MOURY Benoit's profile
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MOURY Benoit

  • Pathologie Végétale, INRA, Avignon, France
  • Adaptation, Evolutionary Epidemiology, Experimental Evolution, Genotype-Phenotype, Molecular Evolution, Phylogenetics / Phylogenomics, Population Genetics / Genomics, Quantitative Genetics, Species interactions
  • recommender

Recommendations:  2

Review:  1

Educational and work
I am working on the durability of plant resistance to pathogens (especially viruses) using multiple approaches (genetics, experimental evolution, epidemiology, population genetics and modelling).

Recommendations:  2

13 Nov 2017
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Epidemiological trade-off between intra- and interannual scales in the evolution of aggressiveness in a local plant pathogen population

The pace of pathogens’ adaptation to their host plants

Recommended by based on reviews by Benoit Moury and 1 anonymous reviewer

Because of their shorter generation times and larger census population sizes, pathogens are usually ahead in the evolutionary race with their hosts. The risks linked to pathogen adaptation are still exacerbated in agronomy, where plant and animal populations are not freely evolving but depend on breeders and growers, and are usually highly genetically homogeneous. As a consequence, the speed of pathogen adaptation is crucial for agriculture sustainability. Unraveling the time scale required for pathogens’ adaptation to their hosts would notably greatly improve our estimation of the risks of pathogen emergence, the efficiency of disease control strategies and the design of epidemiological surveillance schemes. However, the temporal scale of pathogen evolution has received much less attention than its spatial scale [1]. In their study of a wheat fungal disease, Suffert et al. [2] reached contrasting conclusions about the pathogen adaptation depending on the time scale (intra- or inter-annual) and on the host genotype (sympatric or allopatric) considered, questioning the experimental assessment of this important problem.

Suffert et al. [2] sampled two pairs of Zymoseptoria tritici (the causal agent of septoria leaf blotch) sub-populations in a bread wheat field plot, representing (i) isolates collected at the beginning or at the end of an epidemic in a single growing season (2009-2010 intra-annual sampling scale) and (ii) isolates collected from plant debris at the end of growing seasons in 2009 and in 2015 (inter-annual sampling scale). Then, they measured in controlled conditions two aggressiveness traits of the isolates of these four Z. tritici sub-populations, the latent period and the lesion size on leaves, on two wheat cultivars. One of the cultivars was considered as "sympatric" because it was at the source of the studied isolates and was predominant in the growing area before the experiment, whereas the other cultivar was considered as "allopatric" since it replaced the previous one and became predominant in the growing area during the sampling period.

On the sympatric host, at the intra-annual scale, they observed a marginally-significant decrease in latent period and a significant decrease of the between-isolate variance for this trait, which are consistent with a selection of pathogen variants with an enhanced aggressiveness. In contrast, at the inter-annual scale, no difference in the mean or variance of aggressiveness trait values was observed on the sympatric host, suggesting a lack of pathogen adaptation. They interpreted the contrast between observations at the two time scales as the consequence of a trade-off for the pathogen between a gain of aggressiveness after several generations of asexual reproduction at the intra-annual scale and a decrease of the probability to reproduce sexually and to be transmitted from one growing season to the next. Indeed, at the end of the growing season, the most aggressive isolates are located on the upper leaves of plants, where the pathogen density and hence probably also the probability to reproduce sexually, is lower. On the allopatric host, the conclusion about the pathogen stability at the inter-annual scale was somewhat different, since a significant increase in the mean lesion size was observed (isolates corresponding to the intra-annual scale were not checked on the allopatric host). This shows the possibility for the pathogen to evolve at the inter-annual scale, for a given aggressiveness trait and on a given host.

In conclusion, Suffert et al.’s [2] study emphasizes the importance of the experimental design in terms of sampling time scale and host genotype choice to analyze the pathogen adaptation to its host plants. It provides also an interesting scenario, at the crossroad of the pathogen’s reproduction regime, niche partitioning and epidemiological processes, to interpret these contrasted results. Pathogen adaptation to plant cultivars with major-effect resistance genes is usually fast, including in the wheat-Z. tritici system [3]. Therefore, this study will be of great help for future studies on pathogen adaptation to plant partial resistance genes and on strategies of deployment of such resistance at the landscape scale.

References
[1] Penczykowski RM, Laine A-L and Koskella B. 2016. Understanding the ecology and evolution of host–parasite interactions across scales. Evolutionary Applications, 9: 37–52. doi: 10.1111/eva.12294

[2] Suffert F, Goyeau H, Sache I, Carpentier F, Gelisse S, Morais D and Delestre G. 2017. Epidemiological trade-off between intra- and interannual scales in the evolution of aggressiveness in a local plant pathogen population. bioRxiv, 151068, ver. 3 of 12th November 2017. doi: 10.1101/151068

[3] Brown JKM, Chartrain L, Lasserre-Zuber P and Saintenac C. 2015. Genetics of resistance to Zymoseptoria tritici and applications to wheat breeding. Fungal Genetics and Biology, 79: 33–41. doi: 10.1016/j.fgb.2015.04.017

12 Apr 2017
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Genetic drift, purifying selection and vector genotype shape dengue virus intra-host genetic diversity in mosquitoes

Vectors as motors (of virus evolution)

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Many viruses are transmitted by biological vectors, i.e. organisms that transfer the virus from one host to another. Dengue virus (DENV) is one of them. Dengue is a mosquito-borne viral disease that has rapidly spread around the world since the 1940s. One recent estimate indicates 390 million dengue infections per year [1]. As many arthropod-borne vertebrate viruses, DENV has to cross several anatomical barriers in the vector, to multiply in its body and to invade its salivary glands before getting transmissible. As a consequence, vectors are not passive carriers but genuine hosts of the viruses that potentially have important effects on the composition of virus populations and, ultimately, on virus epidemiology and virulence. Within infected vectors, virus populations are expected to acquire new mutations and to undergo genetic drift and selection effects. However, the intensity of these evolutionary forces and the way they shape virus genetic diversity are poorly known.

In their study, Lequime et al. [2] finely disentangled the effects of genetic drift and selection on DENV populations during their infectious cycle within mosquito (Aedes aegypti) vectors. They evidenced that the genetic diversity of viruses within their vectors is shaped by genetic drift, selection and vector genotype. The experimental design consisted in artificial acquisition of purified virus by mosquitoes during a blood meal. The authors monitored the diversity of DENV populations in Ae. aegypti individuals at different time points by high-throughput sequencing (HTS). They estimated the intensity of genetic drift and selection effects exerted on virus populations by comparing the DENV diversity at these sampling time points with the diversity in the purified virus stock (inoculum).

Disentangling the effects of genetic drift and selection remains a methodological challenge because both evolutionary forces operate concomitantly and both reduce genetic diversity. However, selection reduces diversity in a reproducible manner among experimental replicates (here, mosquito individuals): the fittest variants are favoured at the expense of the weakest ones. In contrast, genetic drift reduces diversity in a stochastic manner among replicates. Genetic drift acts equally on all variants irrespectively of their fitness. The strength of genetic drift is frequently evaluated with the effective population size Ne: the lower Ne, the stronger the genetic drift [3]. The estimation of the effective population size of DENV populations by Lequime et al. [2] was based on single-nucleotide polymorphisms (SNPs) that were (i) present both in the inoculum and in the virus populations sampled at the different time points and (ii) that were neutral (or nearly-neutral) and therefore subjected to genetic drift only and insensitive to selection. As expected for viruses that possess small and constrained genomes, such neutral SNPs are extremely rare. Starting from a set of >1800 SNPs across the DENV genome, only three SNPs complied with the neutrality criteria and were enough represented in the sequence dataset for a precise Ne estimation. Using the method described by Monsion et al. [4], Lequime et al. [2] estimated Ne values ranging from 5 to 42 viral genomes (95% confidence intervals ranged from 2 to 161 founding viral genomes). Consequently, narrow bottlenecks occurred at the virus acquisition step, since the blood meal had allowed the ingestion of ca. 3000 infectious virus particles, on average. Interestingly, bottleneck sizes did not differ between mosquito genotypes. Monsion et al.’s [4] formula provides only an approximation of Ne. A corrected formula has been recently published [5]. We applied this exact Ne formula to the means and variances of the frequencies of the three neutral markers estimated before and after the bottlenecks (Table 1 in [2]), and nearly identical Ne estimates were obtained with both formulas.

Selection intensity was estimated from the dN/dS ratio between the nonsynonymous and synonymous substitution rates using the HTS data on DENV populations. DENV genetic diversity increased following initial infection but was restricted by strong purifying selection during virus expansion in the midgut. Again, no differences were detected between mosquito genotypes. However and importantly, significant differences in DENV genetic diversity were detected among mosquito genotypes. As they could not be related to differences in initial genetic drift or to selection intensity, the authors raise interesting alternative hypotheses, including varying rates of de novo mutations due to differences in replicase fidelity or differences in the balancing selection regime. Interestingly, they also suggest that this observation could simply result from a methodological issue linked to the detection threshold of low-frequency SNPs.
 

References

[1] Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, et al. 2013. The global distribution and burden of dengue. Nature 496: 504–7 doi: 10.1038/nature12060

[2] Lequime S, Fontaine A, Gouilh MA, Moltini-Conclois I and Lambrechts L. 2016. Genetic drift, purifying selection and vector genotype shape dengue virus intra-host genetic diversity in mosquitoes. PloS Genetics 12: e1006111 doi: 10.1371/journal.pgen.1006111

[3] Charlesworth B. 2009. Effective population size and patterns of molecular evolution and variation. Nature Reviews Genetics 10: 195-205 doi: 10.1038/nrg2526

[4] Monsion B, Froissart R, Michalakis Y and Blanc S. 2008. Large bottleneck size in cauliflower mosaic virus populations during host plant colonization. PloS Pathogens 4: e1000174 doi: 10.1371/journal.ppat.1000174

[5] Thébaud G and Michalakis Y. 2016. Comment on ‘Large bottleneck size in cauliflower mosaic virus populations during host plant colonization’ by Monsion et al. (2008). PloS Pathogens 12: e1005512 doi: 10.1371/journal.ppat.1005512

Review:  1

13 Nov 2017
article picture

Epidemiological trade-off between intra- and interannual scales in the evolution of aggressiveness in a local plant pathogen population

The pace of pathogens’ adaptation to their host plants

Recommended by based on reviews by Benoit Moury and 1 anonymous reviewer

Because of their shorter generation times and larger census population sizes, pathogens are usually ahead in the evolutionary race with their hosts. The risks linked to pathogen adaptation are still exacerbated in agronomy, where plant and animal populations are not freely evolving but depend on breeders and growers, and are usually highly genetically homogeneous. As a consequence, the speed of pathogen adaptation is crucial for agriculture sustainability. Unraveling the time scale required for pathogens’ adaptation to their hosts would notably greatly improve our estimation of the risks of pathogen emergence, the efficiency of disease control strategies and the design of epidemiological surveillance schemes. However, the temporal scale of pathogen evolution has received much less attention than its spatial scale [1]. In their study of a wheat fungal disease, Suffert et al. [2] reached contrasting conclusions about the pathogen adaptation depending on the time scale (intra- or inter-annual) and on the host genotype (sympatric or allopatric) considered, questioning the experimental assessment of this important problem.

Suffert et al. [2] sampled two pairs of Zymoseptoria tritici (the causal agent of septoria leaf blotch) sub-populations in a bread wheat field plot, representing (i) isolates collected at the beginning or at the end of an epidemic in a single growing season (2009-2010 intra-annual sampling scale) and (ii) isolates collected from plant debris at the end of growing seasons in 2009 and in 2015 (inter-annual sampling scale). Then, they measured in controlled conditions two aggressiveness traits of the isolates of these four Z. tritici sub-populations, the latent period and the lesion size on leaves, on two wheat cultivars. One of the cultivars was considered as "sympatric" because it was at the source of the studied isolates and was predominant in the growing area before the experiment, whereas the other cultivar was considered as "allopatric" since it replaced the previous one and became predominant in the growing area during the sampling period.

On the sympatric host, at the intra-annual scale, they observed a marginally-significant decrease in latent period and a significant decrease of the between-isolate variance for this trait, which are consistent with a selection of pathogen variants with an enhanced aggressiveness. In contrast, at the inter-annual scale, no difference in the mean or variance of aggressiveness trait values was observed on the sympatric host, suggesting a lack of pathogen adaptation. They interpreted the contrast between observations at the two time scales as the consequence of a trade-off for the pathogen between a gain of aggressiveness after several generations of asexual reproduction at the intra-annual scale and a decrease of the probability to reproduce sexually and to be transmitted from one growing season to the next. Indeed, at the end of the growing season, the most aggressive isolates are located on the upper leaves of plants, where the pathogen density and hence probably also the probability to reproduce sexually, is lower. On the allopatric host, the conclusion about the pathogen stability at the inter-annual scale was somewhat different, since a significant increase in the mean lesion size was observed (isolates corresponding to the intra-annual scale were not checked on the allopatric host). This shows the possibility for the pathogen to evolve at the inter-annual scale, for a given aggressiveness trait and on a given host.

In conclusion, Suffert et al.’s [2] study emphasizes the importance of the experimental design in terms of sampling time scale and host genotype choice to analyze the pathogen adaptation to its host plants. It provides also an interesting scenario, at the crossroad of the pathogen’s reproduction regime, niche partitioning and epidemiological processes, to interpret these contrasted results. Pathogen adaptation to plant cultivars with major-effect resistance genes is usually fast, including in the wheat-Z. tritici system [3]. Therefore, this study will be of great help for future studies on pathogen adaptation to plant partial resistance genes and on strategies of deployment of such resistance at the landscape scale.

References
[1] Penczykowski RM, Laine A-L and Koskella B. 2016. Understanding the ecology and evolution of host–parasite interactions across scales. Evolutionary Applications, 9: 37–52. doi: 10.1111/eva.12294

[2] Suffert F, Goyeau H, Sache I, Carpentier F, Gelisse S, Morais D and Delestre G. 2017. Epidemiological trade-off between intra- and interannual scales in the evolution of aggressiveness in a local plant pathogen population. bioRxiv, 151068, ver. 3 of 12th November 2017. doi: 10.1101/151068

[3] Brown JKM, Chartrain L, Lasserre-Zuber P and Saintenac C. 2015. Genetics of resistance to Zymoseptoria tritici and applications to wheat breeding. Fungal Genetics and Biology, 79: 33–41. doi: 10.1016/j.fgb.2015.04.017

avatar

MOURY Benoit

  • Pathologie Végétale, INRA, Avignon, France
  • Adaptation, Evolutionary Epidemiology, Experimental Evolution, Genotype-Phenotype, Molecular Evolution, Phylogenetics / Phylogenomics, Population Genetics / Genomics, Quantitative Genetics, Species interactions
  • recommender

Recommendations:  2

Review:  1

Educational and work
I am working on the durability of plant resistance to pathogens (especially viruses) using multiple approaches (genetics, experimental evolution, epidemiology, population genetics and modelling).