateralis (Ophiocordycipitaceae) complex: three new species of zombie-ant fungi from the Brazilian Amazon. Phytotaxa 220:224–238.
   Web of Science ®Google Scholar
• Araújo JPM, Evans HC, Kepler RM, Hughes DP. 2018. Zombie-ant fungi acriss continents: 15 new species and new combinations within Ophiocordyceps. I. Myrmecophilous hirsutelloid species. Studies in Mycology 90:1–42.
   PubMed Web of Science ®Google Scholar
• Araújo JPM, Hughes DP. 2016. Diversity of entomopathogenic fungi: which groups conquered the insect body? Advances in Genetics 94:1–39.
   Google Scholar
• Araújo JPM, Hughes DP. 2017. The fungal spore: myrmecophilous Ophiocordyceps as a case study. In: Dighton J, White JM, eds. The fungal community: its organization and role in the ecosystem. Boca Raton, Florida: CRC Press. p. 359–367.
   Google Scholar
• Araújo JPM, Hughes DP. 2019. Zombie-ant fungi emerged from non-manipulating, beetle-infecting ancestors. Current Biology 29:3735–3738.
   PubMed Web of Science ®Google Scholar
• Bekker C, Ohm RA, Evans HC, Brachman A, Hughes DP. 2017. Ant-infecting Ophiocordyceps genomes reveal a high diversity of potential behavioral manipulation genes and a possible major role for enterotoxins. Scientific Reports (Nature) 7: 12508.
   PubMed Web of Science ®Google Scholar
• Bequaert J. 1922. Ants in their diverse relations to the plant world. Bulletin of the American Museum of Natural History 45:333–583.
   Google Scholar
• Bolton B. 2007. Taxonomy of the dolichoderine ant genus Technomyrmex Mayr (Hymenoptera: Formicidae) based on worker caste. Contributions of the American Entomological Institute 35:1–149.
   Google Scholar
• Bolton B, Alpert G, Ward PS, Nasrecki P. 2007. Bolton’s catalogue of ants of the world. Cambridge, Massachusetts: Harvard University Press. 512 p.
   Google Scholar
• Bünzli GH, Büttiker WW. 1959. Fungus diseases of lamellicorn larvae in Southern Rhodesia. Bulletin of Entomological Research 50:89–96.
   Google Scholar
• Camargo RX, Oliveira PS. 2012. Natural history of the neotropical arboreal ant, Odontomachus hastatus: nest sites, foraging schedule, and diet. Journal of Insect Science 12:1–9.
   Web of Science ®Google Scholar
• Castlebury LA, Rossman AY, Sung G-H, Hyten SA, Spatafora JW. 2004. Multigene phylogeny reveals nww lineage for Stachybotrys chatarum, the indoor air fungus. Mycological Research 108:1–9.
   Web of Science ®Google Scholar
• Cooke MC 1892. Vegetable wasps and plant worms. London, UK: Society for Promoting Christian Knowledge. 364 p.
   Google Scholar
• Crous PW, Gams W, Stalpers JA, Rovert V, Stegehuis G. 2004. MycoBank: an online initiative to launch mycology into the 21st century. Studies in Mycology 50:12–22.de
   Google Scholar
• de Bekker C, Ohm RA, Loreto RG, Sebastian A, Albert I, Merrow M, Brachmann A, Hughes DP. 2015. Gene expression during zombie ant biting behavior reflects the complexity underlying fungal parasitic behavioral manipulation. BMC Genomics 16:620.
   PubMed Web of Science ®Google Scholar
• de Bekker C, Quevillon LE, Smith PB, Fleming KR, Ghosh D, Patterson AD, Hughes DP. 2014. Species-specific ant brain manipulation by a specialized fungal parasite. BMC Evolutionary Biology 14:166.
   PubMed Web of Science ®Google Scholar
• de Hoog GS. 1974. The genera Blastobotrys, Sporothrix, Calcarisporium and Calcarisporiella gen. nov. Studies in Mycology 7:1–84.
   Google Scholar
• Diaz JAP. 2004. Some observations on the nest structure and colony composition of Pseudomyrmex termitarius (Hymenoptera: Formicidae) in Abello (Antioquia, Colombia). Revista Facultad Nacional de Agronomía Medellín 57:2161–2177.
   Google Scholar
• Edgar RC. 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113. doi:10.1186/1471-2105-5-113
   PubMed Web of Science ®Google Scholar
• Evans HC. 1974. Natural control of arthropods, with special reference to ants (Formicidae), by fungi in the tropical high forest of Ghana. Journal of Applied Ecology 11:37–49.
   Web of Science ®Google Scholar
• Evans HC. 1982. Entomogenous fungi in tropical forest ecosystems: an appraisal. Ecological Entomology 7:47–60.
   Web of Science ®Google Scholar
• Evans HC. 1988a. Coevolution of entomogenous fungi and their insect hosts. In: Pirozynski KA, Hawksworth DL, eds. Coevolution of fungi with plants and animals. London, UK: Academic Press. p. 149–171.
   Google Scholar
• Evans HC. 1988b. Mycopathogens of insects of epigeal and aerial habitats. In: Wilding N, Collins NM, Hammond PM, Webber J, eds. Insect-fungus interactions. London, UK: Academic Press. p. 205–238.
   Google Scholar
• Evans HC. 2001. Entomopathogenic fungi associated with ants (Formicidae): a review. In: Misra JK, Horn BW, eds. Trichomycetes and other fungal groups. Enfield, New Hampshire: Science Publishers. p. 119–144.
   Google Scholar
• Evans HC, Araújo JPM, Halfeld VR, Hughes DP. 2018. Epitypification and re-description of the zombie-ant fungus, Ophiocordyceps unilateralis (Ophiocordycipitaceae). Fungal Systematics & Evolution 1:13–22.
   PubMedGoogle Scholar
• Evans HC, Elliot SL, Hughes DP. 2011a. Hidden diversity behind the zombie-ant fungus Ophiocordyceps unilateralis: four new species described from carpenter ants in Minas Gerais, Brazil. PLoS ONE 6:e17024.
   PubMed Web of Science ®Google Scholar
• Evans HC, Elliot SL, Hughes DP. 2011b. Ophiocordyceps unilateralis: a keystone species for unraveling ecosystem functioning and biodiversity of fungi? Communicative & Integrative Biology 4:598–602.
   Google Scholar
• Evans HC, Groden E, Bischoff JF. 2010. New fungal pathogens of the red ant, Myrmica rubra, from the UK and implications for ant invasions in the USA. Fungal Biology 114:451–466.
   PubMed Web of Science ®Google Scholar
• Evans HC, Samson RA. 1982. Cordyceps species and their anamorphs pathogenic on ants (Formicidae) in tropical forest ecosystems. I. The Cephalotes (Myrmicinae) complex. Transactions of the British Mycological Society 79:431–453.
   Web of Science ®Google Scholar
• Evans HC, Samson, RA. 1984. Cordyceps species and their anamorphs pathogenic on ants (Formicidae) in tropical forest ecosystems. II. The Camponotus (Formicinae) complex. Transactions of the British Mycological Society 82: 127–150.
   Web of Science ®Google Scholar
• Gray JR. 1858. Notices of insects that are known to form the bases of fungoid parasites. Privately printed, London, UK. 40 p.
   Google Scholar
• Hölldobler B. 2010. Communication during foraging and nest re-location in the African stink ant, Paltothyreus tarsatus Fabr. (Hymenoptera, Formicidae, Ponerinae). Ethology 65:40–52.
   Google Scholar
• Hughes DP, Araújo JPM, Loreto RG, Quevillon L, de Bekker C, Evans HC 2016. From so simple a beginning: the evolution of behavioral manipulation by fungi. Advances in Genetics 94:437–469.
   PubMed Web of Science ®Google Scholar
• Hughes DP, Evans HC, Hywel-Jones NJ. 2009. Novel fungal disease in complex leaf-cutting ant societies. Ecological Entomology 34:214–220.
   Web of Science ®Google Scholar
• Hughes DP, Wappler T, Labandeira C. 2011. Ancient death-grip leaf scars reveal ant-fungal parasitism. Biology Letters 7:67–70.
   PubMed Web of Science ®Google Scholar
• Hywel-Jones NL. 1996. Cordyceps myrmecophila-like fungi infecting ants in the leaf litter of tropical forest in Thailand. Mycological Research 100:613–619.
   Web of Science ®Google Scholar
• Johnson D, Sung G-H, Hywel-Jones NL, Luangsa-ard JJ, Bischoff JF, Kepler RM, Spatafora JW. 2009. Systematics and evolution of the genus Torrubiella (Hypocreales, Ascomycota). Mycological Research 113:279–289.
   PubMed Web of Science ®Google Scholar
• Kepler RM, Luangsa-ard JJ, Hywel-Jones NL, Quandt CA, Sung G-H, Rehner SA, Catherina Aime C, Henkel TW, Sanjuán T, Zare R, Chen M, Li Z, Rossman AY, Spatafora JW, Shrestha B. 2017. A phylogenetically-based nomenclature for Cordycipitaceae. IMA Fungus 8:335–353.
   PubMed Web of Science ®Google Scholar
• Khonsanit A, Luangsa-ard JJ, Thanakitpipattana D, Kobmoo N, Piasai O. 2018. Cryptic species within Ophiocordyceps myrmecophila complex on formicine ants from Thailand. Mycological Progress 18:147–161.
   Web of Science ®Google Scholar
• Kobayasi Y. 1939. On the genus Cordyceps and its allies parasitic to Hymenoptera in Japan. Bulletin of the Biogeographical Society of Japan 9:271–290.
   Google Scholar
• Kobayasi Y. 1941. The genus Cordyceps and its allies. Science Reports, Tokyo Bunrika Daigaku, Section B 5:53–260.
   Google Scholar
• Kobmoo N, Mongkolsamrit S, Wutikhun T, Tasanathai K, Khonsanit A, Thanakitpipattana D, Luangsa-ard JJ. 2015. New species of Ophiocordyceps unilateralis, an ubiquitous pathogen of ants from Thailand. Fungal Biology 119:44–52.
   PubMed Web of Science ®Google Scholar
• Loreto RG, Araújo JPM, Kepler RM, Fleming KR, Moreau CS, Hughes DP. 2018. Evidence for convergent evolution of host parasitic manipulation in response to environmental conditions. Evolution 72:2144–2155.
   PubMed Web of Science ®Google Scholar
• MacKay W, MacKay E. 2010. The systematics and biology of the New World ants of the genus Pachycondyla (Hymenoptera: Formicidae). Lewiston, New York: Edwin Mellen Press. 642 p.
   Google Scholar
• Mains EB. 1948. Entomogenous fungi. Mycologia 40:402–416.
   Web of Science ®Google Scholar
• Mains EB. 1949a. New species of Torrubiella, Hirsutella and Gibellula. Mycologia 41:303–310.
   Web of Science ®Google Scholar
• Mains EB. 1949b. Cordyceps bicephala Berk. and C. australis (Speg.) Sacc. Bulletin of the Torrey Botanical Club 76:24–30.
   Google Scholar
• Mains EB 1958. North American entomogenous species of Cordyceps. Mycologia 50:169–222.
   Web of Science ®Google Scholar
• Matsuura Y, Moriyama M, Łukasik P, Vanderpool D, Tanahashi M, Meng X-Y, McCutcheon J, Fukatsu T. 2018. Recurrent symbiont recruitment from fungal parasites in cicadas. Proceedings of National Academy of Sciences of the United States of America 115:5970–5979.
   Web of Science ®Google Scholar
• Minter DW, Brady BL. 1980. Mononematous species of Hirsutella. Transactions of the British Mycological Society 74:271–282.
   Web of Science ®Google Scholar
• Moureau J. 1949. Cordyceps du Congo Belge. Mémoire Institute Royale College Belge 7:1–57.
   Google Scholar
• Moureau J. 1961. Les Cordyceps du Congo. Bulletin de la Société Royale des Sciences de Liège 30:334–339.
   Google Scholar
• Nnakumusana ES. 1987. Historical studies of Cordyceps myrmecophila (Ces.) infection in the ant Paltothyreus tarsatus Fab. (Formicidae: Ponerinae). Applied Entomology and Zoology 22:1–6.
   Google Scholar
• Papierok B, Charpentie MJ. 1982. Les champignons se developpant en Cote d’Ivoire sur la fourmi Paltothyreus tarsatus F., relation entre l’hyphomycete Tilachlidiopsis catenulata sp. nov. et l’ascomycete Cordyceps myrmecophila Cesati 1846. Mycotaxon 14:351–368.
   Google Scholar
• Parratt SR, Laine AL. 2016. The role of hyperparasitism in microbial pathogen ecology and evolution. The ISME Journal 10:1815–1822.
   PubMed Web of Science ®Google Scholar
• Patouillard N. 1892. Une Clavariée entomogène. Revue Mycologique 14:67–70.
   Google Scholar
• Paulian R. 1949. Un naturaliste en Cote d’Ivoire. Lyon, France: Editions Stock. 192 p.
   Google Scholar
• Peeters C, Braun U, Hölldobler B. 2013. Large colonies and striking sexual investment in the African stink ant, Paltothyreus tarsatus (subfamily Ponerinae). African Entomology 21:9–14.
   Web of Science ®Google Scholar
• Petch T. 1931. Notes on entomogenous fungi. Transactions of the British Mycological Society 16:55–75.
   Google Scholar
• Petch T. 1932. Notes on entomogenous fungi. Transactions of the British Mycological Society 16:209–245.
   Google Scholar
• Qu J, Yu LQ, Zhang J, Han W, Zou X. 2018. A new entomopathogenic fungus, Ophiocordyceps ponerus sp. nov., from China. Phytotaxa 343:116–126.
   Web of Science ®Google Scholar
• Quandt CA, Kepler RM, Gams W, Araújo JPM, Ban S, Evans HC, Hughes DP, Humber RA, Hywel-Jones N, Li Z, Luangsa-ard JJ, Rehner SA, Sanjuan T, Sato H, Shrestha B, Sung G-H, Yao Y-J, Zare R, Spatafora JW. 2014. Phylogenetic-based nomenclatural proposals for Ophiocordycipitaceae (Hypocreales) with new combinations in Tolypocladium. IMA Fungus 5:121–134.
   PubMed Web of Science ®Google Scholar
• Robin C. 1853. Histoire Naturelle des Végétaux parasites, qui croissant ser I’homme et sur les animaux vivants. Paris, France: J.-B. Baillière. 732 p.
   Google Scholar
• Saccardo PA. 1883. Sylloge Fungorum II. Pyrenomycetaceae. New York: Friedländer. 815 p.
   Google Scholar
• Samson RA, Evans HC. 1973. Notes on entomogenous fungi from Ghana I. The genera Gibellula and Pseudogibellula. Acta Botanica Neerlandica 22:522–528.
   Web of Science ®Google Scholar
• Samson RA, Evans HC. 1975. Notes on entomogenous fungi from Ghana III. The genus Hymenostilbe. Proceedings of the Koninklijke Nederlandense Akademie van Wetenschappen 78:73–80.
   Google Scholar
• Samson RA, Evans HC, Hoekstra ES. 1982. Notes on entomogenous fungi from Ghana. VI. The genus Cordyceps. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, Series C 85:589–605.
   Google Scholar
• Samson RA, Evans HC, van de Klashorst G. 1981. Notes on entomogenous fungi from Ghana. V. The genera Stilbella and Polycephalomyces. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, Series C 84: 289–301.
   Google Scholar
• Samson RA, van Reenen-Hoekstra ES, Evans HC. 1989. New species of Torrubiella (Ascomycotina: Clavicipitales) on insects from Ghana. Studies in Mycology 31:123–132.
   Google Scholar
• Sanjuán T, Henao LG, Amat G. 2001. Distribución especial de Cordyceps spp. (Ascomycotina: Clavicipitaceae) y su impacto sobre las hormigas en selvas del piedemonte amazónico de Colombia. Revista de Biología Tropical 49:945–955.
   Google Scholar
• Sanjuán TI, Franco-Molano AE, Kepler RM, Spatafora JW, Tabima J, Vasco-Palacios AM, Restrepo S. 2015. Five new species of entomopathogenic fungi from the Amazon and evolution of neotropical Ophiocordyceps. Fungal Biology 119:901–916.
   PubMed Web of Science ®Google Scholar
• Spatafora JW, Quandt CA, Kepler RM, Sung G-H, Shrestha B, Hywel-Jones NL, Luangsa-ard JJ. 2015. New 1F1N species combinations in Ophiocordycipitaceae (Hypocreales). IMA Fungus 6:357–362.
   PubMed Web of Science ®Google Scholar
• Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690.
   PubMed Web of Science ®Google Scholar
• Sung G-H, Hywel-Jones NL, Sung J-M, Luangsa-ard JJ, Shrestha B, Spatafora JW. 2007. Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Studies in Mycology 57:5–59.
   PubMed Web of Science ®Google Scholar
• Vilgalys R, Sun BL. 1994. Ancient and recent patterns of geographic speciation in the oyster mushroom Pleurotus revealed by phylogenetic analysis of ribosomal DNA sequences. Proceedings of National Academy of Sciences of the United States of America 91:4599–4603.
   PubMed Web of Science ®Google Scholar
• Wetterer JK. 2017. Geographic distribution of the African weaver ant, Oecophylla longinoda. Transactions of the American Entomological Society 143:501–510.
   Web of Science ®Google Scholar
• White TJ, Bruns T, Lee S, Taylor JW. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, eds. PCR protocols: a guide to the methods and applications. New York: Academic Press. p. 315–322.
   Google Scholar
• Yanoviak SP, Munk Y, Kaspari M. 2010. Aerial manoeuvrability in wingless gliding ants (Cephalotes atratus). Proceedings of the Royal Society B: Biological Sciences 277:2199–2204.
   Google Scholar