Dobson, A., Lafferty, K. D., Kuris, A. M., Hechinger, R. F. & Jetz, W. Homage to Linnaeus: how many parasites? How many hosts? Proc. Natl Acad. Sci. USA 105, 11482–11489 (2008).
Mideo, N. Parasite adaptations to within-host competition. Trends Parasitol. 25, 261–268 (2009).
Greischar, M. A. et al. Evolutionary consequences of feedbacks between within-host competition and disease control. Evol. Med. Public Health 2020, 30–34 (2020).
Wale, N. et al. Resource limitation prevents the emergence of drug resistance by intensifying within-host competition. Proc. Natl Acad. Sci. USA 114, 13774–13779 (2017).
Bhattacharya, A., Toro Díaz, V. C., Morran, L. T. & Bashey, F. Evolution of increased virulence is associated with decreased spite in the insect-pathogenic bacterium Xenorhabdus nematophila. Biol. Lett. 15, 20190432 (2019).
Susi, H., Barrès, B., Vale, P. F. & Laine, A.-L. Co-infection alters population dynamics of infectious disease. Nat. Commun. 6, 5975 (2015).
Read, A. F. & Taylor, L. H. The ecology of genetically diverse infections. Science 292, 1099–1102 (2001).
Hawley, D. M. & Altizer, S. M. Disease ecology meets ecological immunology: understanding the links between organismal immunity and infection dynamics in natural populations. Funct. Ecol. 25, 48–60 (2011).
Hoverman, J. T., Hoye, B. J. & Johnson, P. T. J. Does timing matter? How priority effects influence the outcome of parasite interactions within hosts. Oecologia 173, 1471–1480 (2013).
Zhan, J. & McDonald, B. A. Experimental measures of pathogen competition and relative fitness. Annu. Rev. Phytopathol. 51, 131–153 (2013).
Hellard, E., Fouchet, D., Vavre, F. & Pontier, D. Parasite–parasite interactions in the wild: how to detect them? Trends Parasitol. 31, 640–652 (2015).
Tollenaere, C., Susi, H. & Laine, A. L. Evolutionary and epidemiological implications of multiple infection in plants. Trends Plant Sci. 21, 80–90 (2015).
Budischak, S. A. et al. Competing for blood: the ecology of parasite resource competition in human malaria–helminth co-infections. Ecol. Lett. 21, 536–545 (2018).
Griffiths, E. C., Pedersen, A. B., Fenton, A. & Petchey, O. L. Analysis of a summary network of co-infection in humans reveals that parasites interact most via shared resources. Proc. R. Soc. B 281, 20132286 (2014).
Ezenwa, V. O. Helminth–microparasite co-infection in wildlife: lessons from ruminants, rodents and rabbits. Parasite Immunol. 38, 527–534 (2016).
Lello, J., Boag, B., Fenton, A., Stevenson, I. R. & Hudson, P. J. Competition and mutualism among the gut helminths of a mammalian host. Nature 428, 840–844 (2004).
Chung, E., Petit, E., Antonovics, J., Pedersen, A. B. & Hood, M. E. Variation in resistance to multiple pathogen species: anther smuts of Silene uniflora. Ecol. Evol. 2, 2304–2314 (2012).
Halliday, F. W., Umbanhowar, J. & Mitchell, C. E. A host immune hormone modifies parasite species interactions and epidemics: insights from a field manipulation. Proc. R. Soc. B 285, 20182075 (2018).
Eswarappa, S. M., Estrela, S. & Brown, S. P. Within-host dynamics of multi-species infections: facilitation, competition and virulence. PLoS ONE 7, e38730 (2012).
Zélé, F., Magalhães, S., Kéfi, S. & Duncan, A. B. Ecology and evolution of facilitation among symbionts. Nat. Commun. 9, 4869 (2018).
Jenner, E. An Inquiry into the Causes and Effects of the Variolae Vaccinae, a Disease Discovered in Some of the Western Countries of England, Particularly Gloucestershire, and Known by the Name of “The Cow Pox” (1798) Vol. 84 (R. Lier, 1923).
Fulton, R. W. Practices and precautions in the use of cross protection for plant virus disease control. Annu. Rev. Phytopathol. 24, 67–81 (1986).
Van Loon, L. C. Induced resistance in plants and the role of pathogenesis-related proteins. Eur. J. Plant Pathol. 103, 753–765 (1997).
Conrath, U. et al. Priming: getting ready for battle. Mol. Plant Microbe Interact. 19, 1062–1071 (2006).
Pieterse, C. M. J. et al. Induced systemic resistance by beneficial microbes. Annu. Rev. Phytopathol. 52, 347–375 (2014).
Spoel, S. H., Johnson, J. S. & Dong, X. Regulation of tradeoffs between plant defenses against pathogens with different lifestyles. Proc. Natl Acad. Sci. USA 104, 18842–18847 (2007).
Kliebenstein, D. J. & Rowe, H. C. Ecological costs of biotrophic versus necrotrophic pathogen resistance, the hypersensitive response and signal transduction. Plant Sci. 174, 551–556 (2008).
Koornneef, A. et al. Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol. 147, 1358–1368 (2008).
Glazebrook, J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205–227 (2005).
Ezenwa, V. O., Etienne, R. S., Luikart, G., Beja-Pereira, A. & Jolles, A. E. Hidden consequences of living in a wormy world: nematode‐induced immune suppression facilitates tuberculosis invasion in African buffalo. Am. Nat. 176, 613–624 (2010).
Clay, P. A., Cortez, M. H., Duffy, M. A. & Rudolf, V. H. W. Priority effects within coinfected hosts can drive unexpected population‐scale patterns of parasite prevalence. Oikos 128, 571–583 (2019).
Clay, P. A., Duffy, M. A. & Rudolf, V. H. W. Within-host priority effects and epidemic timing determine outbreak severity in co-infected populations. Proc. R. Soc. B 287, 20200046 (2020).
Clark, P., Ward, W., Lang, S., Saghbini, A. & Kristan, D. Order of inoculation during Heligmosomoides bakeri and Hymenolepis microstoma coinfection alters parasite life history and host responses. Pathogens 2, 130–152 (2013).
Fukami, T. Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annu. Rev. Ecol. Evol. Syst. 46, 1–23 (2015).
Vannette, R. L. & Fukami, T. Historical contingency in species interactions: towards niche-based predictions. Ecol. Lett. 17, 115–124 (2014).
Halliday, F. W., Umbanhowar, J. & Mitchell, C. E. Interactions among symbionts operate across scales to influence parasite epidemics. Ecol. Lett. 20, 1285–1294 (2017).
Johnson, P. T. J., de Roode, J. C. & Fenton, A. Why infectious disease research needs community ecology. Science 349, 1259504 (2015).
Karvonen, A., Jokela, J. & Laine, A.-L. Importance of sequence and timing in parasite coinfections. Trends Parasitol. 35, 109–118 (2019).
Mordecai, E. A., Gross, K. & Mitchell, C. E. Within-host niche differences and fitness trade-offs promote coexistence of plant viruses. Am. Nat. 187, E13–E26 (2016).
Kuris, A. M., Blaustein, A. R. & Alio, J. J. Hosts as islands. Am. Nat. 116, 570–586 (1980).
Rynkiewicz, E. C., Pedersen, A. B. & Fenton, A. An ecosystem approach to understanding and managing within-host parasite community dynamics. Trends Parasitol. 31, 212–221 (2015).
Sousa, W. P. Interspecific interactions among larval trematode parasites of freshwater and marine snails. Am. Zool. 32, 583–592 (1992).
Graham, A. L. Ecological rules governing helminth microparasite coinfection. Proc. Natl Acad. Sci. USA 105, 566–570 (2008).
Seabloom, E. W. et al. The community ecology of pathogens: coinfection, coexistence and community composition. Ecol. Lett. 18, 401–415 (2015).
Cobey, S. & Lipsitch, M. Pathogen diversity and hidden regimes of apparent competition. Am. Nat. 181, 12–24 (2013).
Greischar, M. A. & Koskella, B. A synthesis of experimental work on parasite local adaptation. Ecol. Lett. 10, 418–434 (2007).
Hoeksema, J. D. & Forde, S. E. A meta-analysis of factors affecting local adaptation between interacting species. Am. Nat. 171, 275–290 (2008).
Burdon, J. J. & Laine, A.-L. Evolutionary Dynamics of Plant Pathogen Interactions (Cambridge Univ. Press, 2019).
Lambrechts, L., Fellous, S. & Koella, J. C. Coevolutionary interactions between host and parasite genotypes. Trends Parasitol. 22, 12–16 (2006).
Ferro, K. et al. Experimental evolution of immunological specificity. Proc. Natl Acad. Sci. USA 116, 20598–20604 (2019).
Westman, S. M., Kloth, K. J., Hanson, J., Ohlsson, A. B. & Albrectsen, B. R. Defence priming in Arabidopsis—a meta-analysis. Sci. Rep. 9, 13309 (2019).
Pedersen, A. B. & Fenton, A. Emphasizing the ecology in parasite community ecology. Trends Ecol. Evol. 22, 133–139 (2007).
Pedersen, A. B. & Fenton, A. The role of antiparasite treatment experiments in assessing the impact of parasites on wildlife. Trends Parasitol. 31, 200–211 (2015).
Laine, A. L. Context-dependent effects of induced resistance under co-infection in a plant–pathogen interaction. Evol. Appl. 4, 696–707 (2011).
Conrath, U., Beckers, G. J. M., Langenbach, C. J. G. & Jaskiewicz, M. R. Priming for enhanced defense. Annu. Rev. Phytopathol. 53, 97–119 (2015).
Douma, J. C., Vermeulen, P. J., Poelman, E. H., Dicke, M. & Anten, N. P. R. When does it pay off to prime for defense? A modeling analysis. N. Phytol. 216, 782–797 (2017).
Mauch-Mani, B., Baccelli, I., Luna, E. & Flors, V. Defense priming: an adaptive part of induced resistance. Annu. Rev. Plant Biol. 68, 485–512 (2017).
Budischak, S. A. et al. Resource limitation alters the consequences of co-infection for both hosts and parasites. Int. J. Parasitol. 45, 455–463 (2015).
Borer, E. T., Laine, A.-L. & Seabloom, E. W. A multiscale approach to plant disease using the metacommunity concept. Annu. Rev. Phytopathol. 54, 397–418 (2016).
Bushnell, W. R. in The Powdery Mildews: A Comprehensive Treatise (eds Belanger, R. R. et al.) 1–12 (APS, 2002).
Warton, D. I., Wright, S. T. & Wang, Y. Distance-based multivariate analyses confound location and dispersion effects. Methods Ecol. Evol. 3, 89–101 (2012).
Wang, Y., Naumann, U., Wright, S. T. & Warton, D. I. Mvabund—an R package for model-based analysis of multivariate abundance data. Methods Ecol. Evol. 3, 471–474 (2012).
Benesh, D. P. & Kalbe, M. Experimental parasite community ecology: intraspecific variation in a large tapeworm affects community assembly. J. Anim. Ecol. 85, 1004–1013 (2016).
Mucha, J. et al. Effect of simulated climate warming on the ectomycorrhizal fungal community of boreal and temperate host species growing near their shared ecotonal range limits. Microb. Ecol. 75, 348–363 (2018).
Chang, A. L., Brown, C. W., Crooks, J. A. & Ruiz, G. M. Dry and wet periods drive rapid shifts in community assembly in an estuarine ecosystem. Glob. Change Biol. 24, e627–e642 (2018).
David, A. S., Seabloom, E. W. & May, G. Disentangling environmental and host sources of fungal endophyte communities in an experimental beachgrass study. Mol. Ecol. 26, 6157–6169 (2017).
Penczykowski, R. M., Parratt, S. R., Barrès, B., Sallinen, S. K. & Laine, A. L. Manipulating host resistance structure reveals impact of pathogen dispersal and environmental heterogeneity on epidemics. Ecology 99, 2853–2863 (2018).
Pieterse, C. M. J. et al. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 28, 489–521 (2012).
Susi, H. & Laine, A.-L. The effectiveness and costs of pathogen resistance strategies in a perennial plant. J. Ecol. 103, 303–315 (2015).
Höckerstedt, L. Evolutionary and Ecological Dimensions of Disease Resistance. PhD dissertation, Univ. of Helsinki (2020); https://helda.helsinki.fi/handle/10138/314983
Macke, E. et al. Diet and genotype of an aquatic invertebrate affect the composition of free-living microbial communities. Front. Microbiol. 11, 380 (2020).
Wagner, M. R. et al. Host genotype and age shape the leaf and root microbiomes of a wild perennial plant. Nat. Commun. 7, 12151 (2016).
Koch, H. & Schmid-Hempel, P. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc. Natl Acad. Sci. USA 108, 19288–19292 (2011).
Biere, A. & Goverse, A. Plant-mediated systemic interactions between pathogens, parasitic nematodes, and herbivores above- and belowground. Annu. Rev. Phytopathol. 54, 499–527 (2016).
Little, T. J., Watt, K. & Ebert, D. Parasite–host specificity: experimental studies on the basis of parasite adaptation. Evolution 60, 31–38 (2006).
Seybold, H. et al. A fungal pathogen induces systemic susceptibility and systemic shifts in wheat metabolome and microbiome composition. Nat. Commun. 11, 1910 (2020).
Cui, J. et al. Pseudomonas syringae manipulates systemic plant defenses against pathogens and herbivores. Proc. Natl Acad. Sci. USA 102, 1791–1796 (2005).
Mideo, N., Alizon, S. & Day, T. Linking within- and between-host dynamics in the evolutionary epidemiology of infectious diseases. Trends Ecol. Evol. 23, 511–517 (2008).
Pedersen, A. B. & Greives, T. J. The interaction of parasites and resources cause crashes in a wild mouse population. J. Anim. Ecol. 77, 370–377 (2008).
Laine, A.-L., Barrès, B., Numminen, E. & Siren, J. P. Variable opportunities for outcrossing result in hotspots of novel genetic variation in a pathogen metapopulation. eLife 8, e47091 (2019).
Vaumourin, E. & Laine, A.-L. Role of temperature and coinfection in mediating pathogen life-history traits. Front. Plant Sci. 9, 1670 (2018).
Numminen, E., Vaumourin, E., Parratt, S. R., Poulin, L. & Laine, A.-L. Variation and correlations between sexual, asexual and natural enemy resistance life-history traits in a natural plant pathogen population. BMC Evol. Biol. 19, 142 (2019).
Tack, A. J. M., Thrall, P. H., Barrett, L. G., Burdon, J. J. & Laine, A.-L. Variation in infectivity and aggressiveness in space and time in wild host–pathogen systems: causes and consequences. J. Evol. Biol. 25, 1918–1936 (2012).
Penczykowski, R. M., Laine, A. L. & Koskella, B. Understanding the ecology and evolution of host–parasite interactions across scales. Evol. Appl. 9, 37–52 (2016).
Rynkiewicz, E. C., Fenton, A. & Pedersen, A. B. Linking community assembly and structure across scales in a wild mouse parasite community. Ecol. Evol. 9, 13752–13763 (2019).
Bolnick, D. I. et al. Why intraspecific trait variation matters in community ecology. Trends Ecol. Evol. 26, 183–192 (2011).
Siefert, A. Incorporating intraspecific variation in tests of trait-based community assembly. Oecologia 170, 767–775 (2012).
Laughlin, D. C. et al. A predictive model of community assembly that incorporates intraspecific trait variation. Ecol. Lett. 15, 1291–1299 (2012).
Shaw, D. J. & Dobson, A. P. Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111, S111–S133 (1995).
Lloyd-Smith, J. O., Schreiber, S. J., Kopp, P. E. & Getz, W. M. Superspreading and the effect of individual variation on disease emergence. Nature 438, 355–359 (2005).
Sagar, G. R. & Harper, J. L. Plantago major L., P. media L. and P. lanceolata. J. Ecol. 52, 189–221 (1964).
Ross, M. D. Inheritance of self-incompatibility in Plantago lanceolata. Heredity (Edinb.) 30, 169–176 (1973).
Ojanen, S. P., Nieminen, M., Meyke, E., Pöyry, J. & Hanski, I. Long-term metapopulation study of the Glanville fritillary butterfly (Melitaea cinxia): survey methods, data management, and long-term population trends. Ecol. Evol. 3, 3713–3737 (2013).
Tollenaere, C. & Laine, A. L. Investigating the production of sexual resting structures in a plant pathogen reveals unexpected self-fertility and genotype-by-environment effects. J. Evol. Biol. 26, 1716–1726 (2013).
Tack, A. & Laine, A. Ecological and evolutionary implications of spatial heterogeneity during the off‐season for a wild plant pathogen. N. Phytol. 65, 297–308 (2014).
Laine, A. L. & Hanski, I. Large-scale spatial dynamics of a specialist plant pathogen in a fragmented landscape. J. Ecol. 94, 217–226 (2006).
Jousimo, J. et al. Ecological and evolutionary effects of fragmentation on infectious disease dynamics. Science 344, 1289–1293 (2014).
Laine, A. L. Resistance variation within and among host populations in a plant-pathogen metapopulation: implications for regional pathogen dynamics. J. Ecol. 92, 990–1000 (2004).
Penczykowski, R. M., Walker, E., Soubeyrand, S. & Laine, A.-L. Linking winter conditions to regional disease dynamics in a wild plant-pathogen metapopulation. N. Phytol. 205, 1142–1152 (2015).
Laine, A. L. Pathogen fitness components and genotypes differ in their sensitivity to nutrient and temperature variation in a wild plant–pathogen association. J. Evol. Biol. 20, 2371–2378 (2007).
Tollenaere, C. et al. SNP design from 454 sequencing of Podosphaera plantaginis transcriptome reveals a genetically diverse pathogen metapopulation with high levels of mixed-genotype infection. PLoS ONE 7, e52492 (2012).
Nicot, P. C., Bardin, M. & Dik, A. J. in The Powdery Mildews: A Comprehensive Treatise (eds Belanger, R. R. et al.) 83–99 (APS, 2002).
Parratt, S. R., Barrès, B., Penczykowski, R. M. & Laine, A.-L. Local adaptation at higher trophic levels: contrasting hyperparasite–pathogen infection dynamics in the field and laboratory. Mol. Ecol. 26, 1964–1979 (2017).
R: A Language and Environment for Statistical Computing v.3.5.2 (R Core Team, 2015); https://doi.org/10.1007/978-3-540-74686-7
Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2014).
Lenth, R. et al. Emmeans: Estimated marginal means, aka least-squares means. R package version 1.3.3 (2018).
Hui, F. K. C. boral—Bayesian ordination and regression analysis of multivariate abundance data in R. Methods Ecol. Evol. 7, 744–750 (2016).
Bedward, M. ggboral: View BORAL model results with ggplot. R package version 0.1.6 (2019).
Ploner, M. & Heinze, G. coxphf: Cox regression with Firth’s penalized likelihood. R package version 1.13 (2015).