Phylogenetic structure of specialization: A new approach that integrates partner availability and phylogenetic diversity to quantify biotic specialization in ecological networks
Pardo‐De la Hoz, Carlos J.; Medeiros, Ian D.; Gibert, Jean P.et al.
Nature and Landscape Conservation; Ecology; Ecology, Evolution, Behavior and Systematics
Abstract :
[en] Biotic specialization holds information about the assembly, evolution, and stability of biological communities. Partner availabilities can play an important role in enabling species interactions, where uneven partner availabilities can bias estimates of biotic specialization when using phylogenetic diversity indices. It is therefore important to account for partner availability when characterizing biotic specialization using phylogenies. We developed an index, phylogenetic structure of specialization (PSS), that avoids bias from uneven partner availabilities by uncoupling the null models for interaction frequency and phylogenetic distance. We incorporate the deviation between observed and random interaction frequencies as weights into the calculation of partner phylogenetic α-diversity. To calculate the PSS index, we then compare observed partner phylogenetic α-diversity to a null distribution generated by randomizing phylogenetic distances among the same number of partners. PSS quantifies the phylogenetic structure (i.e., clustered, overdispersed, or random) of the partners of a focal species. We show with simulations that the PSS index is not correlated with network properties, which allows comparisons across multiple systems. We also implemented PSS on empirical networks of host–parasite, avian seed-dispersal, lichenized fungi–cyanobacteria, and hummingbird pollination interactions. Across these systems, a large proportion of taxa interact with phylogenetically random partners according to PSS, sometimes to a larger extent than detected with an existing method that does not account for partner availability. We also found that many taxa interact with phylogenetically clustered partners, while taxa with overdispersed partners were rare. We argue that species with phylogenetically overdispersed partners have often been misinterpreted as generalists when they should be considered specialists. Our results highlight the important role of randomness in shaping interaction networks, even in highly intimate symbioses, and provide a much-needed quantitative framework to assess the role that evolutionary history and symbiotic specialization play in shaping patterns of biodiversity. PSS is available as an R package at https://github.com/cjpardodelahoz/pss.
Disciplines :
Environmental sciences & ecology
Author, co-author :
Pardo‐De la Hoz, Carlos J. ; Department of Biology Duke University Durham North Carolina USA
Medeiros, Ian D. ; Department of Biology Duke University Durham North Carolina USA
Gibert, Jean P. ; Department of Biology Duke University Durham North Carolina USA
Chagnon, Pierre‐Luc ; Département des Sciences Biologiques Université de Montréal Montréal Québec Canada
Magain, Nicolas ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Biologie de l'évolution et gestion de la biodiversité
Miadlikowska, Jolanta ; Department of Biology Duke University Durham North Carolina USA
Lutzoni, François ; Department of Biology Duke University Durham North Carolina USA
Language :
English
Title :
Phylogenetic structure of specialization: A new approach that integrates partner availability and phylogenetic diversity to quantify biotic specialization in ecological networks
Aizen, M. A., Gleiser, G., Sabatino, M., Gilarranz, L. J., Bascompte, J., & Verdú, M. (2016). The phylogenetic structure of plant-pollinator networks increases with habitat size and isolation. Ecology Letters, 19(1), 29–36. https://doi.org/10.1111/ele.12539
Almeida-Neto, M., Guimarães, P., Guimarães, P. R., Loyola, R. D., & Ulrich, W. (2008). A consistent metric for nestedness analysis in ecological systems: Reconciling concept and measurement. Oikos, 117(8), 1227–1239. https://doi.org/10.1111/j.0030-1299.2008.16644.x
Antonson, N. D., Rubenstein, D. R., Hauber, M. E., & Botero, C. A. (2020). Ecological uncertainty favours the diversification of host use in avian brood parasites. Nature Communications, 11, 4185. https://doi.org/10.1038/s41467-020-18038-y
Arceo-Gómez, G., Barker, D., Stanley, A., Watson, T., & Daniels, J. (2020). Plant–pollinator network structural properties differentially affect pollen transfer dynamics and pollination success. Oecologia, 192, 1037–1045. https://doi.org/10.1007/s00442-020-04637-5
Batstone, R. T., Carscadden, K. A., Afkhami, M. E., & Frederickson, M. E. (2018). Using niche breadth theory to explain generalization in mutualisms. Ecology, 99(5), 1039–1050. https://doi.org/10.1002/ecy.2188
Bello, C., Galetti, M., Montan, D., Pizo, M. A., Mariguela, T. C., Culot, L., Bufalo, F., Labecca, F., Pedrosa, F., Constantini, R., Emer, C., Silva, W. R., da Silva, F. R., Ovaskainen, O., & Jordano, P. (2017). Atlantic frugivory: A plant–frugivore interaction data set for the Atlantic Forest. Ecology, 98(6), 1729. https://doi.org/10.1002/ecy.1818
Bininda-Emonds, O. R. P., Cardillo, M., Jones, K. E., MacPhee, R. D. E., Beck, R. M. D., Grenyer, R., Price, S. A., Vos, R. A., Gittleman, J. L., & Purvis, A. (2007). The delayed rise of present-day mammals. Nature, 446, 507–512. https://doi.org/10.1038/nature05634
Blüthgen, N., Fründ, J., Vázquez, D. P., & Menzel, F. (2008). What do interaction network metrics tell us about specialization and biological traits? Ecology, 89(12), 3387–3399. https://doi.org/10.1890/07-2121.1
Blüthgen, N., Menzel, F., & Blüthgen, N. (2006). Measuring specialization in species interaction networks. BMC Ecology, 6, 9. https://doi.org/10.1186/1472-6785-6-9
Blüthgen, N., Menzel, F., Hovestadt, T., Fiala, B., & Blüthgen, N. (2007). Specialization, constraints, and conflicting interests in mutualistic networks. Current Biology, 17(4), 341–346. https://doi.org/10.1016/j.cub.2006.12.039
Bolmgren, K., & Eriksson, O. (2005). Fleshy fruits – Origins, niche shifts, and diversification. Oikos, 109(2), 255–272. https://doi.org/10.1111/j.0030-1299.2005.12663.x
Cahill, J. F., Kembel, S. W., Lamb, E. G., & Keddy, P. A. (2008). Does phylogenetic relatedness influence the strength of competition among vascular plants? Perspectives in Plant Ecology, Evolution and Systematics, 10(1), 41–50. https://doi.org/10.1016/j.ppees.2007.10.001
Canard, E. F., Mouquet, N., Mouillot, D., Stanko, M., Miklisova, D., & Gravel, D. (2014). Empirical evaluation of neutral interactions in host-parasite networks. The American Naturalist, 183(4), 468–479. https://doi.org/10.1086/675363
Chagnon, P. (2015). Characterizing topology of ecological networks along gradients: The limits of metrics’ standardization. Ecological Complexity, 22, 36–39. https://doi.org/10.1016/j.ecocom.2015.01.004
Chagnon, P., Magain, N., Miadlikowska, J., & Lutzoni, F. (2018). Strong specificity and network modularity at a very fine phylogenetic scale in the lichen genus Peltigera. Oecologia, 187, 767–782. https://doi.org/10.1007/s00442-018-4159-6
Chagnon, P., Magain, N., Miadlikowska, J., & Lutzoni, F. (2019). Species diversification and phylogenetically constrained symbiont switching generated high modularity in the lichen genus Peltigera. Journal of Ecology, 107(4), 1645–1661. https://doi.org/10.1111/1365-2745.13207
Chávez-González, E., Vizentin-Bugoni, J., Vázquez, D. P., MacGregor-Fors, I., Dáttilo, W., & Ortiz-Pulido, R. (2020). Drivers of the structure of plant–hummingbird interaction networks at multiple temporal scales. Oecologia, 193, 913–924. https://doi.org/10.1007/s00442-020-04727-4
Chomicki, G., Weber, M., Antonelli, A., Bascompte, J., & Kiers, E. T. (2019). The impact of mutualisms on species richness. Trends in Ecology & Evolution, 34(8), 698–711. https://doi.org/10.1016/j.tree.2019.03.003
Colwell, R. K., & Futuyma, D. J. (1971). On the measurement of niche breadth and overlap. Ecology, 52(4), 567–576. https://doi.org/10.2307/1934144
Cooper, N., Griffin, R., Franz, M., Omotayo, M., & Nunn, C. L. (2012). Phylogenetic host specificity and understanding parasite sharing in primates. Ecology Letters, 15(12), 1370–1377. https://doi.org/10.1111/j.1461-0248.2012.01858.x
de Vienne, D. M., Refrégier, G., López-Villavicencio, M., Tellier, A., Hood, M. E., & Giraud, T. (2013). Cospeciation vs host-shift speciation: methods for testing, evidence from natural associations and relation to coevolution. New Phytologist, 198, 347–385. https://doi.org/10.1111/nph.12150
Dehling, D. M., Peralta, G., Bender, I. M. A., Blendinger, P. G., Böhning-Gaese, K., Muñoz, M. C., Neuschulz, E. L., Quitián, M., Saavedra, F., Santillán, V., Schleuning, M., & Stouffer, D. B. (2020). Similar composition of functional roles in Andean seed-dispersal networks, despite high species and interaction turnover. Ecology, 101(7), e03028. https://doi.org/10.1002/ecy.3028
Doña, J., Proctor, H., Mironov, S., Serrano, D., & Jovani, R. (2018). Host specificity, infrequent major host switching and the diversification of highly host-specific symbionts: The case of vane-dwelling feather mites. Global Ecology and Biogeography, 27(2), 188–198. https://doi.org/10.1111/geb.12680
Dorado, J., Vázquez, D. P., Stevani, E. L., & Chacoff, N. P. (2011). Rareness and specialization in plant–pollinator networks. Ecology, 92(1), 19–25. https://doi.org/10.1890/10-0794.1
Dormann, C., Gruber, B., & Fründ, J. (2008). Introducing the bipartite package: analysing ecological networks. R News, 8(2), 8–11. https://cran.r-project.org/doc/Rnews/Rnews_2008-2.pdf
Dormann, C. F., & Strauss, R. (2014). A method for detecting modules in quantitative bipartite networks. Methods in Ecology and Evolution, 5(1), 90–98. https://doi.org/10.1111/2041-210X.12139
Eklöf, A., Helmus, M. R., Moore, M., & Allesina, S. (2012). Relevance of evolutionary history for food web structure. Proceedings of the Royal Society B: Biological Sciences, 279(1733), 1588–1596. https://doi.org/10.1098/rspb.2011.2149
Emer, C., Galetti, M., Pizo, M. A., Jordano, P., & Verdú, M. (2019). Defaunation precipitates the extinction of evolutionarily distinct interactions in the Anthropocene. Science Advances, 5, eaav6699. https://doi.org/10.1126/sciadv.aav6699
Esser, H. J., Herre, E. A., Blüthgen, N., Loaiza, J. R., Bermúdez, S. E., & Jansen, P. A. (2016). Host specificity in a diverse Neotropical tick community: An assessment using quantitative network analysis and host phylogeny. Parasites and Vectors, 9, 1–14. https://doi.org/10.1186/s13071-016-1655-6
Faith, D. P. (1992). Conservation evaluation and phylogenetic diveristy. Biological Conservation, 61(1), 1–10. https://doi.org/10.1016/0006-3207(92)91201-3
Fortuna, M. A., Nagavci, A., Barbour, M. A., & Bascompte, J. (2020). Partner fidelity and asymmetric specialization in ecological networks. The American Naturalist, 196(3), 382–389. https://doi.org/10.1086/709961
Fründ, J., McCann, K. S., & Williams, N. M. (2016). Sampling bias is a challenge for quantifying specialization and network structure: Lessons from a quantitative niche model. Oikos, 125(4), 502–513. https://doi.org/10.1111/oik.02256
Futuyma, D. J., & Moreno, G. (1988). The evolution of ecological specialization. Annual Review of Ecology and Systematics, 19, 207–233. https://doi.org/10.1146/annurev.es.19.110188.001231
Gerhold, P., Cahill, J. F., Winter, M., Bartish, I. V., & Prinzing, A. (2015). Phylogenetic patterns are not proxies of community assembly mechanisms (they are far better). Functional Ecology, 29(5), 600–614. https://doi.org/10.1111/1365-2435.12425
Goberna, M., & Verdú, M. (2016). Predicting microbial traits with phylogenies. The ISME Journal, 10, 959–967. https://doi.org/10.1038/ismej.2015.171
Gómez, J. M., Verdú, M., & Perfectti, F. (2010). Ecological interactions are evolutionarily conserved across the entire tree of life. Nature, 465, 918–921. https://doi.org/10.1038/nature09113
Gomulkiewicz, R., Thompson, J. N., Holt, R. D., Nuismer, S. L., & Hochberg, M. E. (2000). Hot spots, cold spots, and the geographic mosaic theory of coevolution. The American Naturalist, 156(2), 156–174. https://doi.org/10.1086/303382
Guimarães, P. R., Jordano, P., & Thompson, J. N. (2011). Evolution and coevolution in mutualistic networks. Ecology Letters, 14(9), 877–885. https://doi.org/10.1111/j.1461-0248.2011.01649.x
Guimarães, P. R., Pires, M. M., Jordano, P., Bascompte, J., & Thompson, J. N. (2017). Indirect effects drive coevolution in mutualistic networks. Nature, 550, 511–514. https://doi.org/10.1038/nature24273
Guimarães, P. R., Rico-Gray, V., dos Reis, S. F., & Thompson, J. N. (2006). Asymmetries in specialization in ant–plant mutualistic networks. Proceedings of the Royal Society B: Biological Sciences, 273(1597), 2041–2047. https://doi.org/10.1098/rspb.2006.3548
Guimarães, P. R., Rico-Gray, V., Oliveira, P. S. S., Izzo, T. J., dos Reis, S. F., & Thompson, J. N. (2007). Interaction intimacy affects structure and coevolutionary dynamics in mutualistic networks. Current Biology, 17(20), 1797–1803. https://doi.org/10.1016/j.cub.2007.09.059
Harvey, E., Gounand, I., Ward, C. L., & Altermatt, F. (2017). Bridging ecology and conservation: from ecological networks to ecosystem function. Journal of Applied Ecology, 54(2), 371–379. https://doi.org/10.1111/1365-2664.12769
Hurlbert, S. (1978). The measurement of niche overlap and some relatives. Ecology, 59(1), 67–77. https://doi.org/10.2307/1936632
Jordano, P. (1987). Patterns of mutualistic interactions in pollination and seed dispersal: Connectance, dependence asymmetries, and coevolution. The American Naturalist, 129(5), 657–677. https://doi.org/10.1086/284665
Jordano, P., Bascompte, J., & Olesen, J. M. (2002). Invariant properties in coevolutionary networks of plant–animal interactions. Ecology Letters, 6(1), 69–81. https://doi.org/10.1046/j.1461-0248.2003.00403.x
Jorge, L. R., Novotny, V., Segar, S. T., Weiblen, G. D., Miller, S. E., Basset, Y., & Lewinsohn, T. M. (2017). Phylogenetic trophic specialization: A robust comparison of herbivorous guilds. Oecologia, 185, 551–559. https://doi.org/10.1007/s00442-017-3980-7
Jorge, L. R., Prado, P. I., Almeida-Neto, M., & Lewinsohn, T. M. (2014). An integrated framework to improve the concept of resource specialisation. Ecology Letters, 17(11), 1341–1350. https://doi.org/10.1111/ele.12347
Junker, R. R., Blüthgen, N., Brehm, T., Binkenstein, J., Paulus, J., Schaefer, H. M., & Stang, M. (2013). Specialization on traits as basis for the niche-breadth of flower visitors and as structuring mechanism of ecological networks. Functional Ecology, 27(2), 329–341. https://doi.org/10.1111/1365-2435.12005
Kembel, S. W. (2009). Disentangling niche and neutral influences on community assembly: Assessing the performance of community phylogenetic structure tests. Ecology Letters, 12(9), 949–960. https://doi.org/10.1111/j.1461-0248.2009.01354.x
Kembel, S. W., Cowan, P. D., Helmus, M. R., Cornwell, W. K., Morlon, H., Ackerly, D. D., Blomberg, S. P., & Webb, C. O. (2010). Picante: R tools for integrating phylogenies and ecology. Bioinformatics, 26(11), 1463–1464. https://doi.org/10.1093/bioinformatics/btq166
Krasnov, B. R., Fortuna, M. A., Mouillot, D., Khokhlova, I. S., Shenbrot, G. I., & Poulin, R. (2012). Phylogenetic signal in module composition and species connectivity in compartmentalized host-parasite networks. The American Naturalist, 179(4), 501–511. https://doi.org/10.1086/664612
Kullback, S., & Leibler, R. A. (1951). On information and sufficiency. The Annals of Mathematical Statistics, 22(1), 79–86. https://doi.org/10.1214/aoms/1177729694
Lane, B., Spier, T., Wiederholt, J., & Meagher, S. (2014). Host specificity of a parasitic fluke: Is Posthodiplostomum minimum a centrarchid-infecting generalist or specialist? Journal of Parasitology, 101(1), 6–17. https://doi.org/10.1645/14-584.1
Lessard, J., Belmaker, J., Myers, J. A., Chase, J. M., & Rahbek, C. (2012). Inferring local ecological processes amid species pool influences. Trends in Ecology & Evolution, 27(11), 600–607. https://doi.org/10.1016/j.tree.2012.07.006
Lu, J., Magain, N., Miadlikowska, J., Coyle, J. R., Truong, C., & Lutzoni, F. (2018). Bioclimatic factors at an intrabiome scale are more limiting than cyanobiont availability for the lichen-forming genus Peltigera. American Journal of Botany, 105(7), 1198–1211. https://doi.org/10.1002/ajb2.1119
Magain, N., Miadlikowska, J., Goffinet, B., Sérusiaux, E., & Lutzoni, F. (2017). Macroevolution of specificity in cyanolichens of the genus Peltigera section Polydactylon (Lecanoromycetes, Ascomycota). Systematic Biology, 66(1), 74–99. https://doi.org/10.1093/sysbio/syw065
Magain, N., Miadlikowska, J., Mueller, O., Gajdeczka, M., Truong, C., Salamov, A. A., Dubchak, I., Grigoriev, I. V., Goffinet, B., Sérusiaux, E., & Lutzoni, F. (2017). Conserved genomic collinearity as a source of broadly applicable, fast evolving, markers to resolve species complexes: A case study using the lichen-forming genus Peltigera section Polydactylon. Molecular Phylogenetics and Evolution, 117, 10–29. https://doi.org/10.1016/j.ympev.2017.08.013
Magain, N., Truong, C., Goward, T., Niu, D., Goffinet, B., Sérusiaux, E., Vitikainen, O., Lutzoni, F., & Miadlikowska, J. (2018). Species delimitation at a global scale reveals high species richness with complex biogeography and patterns of symbiont association in Peltigera section Peltigera (lichenized Ascomycota: Lecanoromycetes). Taxon, 67(5), 836–870. https://doi.org/10.12705/675.3
Maglianesi, M. A., Blüthgen, N., Böhning-Gaese, K., & Schleuning, M. (2014). Morphological traits determine specialization and resource use in plant–hummingbird networks in the neotropics. Ecology, 95(12), 3325–3334. https://doi.org/10.1890/13-2261.1
Maherali, H., & Klironomos, J. N. (2007). Influence of phylogeny on fungal community assembly and ecosystem functioning. Science, 316, 1746–1748. https://doi.org/10.1126/science.1143082
Mayfield, M. M., & Levine, J. M. (2010). Opposing effects of competitive exclusion on the phylogenetic structure of communities. Ecology Letters, 13(9), 1085–1093. https://doi.org/10.1111/j.1461-0248.2010.01509.x
McGuire, J. A., Witt, C. C., Remsen, J. V., Corl, A., Rabosky, D. L., Altshuler, D. L., & Dudley, R. (2014). Molecular phylogenetics and the diversification of hummingbirds. Current Biology, 24, 910–916. https://doi.org/10.1016/j.cub.2014.03.016
Mello, M. A. R., Felix, G. M., Pinheiro, R. B. P., Muylaert, R. L., Geiselman, C., Santana, S. E., Tschapka, M., Lotfi, N., Rodrigues, F. A., & Stevens, R. D. (2019). Insights into the assembly rules of a continent-wide multilayer network. Nature Ecology & Evolution, 3, 1525–1532. https://doi.org/10.1038/s41559-019-1002-3
Miadlikowska, J., Magain, N., Pardo-De la Hoz, C. J., Niu, D., Goward, T., Sérusiaux, E., & Lutzoni, F. (2018). Species in section Peltidea (aphthosa group) of the genus Peltigera remain cryptic after molecular phylogenetic revision. Plant and Fungal Systematics, 63(2), 45–64. https://doi.org/10.2478/pfs-2018-0007
Miadlikowska, J., Richardson, D., Magain, N., Ball, B., Anderson, F., Cameron, R., Lendemer, J., Truong, C., & Lutzoni, F. (2014). Phylogenetic placement, species delimitation, and cyanobiont identity of endangered aquatic Peltigera species (lichen-forming Ascomycota, Lecanoromycetes). American Journal of Botany, 101(7), 1141–1156. https://doi.org/10.3732/ajb.1400267
Miller, E. T., Farine, D. R., & Trisos, C. H. (2017). Phylogenetic community structure metrics and null models: A review with new methods and software. Ecography, 40, 461–477. https://doi.org/10.1111/ecog.02070
Nelson, J. M., Hauser, D. A., & Li, F. W. (2021). The diversity and community structure of symbiotic cyanobacteria in hornworts inferred from long-read amplicon sequencing. American Journal of Botany, 108(9), 1731–1744. https://doi.org/10.1002/ajb2.1729
O’Brien, H. E., Miadlikowska, J., & Lutzoni, F. (2005). Assessing host specialization in symbiotic cyanobacteria associated with four closely related species of the lichen fungus Peltigera. European Journal of Phycology, 40(4), 363–378. https://doi.org/10.1080/09670260500342647
O’Brien, H. E., Miadlikowska, J., & Lutzoni, F. (2013). Assessing population structure and host specialization in lichenized cyanobacteria. New Phytologist, 198, 557–566. https://doi.org/10.1111/nph.12165
Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., & McGlinn, D. (2019). vegan: Community ecology package. R package version 2.5-4. R Foundation for Statistical Computing.
Olesen, J. M., Bascompte, J., Dupont, Y. L., & Jordano, P. (2007). The modularity of pollination networks. Proceedings of the National Academy of Sciences of the United States of America, 104(50), 19891–19896. https://doi.org/10.1073/pnas.0706375104
Paradis, E., Claude, J., & Strimmer, K. (2004). APE: Analyses of phylogenetics and evolution in R language. Bioinformatics, 20(2), 289–290. https://doi.org/10.1093/bioinformatics/btg412
Pardo-De la Hoz, C. J., Magain, N., Lutzoni, F., Goward, T., Restrepo, S., & Miadlikowska, J. (2018). Contrasting symbiotic patterns in two closely related lineages of trimembered lichens of the genus Peltigera. Frontiers in Microbiology, 9, 2770. https://doi.org/10.3389/fmicb.2018.02770
Peralta, G., Vázquez, D. P., Chacoff, N. P., Lomáscolo, S. B., Perry, G. L. W., & Tylianakis, J. M. (2020). Trait matching and phenological overlap increase the spatio-temporal stability and functionality of plant–pollinator interactions. Ecology Letters, 23(7), 1107–1116. https://doi.org/10.1111/ele.13510
Pinheiro, R. B. P., Félix, G. M. F., Chaves, A. V., Lacorte, G. A., Santos, F. R., Braga, É. M., & Mello, M. A. R. (2016). Trade-offs and resource breadth processes as drivers of performance and specificity in a host–parasite system: a new integrative hypothesis. International Journal for Parasitology, 46(2), 115–121. https://doi.org/10.1016/j.ijpara.2015.10.002
Pinheiro, R. B. P., Felix, G. M. F., Dormann, C. F., & Mello, M. A. R. (2019). A new model explaining the origin of different topologies in interaction networks. Ecology, 100(9), 1–10. https://doi.org/10.1002/ecy.2796
Poisot, T., Bever, J. D., Nemri, A., Thrall, P. H., & Hochberg, M. E. (2011). A conceptual framework for the evolution of ecological specialisation. Ecology Letters, 14(9), 841–851. https://doi.org/10.1111/j.1461-0248.2011.01645.x
Poisot, T., Stouffer, D. B., & Gravel, D. (2015). Beyond species: Why ecological interaction networks vary through space and time. Oikos, 124(3), 243–251. https://doi.org/10.1111/oik.01719
Põlme, S., Bahram, M., Jacquemyn, H., Kennedy, P., Kohout, P., Moora, M., Oja, J., Öpik, M., Pecoraro, L., & Tedersoo, L. (2018). Host preference and network properties in biotrophic plant–fungal associations. New Phytologist, 217, 1230–1239. https://doi.org/10.1111/nph.14895
Poulin, R., Krasnov, B. R., & Mouillot, D. (2011). Host specificity in phylogenetic and geographic space. Trends in Parasitology, 27(8), 355–361. https://doi.org/10.1016/j.pt.2011.05.003
Rezende, E. L., Lavabre, J. E., Guimarães, P. R., Jordano, P., & Bascompte, J. (2007). Non-random coextinctions in phylogenetically structured mutualistic networks. Nature, 448, 925–928. https://doi.org/10.1038/nature05956
Rivera-Hutinel, A., Bustamante, R. O., Marín, V. H., & Medel, R. (2012). Effects of sampling completeness on the structure of plant–pollinator networks. Ecology, 93(7), 1593–1603. https://doi.org/10.1890/11-1803.1
Schleuning, M., Fründ, J., Klein, A.-M., Abrahamczyk, S., Alarcón, R., Albrecht, M., Andersson, G. K. S., Bazarian, S., Böhning-Gaese, K., Bommarco, R., Dalsgaard, B. O., Dehling, D. M., Gotlieb, A., Hagen, M., Hickler, T., Holzschuh, A., Kaiser-Bunbury, C. N., Kreft, H., Morris, R. J., … Blüthgen, N. (2012). Specialization of mutualistic interaction networks decreases toward tropical latitudes. Current Biology, 22(20), 1925–1931. https://doi.org/10.1016/j.cub.2012.08.015
Segar, S. T., Fayle, T. M., Srivastava, D. S., Lewinsohn, T. M., Lewis, O. T., Novotny, V., Kitching, R. L., & Maunsell, S. C. (2020). The role of evolution in shaping ecological networks. Trends in Ecology & Evolution, 35(5), 454–466. https://doi.org/10.1016/j.tree.2020.01.004
Simmons, B. I., Vizentin-Bugoni, J., Maruyama, P. K., Cotton, P. A., Marín-Gómez, O. H., Lara, C., Rosero-Lasprilla, L., Maglianesi, M. A., Ortiz-Pulido, R., Rocca, M. A., Rodrigues, L. C., Tinoco, B. A., Vasconcelos, M. F., Sazima, M., Martín González, A. M., Sonne, J., Rahbek, C., Dicks, L. V., Dalsgaard, B. O., & Sutherland, W. J. (2019). Abundance drives broad patterns of generalisation in plant–hummingbird pollination networks. Oikos, 128(9), 1287–1295. https://doi.org/10.1111/oik.06104
Sonne, J., Vizentin-Bugoni, J., Maruyama, P. K., Araujo, A. C., Chávez-González, E., Coelho, A. G., Cotton, P. A., Marín-Gómez, O. H., Lara, C., Lasprilla, L. R., Machado, C. G., Maglianesi, M. A., Malucelli, T. S., González, A. M. M., Oliveira, G. M., Oliveira, P. E., Ortiz-Pulido, R., Rocca, M. A., Rodrigues, L. C., … Dalsgaard, B. O. (2020). Ecological mechanisms explaining interactions within plant–hummingbird networks: Morphological matching increases towards lower latitudes. Proceedings of the Royal Society B: Biological Sciences, 287(1922), 20192873. https://doi.org/10.1098/rspb.2019.2873
Stang, M., Klinkhamer, P. G. L., & van der Meijden, E. (2007). Asymmetric specialization and extinction risk in plant–flower visitor webs: A matter of morphology or abundance? Oecologia, 151, 442–453. https://doi.org/10.1007/s00442-006-0585-y
Stanko, M., Miklisová, D., Goüy de Bellocq, J., & Morand, S. (2002). Mammal density and patterns of ectoparasite species richness and abundance. Oecologia, 131, 289–295. https://doi.org/10.1007/s00442-002-0889-5
Swenson, N. G. (2013). The assembly of tropical tree communities – The advances and shortcomings of phylogenetic and functional trait analyses. Ecography, 36(3), 264–276. https://doi.org/10.1111/j.1600-0587.2012.00121.x
Swenson, N. G. (2014). Functional and phylogenetic ecology in R. Springer. https://doi.org/10.1007/978-1-4614-9542-0
Thines, M. (2019). An evolutionary framework for host shifts – Jumping ships for survival. New Phytologist, 224, 605–617. https://doi.org/10.1111/nph.16092
Toju, H., Guimarães, P. R., Olesen, J. M., & Thompson, J. N. (2014). Assembly of complex plant–fungus networks. Nature Communications, 5, 5273. https://doi.org/10.1038/ncomms6273
Tucker, C. M., Cadotte, M. W., Carvalho, S. B., Davies, T. J., Ferrier, S., Fritz, S. A., Grenyer, R., Helmus, M. R., Jin, L. S., Mooers, A. O., Pavoine, S., Purschke, O., Redding, D. W., Rosauer, D. F., Winter, M., & Mazel, F. (2017). A guide to phylogenetic metrics for conservation, community ecology and macroecology. Biological Reviews, 92(2), 698–715. https://doi.org/10.1111/brv.12252
Vamosi, J. C., Armbruster, W. S., & Renner, S. S. (2014). Evolutionary ecology of specialization: Insights from phylogenetic analysis. Proceedings of the Royal Society B: Biological Sciences, 281(1795), 20142004. https://doi.org/10.1098/rspb.2014.2004
Vázquez, D. P., Blüthgen, N., Cagnolo, L., & Chacoff, N. P. (2009). Uniting pattern and process in plant–animal mutualistic networks: A review. Annals of Botany, 103(9), 1445–1457. https://doi.org/10.1093/aob/mcp057
Vázquez, D. P., Melián, C. J., Williams, N. M., Blüthgen, N., Krasnov, B. R., & Poulin, R. (2007). Species abundance and asymmetric interaction strength in ecological networks. Oikos, 116(7), 1120–1127. https://doi.org/10.1111/j.0030-1299.2007.15828.x
Vizentin-Bugoni, J., Maruyama, P. K., & Sazima, M. (2014). Processes entangling interactions in communities: Forbidden links are more important than abundance in a hummingbird–plant network. Proceedings of the Royal Society B: Biological Sciences, 281(1780), 20132397. https://doi.org/10.1098/rspb.2013.2397
Webb, C. O. (2000). Exploring the phylogenetic structure of ecological communities: An example for rain forest trees. The American Naturalist, 156(2), 145–155. https://doi.org/10.1086/303378
Webb, C. O., Ackerly, D. D., & Kembel, S. W. (2008). Phylocom: Software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics, 24(18), 2098–2100. https://doi.org/10.1093/bioinformatics/btn358
Webb, C. O., Ackerly, D. D., McPeek, M. A., & Donoghue, M. J. (2002). Phylogenies and community ecology. Annual Review of Ecology and Systematics, 33, 475–505. https://doi.org/10.1146/annurev.ecolsys.33.010802.150448
Young, J., Valdovinos, F. S., & Newman, M. E. J. (2021). Reconstruction of plant–pollinator networks from observational data. Nature Communications, 12, 3911. https://doi.org/10.1038/s41467-021-24149-x
Zanata, T. B., Dalsgaard, B. O., Passos, F. C., Cotton, P. A., Roper, J. J., Maruyama, P. K., Fischer, E., Schleuning, M., Martín González, A. M., Vizentin-Bugoni, J., Franklin, D. C., Abrahamczyk, S., Alárcon, R., Araujo, A. C., Araújo, F. P., Azevedo-Junior, S. M. D., Baquero, A. C., Böhning-Gaese, K., Carstensen, D. W., … Varassin, I. G. (2017). Global patterns of interaction specialization in bird–flower networks. Journal of Biogeography, 44(8), 1891–1910. https://doi.org/10.1111/jbi.13045
Zanne, A. E., Tank, D. C., Cornwell, W. K., Eastman, J. M., Smith, S. A., Fitzjohn, R. G., McGlinn, D. J., O’Meara, B. C., Moles, A. T., Reich, P. B., Royer, D. L., Soltis, D. E., Stevens, P. F., Westboy, M., Wright, I. J., Aarssen, L., Bertin, R. I., Calaminus, A., Govaerts, R., … Beaulieu, J. M. (2014). Three keys to the radiation of angiosperms into freezing environments. Nature, 506, 89–92. https://doi.org/10.1038/nature12872
Zhu, Q., Hastriter, M. W., Whiting, M. F., & Dittmar, K. (2015). Fleas (Siphonaptera) are Cretaceous, and evolved with Theria. Molecular Phylogenetics and Evolution, 90, 129–139. https://doi.org/10.1016/j.ympev.2015.04.027