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Interaction specificity between leaf-cutting ants and vertically transmitted Pseudonocardia bacteria
- 作者:Sandra B Andersen (1) (2)
Sze Huei Yek (1) (3) David R Nash (1) Jacobus J Boomsma (1)
1. Centre for Social Evolution ; Department of Biology ; University of Copenhagen ; Universitetsparken 15 ; 2100 ; Copenhagen ; Denmark 2. Current address ; Novo Nordisk Foundation Center for Biosustainability ; Technical University of Denmark ; H酶rsholm ; Denmark 3. Current address ; Department of Genetics ; Forestry and Agricultural Biotechnology Institute (FABI) ; University of Pretoria ; Pretoria ; South Africa
- 关键词:Attine ant mutualism ; Cross ; fostering ; Prophylactic defences ; Host ; symbiont coevolution
- 刊名:BMC Evolutionary Biology
- 出版年:2015
- 出版时间:December 2015
- 年:2015
- 卷:15
- 期:1
- 全文大小:1,223 KB
- 参考文献:1. Herre, EA, Knowlton, N, Mueller, UG, Rehner, SA (1999) The evolution of mutualisms: exploring the paths between conflict and cooperation. Trends Ecol Evol 14: pp. 49-53 CrossRef
2. Queller, DC, Strassmann, JE (2009) Beyond society: the evolution of organismality. Philos Trans R Soc B-Biological Sci 364: pp. 3143-55 CrossRef 3. Telfer, S, Lambin, X, Birtles, R, Beldomenico, P, Burthe, S, Paterson, S (2010) Species interactions in a parasite community drive infection risk in a wildlife population. Science (80-) 330: pp. 243-6 CrossRef 4. Palmer, TM, Doak, DF, Stanton, ML, Bronstein, JL, Kiers, ET, Young, TP (2010) Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism. Proc Natl Acad Sci U S A 107: pp. 17234-9 CrossRef 5. Roode, JC, Pansini, R, Cheesman, SJ, Helinski, MEH, Huijben, S, Wargo, AR (2005) Virulence and competitive ability in genetically diverse malaria infections. Proc Natl Acad Sci U S A 102: pp. 7624-8 CrossRef 6. Qin, J, Li, R, Raes, J, Arumugam, M, Burgdorf, KS, Manichanh, C (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: pp. 59-65 CrossRef 7. Guimar茫es, PR, Jordano, P, Thompson, JN (2011) Evolution and coevolution in mutualistic networks. Ecol Lett 14: pp. 877-85 CrossRef 8. Mueller, UG, Gerardo, NM, Aanen, DK, Six, DL, Schultz, TR (2005) The evolution of agriculture in insects. Annu Rev Ecol Evol Syst 36: pp. 563-95 CrossRef 9. Mueller, UG, Rehner, SA, Schultz, TR (1998) The Evolution of Agriculture in Ants. Science (80-) 281: pp. 2034-8 CrossRef 10. Currie, CR, Bot, ANM, Boomsma, JJ (2003) Experimental evidence of a tripartite mutualism: bacteria protect ant fungus gardens from specialized parasites. Oikos 101: pp. 91-102 CrossRef 11. Mehdiabadi, NJ, Hughes, B, Mueller, UG (2006) Cooperation, conflict, and coevolution in the attine ant-fungus symbiosis. Behav Ecol 17: pp. 291-6 CrossRef 12. Poulsen, M, Boomsma, JJ (2005) Mutualistic fungi control crop diversity in fungus-growing ants. Science (80-) 307: pp. 741-4 CrossRef 13. Ivens, ABF, Nash, DR, Poulsen, M, Boomsma, JJ (2009) Caste-specific symbiont policing by workers of Acromyrmex fungus-growing ants. Behav Ecol 20: pp. 378-84 CrossRef 14. Mueller, UG, Scott, JJ, Ishak, HD, Cooper, M, Rodrigues, A (2010) Monoculture of leafcutter ant gardens. PLoS One 5: pp. e12668 CrossRef 15. Schultz, TR, Brady, SG (2008) Major evolutionary transitions in ant agriculture. Proc Natl Acad Sci 105: pp. 5435-40 CrossRef 16. Holldobler, B, Wilson, EO (1990) The ants. CrossRef 17. Currie, CR, Scott, JA, Summerbell, RC, Malloch, D (1999) Fungus-growing ants use antibiotic-producing bacteria to control garden parasites. Nature 398: pp. 701-4 CrossRef 18. Little, AEF, Currie, CR (2007) Symbiotic complexity: discovery of a fifth symbiont in the attine ant-microbe symbiosis. Biol Lett 3: pp. 501-4 CrossRef 19. 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: pp. 78-92 CrossRef 20. Currie, CR, Wong, B, Stuart, AE, Schultz, TR, Rehner, SA, Mueller, UG (2003) Ancient tripartite coevolution in the attine ant-microbe symbiosis. Science (80-) 299: pp. 386-8 CrossRef 21. Yek SH, Boomsma JJ, Poulsen M. Towards a better understanding of the evolution of specialized parasites of fungus-growing ant crops. Psyche (Stuttg) 2012. Article ID 239392. 22. Currie, CR, Poulsen, M, Mendenhall, J, Boomsma, JJ, Billen, J (2006) Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants. Science (80-) 311: pp. 81-3 CrossRef 23. Fern谩ndez-Mar铆n, H, Zimmerman, JK, Nash, DR, Boomsma, JJ, Wcislo, WT (2009) Reduced biological control and enhanced chemical pest management in the evolution of fungus farming in ants. Proc R Soc B Biol Sci 276: pp. 2263-9 CrossRef 24. Fern谩ndez-Mar铆n, H, Bruner, G, Gomez, EB, Nash, DR, Boomsma, JJ, Wcislo, WT (2013) Dynamic disease management in Trachymyrmex fungus-growing ants (Attini: Formicidae). Am Nat 181: pp. 571-82 CrossRef 25. Kost, C, Lakatos, T, B枚ttcher, I, Arendholz, W-R, Redenbach, M, Wirth, R (2007) Non-specific association between filamentous bacteria and fungus-growing ants. Naturwissenschaften 94: pp. 821-8 CrossRef 26. Mueller, UG, Dash, D, Rabeling, C, Rodrigues, A, Brown, J (2008) Coevolution between attine ants and actinomycete bacteria: a reevaluation. Evolution (N Y) 62: pp. 2894-912 27. Haeder, S, Wirth, R, Herz, H, Spiteller, D (2009) Candicidin-producing Streptomyces support leaf-cutting ants to protect their fungus garden against the pathogenic fungus Escovopsis. Proc Natl Acad Sci 106: pp. 4742-6 CrossRef 28. Sen, R, Ishak, HD, Estrada, D, Dowd, SE, Hong, E, Mueller, UG (2009) Generalized antifungal activity and 454-screening of Pseudonocardia and Amycolatopsis bacteria in nests of fungus-growing ants. Proc Natl Acad Sci 106: pp. 17805-10 CrossRef 29. Barke, J, Seipke, R, Gruschow, S, Heavens, D, Drou, N, Bibb, M (2010) A mixed community of actinomycetes produce multiple antibiotics for the fungus farming ant Acromyrmex octospinosus. BMC Biol 8: pp. 109 CrossRef 30. Cafaro, MJ, Poulsen, M, Little, AEF, Price, SL, Gerardo, NM, Wong, B (2011) Specificity in the symbiotic association between fungus-growing ants and protective Pseudonocardia bacteria. Proc R Soc B Biol Sci 278: pp. 1814-22 CrossRef 31. Ishak HD, Miller JL, Sen R, Dowd SE, Meyer E, Mueller UG. Microbiomes of ant castes implicate new microbial roles in the fungus-growing ant Trachymyrmex septentrionalis. / Sci Rep 2011: article number 204. 32. Zucchi, TD, Guidolin, AS, C么nsoli, FL (2011) Isolation and characterization of actinobacteria ectosymbionts from Acromyrmex subterraneus brunneus (Hymenoptera, Formicidae). Microbiol Res 166: pp. 68-76 CrossRef 33. Andersen, SB, Hansen, LH, Sapountzis, P, S酶rensen, SJ, Boomsma, JJ (2013) Specificity and stability of the Acromyrmex-Pseudonocardia symbiosis. Mol Ecol 22: pp. 4307-21 CrossRef 34. Poulsen, M, Bot, ANM, Currie, CR, Nielsen, MG, Boomsma, JJ (2003) Within-colony transmission and the cost of a mutualistic bacterium in the leaf-cutting ant Acromyrmex octospinosus. Funct Ecol 17: pp. 260-9 CrossRef 35. Mattoso, TC, Moreira, DDO, Samuels, RI (2011) Symbiotic bacteria on the cuticle of the leaf-cutting ant Acromyrmex subterraneus subterraneus protect workers from attack by entomopathogenic fungi. Biol Lett 8: pp. 461-4 CrossRef 36. Poulsen, M, Cafaro, MJ, Erhardt, DP, Little, AEF, Gerardo, NM, Tebbets, B (2010) Variation in Pseudonocardia antibiotic defence helps govern parasite-induced morbidity in Acromyrmex leaf-cutting ants. Environ Microbiol Rep 2: pp. 534-40 CrossRef 37. Poulsen, M, Cafaro, M, Boomsma, JJ, Currie, CR (2005) Specificity of the mutualistic association between actinomycete bacteria and two sympatric species of Acromyrmex leaf-cutting ants. Mol Ecol 14: pp. 3597-604 CrossRef 38. Poulsen, M, Bot, ANM, Boomsma, JJ (2003) The effect of metapleural gland secretion on the growth of a mutualistic bacterium on the cuticle of leaf-cutting ants. Naturwissenschaften 90: pp. 406-9 CrossRef 39. Schoenian, I, Spiteller, M, Ghaste, M, Wirth, R, Herz, H, Spiteller, D (2011) Chemical basis of the synergism and antagonism in microbial communities in the nests of leaf-cutting ants. Proc Natl Acad Sci U S A 108: pp. 1955-60 CrossRef 40. Seipke, RF, Barke, J, Brearley, C, Hill, L, Yu, DW, Goss, RJM (2011) A single Streptomyces symbiont makes multiple antifungals to support the fungus farming ant Acromyrmex octospinosus. PLoS One 6: pp. e22028 CrossRef 41. Scheuring, I, Yu, DW (2012) How to assemble a beneficial microbiome in three easy steps. Ecol Lett 15: pp. 1300-7 CrossRef 42. Armitage, SAO, Broch, JF, Mar铆n, HF, Nash, DR, Boomsma, JJ (2011) Immune defense in leaf-cutting ants: a cross-fostering approach. Evolution (N Y) 65: pp. 1791-9 43. Zhang, MM, Poulsen, M, Currie, CR (2007) Symbiont recognition of mutualistic bacteria by Acromyrmex leaf-cutting ants. ISME J 1: pp. 313-20 44. Mueller, U, Ishak, H, Lee, J, Sen, R, Gutell, R (2010) Placement of attine ant-associated Pseudonocardia in a global Pseudonocardia phylogeny (Pseudonocardiaceae, Actinomycetales): a test of two symbiont-association models. Antonie Van Leeuwenhoek 98: pp. 195-212 CrossRef 45. Caldera, EJ, Currie, CR (2012) The population structure of antibiotic-producing bacterial symbionts of Apterostigma dentigerum ants: impacts of coevolution and multipartite symbiosis. Am Nat 180: pp. 604-17 CrossRef 46. Armitage, SAO, Fern谩ndez-Mar铆n, H, Wcislo, WT, Boomsma, JJ (2012) An evaluation of the possible adaptive function of fungal brood covering by attine ants. Evolution (N Y) 66: pp. 1966-75 47. Marsh, SE, Poulsen, M, Pinto-Tom谩s, A, Currie, CR (2014) Interaction between workers during a short time window is required for bacterial symbiont transmission in Acromyrmex leaf-cutting ants. PLoS One 9: pp. e103269 CrossRef 48. Currie, CC, Stuart, AE (2001) Weeding and grooming of pathogens in agriculture by ants. Proc R Soc B Biol Sci 268: pp. 1033-9 CrossRef 49. Abramowski, D, Currie, CR, Poulsen, M (2010) Caste specialization in behavioral defenses against fungus garden parasites in Acromyrmex octospinosus leaf-cutting ants. Insectes Soc 58: pp. 65-75 CrossRef 50. Currie, CR, Mueller, UG, Malloch, D (1999) The agricultural pathology of ant fungus gardens. Proc Natl Acad Sci U S A 96: pp. 7998-8002 CrossRef 51. Gerardo, NM, Mueller, UG, Price, SL, Currie, CR (2004) Exploiting a mutualism: parasite specialization on cultivars within the fungus-growing ant symbiosis. Proc Biol Sci 271: pp. 1791-8 CrossRef 52. Gerardo, NM, Jacobs, SR, Currie, CR, Mueller, UG (2006) Ancient host-pathogen associations maintained by specificity of chemotaxis and antibiosis. Plos Biol 4: pp. 1358-63 CrossRef 53. Mikheyev, AS, Mueller, UG, Abbot, P (2010) Comparative dating of attine ant and lepiotaceous cultivar phylogenies reveals coevolutionary synchrony and discord. Am Nat 175: pp. E126-33 CrossRef 54. Oh, D-C, Poulsen, M, Currie, CR, Clardy, J (2009) Dentigerumycin: a bacterial mediator of an ant-fungus symbiosis. Nat Chem Biol 5: pp. 391-3 CrossRef 55. Brockmann, HJ, Grafen, A, Dawkins, R (1979) Evolutionarily stable nesting strategy in a digger wasp. J Theor Biol 77: pp. 473-96 CrossRef 56. Poulsen, M, Bot, ANM, Currie, CR, Boomsma, JJ (2002) Mutualistic bacteria and a possible trade-off between alternative defence mechanisms in Acromyrmex leaf-cutting ants. Insectes Soc 49: pp. 15-9 CrossRef 57. Andersen SB, Yek SH, Nash DR, Boomsma JJ. JJData from: Interaction specificity between leaf-cutting ants and vertically transmitted Pseudonocardia bacteria. Dryad Digital Repository 2015. dx.doi.org/10.5061/dryad.53vg0. 58. Muchovej, JJ, Della Lucia, TM (1990) Escovopsis, a new genus from leaf cutting ant nests to replace Phialocladus nomem invalidum. Mycotaxon 37: pp. 191-5 59. Bot, ANM, Currie, CR, Hart, AG, Boomsma, JJ (2001) Waste management in leaf-cutting ants. Ethol Ecol Evol 13: pp. 225-37 CrossRef 60. Fern谩ndez-Mar铆n, H, Zimmermann, JK, Wcislo, WT (2003) Nest-founding in Acromyrmex octospinosus (Hymenoptera, Formicidae, Attini): demography and putative prophylactic behaviors. Insectes Soc 50: pp. 304-8 CrossRef 61. Faul, F, Erdfelder, E, Buchner, A, Lang, A-G (2009) Statistical power analyses using G*Power 3.1: tests for correlation and regression analyses. Behav Res Methods 41: pp. 1149-60 CrossRef 62. Cohen J. Statistical Power Analysis for the Behavioral Sciences. L. Erlbaum Associates; 1969:273-406. 63. Joliffe, IT (1972) Discarding variables in a principal component analysis I: artificial data. Appl Stat 21: pp. 160-73 CrossRef
- 刊物主题:Evolutionary Biology; Animal Systematics/Taxonomy/Biogeography; Entomology; Genetics and Population Dynamics; Life Sciences, general;
- 出版者:BioMed Central
- ISSN:1471-2148
文摘
Background The obligate mutualism between fungus-growing ants and microbial symbionts offers excellent opportunities to study the specificity and stability of multi-species interactions. In addition to cultivating fungus gardens, these ants have domesticated actinomycete bacteria to defend gardens against the fungal parasite Escovopsis and possibly other pathogens. Panamanian Acromyrmex echinatior leaf-cutting ants primarily associate with actinomycetes of the genus Pseudonocardia. Colonies are inoculated with one of two vertically transmitted phylotypes (Ps1 or Ps2), and maintain the same phylotype over their lifetime. We performed a cross-fostering experiment to test whether co-adaptations between ants and bacterial phylotypes have evolved, and how this affects bacterial growth and ant prophylactic behavior after infection with Escovopsis. Results We show that Pseudonocardia readily colonized ants irrespective of their colony of origin, but that the Ps2 phylotype, which was previously shown to be better able to maintain its monocultural integrity after workers became foragers than Ps1, reached a higher final cover when grown on its native host than on alternative hosts. The frequencies of major grooming and weeding behaviors co-varied with symbiont/host combinations, showing that ant behavior also was affected when cuticular actinomycete phylotypes were swapped. Conclusion These results show that the interactions between leaf-cutting ants and Pseudonocardia bear signatures of mutual co-adaptation within a single ant population.
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