Browse by volume Browse by section Browse by topic Browse by conference

Section: Evolutionary Biology
Topic: Evolution, Biology of interactions

Do closely related species interact with similar partners? Testing for phylogenetic signal in bipartite interaction networks

Perez-Lamarque, Benoît1, 2  ; Maliet, Odile1 ; Pichon, Benoît3, 1; Selosse, Marc-André2, 4, 5 ; Martos, Florent2 ; Morlon, Hélène1 
1 Institut de biologie de l’École normale supérieure (IBENS), École normale supérieure, CNRS, INSERM, Université PSL, 46 rue d’Ulm, 75 005 Paris, France
2 Institut de Systématique, Évolution, Biodiversité (ISYEB), Muséum national d’histoire naturelle, CNRS, Sorbonne Université, EPHE, UA, CP39, 57 rue Cuvier 75 005 Paris, France
3 Institut d’écologie et des sciences de l’environnement (iEES), Sorbonne Université, CNRS, UPEC, CNRS, IRD, INRA, 75 005 Paris, France
4 Department of Plant Taxonomy and Nature Conservation, University of Gdansk, Wita Stwosza 59, 80-308 Gdansk, Poland
5 Institut universitaire de France (IUF), Paris, France

10.24072/pcjournal.179 - Peer Community Journal, Volume 2 (2022), article no. e59.

Get full text PDF Peer reviewed and recommended by PCI

Whether interactions between species are conserved on evolutionary time-scales has spurred the development of both correlative and process-based approaches for testing phylogenetic signal in interspecific interactions: do closely related species interact with similar partners? Here we use simulations to test the statistical performances of the two approaches that are the most widely used in the field: Mantel tests and the Phylogenetic Bipartite Linear Model (PBLM). Mantel tests investigate the correlation between phylogenetic distances and dissimilarities in sets of interacting partners, while PBLM is a process-based approach that relies on strong assumptions about how interactions evolve. We find that PBLM often detects a phylogenetic signal when it should not. Simple Mantel tests instead have infrequent false positives and moderate statistical power; however, they often artifactually detect that closely related species interact with dissimilar partners. Partial Mantel tests, which are used to partial out the phylogenetic signal in the number of partners, actually fail at correcting for this confounding effect, and we instead recommend evaluating the significance of Mantel tests with network permutations constraining the number of partners. We also explore the ability of simple Mantel tests to analyze clade- specific phylogenetic signals. We provide general guidelines and an application on an interaction network between orchids and mycorrhizal fungi.

Published online:
DOI: 10.24072/pcjournal.179
Type: Research article
Perez-Lamarque, Benoît 1, 2; Maliet, Odile 1; Pichon, Benoît 3, 1; Selosse, Marc-André 2, 4, 5; Martos, Florent 2; Morlon, Hélène 1

1 Institut de biologie de l’École normale supérieure (IBENS), École normale supérieure, CNRS, INSERM, Université PSL, 46 rue d’Ulm, 75 005 Paris, France
2 Institut de Systématique, Évolution, Biodiversité (ISYEB), Muséum national d’histoire naturelle, CNRS, Sorbonne Université, EPHE, UA, CP39, 57 rue Cuvier 75 005 Paris, France
3 Institut d’écologie et des sciences de l’environnement (iEES), Sorbonne Université, CNRS, UPEC, CNRS, IRD, INRA, 75 005 Paris, France
4 Department of Plant Taxonomy and Nature Conservation, University of Gdansk, Wita Stwosza 59, 80-308 Gdansk, Poland
5 Institut universitaire de France (IUF), Paris, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
@article{10_24072_pcjournal_179,
     author = {Perez-Lamarque, Beno{\^\i}t and Maliet, Odile and Pichon, Beno{\^\i}t and Selosse, Marc-Andr\'e and Martos, Florent and Morlon, H\'el\`ene},
     title = {Do closely related species interact with similar partners? {Testing} for phylogenetic signal in bipartite interaction networks},
     journal = {Peer Community Journal},
     eid = {e59},
     publisher = {Peer Community In},
     volume = {2},
     year = {2022},
     doi = {10.24072/pcjournal.179},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.179/}
}
TY  - JOUR
AU  - Perez-Lamarque, Benoît
AU  - Maliet, Odile
AU  - Pichon, Benoît
AU  - Selosse, Marc-André
AU  - Martos, Florent
AU  - Morlon, Hélène
TI  - Do closely related species interact with similar partners? Testing for phylogenetic signal in bipartite interaction networks
JO  - Peer Community Journal
PY  - 2022
VL  - 2
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.179/
DO  - 10.24072/pcjournal.179
ID  - 10_24072_pcjournal_179
ER  - 
%0 Journal Article
%A Perez-Lamarque, Benoît
%A Maliet, Odile
%A Pichon, Benoît
%A Selosse, Marc-André
%A Martos, Florent
%A Morlon, Hélène
%T Do closely related species interact with similar partners? Testing for phylogenetic signal in bipartite interaction networks
%J Peer Community Journal
%D 2022
%V 2
%I Peer Community In
%U https://peercommunityjournal.org/articles/10.24072/pcjournal.179/
%R 10.24072/pcjournal.179
%F 10_24072_pcjournal_179
Perez-Lamarque, Benoît; Maliet, Odile; Pichon, Benoît; Selosse, Marc-André; Martos, Florent; Morlon, Hélène. Do closely related species interact with similar partners? Testing for phylogenetic signal in bipartite interaction networks. Peer Community Journal, Volume 2 (2022), article  no. e59. doi : 10.24072/pcjournal.179. https://peercommunityjournal.org/articles/10.24072/pcjournal.179/

Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100150

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

[1] Aizen, M. A.; Gleiser, G.; Sabatino, M.; Gilarranz, L. J.; Bascompte, J.; Verdú, M. The phylogenetic structure of plant-pollinator networks increases with habitat size and isolation, Ecology Letters, Volume 19 (2016) no. 1, pp. 29-36 | DOI

[2] Bascompte, J.; Jordano, P. Mutualistic networks. Monographs in population biology (Princeton, Vol. 7), Princeton University Press, Princeton, 2013 | DOI

[3] Bascompte, J.; Jordano, P.; Melián, C. J.; Olesen, J. M. The nested assembly of plant–animal mutualistic networks, Proceedings of the National Academy of Sciences, Volume 100 (2003) no. 16, pp. 9383-9387 | DOI

[4] Baselga, A. Partitioning the turnover and nestedness components of beta diversity, Global Ecology and Biogeography, Volume 19 (2010) no. 1, pp. 134-143 | DOI

[5] Baselga, A.; Orme, C. D. L. betapart: an R package for the study of beta diversity, Methods in Ecology and Evolution, Volume 3 (2012) no. 5, pp. 808-812 | DOI

[6] Blomberg, S. P.; Garland, T.; Ives, A. R. Testing for phylogenetic signal in comparative data: behavioral traits are more labile, Evolution, Volume 57 (2003) no. 4, pp. 717-745 | DOI

[7] Braga, M. P.; Janz, N.; Nylin, S.; Ronquist, F.; Landis, M. J. Phylogenetic reconstruction of ancestral ecological networks through time for pierid butterflies and their host plants, Ecology Letters, Volume 24 (2021) no. 10, pp. 2134-2145 | DOI

[8] Calatayud, J.; Hórreo, J. L.; Madrigal-González, J.; Migeon, A.; Rodríguez, M. Á.; Magalhães, S.; Hortal, J. Geography and major host evolutionary transitions shape the resource use of plant parasites, Proceedings of the National Academy of Sciences, Volume 113 (2016) no. 35, pp. 9840-9845 | DOI

[9] Cattin, M.-F.; Bersier, L.-F.; Banašek-Richter, C.; Baltensperger, R.; Gabriel, J.-P. Phylogenetic constraints and adaptation explain food-web structure, Nature, Volume 427 (2004) no. 6977, pp. 835-839 | DOI

[10] Clavel, J.; Escarguel, G.; Merceron, G. mv morph: an r package for fitting multivariate evolutionary models to morphometric data, Methods in Ecology and Evolution, Volume 6 (2015) no. 11, pp. 1311-1319 | DOI

[11] Corro, E. J.; Villalobos, F.; Lira-Noriega, A.; Guevara, R.; Guimarães, P. R.; Dáttilo, W. Annual precipitation predicts the phylogenetic signal in bat–fruit interaction networks across the Neotropics, Biology Letters, Volume 17 (2021) no. 12 | DOI

[12] Elias, M.; Fontaine, C.; Frank van Veen, F. Evolutionary History and Ecological Processes Shape a Local Multilevel Antagonistic Network, Current Biology, Volume 23 (2013) no. 14, pp. 1355-1359 | DOI

[13] Felsenstein, J. Phylogenies and the Comparative Method, The American Naturalist, Volume 125 (1985) no. 1, pp. 1-15 | DOI

[14] Fontaine, C.; Guimarães, P. R.; Kéfi, S.; Loeuille, N.; Memmott, J.; van der Putten, W. H.; van Veen, F. J. F.; Thébault, E. The ecological and evolutionary implications of merging different types of networks, Ecology Letters, Volume 14 (2011) no. 11, pp. 1170-1181 | DOI

[15] Fontaine, C.; Thébault, E. Comparing the conservatism of ecological interactions in plant–pollinator and plant–herbivore networks, Population Ecology, Volume 57 (2015) no. 1, pp. 29-36 | DOI

[16] Fortuna, M. A.; Ortega, R.; Bascompte, J. The Web of Life, arXiv (2014) | DOI

[17] Futuyma, D. J.; Agrawal, A. A. Macroevolution and the biological diversity of plants and herbivores, Proceedings of the National Academy of Sciences, Volume 106 (2009) no. 43, pp. 18054-18061 | DOI

[18] Givnish, T. J.; Spalink, D.; Ames, M.; Lyon, S. P.; Hunter, S. J.; Zuluaga, A.; Iles, W. J. D.; Clements, M. A.; Arroyo, M. T. K.; Leebens-Mack, J.; Endara, L.; Kriebel, R.; Neubig, K. M.; Whitten, W. M.; Williams, N. H.; Cameron, K. M. Orchid phylogenomics and multiple drivers of their extraordinary diversification, Proceedings of the Royal Society B: Biological Sciences, Volume 282 (2015) no. 1814 | DOI

[19] Gómez, J. M.; Verdú, M.; Perfectti, F. Ecological interactions are evolutionarily conserved across the entire tree of life, Nature, Volume 465 (2010) no. 7300, pp. 918-921 | DOI

[20] Goolsby, E. W. Phylogenetic Comparative Methods for Evaluating the Evolutionary History of Function-Valued Traits, Systematic Biology, Volume 64 (2015) no. 4, pp. 568-578 | DOI

[21] Goslee, S. C.; Urban, D. L. The ecodist Package for Dissimilarity-based Analysis of Ecological Data, Journal of Statistical Software, Volume 22 (2007) no. 7, pp. 1-19 | DOI

[22] Guillot, G.; Rousset, F. Dismantling the Mantel tests, Methods in Ecology and Evolution, Volume 4 (2013) no. 4, pp. 336-344 | DOI

[23] Hadfield, J. D.; Krasnov, B. R.; Poulin, R.; Nakagawa, S. A Tale of Two Phylogenies: Comparative Analyses of Ecological Interactions, The American Naturalist, Volume 183 (2014) no. 2, pp. 174-187 | DOI

[24] Harmon, L. J.; Andreazzi, C. S.; Débarre, F.; Drury, J.; Goldberg, E. E.; Martins, A. B.; Melián, C. J.; Narwani, A.; Nuismer, S. L.; Pennell, M. W.; Rudman, S. M.; Seehausen, O.; Silvestro, D.; Weber, M.; Matthews, B. Detecting the macroevolutionary signal of species interactions, Journal of Evolutionary Biology, Volume 32 (2019) no. 8, pp. 769-782 | DOI

[25] Harmon, L. J.; Glor, R. E. Poor statistical performance of the mantel test in phylogenetic comparative analyses, Evolution, Volume 64 (2010) no. 7, pp. 2173-2178 | DOI

[26] Ives, A. R.; Godfray, H. C. J. Phylogenetic Analysis of Trophic Associations, The American Naturalist, Volume 168 (2006) no. 1 | DOI

[27] Jacquemyn, H.; Merckx, V.; Brys, R.; Tyteca, D.; Cammue, B. P. A.; Honnay, O.; Lievens, B. Analysis of network architecture reveals phylogenetic constraints on mycorrhizal specificity in the genus Orchis (Orchidaceae), New Phytologist, Volume 192 (2011) no. 2, pp. 518-528 | DOI

[28] Kembel, S. W.; Cowan, P. D.; Helmus, M. R.; Cornwell, W. K.; Morlon, H.; Ackerly, D. D.; Blomberg, S. P.; Webb, C. O. Picante: R tools for integrating phylogenies and ecology, Bioinformatics, Volume 26 (2010) no. 11, pp. 1463-1464 | DOI

[29] Krasnov, B. R.; Fortuna, M. A.; Mouillot, D.; Khokhlova, I. S.; Shenbrot, G. I.; Poulin, R. Phylogenetic Signal in Module Composition and Species Connectivity in Compartmentalized Host-Parasite Networks, The American Naturalist, Volume 179 (2012) no. 4, pp. 501-511 | DOI

[30] Lajoie, G.; Kembel, S. W. Plant‐bacteria associations are phylogenetically structured in the phyllosphere, Molecular Ecology, Volume 30 (2021) no. 21, pp. 5572-5587 | DOI

[31] Leprieur, F.; Albouy, C.; De Bortoli, J.; Cowman, P. F.; Bellwood, D. R.; Mouillot, D. Quantifying Phylogenetic Beta Diversity: Distinguishing between ‘True’ Turnover of Lineages and Phylogenetic Diversity Gradients, PLoS ONE, Volume 7 (2012) no. 8 | DOI

[32] Li, D.; Dinnage, R.; Nell, L. A.; Helmus, M. R.; Ives, A. R. phyr: An r package for phylogenetic species‐distribution modelling in ecological communities, Methods in Ecology and Evolution, Volume 11 (2020) no. 11, pp. 1455-1463 | DOI

[33] Losos, J. B. Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species, Ecology Letters, Volume 11 (2008) no. 10, pp. 995-1003 | DOI

[34] Lozupone, C.; Lladser, M. E.; Knights, D.; Stombaugh, J.; Knight, R. UniFrac: an effective distance metric for microbial community comparison, The ISME Journal, Volume 5 (2011) no. 2, pp. 169-172 | DOI

[35] Maliet, O.; Loeuille, N.; Morlon, H. An individual‐based model for the eco‐evolutionary emergence of bipartite interaction networks, Ecology Letters, Volume 23 (2020) no. 11, pp. 1623-1634 | DOI

[36] Mantel, N. The detection of disease clustering and a generalized regression approach, Volume 27 (1967) no. 2, pp. 209-220

[37] Martín González, A. M.; Dalsgaard, B.; Nogués-Bravo, D.; Graham, C. H.; Schleuning, M.; Maruyama, P. K.; Abrahamczyk, S.; Alarcón, R.; Araujo, A. C.; Araújo, F. P.; de Azevedo, S. M.; Baquero, A. C.; Cotton, P. A.; Ingversen, T. T.; Kohler, G.; Lara, C.; Las-Casas, F. M. G.; Machado, A. O.; Machado, C. G.; Maglianesi, M. A.; McGuire, J. A.; Moura, A. C.; Oliveira, G. M.; Oliveira, P. E.; Ornelas, J. F.; Rodrigues, L. d. C.; Rosero-Lasprilla, L.; Rui, A. M.; Sazima, M.; Timmermann, A.; Varassin, I. G.; Vizentin-Bugoni, J.; Wang, Z.; Watts, S.; Rahbek, C.; Martinez, N. D. The macroecology of phylogenetically structured hummingbird-plant networks, Global Ecology and Biogeography, Volume 24 (2015) no. 11, pp. 1212-1224 | DOI

[38] Martos, F.; Munoz, F.; Pailler, T.; Kottke, I.; Gonneau, C.; Selosse, M.-A. The role of epiphytism in architecture and evolutionary constraint within mycorrhizal networks of tropical orchids, Molecular Ecology, Volume 21 (2012) no. 20, pp. 5098-5109 | DOI

[39] Michalska-Smith, M. J.; Allesina, S. Telling ecological networks apart by their structure: A computational challenge, PLOS Computational Biology, Volume 15 (2019) no. 6 | DOI

[40] Morlon, H.; Lewitus, E.; Condamine, F. L.; Manceau, M.; Clavel, J.; Drury, J. RPANDA: an R package for macroevolutionary analyses on phylogenetic trees, Methods in Ecology and Evolution, Volume 7 (2016) no. 5, pp. 589-597 | DOI

[41] Münkemüller, T.; Lavergne, S.; Bzeznik, B.; Dray, S.; Jombart, T.; Schiffers, K.; Thuiller, W. How to measure and test phylogenetic signal, Methods in Ecology and Evolution, Volume 3 (2012) no. 4, pp. 743-756 | DOI

[42] Pagel, M. Inferring the historical patterns of biological evolution, Nature, Volume 401 (1999) no. 6756, pp. 877-884 | DOI

[43] Paradis, E. Molecular dating of phylogenies by likelihood methods: A comparison of models and a new information criterion, Molecular Phylogenetics and Evolution, Volume 67 (2013) no. 2, pp. 436-444 | DOI

[44] Paradis, E.; Claude, J.; Strimmer, K. APE: Analyses of Phylogenetics and Evolution in R language, Bioinformatics, Volume 20 (2004) no. 2, pp. 289-290 | DOI

[45] Peralta, G. Merging evolutionary history into species interaction networks, Functional Ecology, Volume 30 (2016) no. 12, pp. 1917-1925 | DOI

[46] Perez-Lamarque, B.; Petrolli, R.; Strullu-Derrien, C.; Strasberg, D.; Morlon, H.; Selosse, M.-A.; Martos, F. Structure and specialization of mycorrhizal networks in phylogenetically diverse tropical communities, Environmental Microbiome, Volume 17 (2022) no. 1 | DOI

[47] Perez‐Lamarque, B.; Morlon, H. Characterizing symbiont inheritance during host–microbiota evolution: Application to the great apes gut microbiota, Molecular Ecology Resources, Volume 19 (2019) no. 6, pp. 1659-1671 | DOI

[48] R Core Team R: A language and environment for statistical computing, R Foundation for Statistical Computing, 2022 (http://www.r-project.org/index.html)

[49] Rafferty, N. E.; Ives, A. R. Phylogenetic trait-based analyses of ecological networks, Ecology, Volume 94 (2013) no. 10, pp. 2321-2333 | DOI

[50] Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things), Methods in Ecology and Evolution, Volume 3 (2012) no. 2, pp. 217-223 | DOI

[51] Rezende, E. L.; Lavabre, J. E.; Guimarães, P. R.; Jordano, P.; Bascompte, J. Non-random coextinctions in phylogenetically structured mutualistic networks, Nature, Volume 448 (2007) no. 7156, pp. 925-928 | DOI

[52] Rohr, R. P.; Bascompte, J. Components of Phylogenetic Signal in Antagonistic and Mutualistic Networks, The American Naturalist, Volume 184 (2014) no. 5, pp. 556-564 | DOI

[53] Sanders, J. G.; Powell, S.; Kronauer, D. J. C.; Vasconcelos, H. L.; Frederickson, M. E.; Pierce, N. E. Stability and phylogenetic correlation in gut microbiota: lessons from ants and apes, Molecular Ecology, Volume 23 (2014) no. 6, pp. 1268-1283 | DOI

[54] Song, S. J.; Sanders, J. G.; Delsuc, F.; Metcalf, J.; Amato, K.; Taylor, M. W.; Mazel, F.; Lutz, H. L.; Winker, K.; Graves, G. R.; Humphrey, G.; Gilbert, J. A.; Hackett, S. J.; White, K. P.; Skeen, H. R.; Kurtis, S. M.; Withrow, J.; Braile, T.; Miller, M.; McCracken, K. G.; Maley, J. M.; Ezenwa, V. O.; Williams, A.; Blanton, J. M.; McKenzie, V. J.; Knight, R. Comparative Analyses of Vertebrate Gut Microbiomes Reveal Convergence between Birds and Bats, mBio, Volume 11 (2020) no. 1 | DOI

[55] Vázquez, D. P.; Chacoff, N. P.; Cagnolo, L. Evaluating multiple determinants of the structure of plant–animal mutualistic networks, Ecology, Volume 90 (2009) no. 8, pp. 2039-2046 | DOI

[56] Xing, X.; Jacquemyn, H.; Gai, X.; Gao, Y.; Liu, Q.; Zhao, Z.; Guo, S. The impact of life form on the architecture of orchid mycorrhizal networks in tropical forest, Oikos, Volume 128 (2019) no. 9, pp. 1254-1264 | DOI

[57] Xing, X.; Liu, Q.; Gao, Y.; Shao, S.; Guo, L.; Jacquemyn, H.; Zhao, Z.; Guo, S. The Architecture of the Network of Orchid–Fungus Interactions in Nine Co-occurring Dendrobium Species, Frontiers in Ecology and Evolution, Volume 8 (2020) | DOI

Cited by Sources: