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Assessing the effects of quantitative host resistance on the life-history traits of sporulating parasites with growing lesions.

ABSTRACT: Assessing life-history traits of parasites on resistant hosts is crucial in evolutionary ecology. In the particular case of sporulating pathogens with growing lesions, phenotyping is difficult because one needs to disentangle properly pathogen spread from sporulation. By considering Phytophthora infestans on potato, we use mathematical modelling to tackle this issue and refine the assessment of pathogen response to quantitative host resistance. We elaborate a parsimonious leaf-scale model by convolving a lesion growth model and a sporulation function, after a latency period. This model is fitted to data obtained on two isolates inoculated on three cultivars with contrasted resistance level. Our results confirm a significant host-pathogen interaction on the various estimated traits, and a reduction of both pathogen spread and spore production, induced by host resistance. Most interestingly, we highlight that quantitative resistance also changes the sporulation function, the mode of which is significantly time-lagged. This alteration of the infectious period distribution on resistant hosts may have strong impacts on the dynamics of parasite populations, and should be considered when assessing the durability of disease control tactics based on plant resistance management. This inter-disciplinary work also supports the relevance of mechanistic models for analysing phenotypic data of plant-pathogen interactions.

SUBMITTER: Leclerc M

PROVIDER: S-EPMC6790771 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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Assessing the effects of quantitative host resistance on the life-history traits of sporulating parasites with growing lesions.

Leclerc Melen M Clément Julie A J JAJ Andrivon Didier D Hamelin Frédéric M FM

Proceedings. Biological sciences 20191002 1912

Assessing life-history traits of parasites on resistant hosts is crucial in evolutionary ecology. In the particular case of sporulating pathogens with growing lesions, phenotyping is difficult because one needs to disentangle properly pathogen spread from sporulation. By considering <i>Phytophthora infestans</i> on potato, we use mathematical modelling to tackle this issue and refine the assessment of pathogen response to quantitative host resistance. We elaborate a parsimonious leaf-scale model ...[more]

PMID: 31575367

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Project description:There is growing interest in the role that life-history traits of hosts, such as their 'pace-of-life', play in the evolution of resistance and tolerance to parasites. Theory suggests that, relative to host species that have high syntopy (local spatial and temporal overlap) with parasites, host species with low syntopy should have lower selection pressures for more constitutive (always present) and costly defences, such as tolerance, and greater reliance on more inducible and cheaper defences, such as behaviour. Consequently, we postulated that the degree of host-parasite syntopy, which is negatively correlated with host pace-of-life (an axis reflecting the developmental rate of tadpoles and the inverse of their size at metamorphosis) in our tadpole-parasitic cercarial (trematode) system, would be a negative and positive predictor of behavioural resistance and tolerance, respectively. To test these hypotheses, we exposed seven tadpole species to a range of parasite (cercarial) doses crossed with anaesthesia treatments that controlled for anti-parasite behaviour. We quantified host behaviour, successful and unsuccessful infections, and each species' reaction norm for behavioural resistance and tolerance, defined as the slope between cercarial exposure (or attempted infections) and anti-cercarial behaviours and mass change, respectively. Hence, tolerance is capturing any cost of parasite exposure. As hypothesized, tadpole pace-of-life was a significant positive predictor of behavioural resistance and negative predictor of tolerance, a result that is consistent with a trade-off between behavioural resistance and tolerance across species that warrants further investigation. Moreover, these results were robust to considerations of phylogeny, all possible re-orderings of the three fastest or slowest paced species, and various measurements of tolerance. These results suggest that host pace-of-life and host-parasite syntopy are powerful drivers of both the strength and type of host defence strategies against parasites. Future research should evaluate how often and how strongly host pace-of-life and host-parasite syntopy are correlated and which is the better predictor of the strength and type of host investments in anti-parasite defences.

Project description:BackgroundOrganisms live in environments that vary. For life-history traits that vary across environments, fitness will be maximised when the phenotype is appropriately matched to the environmental conditions. For the free-living nematode Caenorhabditis elegans, we have investigated how two major life-history traits, (i) the development of environmentally resistant dauer larvae and (ii) reproduction, respond to environmental stress (high population density and low food availability), and how these traits vary between lines and the genetic basis of this variation.ResultsWe found that lines of C. elegans vary in their phenotypic plasticity of dauer larva development, i.e. there is variation in the likelihood of developing into a dauer larva for the same environmental change. There was also variation in how lifetime fecundity and the rate of reproduction changed under conditions of environmental stress. These traits were related, such that lines that are highly plastic for dauer larva development also maintain a high population growth rate when stressed. We identified quantitative trait loci (QTL) on two chromosomes that control the dauer larva development and population size phenotypes. The QTLs affecting the dauer larva development and population size phenotypes on chromosome II are closely linked, but are genetically separable. This chromosome II QTL controlling dauer larva development does not encompass any loci previously identified to control dauer larva development. This chromosome II region contains many predicted 7-transmembrane receptors. Such proteins are often involved in information transduction, which is clearly relevant to the control of dauer larva development.ConclusionC. elegans alters both its larval development and adult reproductive strategy in response to environmental stress. Together the phenotypic and genotypic data suggest that these two major life-history traits are co-ordinated responses to environmental stress and that they are, at least in part, controlled by the same genomic regions.

Project description:Plants use their roots to forage for nutrients in heterogeneous soil environments, but different plant species vastly differ in the intensity of foraging they perform. This diversity suggests the existence of constraints on foraging at the species level. We therefore examined the relationships between the intensity of root foraging and plant body traits across species in order to estimate the degree of coordination between plant body traits and root foraging as a form of plant behavior. We cultivated 37 perennial herbaceous Central European species from open terrestrial habitats in pots with three different spatial gradients of nutrient availability (steep, shallow, and no gradient). We assessed the intensity of foraging as differences in root placement inside pots with and without a spatial gradient of resource supply. For the same set of species, we retrieved data about body traits from available databases: maximum height at maturity, mean area of leaf, specific leaf area, shoot lifespan, ability to self-propagate clonally, maximal lateral spread (in clonal plants only), realized vegetative growth in cultivation, and realized seed regeneration in cultivation. Clonal plants and plants with extensive vegetative growth showed considerably weaker foraging than their non-clonal or slow-growing counterparts. There was no phylogenetic signal in the amount of expressed root foraging intensity. Since clonal plants foraged less than non-clonals and foraging intensity did not seem to be correlated with species phylogeny, we hypothesize that clonal growth itself (i.e., the ability to develop at least partly self-sustaining ramets) may be an answer to soil heterogeneity. Whereas unitary plants use roots as organs specialized for both resource acquisition and transport to overcome spatial heterogeneity in resource supply, clonal plants separate these two functions. Becoming a clonal plant allows higher specialization at the organ level, since a typical clonal plant can be viewed as a network of self-sustainable harvesting units connected together with specialized high-throughput connection organs. This may be an effective alternative for coping with spatial heterogeneity in resource availability.

Dataset Information

Assessing the effects of quantitative host resistance on the life-history traits of sporulating parasites with growing lesions.

Publications

Assessing the effects of quantitative host resistance on the life-history traits of sporulating parasites with growing lesions.

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