Evolutionary criteria outperform operational approaches in producing ecologically relevant fungal species inventories

Molecular Ecology

Volumn 20, Issue 3, 2011, Pages 655-666

  Powell, Jeff R ^a   Monaghan, Michael T ^b   Öpik, Maarja ^c   Rillig, Matthias C ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

^c UNIVERSITY OF TARTU   (Estonia)

Author keywords

arbuscular mycorrhizal fungi; biodiversity; coalescent; GMYC model; operational taxonomic unit

Indexed keywords

FUNGAL DNA; FUNGAL RNA; RIBOSOME DNA; RNA 18S;

ARTICLE; BIODIVERSITY; BIOLOGICAL MODEL; BIOLOGY; CHEMISTRY; CLASSIFICATION; CLUSTER ANALYSIS; DNA SEQUENCE; ECUADOR; ESTONIA; EVOLUTION; FUNGUS; GENETIC VARIABILITY; GENETICS; METHODOLOGY; PHYLOGENY; SPECIES DIFFERENCE; SPECIES DIFFERENTIATION; STATISTICAL MODEL; TIME;

BIODIVERSITY; BIOLOGICAL EVOLUTION; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; DNA, FUNGAL; DNA, RIBOSOMAL; ECUADOR; ESTONIA; FUNGI; GENETIC SPECIATION; GENETIC VARIATION; LIKELIHOOD FUNCTIONS; MODELS, GENETIC; PHYLOGENY; RNA, FUNGAL; RNA, RIBOSOMAL, 18S; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; TIME FACTORS;

ARBUSCULAR; FUNGI; OTUS;

EID: 78751671066     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2010.04964.x     Document Type: Article

References (75)

1. Ahrens D, Monaghan MT, Vogler AP, (2007) DNA-based taxonomy for associating adults and larvae in multi-species assemblages of chafers (Coleoptera: Scarabaeidae). Molecular Phylogenetics and Evolution, 44, 436-449.
2. Barraclough TG, Hughes M, Ashford-Hodges N, Fujisawa T, (2009) Inferring evolutionarily significant units of bacterial diversity from broad environmental surveys of single-locus data. Biology Letters, 5, 425-428.
3. Birõ I, Takács T, (2007) Effects of Glomus mosseae strains of different origin on plant macro and micronutrient uptake in Cd-polluted and unpolluted soils. Acta Agronomica Hungarica, 55, 183-192.
4. Birõ I, Németha T, Takács T, (2009) Changes of parameters of infectivity and efficiency of different Glomus mosseae arbuscular mycorrhizal fungi strains in cadmium-loaded soils. Communications in Soil Science and Plant Analysis, 40, 227-239.
5. Bode S, Adolfsson S, Lamatsch D, et al. (2010) Exceptional cryptic diversity and multiple origins of parthenogenesis in a freshwater ostracod. Molecular Phylogenetics and Evolution, 54, 542-552.
6. Clapp JP, Fitter AH, Young JPW, (1999) Ribosomal small subunit sequence variation within 19 spores of an arbuscular mycorrhizal fungus, Scutellospora sp. Molecular Ecology, 8, 915-921.
7. Clapp JP, Rodriguez A, Dodd JC, (2001) Inter- and intra-isolate rRNA large subunit variation in Glomus coronatum spores. New Phytologist, 149, 539-554.
8. Croll D, Sanders, IR, (2009) Recombination in Glomus intraradices, a supposed ancient asexual arbuscular mycorrhizal fungus. BMC Evolutionary Biology, 9, 13.
9. Croll D, Wille L, Gamper HA, et al. (2008). Genetic diversity and host plant preferences revealed by simple sequence repeat and mitochondrial markers in a population of the arbuscular mycorrhizal fungus Glomus intraradices. New Phytologist, 178, 672-687.
10. Croll D, Giovannetti M, Koch AM, et al. (2009) Nonself vegetative fusion and genetic exchange in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytologist, 181, 924-937.
11. Dray S, Dufour AB, (2007) The ade4 package: implementing the duality diagram for ecologists. Journal of Statistical Software, 22, 1-22.
12. Drummond A, Rambaut A, (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.
13. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high through put. Nucleic Acids Research, 32, 1792-1797.
14. Ehinger M, Koch AM, Sanders IR, (2009) Changes in arbuscular mycorrhizal fungal phenotypes and genotypes in response to plant species identity and phosphorus concentration. New Phytologist, 184, 412-423.
15. Ezard T, Fujisawa T, Barraclough T, (2009) splits: SPecies' LImits by Threshold Statistics. Rpackage version 1.0-11/r29. Available from.
16. Fontaneto D, Herniou EA, Boschetti C, et al. (2007) Independently evolving species in asexual bdelloid rotifers. PLoS Biology, 5, e87.
17. Fraser C, Alm EJ, Polz MF, Spratt BG, Hanage WP, (2009) The bacterial species challenge: making sense of genetic and ecological diversity. Science, 323, 741-746.
18. Gevers D, Cohan FM, Lawrence JG, et al. (2005) Opinion: re-evaluating prokaryotic species. Nature Reviews Microbiology, 3, 733-739.
19. Giovannetti M, Azzolini D, Citernesi AS, (1999) Anastomosis formation and nuclear and proto plasmic exchange in arbuscular mycorrhizal fungi. Applied and Environmental Microbiology, 65, 5571-5575.
20. Hanage WP, Fraser C, Spratt BG, (2006) Sequences, sequence clusters and bacterial species. Philosophical Transactions of the Royal Society B: Biological Sciences, 361, 1917-1927.
21. Hart MM, Reader RJ, (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytologist, 153, 335-344.
22. Hart M, Reader R, Klironomos J, (2003) Plant coexistence mediated by arbuscular mycorrhizal fungi. Trends in Ecology & Evolution, 18, 418-423.
23. Haug I, Wubet T, Weiß M, et al. (2010) Species-rich but distinct arbuscular mycorrhizal communities in reforestation plots on degraded pastures and in neighboring pristine tropical mountain rain forest. Tropical Ecology, 51, 125-148.
24. van der Heijden MGA, Klironomos JN, Ursic M, et al. (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature, 396, 69-72.
25. Helgason T, Daniell TJ, Husband R, Fitter AH, Young JPW, (1998) Ploughing up the wood-wide web ? Nature, 394, 431.
26. Hibbett DS, Ohman A, Kirk PM, (2009) Fungal ecology catches fire. New Phytologist, 184, 279-282.
27. Hill MO, Smith AJE, (1976) Principal component analysis of taxonomic data with multi-state discrete characters. Taxon, 25, 249-255.
28. Jany J, Pawlowska TE, (2010) Multinucleate spores contribute to evolutionary longevity of asexual Glomeromycota. The American Naturalist, 175, 424-435.
29. Johnson NC, (2010) Resource stoichiometry elucidates the structure and function of arbuscular mycorrhizas across scales. New Phytologist, 185, 631-647.
30. Johnson NC, Tilman D, Wedin D, (1992) Plant and soil controls on mycorrhizal fungal communities. Ecology, 73, 2034-2042.
31. Johnson D, IJdo M, Genney DR, Anderson IC, Alexander IJ, (2005) How do plants regulate the function, community structure, and diversity of mycorrhizal fungi ? Journal of Experimental Botany, 56, 1751-1760.
32. Jousselin E, Desdevises Y, Coeur d'acier A, (2009) Fine-scale cospeciation between Brachycaudus and Buchnera aphidicola: bacterial genome helps define species and evolutionary relationships in aphids. Proceedings of the Royal Society B: Biological Sciences, 276, 187-196.
33. Kingman JFC, (1982) On the genealogy of large populations. Journal of Applied Probability, 19, 27-43.
34. Klironomos JN, McCune J, Hart M, Neville J, (2000) The influence of arbuscular mycorrhizae on the relationship between plant diversity and productivity. Ecology Letters, 3, 137-141.
35. Koch AM, Kuhn G, Fontanillas P, Fumagalli L, Goudet J, Sanders IR, (2004) High genetic variability and low local diversity in a population of arbuscular mycorrhizal fungi. Proceedings of the National Academy of Sciences of the United States of America, 101, 2369-2374.
36. Koch AM, Croll D, Sanders, IR, (2006) Genetic variability in a population of arbuscular mycorrhizal fungi causes variation in plant growth. Ecology Letters, 9, 103-110.
37. Koeppel A, Perry EB, Sikorski J, et al. (2008) Identifying the fundamental units of bacterial diversity: a paradigm shift to incorporate ecology into bacterial systematics. Proceedings of the National Academy of Sciences of the United States of America, 105, 2504-2509.
38. Kottke I, Haug I, Setaro S, et al. (2008) Guilds of mycorrhizal fungi and their relation to trees, ericads, orchids and liverworts in a neotropical mountain rain forest. Basic and Applied Ecology, 9, 13-23.
39. Legendre P, Anderson MJ, (1999) Distance-based redundancy analysis: testing multispecies esponses in multifactorial ecological experiments. Ecological Monographs, 69, 1-24.
40. Leliaert F, Verbruggen H, Wysor B, De Clerck O, (2009) DNA taxonomy in morphologically plastic taxa: algorithmic species delimitation in the Boodlea complex (Chlorophyta: Cladophorales). Molecular Phylogenetics and Evolution, 53, 122-133.
41. Liesack W, Stackebrandt E, (1992) Unculturable microbes detected by molecular sequences and probes. Biodiversity and Conservation, 1, 250-262.
42. Maherali H, Klironomos JN, (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Science, 316, 1746-1748.
43. McQuarrie ADR, Tsai C, (1998) Regression and Time Series Model Selection. World Scientific, Singapore.
44. Monaghan MT, Wild R, Elliot M, et al. (2009) Accelerated species inventory on madagascar using coalescent-based models of species delineation. Systematic Biology, 58, 298-311.
45. Morton JB, Bentivenga SP, (1994) Levels of diverstity in endomycorrhizal fungi (Glomales, Zygomycetes) and their role in defining taxonomic and non-taxonomic groups. Plant and Soil, 159, 47-59.
46. Mummey DL, Rillig MC, Holben WE, (2005) Neighboring plant influences on arbuscular my corrhizal fungal community composition as assessed by T-RFLP analysis. Plant and Soil, 271, 83-90.
47. Munkvold L, Kjøller R, Vestberg M, Rosendahl S, Jakobsen I, (2004) High functional diversity within species of arbuscular mycorrhizal fungi. New Phytologist, 164, 357-364.
48. 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. Evolutionary Bioinformatics, 4, 193-201.
49. Oksanen J, Blanchet FG, Kindt R, et al. (2010) vegan: Community Ecology Package. R package version 1.17-0. Available from.
50. Öpik M, Moora M, Liira J, KÃ̈ljalg U, Zobel M, Sen R, (2003) Divergent arbuscular mycorrhizal fungal communities colonize roots of Pulsatilla spp. in boreal scots pine forest and grassland soils. New Phytologist, 160, 581-593.
51. Öpik M, Moora M, Liira J, Zobel M, (2006) Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. Journal of Ecology, 94, 778-790.
52. Öpik M, Moora M, Zobel M, et al. (2008) High diversity of arbuscular mycorrhizal fungi in a boreal herb-rich coniferous forest. New Phytologist, 179, 867-876.
53. Öpik M, Metsis M, Daniell TJ, Zobel M, Moora M, (2009) Large-scale parallel 454 sequencing reveals host ecological group specificity of arbuscular mycorrhizal fungi in a boreonemoral forest. New Phytologist, 184, 424-437.
54. Öpik M, Vanatoa A, Vanatoa E, et al. (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytologist, 188, 223-241.
55. Papadopoulou A, Anastasiou I, Keskin B, Vogler AP, (2009) Comparative phylogeography of tenebrionid beetles in the Aegean archipelago: the effect of dispersal ability and habitat preference. Molecular Ecology, 18, 2503-2517.
56. Paradis E, Claude J, Strimmer K, (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics, 20, 289-290.
57. Pawlowska TE, Taylor JW, (2004) Organization of genetic variation in individuals of arbuscular mycorrhizal fungi. Nature, 427, 733-737.
58. Pons J, Barraclough TG, Gomez-Zurita J, et al. (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology, 55, 595-609.
59. Posada D, Crandall K, (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics, 14, 817-818.
60. Powell JR, Parrent JL, Hart MM, Klironomos JN, Rillig MC, Maherali H, (2009) Phylogenetic trait conservatism and the evolution of functional trade-offs in arbuscular mycorrhizal fungi. Proceedings of the Royal Society B: Biological Sciences, 276, 4237-4245.
61. R Development Core Team (2009) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Available from.
62. Rodriguez A, Clap, JP, Dodd JC, (2004) Ribosomal RNA gene sequence diversity in arbuscular mycorrhizal fungi (Glomeromycota). Journal of Ecology, 92, 986-989.
63. Rosendahl S, Taylor JW, (1997) Development of multiple genetic markers for studies of genetic variation in arbuscular mycorrhizal fungi using AFLP. Molecular Ecology, 6, 821-829.
64. Rosendahl S, McGee P, Morton JB, (2009). Lack of global population genetic differentiation in the arbuscular mycorrhizal fungus Glomus mosseae suggests a recent range expansion which may have coincided with the spread of agriculture. Molecular Ecology, 18, 4316-4329.
65. SÃkorová Z, Ineichen K, Wiemken A, Redecker D, (2007) The cultivation bias: different communities of arbuscular mycorrhizal fungi detected in roots from the field, from bait plants transplanted to the field, and from a greenhouse trap experiment. Mycorrhiza, 18, 1-14.
66. Schenck NC, Smith GS, (1982) Additional new and unreported species of mycorrhizal fungi (Endogonaceae) from Florida. Mycologia, 74, 77-92.
67. Scheublin TR, Ridgway KP, Young JPW, van der Heijden MGA, (2004) Nonlegumes, legumes, and root nodules harbor different arbuscular mycorrhizal fungal communities. Applied and Environmental Microbiology, 70, 6240-6246.
68. Schloss PD, Westcott SL, Ryabin T, et al. (2009) Introducing mothur: open-source, platform independent, community-supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75, 7537-7541.
69. Seifert KA, Samson RA, deWaard JR, et al. (2007) Prospects for fungus identification using CO1 DNA barcodes, with Penicillium as a test case. Proceedings of the National Academy of Sciences of the United States of America, 104, 3901-3906.
70. Sikes BA, Cottenie K, Klironomos JN, (2009) Plant and fungal identity determines pathogen protection of plant roots by arbuscular mycorrhizas. Journal of Ecology, 97, 1274-1280.
71. Smith SE, Read DJ, (2008) Mycorrhizal Symbiosis, 3rd edn. Academic Press, London.
72. Stackebrandt E, Goebel BM, (1994) Taxonomic note: a place for DNA-DNA reassociation and 16S rRNA sequence analysis in the present species definition in bacteriology. International Journal of Systematic and Evolutionary Bacteriology, 44, 846-849.
73. Vogler AP, Monaghan MT, (2007) Recent advances in DNA taxonomy. Journal of Zoological Systematics and Evolutionary Research, 45, 1-10.
74. Wehner J, Antunes PM, Powell JR, Mazukatow J, Rillig MC, (2010) Plant pathogen protection by arbuscular mycorrhizas: a role for fungal diversity? Pedobiologia, 53, 197-201.
75. Yule GU, (1925) A mathematical theory of evolution, based on the conclusions of Dr. J. C. Willis, F.R.S. Philosophical Transactions of the Royal Society of London. Series B, Containing Papers of a Biological Character, 213, 21-87.