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The quasi-universality of nestedness in the structure of quantitative plant-parasite interactions
Nestedness and modularity in plant-parasite infection networksRecommended by Santiago Elena based on reviews by Rubén González and 2 anonymous reviewers
In a landmark paper, Flores et al. (2011) showed that the interactions between bacteria and their viruses could be nicely described using a bipartite infection networks. Two quantitative properties of these networks were of particular interest, namely modularity and nestedness. Modularity emerges when groups of host species (or genotypes) shared groups of viruses. Nestedness provided a view of the degree of specialization of both partners: high nestedness suggests that hosts differ in their susceptibility to infection, with some highly susceptible host genotypes selecting for very specialized viruses while strongly resistant host genotypes select for generalist viruses. Translated to the plant pathology parlance, this extreme case would be equivalent to a gene-for-gene infection model (Flor 1956): new mutations confer hosts with resistance to recently evolved viruses while maintaining resistance to past viruses. Likewise, virus mutations for expanding host range evolve without losing the ability to infect ancestral host genotypes. By contrast, a non-nested network would represent a matching-allele infection model (Frank 2000) in which each interacting organism evolves by losing its capacity to resist/infect its ancestral partners, resembling a Red Queen dynamic. Obviously, the reality is more complex and may lie anywhere between these two extreme situations.
Recently, Valverde et al. (2020) developed a model to explain the emergence of nestedness and modularity in plant-virus infection networks across diverse habitats. They found that local modularity could coexist with global nestedness and that intraspecific competition was the main driver of the evolution of ecosystems in a continuum between nested-modular and nested networks. These predictions were tested with field data showing the association between plant host species and different viruses in different agroecosystems (Valverde et al. 2020). The effect of interspecific competition in the structure of empirical plant host-virus infection networks was also tested by McLeish et al. (2019). Besides data from agroecosystems, evolution experiments have also shown the pervasive emergence of nestedness during the diversification of independently-evolved lineages of potyviruses in Arabidopsis thaliana genotypes that differ in their susceptibility to infection (Hillung et al. 2014; González et al. 2019; Navarro et al. 2020).
In their study, Moury et al. (2021) have expanded all these previous observations to a diverse set of pathosystems that range from viruses, bacteria, oomycetes, fungi, nematodes to insects. While modularity was barely seen in only a few of the systems, nestedness was a common trend (observed in ~94% of all systems). This nestedness, as seen in previous studies and as predicted by theory, emerged as a consequence of the existence of generalist and specialist strains of the parasites that differed in their capacity to infect more or less resistant plant genotypes.
As pointed out by Moury et al. (2021) in their conclusions, the ubiquity of nestedness in plant-parasite infection matrices has strong implications for the evolution and management of infectious diseases.
Flor, H. H. (1956). The complementary genic systems in flax and flax rust. In Advances in genetics, 8, 29-54. https://doi.org/10.1016/S0065-2660(08)60498-8
Flores, C. O., Meyer, J. R., Valverde, S., Farr, L., and Weitz, J. S. (2011). Statistical structure of host–phage interactions. Proceedings of the National Academy of Sciences, 108, E288-E297. https://doi.org/10.1073/pnas.1101595108
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González, R., Butković, A., and Elena, S. F. (2019). Role of host genetic diversity for susceptibility-to-infection in the evolution of virulence of a plant virus. Virus evolution, 5(2), vez024. https://doi.org/10.1093/ve/vez052
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McLeish, M., Sacristán, S., Fraile, A., and García-Arenal, F. (2019). Coinfection organizes epidemiological networks of viruses and hosts and reveals hubs of transmission. Phytopathology, 109, 1003-1010. https://doi.org/10.1094/PHYTO-08-18-0293-R
Moury B, Audergon J-M, Baudracco-Arnas S, Krima SB, Bertrand F, Boissot N, Buisson M, Caffier V, Cantet M, Chanéac S, Constant C, Delmotte F, Dogimont C, Doumayrou J, Fabre F, Fournet S, Grimault V, Jaunet T, Justafré I, Lefebvre V, Losdat D, Marcel TC, Montarry J, Morris CE, Omrani M, Paineau M, Perrot S, Pilet-Nayel M-L and Ruellan Y (2021) The quasi-universality of nestedness in the structure of quantitative plant-parasite interactions. bioRxiv, 2021.03.03.433745, ver. 4 recommended and peer-reviewed by PCI Evolutionary Biology. https://doi.org/10.1101/2021.03.03.433745
Navarro, R., Ambros, S., Martinez, F., Wu, B., Carrasco, J. L., and Elena, S. F. (2020). Defects in plant immunity modulate the rates and patterns of RNA virus evolution. bioRxiv. doi: https://doi.org/10.1101/2020.10.13.337402
Valverde, S., Vidiella, B., Montañez, R., Fraile, A., Sacristán, S., and García-Arenal, F. (2020). Coexistence of nestedness and modularity in host–pathogen infection networks. Nature ecology & evolution, 4, 568-577. https://doi.org/10.1038/s41559-020-1130-9