Assembly of complex plant–fungus networks

Species in ecological communities build complex webs of interaction. Although revealing the architecture of these networks is fundamental to understanding ecological and evolutionary dynamics in nature, it has been difficult to characterize the structure of most species-rich ecological systems. By overcoming this limitation through next-generation sequencing technology, we herein uncover the network architecture of below-ground plant–fungus symbioses, which are ubiquitous to terrestrial ecosystems. The examined symbiotic network of a temperate forest in Japan includes 33 plant species and 387 functionally and phylogenetically diverse fungal taxa, and the overall network architecture differs fundamentally from that of other ecological networks. In contrast to results for other ecological networks and theoretical predictions for symbiotic networks, the plant–fungus network shows moderate or relatively low levels of interaction specialization and modularity and an unusual pattern of ‘nested’ network architecture. These results suggest that species-rich ecological networks are more architecturally diverse than previously recognized.

[1]  R. Koide,et al.  Vesicular-arbuscular mycorrhizal infection of Quercus rubra seedlings. , 2001, The New phytologist.

[2]  Carsten F. Dormann,et al.  Indices, Graphs and Null Models: Analyzing Bipartite Ecological Networks , 2009 .

[3]  C. Darwin The Origin of Species by Means of Natural Selection, Or, The Preservation of Favoured Races in the Struggle for Life , 1859 .

[4]  Lewi Stone,et al.  Competitive exclusion, or species aggregation? , 1992, Oecologia.

[5]  Makoto Kato,et al.  Insect-flower Relationship in the Primary Beech Forest of Ashu, Kyoto : An Overview of the Flowering Phenology and the Seasonal Pattern of Insect Visits , 1990 .

[6]  J. Thompson,et al.  Geographic structure and dynamics of coevolutionary selection , 2002, Nature.

[7]  Louis-Félix Bersier,et al.  QUANTITATIVE DESCRIPTORS OF FOOD-WEB MATRICES , 2002 .

[8]  Werner Ulrich,et al.  A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement , 2008 .

[9]  Nils Blüthgen,et al.  Specialization, Constraints, and Conflicting Interests in Mutualistic Networks , 2007, Current Biology.

[10]  Stefano Allesina,et al.  The ghost of nestedness in ecological networks , 2013, Nature Communications.

[11]  M. Barber Modularity and community detection in bipartite networks. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[12]  B. Deagle,et al.  Analysis of Australian fur seal diet by pyrosequencing prey DNA in faeces , 2009, Molecular ecology.

[13]  E. Kiers,et al.  Sanctions, Cooperation, and the Stability of Plant-Rhizosphere Mutualisms , 2008 .

[14]  K. Nara,et al.  ECTOMYCORRHIZAL FUNGI ON ESTABLISHED SHRUBS FACILITATE SUBSEQUENT SEEDLING ESTABLISHMENT OF SUCCESSIONAL PLANT SPECIES , 2004 .

[15]  J. Pitchford,et al.  Disentangling nestedness from models of ecological complexity , 2012, Nature.

[16]  P. Asprelli,et al.  THE GEOGRAPHIC MOSAIC OF COEVOLUTION , 2007 .

[17]  Paul D N Hebert,et al.  DNA barcodes reveal cryptic host-specificity within the presumed polyphagous members of a genus of parasitoid flies (Diptera: Tachinidae). , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[18]  S. West,et al.  Reciprocal Rewards Stabilize Cooperation in the Mycorrhizal Symbiosis , 2011, Science.

[19]  Jordi Bascompte,et al.  The architecture of mutualistic networks minimizes competition and increases biodiversity , 2009, Nature.

[20]  Rudolf P. Rohr,et al.  On the structural stability of mutualistic systems , 2014, Science.

[21]  Luiz Fernando Bittencourt,et al.  MODULAR: Software for the Autonomous Computation of Modularity in Large Network Sets , 2013, ArXiv.

[22]  Paulo R. Guimarães,et al.  Interaction Intimacy Affects Structure and Coevolutionary Dynamics in Mutualistic Networks , 2007, Current Biology.

[23]  Akifumi S. Tanabe,et al.  Community composition of root-associated fungi in a Quercus-dominated temperate forest: “codominance” of mycorrhizal and root-endophytic fungi , 2013, Ecology and evolution.

[24]  P. Hebert,et al.  Complementary molecular information changes our perception of food web structure , 2014, Proceedings of the National Academy of Sciences.

[25]  K. Newsham A meta-analysis of plant responses to dark septate root endophytes. , 2011, The New phytologist.

[26]  Roger Guimerà,et al.  Cartography of complex networks: modules and universal roles , 2005, Journal of statistical mechanics.

[27]  J. Bever,et al.  Arbuscular Mycorrhizal Fungi: More Diverse than Meets the Eye, and the Ecological Tale of Why , 2001 .

[28]  A. Valiente‐Banuet,et al.  The network structure of plant-arbuscular mycorrhizal fungi. , 2012, The New phytologist.

[29]  Michael J. O. Pocock,et al.  The Robustness and Restoration of a Network of Ecological Networks , 2012, Science.

[30]  D. Inouye,et al.  ARE NECTAR ROBBERS CHEATERS OR MUTUALISTS , 2000 .

[31]  E. Maris,et al.  Two Sides of the Same Coin , 2010, Psychological science.

[32]  Daniel B. Stouffer,et al.  Nestedness versus modularity in ecological networks: two sides of the same coin? , 2010, The Journal of animal ecology.

[33]  Jordi Bascompte,et al.  Non-random coextinctions in phylogenetically structured mutualistic networks , 2007, Nature.

[34]  R. Henrik Nilsson,et al.  Intraspecific ITS Variability in the Kingdom Fungi as Expressed in the International Sequence Databases and Its Implications for Molecular Species Identification , 2008, Evolutionary bioinformatics online.

[35]  Owen T Lewis,et al.  Antagonistic interaction networks are structured independently of latitude and host guild , 2013, Ecology letters.

[36]  J. Bascompte,et al.  The modularity of pollination networks , 2007, Proceedings of the National Academy of Sciences.

[37]  A. Mougi,et al.  Diversity of Interaction Types and Ecological Community Stability , 2012, Science.

[38]  O. Alizadeh,et al.  Mycorrhizal Symbiosis , 1986, Forest Science.

[39]  Mathias M Pires,et al.  Interaction intimacy organizes networks of antagonistic interactions in different ways , 2013, Journal of The Royal Society Interface.

[40]  Kohmei Kadowaki,et al.  How are plant and fungal communities linked to each other in belowground ecosystems? A massively parallel pyrosequencing analysis of the association specificity of root-associated fungi and their host plants , 2013, Ecology and evolution.

[41]  A. Maritan,et al.  Emergence of structural and dynamical properties of ecological mutualistic networks , 2013, Nature.

[42]  Paulo R. Guimarães,et al.  On nestedness analyses: rethinking matrix temperature and anti‐nestedness , 2007 .

[43]  Colin Fontaine,et al.  Stability of Ecological Communities and the Architecture of Mutualistic and Trophic Networks , 2010, Science.

[44]  Mohammad Bahram,et al.  Network perspectives of ectomycorrhizal associations , 2014 .

[45]  Pedro Jordano,et al.  Evolution and Coevolution in Mutualistic Networks , 2022 .

[46]  Makoto Kato,et al.  Insect-flower Relationship in the Temperate Deciduous Forest of Kibune, Kyoto : An Overview of the Flowering Phenology and the Seasonal Pattern of Insect Visits , 1990 .

[47]  Rodolfo Dirzo,et al.  Analysis of a hyper-diverse seed dispersal network: modularity and underlying mechanisms. , 2011, Ecology letters.

[48]  D. Garlaschelli,et al.  On the application of network theory to arbuscular mycorrhizal fungi-plant interactions: the importance of basic assumptions. , 2012, The New phytologist.

[49]  Neal M. Williams,et al.  Species abundance and asymmetric interaction strength in ecological networks , 2007 .

[50]  A. Valiente‐Banuet,et al.  Plant facilitation occurs between species differing in their associated arbuscular mycorrhizal fungi. , 2012, The New phytologist.

[51]  M E J Newman,et al.  Finding and evaluating community structure in networks. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[52]  L. Tedersoo,et al.  Ascomycetes associated with ectomycorrhizas: molecular diversity and ecology with particular reference to the Helotiales. , 2009, Environmental microbiology.

[53]  Alfried P Vogler,et al.  DNA barcoding insect–host plant associations , 2009, Proceedings of the Royal Society B: Biological Sciences.

[54]  Mário Almeida-Neto,et al.  A straightforward computational approach for measuring nestedness using quantitative matrices , 2011, Environ. Model. Softw..

[55]  M. Zobel,et al.  Arbuscular mycorrhizal fungal communities in plant roots are not random assemblages. , 2011, FEMS microbiology ecology.

[56]  Carlos J. Melián,et al.  The nested assembly of plant–animal mutualistic networks , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[57]  A. Gray,et al.  I. THE ORIGIN OF SPECIES BY MEANS OF NATURAL SELECTION , 1963 .

[58]  Si Tang,et al.  Stability criteria for complex ecosystems , 2011, Nature.