Nuclear populations of the multinucleate fungus of leafcutter ants can be dekaryotized and recombined to manipulate growth of nutritive hyphal nodules harvested by the ants

LITERATURE CITED

• Adams RMM, Mueller UG, Green AM Narozniak JM. 2000. Garden sharing and garden stealing in fungus-growing ants. Naturwissenschaften 87: 491–493.
   Google Scholar
• Albertin W, Marullo P. 2012. Polyploidy in fungi: evolution after whole-genome duplication. Proceedings of the Royal Society B: Biological Sciences 279:2497–2509.
   Google Scholar
• Alic M, Letzring C, Gold MH. 1987. Mating system and basidiospore formation in the lignin-degrading basidiomycete Phanerochaete chrysosporium. Applied and Environmental Microbiology 53:1464–1469.
   Google Scholar
• Autuori M. 1950. Contribuição para o conhecimento da saúva (Atta spp.-Hymenoptera-Formicidae) V. Número de formas aladas e redução dos sauveiros iniciais. Arquivos do Instituto Biológico (Sao Paulo) 19:325–331.
   Google Scholar
• Bacci M, Solomon SE, Mueller UG, Martins VG, Carvalho AOR, Vieira LGE, Silva-Pinhati ACO. 2009 Phylogeny of leafcutter ants in the genus Atta Fabricius (Formicidae: Attini) based on mitochondrial and nuclear DNA sequences. Molecular Phylogenetics and Evolution 51:427–437.
   PubMed Web of Science ®Google Scholar
• Cahan S, Julian GE. 1999. Fitness consequences of cooperative colony founding in the desert leaf-cutter ant Acromyrmex versicolor. Behavioral Ecology 10:585–591.
   Google Scholar
• Campbell MA, Ganley ARD, Gabaldón T, Cox MP. 2016. The case of the missing ancient fungal polyploids. American Naturalist 188:602–614.
   Web of Science ®Google Scholar
• Castle AJ, Horgan PA, Anderson JB. 1988. Crosses among homokaryons from commercial and wild-collected strains of the mushroom Agaricus brunnescens (= A. bisporus). Applied and Environmental Microbiology 54:1643–1648.
   Google Scholar
• Chapela IH, Rehner SA, Schultz TR, Mueller UG. 1994. Evolutionary history of the symbiosis between fungus-growing ants and their fungi. Science 266:1691–1694.
   PubMed Web of Science ®Google Scholar
• De Fine Licht HH, Andersen A, Aanen DK. 2005. Termitomyces sp. associated with the termite Macrotermes natalensis has a heterothallic mating system and multinucleate cells. Mycological Research 109:314– 318.
   Google Scholar
• De Fine Licht HH, Boomsma JJ. 2010. Forage collection, substrate preparation, and diet composition in fungus-growing ants. Ecological Entomology 35:259–269.
   Web of Science ®Google Scholar
• De Fine Licht HH, Boomsma JJ, Tunlid A. 2014. Symbiotic adaptations in the fungal cultivar of leaf-cutting ants. Nature Communications 5:5675.
   Google Scholar
• De Fine Licht HH, Schiøtt M, Mueller UG, Boomsma JJ. 2010. Evolutionary transitions in enzyme activity of ant fungus gardens. Evolution 64:2055–2069.
   Google Scholar
• De Fine Licht HH, Schiøtt M, Rogowska-Wrzesinska A, Nygaard S, Roepstorff P, Boomsma JJ. 2013. Laccase detoxification mediates the nutritional alliance between leaf-cutting ants and fungus-garden symbionts. Proceedings of the National Academy of Sciences of the United States of America 110:583–587.
   Google Scholar
• Della Lucia TMC. 2011. Formigas cortadeiras: da bioecologia ao manejo. Viçosa, Brasil: Editora Universidade Federal de Viçosa. 421 p.
   Google Scholar
• DeWoody JA, Schupp J, Kenefic L, Busch J, Murfitt L, Keim P. 2004. Universal method for producing ROX-labeled size standards suitable for automated genotyping. BioTechniques 37:348–352.
   Google Scholar
• Dias ES, Labory CRG, Herrera KMS, Alves AA, Torres GA, Rinker DL. 2008. Cytological studies of Agaricus brasiliensis. World Journal of Microbiology and Biotechnology 24:2473–2479.
   Google Scholar
• Gerardo NM, Mueller UG, Currie CR. 2006. Complex host-pathogen coevolution in the Apterostigma fungus-growing ant-microbe symbiosis. BMC Evolution Biology 6:88.
   Google Scholar
• Gladfelter A, Berman J. 2009. Dancing genomes: fungal nuclear positioning. Nature Reviews Microbiology 7:875–886.
   PubMed Web of Science ®Google Scholar
• Gladfelter AS, Hungerbuehler AK, Philippsen P. 2006. Asynchronous nuclear division cycles in multinucleated cells. Journal of Cell Biology 172:347–362.Green A, Adams RMM, Mueller UG. 2002. Extensive exchange of fungal cultivars between two sympatric species of fungus-growing ants. Molecular Ecology 11:191–195.
   Google Scholar
• Harder CB, Aanen DK. 2009. Unilateral nuclear migration in Basidiomycetes: pheromone interaction, genomic conflicts and mating-system reversion. Fungal Biology Reviews 23:48–54.
   Google Scholar
• Heim R. 1957. A propos du Rozites gongylophora A. Möller. Revue de Mycologie 22:293–299.
   Google Scholar
• Hervey A, Rogerson CT, Leong I. 1977. Studies on fungi cultivated by ants. Brittonia 29:226–236.
   Web of Science ®Google Scholar
• James TY. 2015. Why mushrooms have evolved to be so promiscuous: insights from evolutionary and ecological patterns. Fungal Biology Reviews 29:167–178.
   Google Scholar
• James TY, Stenlid J, Olson A, Johannesson H. 2008. Evolutionary significance of imbalanced nuclear ratios within heterokaryons of the basidiomycete fungus Heterobasidion parviporum. Evolution 62:2279–2296.
   PubMed Web of Science ®Google Scholar
• Kamzolkina O, Volkova V, Kozlova M, Pancheva E, Dyakov Yu, Callac P. 2006. Karyological evidence for meiosis in the three different types of life cycles existing in Agaricus bisporus. Mycologia 98:763–770.
   Web of Science ®Google Scholar
• Kerrigan RW, Baller LM, Horgen PA, Anderson JB. 1992. Strategies for the efficient recovery of Agaricus bisporus homokaryons. Mycologia 84:575–579.
   Web of Science ®Google Scholar
• Kondrashov AS. 1994. The asexual ploidy cycle and the origin of sex. Nature 370:213–216.
   PubMed Web of Science ®Google Scholar
• Kooij PW, Aanen DK, Schiøtt M, Boomsma JJ. 2015. Evolutionarily advanced ant farmers rear polyploid fungal crops. Journal of Evolutionary Biology 28:1911–1924.
   Web of Science ®Google Scholar
• Kreisel H. 1972. Pilze aus Pilzgärten von Atta insularis in Kuba. Journal of Basic Microbiology 12:643–654.
   Google Scholar
• Ma L-J, Ibrahim AS, Skory C, Grabherr MG, Burger G, Butler M, Elias M, et al. 2009. Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS Genetics 5:e1000549.
   PubMed Web of Science ®Google Scholar
• Marti HE, Carlson AL, Brown BV, Mueller UG. 2015. Foundress queen mortality and early colony growth of the leafcutter ant, Atta texana (Formicidae, Hymenoptera). Insectes Sociaux 62:357–363.
   Google Scholar
• McClaren M. 1970. Chemical dedikaryotization of Coprinus myceliocephalus (Agaricales). Canadian Journal of Botany 48:787–790.
   Google Scholar
• Meirelles LA, McFrederick QS, Rodrigues A, Mantovani JD, de Melo Rodovalho C, Ferreira CH, Bacci M, Mueller UG. 2016. Bacterial microbiomes from vertically-transmitted fungal inocula of the leaf-cutting ant Atta texana. Environmental Microbiology Reports 8:630–640.
   Google Scholar
• Mikheyev AS, Mueller UG, Abbott P. 2006. Cryptic sex and many-to-one co-evolution in the fungus-growing ant symbiosis. Proceedings of the National Academy of Sciences of the United States of America 103:10702–10706.
   Google Scholar
• Mikheyev AS, Mueller UG, Abbott P. 2010. Comparative dating of attine ant and lepiotaceous cultivar phylogenies reveals co-evolutionary synchrony and discord. American Naturalist 175:E126–E133.
   Google Scholar
• Mikheyev AS, Mueller UG, Boomsma JJ. 2007. Population genetic signatures of diffuse co-evolution between leaf-cutting ants and their cultivar fungi. Molecular Ecology 16:209–216.
   PubMedGoogle Scholar
• Mikheyev AS, Vo T, Mueller UG. 2008. Phylogeography of post-Pleistocene population expansion in a fungus-gardening ant and its microbial mutualists. Molecular Ecology 17:4480–4488.
   Google Scholar
• Miles PG, Raper JR. 1956. Recovery of the component strains from dikaryotic mycelia. Mycologia 48:484–494.
   Web of Science ®Google Scholar
• Mintzer AC. 1987. Primary polygyny in the ant Atta texana: number and weight of females and colony foundation success in the laboratory. Insectes Sociaux 34:108–117.
   Web of Science ®Google Scholar
• Mohali S. 1998. Ultrastructural study of the mutualistic fungus of the ant Atta cephalotes. Revista de Ecología Latinoamericana 5:1–6.
   Google Scholar
• Möller A. 1893. Die Pilzgärten einiger südamerikanischer Ameisen. Jena, Germany: Verlag Gustav Fisher. 127 p.Mueller UG. 2002. Ant versus fungus versus mutualism: ant-cultivar conflict and the deconstruction of the attine ant-fungus symbiosis. American Naturalist 160: S67–S98.
   Google Scholar
• Mueller UG. 2015. The attine ant-fungus mutualism. In: Bronstein JL, ed. Mutualism. Oxford, UK: Oxford University Press. p. 78–79.
   Google Scholar
• Mueller UG, Gerardo NM, Aanen D K, Six DL, Schultz TR. 2005. The evolution of agriculture in insects. Annual Review of Ecology, Evolution, and Systematics 36:563–595.
   Web of Science ®Google Scholar
• Mueller UG, Ishak HD, Bruschi SM, Smith CC, Herman JJ, Solomon SE, Mikheyev AS, Rabeling C, Scott JJ, Cooper M, Rodrigues A, Ortiz A, Brandão CRF, Lattke JE, Pagnocca FC, Rehner SA, Schultz TR, Vasconcelos HL, Adams RMM, Bollazzi M, Clark RM, Himler AG, LaPolla JS, Leal IR, Johnson RA, Roces F, Sosa-Calvo J, Wirth R, Bacci M Jr. 2017. Biogeography of mutualistic fungi cultivated by leafcutter ants. Molecular Ecology. 26:6921–6937.
   Google Scholar
• Mueller UG, Lipari SE, Milgroom MG. 1996. Amplified fragment length polymorphism (AFLP) fingerprinting of fungi cultured by the fungus-growing ant Cyphomyrmex minutus. Molecular Ecology 5:119–122.
   PubMed Web of Science ®Google Scholar
• Mueller UG, Mikheyev AS, Hong E, Sen R, Warren DL, Solomon SE, Ishak HD, Cooper M, Miller JL, Shaffer KA, Juenger TE. 2011a. Evolution of cold-tolerant fungal symbionts permits winter fungiculture by leafcutter ants at the northern frontier of a tropical ant-fungus symbiosis. Proceedings of the National Academy of Sciences of the United States of America 108:4053–4056.
   Google Scholar
• Mueller UG, Mikheyev AS, Solomon SE, Cooper M. 2011b. Frontier mutualism: coevolutionary patterns at the northern range limit of the leaf-cutter ant-fungus symbiosis. Proceedings of the Royal Society B: Biological Sciences 278:3050–3059.
   Google Scholar
• Mueller UG, Rehner SA, Schultz TD. 1998. The evolution of agriculture in ants. Science 281:2034–2038.
   PubMed Web of Science ®Google Scholar
• Mueller UG, Scott JJ, Ishak HD, Cooper M, Rodrigues A. 2010. Monoculture of leafcutter ant gardens. PLoS ONE 5:e12668.
   PubMed Web of Science ®Google Scholar
• Nobre T, Koopmanschap B, Baars JJP, Sonnenberg ASM, Aanen DK. 2014. The scope for nuclear selection within Termitomyces fungi associated with fungus-growing termites is limited. BMC Evolutionary Biology 14:121.
   Google Scholar
• Otto SP, Lenormand T. 2002. Resolving the paradox of sex and recombination. Nature Reviews Genetics 3:252–261.
   PubMed Web of Science ®Google Scholar
• Pagnocca FC, Bacci M, Fungaro MH, Bueno OC, Hebling MJ, Sant’Anna A, Capelari M. 2001. RAPD analysis of the sexual state and sterile mycelium of the fungus cultivated by the leaf-cutting ant Acromyrmex hispidus fallax. Mycological Research 105:173–176.
   Google Scholar
• Pontecorvo G. 1956. The parasexual cycle in fungi. Annual Review of Microbiology 10:393–400.
   PubMed Web of Science ®Google Scholar
• Preibisch S, Saalfeld S, Tomancak P. 2009. Globally optimal stitching of tiled 3D microscopic image acquisitions. Bioinformatics 25:1463–1465.
   PubMed Web of Science ®Google Scholar
• R Core Team. 2014. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. [cited 2017 Jul 01]. Available from: http://www.R-project.org
   Google Scholar
• Rissing SW, Pollock GB, Higgins MR, Hagen RH, Smith DR. 1989. Foraging specialization without relatedness or dominance among co-founding ant queens. Nature 338:420–422.
   Google Scholar
• Saksena KN, Marino R, Haller MN, Lemke PA. 1976. Study on development of Agaricus bisporus by fluorescent microscopy and scanning electron microscopy. Journal of Bacteriology 126:417–428.
   Google Scholar
• Scott JJ, Kweskin M, Cooper M, Mueller UG. 2009. Polymorphic microsatellite markers for the symbiotic fungi (Attamyces) cultivated by leaf-cutter ants (Attini, Formicidae). Molecular Ecology Resources 9:1391–1394.
   Google Scholar
• Seal JN, Gus J, Mueller UG. 2012. Fungus-gardening ants prefer native fungal species: do ants control their crops? Behavioral Ecology 23:1250–1256.
   Google Scholar
• Seal JN, Mueller UG. 2014a. Instability of novel ant-fungal associations constrains horizontal exchange of fungal symbionts. Evolutionary Ecology 28:157–176.
   Google Scholar
• Seal JN, Schiøtt M, Mueller UG. 2014b. Ant-fungal species combinations engineer physiological activity of fungus gardens. Journal of Experimental Biology 217:2540–2547.
   Google Scholar
• Sen R, Ishak HD, Kniffin TR, Mueller UG. 2010. Construction of chimaeric gardens through fungal intercropping: a symbiont choice experiment in the leafcutter ant Atta texana (Attini, Formicidae). Behavioral Ecology and Sociobiology 64:1125–1133.
   Google Scholar
• Shelest E, Voigt K. 2014. Genomics to study basal lineage fungal biology: phylogenomics suggests a common origin. In: Nowrousian M, ed. The Mycota XIII: fungal genomics. Berlin, Germany: Springer-Verlag. p. 31–60.
   Google Scholar
• Vo TL, Mikheyev AS, Mueller UG. 2009. Free-living fungal symbionts (Lepiotaceae) of fungus-growing ants (Attini: Formicidae). Mycologia 101:206–210.
   Web of Science ®Google Scholar
• Wang Y, Mueller UG, Clardy JC. 1999. Antifungal diketopiperazines from the symbiotic fungus of the fungus-growing ant Cyphomyrmex minutus. Journal of Chemical Ecology 25:935–941.
   Web of Science ®Google Scholar
• Weber NA. 1972. Gardening ants: the attines. Memoirs of the American Philosophical Society 92. Philadelphia, Pennsylvania: American Philosophical Society. 146 p.
   Google Scholar
• Zhao J, Chang ST. 1993. Monokaryotization by protoplasting heterothallic species of edible mushrooms. World Journal of Microbiology and Biotechnology 9:538–543.
   Web of Science ®Google Scholar