Repeated Evolution of Fungal Cultivar Specificity in Independently Evolved Ant-Plant-Fungus Symbioses

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Blatrix, Rumsaïs ^a   Debaud, Sarah ^a   Salas Lopez, Alex ^a   Born, Céline ^a   Benoit, Laure ^a   McKey, Doyle B ^a,b   Attéké, Christiane ^c   Djiéto Lordon, Champlain ^d  

^a CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^b INSTITUT UNIVERSITAIRE DE FRANCE   (France)

^c UNIVERSITÉ DES SCIENCES ET TECHNIQUES DE MASUKU   (Gabon)

^d UNIVERSITY OF YAOUNDÉ I   (Cameroon)

Author keywords

[No Author keywords available]

Indexed keywords

INTERNAL TRANSCRIBED SPACER; RIBOSOME DNA;

AGRICULTURE; ANT; APHOMOMYRMEX AFER; ARTICLE; BARTERIA FISTULOSA; CHAETOTHYRIALES; CULTIVAR; DNA BARCODING; FUNGAL COMMUNITY; FUNGUS; FUNGUS HYPHAE; HABITAT PATCHINESS; LEONARDOXA AFRICANA; LEONARDOXA LETOUZEYI; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PETALOMYRMEX PHYLAX; PLANT INSECT INTERACTION; SEQUENCE ANALYSIS; SPECIES DIFFERENCE; SPECIES DISTRIBUTION; SPECIES IDENTIFICATION; SYMBIONT; TAXON; TETRAPONERA AETHIOPS;

AFRICA; ANIMALS; ANTS; ASCOMYCOTA; BIOLOGICAL EVOLUTION; DNA, FUNGAL; DNA, INTERGENIC; DNA, RIBOSOMAL; FABACEAE; PHYLOGENY; PHYLOGEOGRAPHY; SYMBIOSIS;

EID: 84880842819     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068101     Document Type: Article

References (55)

1. Davidson DW, McKey D, (1993) The evolutionary ecology of symbiotic ant-plant relationships. J Hymenopt Res 2: 13-83.
2. McKey D, Gaume L, Brouat C, Di Giusto B, Pascal L, et al. (2005) The trophic structure of tropical ant-plant-herbivore interactions: community consequences and coevolutionary dynamics. In: Burslem D, Pinard M, Hartley S, editors. Biotic interactions in the tropics: their role in the maintenance of species diversity. Cambridge: Cambridge University Press. pp. 386-413.
3. Frederickson ME, Greene MJ, Gordon DM, (2005) "Devil's gardens" bedevilled by ants. Nature 437: 495-496.
4. Letourneau DK, (1998) Ants, stem-borers, and fungal pathogens: experimental tests of a fitness advantage in Piper ant-plants. Ecology 79: 593-603.
5. Rosumek FB, Silveira FAO, Neves FD, Barbosa NPD, Diniz L, et al. (2009) Ants on plants: a meta-analysis of the role of ants as plant biotic defenses. Oecologia 160: 537-549.
6. Rico-Gray V, Oliveira PS (2007) The ecology and evolution of ant-plant interactions. Chicago: The University of Chicago Press. 331 p.
7. Blatrix R, Bouamer S, Morand S, Selosse MA, (2009) Ant-plant mutualisms should be viewed as symbiotic communities. Plant Signal Behav 4: 554-556.
8. Eilmus S, Heil M, (2009) Bacterial associates of arboreal ants and their putative functions in an obligate ant-plant mutualism. Appl Environ Microbiol 75: 4324-4332.
9. Gullan PJ (1997) Relationships with ants. In: Ben-Dov Y, Hodgson CJ, editors. Soft scale insects: their biology, natural enemies and control. Amsterdam: Elsevier Science. pp. 351-373.
10. Voglmayr H, Mayer V, Maschwitz U, Moog J, Djiéto-Lordon C, et al. (2011) The diversity of ant-associated black yeasts: Insights into a newly discovered world of symbiotic interactions. Fungal Biol 115: 1077-1091.
11. Rezende EL, Lavabre JE, Guimaraes PR, Jordano P, Bascompte J, (2007) Non-random coextinctions in phylogenetically structured mutualistic networks. Nature 448: 925-926.
12. Vazquez DP, Bluthgen N, Cagnolo L, Chacoff NP, (2009) Uniting pattern and process in plant-animal mutualistic networks: a review. Ann Bot 103: 1445-1457.
13. Bailey IW, (1920) Some relations between ants and fungi. Ecology 1: 174-189.
14. Janzen DH, (1972) Protection of Barteria (Passifloraceae) by Pachysima ants (Pseudomyrmecinae) in a Nigerian rain-forest. Ecology 53: 885-892.
15. Miehe H, (1911) Untersuchungen über die javanische Myrmecodia. Abhandl Math Phys Kl K Säch Gesell Wiss 32: 312-361.
16. Blatrix R, Djiéto-Lordon C, Mondolot L, La Fisca P, Voglmayr H, et al. (2012) Plant-ants use symbiotic fungi as a food source: new insight into the nutritional ecology of ant-plant interactions. Proc R Soc B 279: 3940-3947.
17. Defossez E, Selosse MA, Dubois MP, Mondolot L, Faccio A, et al. (2009) Ant-plants and fungi: a new threeway symbiosis. New Phytol 182: 942-949.
18. Defossez E, Djiéto-Lordon C, McKey D, Selosse MA, Blatrix R, (2011) Plant-ants feed their host plant, but above all a fungal symbiont to recycle nitrogen. Proc R Soc B 278: 1419-1426.
19. Mueller UG, Gerardo NM, Aanen DK, Six DL, Schultz TR, (2005) The evolution of agriculture in insects. Annu Rev Ecol Evol Syst 36: 563-595.
20. Hata H, Kato M, (2006) A novel obligate cultivation mutualism between damselfish and Polysiphonia algae. Biol Lett 2: 593-596.
21. Silliman BR, Newell SY, (2003) Fungal farming in a snail. Proc Natl Acad Sci U S A 100: 15643-15648.
22. Heath JJ, Stireman JO III, (2010) Dissecting the association between a gall midge, Asteromyia carbonifera, and its symbiotic fungus, Botryosphaeria dothidea. Entomol Exp Appl 137: 36-49.
23. Lauth J, Ruiz-Gonzalez MX, Orivel J, (2011) New findings in insect fungiculture. Have ants developed non-food, agricultural products? Commun Integr Biol 4: 728-730.
24. Mayer VE, Voglmayr H, (2009) Mycelial carton galleries of Azteca brevis (Formicidae) as a multi-species network. Proc R Soc B 276: 3265-3273.
25. McKey D, (2000) Leonardoxa africana (Leguminosae: Caesalpinioideae): a complex of mostly allopatric subspecies. Adansonia 22: 71-109.
26. Gaume L, McKey D, Terrin S, (1998) Ant-plant-homopteran mutualism: how the third partner affects the interaction between a plant-specialist ant and its myrmecophyte host. Proc R Soc Lond B 265: 569-575.
27. Breteler FJ, (1999) Barteria Hook. f. (Passifloraceae) revised. Adansonia 21: 306-318.
28. Peccoud J, Piatscheck F, Yockteng R, Garcia M, Sauve M, et al. (2013) Multi-locus phylogenies of the genus Barteria (Passifloraceae) portray complex patterns in the evolution of myrmecophytism. Mol Phylogenet Evol 66: 824-832.
29. Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, et al. (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proc Natl Acad Sci U S A 109: 6241-6246.
30. Gardes M, Bruns TD, (1993) ITS primers with enhanced specificity for basidiomycetes- Application to the identification of mycorrhizae and rusts. Mol Ecol 2: 113-118.
31. White TJ, Bruns TD, 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, editors. PCR protocols: a guide to methods and applications. San Diego: Academic Press. pp. 315-322.
32. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
33. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307-321.
34. Blaxter M, Mann J, Chapman T, Thomas F, Whitton C, et al. (2005) Defining operational taxonomic units using DNA barcode data. Philosophical Transactions of the Royal Society B-Biological Sciences 360: 1935-1943.
35. Nilsson RH, Kristiansson E, Ryberg M, Hallenberg N, Larsson KH, (2008) Intraspecific ITS variability in the kingdom Fungi as expressed in the international sequence databases and its implications for molecular species identification. Evol Bioinform 4: 193-201.
36. Ruiz-González MX, Male PJG, Leroy C, Dejean A, Gryta H, et al. (2011) Specific, non-nutritional association between an ascomycete fungus and Allomerus plant-ants. Biol Lett 7: 475-479.
37. Mueller UG, Scott JJ, Ishak HD, Cooper M, Rodrigues A, (2010) Monoculture of leafcutter ant gardens. Plos One 5.
38. Silva-Pinhati ACO, Bacci M, Hinkle G, Sogin ML, Pagnocca FC, et al. (2004) Low variation in ribosomal DNA and internal transcribed spacers of the symbiotic fungi of leaf-cutting ants (Attini: Formicidae). Braz J Med Biol Res 37: 1463-1472.
39. Green AM, Mueller UG, Adams RMM, (2002) Extensive exchange of fungal cultivars between sympatric species of fungus-growing ants. Mol Ecol 11: 191-195.
40. Mueller UG, Rehner SA, Schultz TR, (1998) The evolution of agriculture in ants. Science 281: 2034-2038.
41. Aanen DK, Eggleton P, Rouland-Lefevre C, Guldberg-Froslev T, Rosendahl S, et al. (2002) The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proc Natl Acad Sci U S A 99: 14887-14892.
42. Aanen DK, Licht HHD, Debets AJM, Kerstes NAG, Hoekstra RF, et al. (2009) High symbiont relatedness stabilizes mutualistic cooperation in fungus-growing termites. Science 326: 1103-1106.
43. Poulsen M, Boomsma JJ, (2005) Mutualistic fungi control crop diversity in fungus-growing ants. Science 307: 741-744.
44. Batra LR, (1966) Ambrosia fungi: extent of specificity to ambrosia beetles. Science 153: 193-195.
45. Haanstad JO, Norris DM, (1985) Microbial symbiotes of the ambrosia beetle Xyloterinus politus. Microb Ecol 11: 267-276.
46. Batra LR, (1985) Ambrosia beetles and their associated fungi: research trends and techniques. Proc Indian Acad Sci (Plant Sci) 94: 137-148.
47. Caldera EJ, Poulsen M, Suen G, Currie CR, (2009) Insect symbioses: a case study of past, present, and future fungus-growing ant research. Environ Entomol 38: 78-92.
48. Barke J, Seipke RF, Gruschow S, Heavens D, Drou N, et al. (2010) A mixed community of actinomycetes produce multiple antibiotics for the fungus farming ant Acromyrmex octospinosus. BMC Biol 8: 109.
49. Mueller UG, (2012) Symbiont recruitment versus ant-symbiont co-evolution in the attine ant-microbe symbiosis. Curr Opin Microbiol 15: 269-277.
50. Sen R, Ishak HD, Estrada D, Dowd SE, Hong EK, et al. (2009) Generalized antifungal activity and 454-screening of Pseudonocardia and Amycolatopsis bacteria in nests of fungus-growing ants. Proc Natl Acad Sci U S A 106: 17805-17810.
51. 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.
52. Mueller UG, (2002) Ant versus fungus versus mutualism: ant-cultivar conflict and the deconstruction of the attine ant-fungus symbiosis. Am Nat 160, supplement: S67-S98.
53. Mikheyev AS, Mueller UG, Abbot P, (2006) Cryptic sex and many-to-one colevolution in the fungus-growing ant symbiosis. Proc Natl Acad Sci U S A 103: 10702-10706.
54. Yumoto T, Maruhashi T, (1999) Pruning behavior and intercolony competition of Tetraponera (Pachysima) aethiops (Pseudomyrmecinae, Hymenoptera) in Barteria fistulosa in a tropical forest, Democratic Republic of Congo. Ecol Res 14: 393-404.
55. Gebhardt H, Bergerow D, Oberwinkler F, (2004) Identification of the ambrosia fungus of Xyleborus monographus and X. dryographus (Curculionidae, Scolytinae). Mycol Prog 3: 95-101.