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The average frequency of host resistance across the metapopulation at 1000 generations for hosts with death rates of 0.05, 0.25, and 0.5, respectively, as a function of the disease transmission rate of the susceptible genotype. Black circles represent parameter ranges for which a long-term pathogen persistence was possible, while grey circles indicate parameter values that resulted in the pathogen going extinct in less than 1000 generations (see Fig. 1). Each point represents the mean of 50 random runs at 1000 generations.
Source publication
Abstract
Questions: How do disease transmission rates, host longevity, and spatial structure interact to determine disease dynamics and evolution of host resistance in systems where host sterility is the major consequence of infection?
Features of model: A spatially explicit two-dimensional simulation model with deterministic within-population b...
Citations
... (Clark et al. 2017)] and evolutionary models have considered the evolution of resistance in populations with no age structure (e.g. Antonovics and Thrall 1994;Boots and Haraguchi 1999;Carlsson-Graner and Thrall 2006;Miller et al. 2007;Donnelly et al. 2015). In contrast, the evolution of age-structured resistance has received relatively little attention. ...
Many organisms experience an increase in disease resistance as they age, but the time of life at which this change occurs varies. Increases in resistance are partially due to prior exposure and physiological constraints, but these cannot fully explain the observed patterns of age-related resistance. An alternative explanation is that developing resistance at an earlier age incurs costs to other life-history traits. Here, we explore how trade-offs with host reproduction or mortality affect the evolution of the onset of resistance, depending on when during the host’s life cycle the costs are paid (only when resistance is developing, only when resistant or throughout the lifetime). We find that the timing of the costs is crucial to determining evolutionary outcomes, often making the difference between resistance developing at an early or late age. Accurate modelling of biological systems therefore relies on knowing not only the shape of trade-offs but also when they take effect. We also find that the evolution of the rate of onset of resistance can result in evolutionary branching. This provides an alternative, possible evolutionary history of populations which are dimorphic in disease resistance, where the rate of onset of resistance has diversified rather than the level of resistance.
Supplementary Information
The online version contains supplementary material available at 10.1007/s11538-023-01144-5.
... The highly variable interannual infection and recovery rates indicated a surprisingly dynamic system, which would be typically expected only in hosts with higher annual mortality rates and shorter lifespans (reviewed in Carlsson-Granér and Thrall, 2006). Some of the observed infections and recoveries could be accounted for by plants that changed their disease state multiple times during the study. ...
Pollinator-transmitted pathogens typically hinder sexual reproduction of their hosts and affect pollen flow among remaining healthy individuals in a population. The extent to which a pathogen also influences host’s population growth depends on the importance of sexual reproduction for the host’s life cycle. Such pathogen impact cannot be traced by measuring only the vital rates directly affected by the pathogen, and thus a study of the host’s entire life cycle is necessary.
In this study, we aimed to quantify the effects of the pollinator-transmitted anther smut pathogen Microbotryum carthusianorum on population growth rate in three populations of the long-lived perennial Dianthus carthusianorum. We followed plant individuals over three years and measured their size, disease state, and reproduction. We then constructed an Integral Projection Model (IPM). To evaluate the pathogen impact, we performed a stochastic analysis of the IPM for real diseased populations as well as for simulated populations without the pathogen. As the populations also hosted predispersal seed predators, the same approach was used to evaluate their impact.
Stochastic population growth rates indicated two of the real populations to be increasing, and one to be declining. Comparison with the simulated healthy populations showed that the pathogen impact on the growth rate was negative and relatively strong, because the growth rate was highly sensitive to changes in sexual reproduction. However, the pathogen did not appear to cause the decline in the one decreasing population, since the growth rate there was impaired more substantially by high rates of predispersal seed predation and low germination rates than by the castration of diseased flowers.
Overall, our study suggests that D. carthusianorum is highly vulnerable to biotic interactions affecting sexual reproduction pathway. Additionally, our study illustrated several complexities in disease dynamics (e.g., occurrence of partially or fully asymptomatic plants) that need to be incorporated into the assessment of the impact of pollinator-transmitted pathogens on long-lived perennials.
... To date, theoretical models have explored the spread of disease in age-structured populations [3] or the evolution of immunity in populations with no age structure [46][47][48][49][50]. However, the evolution of innate, infection-preventing resistance at different life stages has received little attention. ...
... Previous theory has almost entirely focused on the evolution of resistance in populations without age structure [46][47][48][49][50]. Our model was an extension of the one explored by Ashby & Bruns, which considered the evolution of juvenile susceptibility (the inverse of resistance) subject to trade-offs with reproduction or maturation [51]. ...
Innate, infection-preventing resistance often varies between host life stages. Juveniles are more resistant than adults in some species, whereas the opposite pattern is true in others. This variation cannot always be explained by prior exposure or physiological constraints and so it has been hypothesized that trade-offs with other life-history traits may be involved. However, little is known about how trade-offs between various life-history traits and resistance at different life stages affect the evolution of age-specific resistance. Here, we use a mathematical model to explore how trade-offs with natural mortality, reproduction and maturation combine to affect the evolution of resistance at different life stages. Our results show that certain combinations of trade-offs have substantial effects on whether adults or juveniles are more resistant, with trade-offs between juvenile resistance and adult reproduction inherently more costly than trade-offs involving maturation or mortality (all else being equal), resulting in consistent evolution of lower resistance at the juvenile stage even when infection causes a lifelong fecundity reduction. Our model demonstrates how the differences between patterns of age-structured resistance seen in nature may be explained by variation in the trade-offs involved and our results suggest conditions under which trade-offs tend to select for lower resistance in juveniles than adults.
... Tato data poměrně odpovídají i pozorování jiných, příbuzných druhů, jako jsou silenky, v jejichž populacích tyto housenky dokázaly predovat až na 50 % všech plodů (Biere & Honders, 1996b). starší populační a modelovací studie tuto možnost úplně vylučují (Carlsson & Elmquist, 1992;Carlsson-Granér & Thrall, 2006), případně ji v modelech zanedbávají (Alexander & Antonovics, 1988). I novější populační studie však vychází z předpokladu, že nakažené rostliny se nemohou rozmnožovat, čímž ignoruje i částečné nákazy, zmiňované výše, a dokonce jsou zde rostliny, které střídají status nákazy, z populačního vzorku vyřazeny s odůvodněním pravděpodobné chyby správného určení dané lodyhy . ...
... Likewise, well-fed Daphnia infected with the bacterium Pasteuria ramosa have increased survival but also produce more of the bacterial transmission-stage spores relative to undernourished Daphnia [17]. Even if the only observable effect is increased survival or longevity of the host, the parasite may benefit indirectly by having more time for reproduction and/or transmission to a new host [18]. ...
Parasites often modify host foraging behavior, for example, by spurring changes to nutrient intake ratios or triggering self-medication. The gut parasite, Nosema ceranae, increases energy needs of the European or Western honey bee (Apis mellifera), but little is known about how infection affects foraging behavior. We used a combination of experiments and observations of caged and free-flying individual bees and hives to determine how N. ceranae affects honey bee foraging behavior. In an experiment with caged bees, we found that infected bees with access to a high-quality pollen were more likely to survive than infected bees with access to a lower quality pollen or no pollen. Non-infected bees showed no difference in survival with pollen quality. We then tested free-flying bees in an arena of artificial flowers and found that pollen foraging bees chose pollen commensurate with their infection status; twice as many infected bees selected the higher quality pollen than the lower quality pollen, while healthy bees showed no preference between pollen types. However, healthy and infected bees visited sucrose and pollen flowers in the same proportions. Among hive-level observations, we found no significant correlations between N. ceranae infection intensity in the hive and the proportion of bees returning with pollen. Our results indicate that N. ceranae-infected bees benefit from increased pollen quality and will selectively forage for higher quality while foraging for pollen, but infection status does not lead to increased pollen foraging at either the individual or hive levels.
... The fact that juvenile susceptibility is lowest among hosts with intermediate lifespans contrasts with results from non-age-structured models, where innate susceptibility is typically predicted to decrease with lifespan [26][27][28][29][30][31] (although see exceptions in [28] and [31]). In both types of model, disease prevalence increases with host lifespan, which makes susceptibility more costly. ...
Infection prior to reproduction usually carries greater fitness costs for hosts than infection later in life, suggesting selection should tend to favour juvenile resistance. Yet, juveniles are generally more susceptible than adults across a wide spectrum of host taxa. While physiological constraints and a lack of prior exposure can explain some of this pattern, studies in plants and insects suggest that hosts may trade off juvenile susceptibility against other life-history traits. However, it is unclear precisely how trade-offs shape the evolution of juvenile susceptibility. Here, we theoretically explore the evolution of juvenile susceptibility subject to trade-offs with maturation or reproduction, which could realistically occur due to resource allocation during development (e.g. prioritizing growth over immune defence). We show how host lifespan, the probability of maturation (i.e. of reaching the adult stage) and transmission mode affect the results. Our key finding is that elevated juvenile susceptibility is expected to evolve over a wide range of conditions, but should be lowest when hosts have moderate lifespans and an intermediate probability of reaching the adult stage. Our results elucidate how interactions between trade-offs and the epidemiological-demographic structure of the population can lead to the evolution of elevated juvenile susceptibility.
... For example, the anther smut pathogen Microbotryum violaceum causes infected plants to produce flowers with anthers containing fungal spores that are transmitted to new hosts via pollinators, reducing population growth (13,30). Empirical work with this pathogen has demonstrated that spatial aggregation of host individuals can reduce disease prevalence, whereas patchy, discontinuous host populations are less diseased (5,31). Thus, the spatial organization and connectivity of host individuals (patches, in this conception) may alter the rate of infection spread and total prevalence across the metapopulation of hosts. ...
Plant disease arises from the interaction of processes occurring at multiple spatial and temporal scales. With new tools such as next-generation sequencing, we are learning about the diversity of microbes circulating within and among plant populations and often coinhabiting host individuals. The proliferation of pathogenic microbes depends on single-species dynamics and multispecies interactions occurring within and among host cells, the spatial organization and genetic landscape of hosts, the frequency and mode of transmission among hosts and host populations, and the abiotic environmental context. Here, we examine empirical evidence from these multiple scales to assess the utility of metacommunity theory, a theoretical framework developed for free-living organisms to further our understanding of and assist in predicting plant-pathogen infection and spread. We suggest that deeper understanding of disease dynamics can arise through the application of this conceptual framework at scales ranging from individual cells to landscapes. In addition, we use this multiscale theoretical perspective to synthesize existing knowledge, generate novel hypotheses, and point toward promising future opportunities for the study of plant pathogens in natural populations. Expected final online publication date for the Annual Review of Phytopathology Volume 54 is August 04, 2016. Please see http://www.annualreviews.org/catalog/pubdates.aspx for revised estimates.
... All rights reserved. Granér & Thrall 2006;Carlsson-Granér et al. 2014). This was explained by lower population connectedness preventing the maintenance and selection for resistant host genotypes. ...
Cold-adapted organisms with current arctic-alpine distributions have persisted during the last glaciation in multiple ice-free refugia, leaving footprints in their population structure that contrast with temperate plants and animals. However, pathogens that live within hosts having arctic-alpine distributions have been little studied. Here, we therefore investigated the geographical range and population structure of a fungus parasitizing an arctic-alpine plant. A total of 1437 herbarium specimens of the plant Silene acaulis were examined, and the anther smut pathogen Microbotryum silenes-acaulis was present throughout the host's geographic range. There was significantly greater incidence of anther smut disease in more northern latitudes and where the host locations were less dense, indicating a major influence of environmental factors and/or host demographic structure on the pathogen distribution. Genetic analyses with seven microsatellite markers on recent collections of 195 M. silenes-acaulis individuals revealed three main genetic clusters, in North America, northern Europe and southern Europe, likely corresponding to differentiation in distinct refugia during the last glaciation. The lower genetic diversity in northern Europe indicates postglacial recolonization northwards from southern refugia. This study combining herbarium surveys and population genetics thus uniquely reveals the effects of climate and environmental factors on a plant pathogen species with an arctic-alpine distribution. This article is protected by copyright. All rights reserved.
... This spatial structuring of populations can have substantial effects on host and pathogen numerical and genetic dynamics. For example, pathogen persistence is generally expected to be higher in systems of partially connected host populations than in isolated local populations (Thrall and Antonovics 1995;Thrall and Burdon 1999;Thompson 1999;Carlsson-Granér and Thrall 2002;2006). This is partly because the level of among-population disease dispersal increases as host populations become more connected, which may stabilize local fluctuations in pathogen numbers as well as rescue the pathogen from regional extinction (Thrall and Antonovics 1995;Brooks et al. 2008). ...
... However, although increasing the degree of among-population connectedness may initially result in greater disease spread, host resistance genes may also spread more easily among populations, depending on the extent of gene flow and host dispersal ability. This is likely to increase effective host population size and the encounter rate between particular host and pathogen genotypes, which may favor selection of host resistance Thrall and Burdon 2003;Brown and Tellier 2011) and ultimately reduce disease levels in local populations Carlsson-Granér and Thrall 2002;Antonovics 2004;Jousimo et al. 2014). However, resistance polymorphism can be maintained even in highly connected situations as a result of population turnover and heterogeneity in disease prevalence combined with a lower per-capita reproduction associated with resistance (Boots and Haraguchi 1999;Carlsson-Granér and Thrall 2002;Carlsson-Granér and Pettersson 2005;Brown and Tellier 2011;Gibert et al. 2013;Moreno-Gámez et al. 2013), which can mediate host-pathogen coexistence at the metapopulation level (Thrall and Antonovics 1995;Brooks et al. 2008). ...
... This is likely to increase effective host population size and the encounter rate between particular host and pathogen genotypes, which may favor selection of host resistance Thrall and Burdon 2003;Brown and Tellier 2011) and ultimately reduce disease levels in local populations Carlsson-Granér and Thrall 2002;Antonovics 2004;Jousimo et al. 2014). However, resistance polymorphism can be maintained even in highly connected situations as a result of population turnover and heterogeneity in disease prevalence combined with a lower per-capita reproduction associated with resistance (Boots and Haraguchi 1999;Carlsson-Granér and Thrall 2002;Carlsson-Granér and Pettersson 2005;Brown and Tellier 2011;Gibert et al. 2013;Moreno-Gámez et al. 2013), which can mediate host-pathogen coexistence at the metapopulation level (Thrall and Antonovics 1995;Brooks et al. 2008). ...
Theory predicts that hosts and pathogens will evolve higher resistance and aggressiveness in systems where populations are spatially connected than in situations where populations are isolated and dispersal is more local. In a large cross-inoculation experiment we surveyed patterns of host resistance and pathogen infectivity in anther-smut diseased Viscaria alpina populations from three contrasting areas where populations range from continuous, through patchy but spatially connected to highly isolated demes. In agreement with theory, isolated populations of V. alpina were more susceptible on average than either patchily distributed or continuous populations. While increased dispersal in connected systems increases disease spread, it may also increase host gene flow and the potential for greater host resistance to evolve. In the Viscaria-Microbotryum system, pathogen infectivity mirrored patterns of host resistance with strains from the isolated populations being the least infective and strains from the more resistant continuous populations being the most infective on average, suggesting that high resistance selects for high infectivity. To our knowledge this study is the first to characterize the impacts of varying spatial connectivity on patterns of host resistance and pathogen infectivity in a natural system. This article is protected by copyright. All rights reserved.
This article is protected by copyright. All rights reserved.
... The Caryophyllaceous hosts of the anther-smut vary from short-lived biennial to long-lived perennial species (Thrall et al. 1993). Disease transmission rates have been shown to be higher in shorter-than in longer-lived host species (Carlsson-Granér and Thrall 2006) and anther-smuts consist of several sibling species specialized on different host species (Le Gac et al. 2007;Lutz et al. 2008). Our study species are 'relatively' short-lived; S. dioica plants live on average 6 years (2009) and some up to 20 years (Carlsson-Granér unpubl.), ...
... While variation in host and pathogen life history is likely to have significant influences on the evolution of host resistance and pathogen fitness traits (e.g. transmission rate, infectivity, aggressiveness (Kirchner and Roy 1999;Thrall and Burdon 2004;Carlsson-Granér and Thrall 2006;Gibson et al. 2013), it has largely been ignored in studies of host-pathogen coevolution. Moreover, in the anther-smut host systems, there is a need for studies of host-parasite specificity, the genetic control of host resistance and pathogen infectivity and aggressiveness. ...
We use data from species of the anther-smut fungi and the host plants Lychnis alpina and Silene dioica to show that spatial structuring at different scales can influence patterns of disease and host resistance. Patterns of disease and host resistance were surveyed in an archipelago subject to land-uplift where populations of S. dioica constitute an age-structured metapopulation, and in three contrasting areas within the mainland range of L. alpina, where population distributions range from continuous, through patchy but spatially connected to highly isolated demes. In S. dioica, disease levels depend on the age, size and density of local patches and populations. Disease is most predictably found in larger dense host patches and populations of intermediate age, and more frequently goes extinct in small old populations. The rate of local disease spread is affected by the level of host resistance; S. dioica populations showing an increase in disease over time are more susceptible than populations where the disease has remained at low levels. Among-population variation in resistance is driven by founding events and populations remain differentiated due to limited gene flow between islands. As observed in the L. alpina system, when populations are more connected, a greater fraction of populations have disease present. Results from a simulation model argue that, while increased dispersal in connected systems can increase disease spread, it may also favour selection of host resistance which ultimately reduces disease levels within populations. This could explain the observed lower disease prevalence in L. alpina in regions where populations are more continuous.
