Biology subjects

Carpentier, F.

Publications and source records attributed to Carpentier, F..

12 recordsLinked to original sources

bioRxiv2026

Non-canonical sex chromosome evolution revealed by extreme heterogeneity in homomorphic Y chromosome differentiation in the common frog

Sex chromosome evolution is often viewed as a unidirectional process in which recombination suppression expands around a sex-determining locus, leading eventually to Y-chromosome degeneration. Yet many vertebrates, including frogs, retain homomorphic sex chromosomes and polymorphic differentiation despite long-term recombination suppression, which is quite puzzling. Here, we combine pooled whole-genome resequencing, doubled-haploid YY genomes, and RNA-seq to understand the dynamics of homomorphic sex chromosome evolution in a Swiss Alpine population of the common frog, Rana temporaria, where multiple Y haplotypes coexist. We show that two fully differentiated Y haplotypes carry exceptionally large nonrecombining regions spanning [~]90% of the sex chromosome ([~]618-625 Mb), whereas semi-differentiated Y haplotype retains only a 4.64 Mb Dmrt1-linked sex-determining region, and XX males are genetically indistinguishable from XX females. The large NRRs show limited degeneration, with no evidence of gene loss, Y-linked copy decay, faster-X evolution or enrichment of sex-biased genes, and only modest repeat accumulation. Surprisingly, the coexisting Y haplotypes are neither independent sex-determining systems nor successive stages of a single degeneration trajectory. Instead, they share an ancestral Dmrt1-linked region whose X-Y divergence dates to [~]3.47-5.70 Mya, while present-day Y copies of this region remain nearly identical and the large NRRs have accumulated private mutations independently. We thus propose that the Y chromosome undergoes cyclic dynamics of differentiation: extreme heterochiasmy promotes rapid large NRRs formation, sex-reversed XY females recurrently restore X-Y recombination, gene conversion and/or rare Y-Y recombination may homogenize Y copies at the Dmrt1-linked region, and renewed male transmission drives subsequent Y-specific differentiation. The findings provide a genome-wide resolution to a central paradox in sex chromosome evolution: how sex chromosomes can experience extensive recombination suppression yet remain homomorphic and only weakly degenerated. By showing that heterochiasmy and sex reversal uncouple the physical extent, age, and degeneration of sex-linked regions, our study reframes homomorphic sex chromosomes as dynamic, repeatedly regenerated systems shaped by alternating phases of recombination suppression, restored X-Y recombination and renewed Y differentiation. Significance statementWhy many vertebrate sex chromosomes remain homomorphic despite long-term recombination suppression remains unresolved. Using whole-genome population genomics, doubled-haploid YY genomes, and transcriptomics in the common frog, we show that multiple coexisting Y haplotypes in a single pond share an old Dmrt1-linked sex-determining region but carry younger, independently differentiated Y chromosomes. This genome-wide resolution reveals that extreme heterochiasmy, where recombination is largely restricted to chromosome ends in males, can rapidly generate very large nonrecombining regions, while sex-reversed XY females can restore X-Y recombination and reduce divergence outside the Dmrt1-linked region. These opposing processes generate cyclic dynamics of Y differentiation rather than a directional path towards degeneration. Our study provides a mechanistic explanation for the persistence of co-existing multiple Y haplotypes in one population, maintenance of homomorphic sex chromosomes, and a broadly relevant framework for sex chromosome evolution in lineages with heterochiasmy and sex reversal.

evolutionary biology↗

bioRxiv2024

Diverging Arabidopsis populations quickly accumulate pollen-acting genetic incompatibilities

The process by which species diverge from one another, gradually accumulate genetic incompatibilities and eventually reach full-fledged reproductive isolation is a key question in evolutionary biology. However, the nature of reproductive barriers, the pace at which they accumulate and their genomic distribution remain poorly documented. The disruption of co-adapted epistatic interactions in hybrids and the accumulation of selfish genetic elements are proposed contributors to this process, and can lead to the distortion of the mendelian segregation of the affected loci across the genome. In this study we detect and quantify segregation distortion across the genomes of crosses produced from a diverse sampling of Arabidopsis lyrata and A. halleri populations, two species at the early stages of speciation and that can still interbreed. We show that both the frequency of occurrence and the magnitude of distortion loci increase as the parents genetic distance from one another increases. We also observe that distorter loci evolve rapidly, as they occur not only within interspecific hybrids, but also in intraspecific hybrids produced from isolated population crosses. Finally, we identify both genome-wide non-independence and two specific genomic regions on different chromosomes where opposite distortion effects are repeatedly observed across multiple F1 individuals, suggesting negative epistasis is a major contributor to the evolution of hybrid segregation distortion. Our study demonstrates that pollen-acting segregation distortion is ubiquitous, and contributes not only to the ongoing reproductive isolation between A. halleri and A. lyrata, but also between very recently diverged populations of the same species.

genomics↗

bioRxiv2022

Preventing multiple resistance above all: new insights for managing fungal adaptation

Sustainable crop protection is crucial for food security, but is threatened by the adaptation of diverse, evolving pathogen population. Resistance can be managed by maximizing selection pressure diversity, by dose variation and the spatial and temporal combination of active ingredients. We explored the interplay between operational drivers for maximizing management strategy sustainability relative to the resistance status of fungal populations. We applied an experimental evolution approach to three artificial populations of an economically important wheat pathogen, Zymoseptoria tritici, differing in initial resistance status. We revealed that diversified selection pressure limited the selection of resistance in naive populations and those with low frequencies of single. Increasing the number of modes of action delayed resistance development most effectively -- ahead of increasing the number of fungicides, fungicide choice based on resistance risk and temporal variation in fungicide exposure -- but favored generalism in the evolved populations. However, the prior presence of multiple resistant resistant isolates and their subsequent selection in populations overrode the effects of diversity in management strategies, incidentally invalidating any universal ranking. Initial resistance composition must therefore be considered specifically in sustainable resistance management, to address real-world field situation. Abbreviated summaryExperimental evolution is a relevant tool for exploring the determinants of antifungal adaptation in fungi. Here, using the model species Z. tritici and two fungicidal modes of action associated with contrasting resistance risks, we have demonstrated that initial population composition, and in particular the presence of multiple resistance, represents the main determinant of adaptive trajectories. Originality-Significance StatementPesticides are part of microbe environment in agricultural systems and may select for resistance. This adaptation of pathogens is a burden for plant health. Using an original multicriteria assessment and experimental evolution, we revealed that multi-fungicide use, selecting for multiple resistance, trumped any other driver of selection, invalidating any universal ranking of management strategies, a dispute extensively illustrated in literature and still inconclusive, especially in agriculture. This outcome refocuses the debate on population diversity and evolution rather than on the intrinsic properties of strategies, as mostly acclaimed in literature. From a practical point of view, our results highlight the importance of considering local population composition when recommending spraying programs. This practice is currently not generalized in agriculture but may be timely to effectively delay resistance evolution and reduce pesticide load in agricultural systems, a growing social demand, since resistance monitoring at relatively fine spatial scales and at low frequency may become commonplace in a near future with the rise of new molecular biology technologies

evolutionary biology↗

bioRxiv2021

Onset and stepwise extensions of recombination suppression are common in mating-type chromosomes of Microbotryum anther-smut fungi

Sex chromosomes and mating-type chromosomes can display large genomic regions without recombination. Recombination suppression often extended stepwise with time away from the sex- or mating-type-determining genes, generating evolutionary strata of differentiation between alternative sex or mating-type chromosomes. In anther-smut fungi of the Microbotryum genus, recombination suppression evolved repeatedly, linking the two mating-type loci and extended multiple times in regions distal to the mating-type genes. Here, we obtained high-quality genome assemblies of alternative mating types for four Microbotryum fungi. We found an additional event of independent chromosomal rearrangements bringing the two mating-type loci on the same chromosome followed by recombination suppression linking them. We also found, in a new clade analysed here, that recombination suppression between the two mating-type loci occurred in several steps, with first an ancestral recombination suppression between one of the mating-type locus and its centromere; later, completion of recombination suppression up to the second mating-type locus occurred independently in three species. The estimated dates of recombination suppression between the mating-type loci ranged from 0.15 to 3.58 million years ago. In total, this makes at least nine independent events of linkage between the mating-type loci across the Microbotryum genus. Several mating-type locus linkage events occurred through the same types of chromosomal rearrangements, where similar chromosome fissions at centromeres represent convergence in the genomic changes leading to the phenotypic convergence. These findings further highlight Microbotryum fungi as excellent models to study the evolution of recombination suppression.

evolutionary biology↗

bioRxiv2021

Why do fungicide mixtures delay the evolution of resistance? An experimental evolutionary approach

Pesticide resistance poses a critical threat to agriculture, human health and biodiversity. Mixtures of fungicides are recommended and widely used in resistance management strategies. However, the components of the efficiency of such mixtures remain unclear. We performed an experimental evolution study on the fungal pathogen Z. tritici, to determine how mixtures managed resistance. We compared the effect of the continuous use of single active ingredients to that of mixtures, at the minimal dose providing full control of the disease, which we refer to as the "efficient" dose. We found that the performance of efficient-dose mixtures against an initially susceptible population depended strongly on the components of the mixture. Such mixtures were either as durable as the best mixture component used alone, or worse than all components used alone. Moreover, efficient-dose mixture regimes probably select for generalist resistance profiles as a result of the combination of selection pressures exerted by the various components and their lower doses. Our results indicate that mixtures should not be considered a universal strategy. Experimental evaluations of specificities for the pathogens targeted, their interactions with fungicides and the interactions between fungicides are crucial for the design of sustainable resistance management strategies.

evolutionary biology↗

bioRxiv2021

Tempo of degeneration across independently evolved non-recombining regions

Recombination is beneficial over the long term, allowing more effective selection. Despite long-term advantages of recombination, local recombination suppression can evolve and lead to genomic degeneration, in particular on sex chromosomes. Here, we investigated the tempo of degeneration in non-recombining regions, i.e., the function curve for the accumulation of deleterious mutations over time, leveraging on 22 independent events of recombination suppression identified on mating-type chromosomes of anther-smut fungi, including newly identified ones. Using previously available and newly generated high-quality genome assemblies of alternative mating types of 13 Microbotryum species, we estimated degeneration levels in terms of accumulation of non-optimal codons and non-synonymous substitutions in non-recombining regions. We found a reduced frequency of optimal codons in the non-recombining regions compared to autosomes, that was not due to less frequent GC-biased gene conversion or lower ancestral expression levels compared to recombining regions. The frequency of optimal codons rapidly decreased following recombination suppression and reached an asymptote after ca 3 Mya. The strength of purifying selection remained virtually constant at dN/dS = 0.55, i.e. at an intermediate level between purifying selection and neutral evolution. Accordingly, non-synonymous differences between mating-type chromosomes increased linearly with stratum age, at a rate of 0.015 per MY. We thus develop a method for disentangling effects of reduced selection efficacy from GC-biased gene conversion in the evolution of codon usage and we quantify the tempo of degeneration in non-recombining regions, which is important for our knowledge on genomic evolution and on the maintenance of regions without recombination.

evolutionary biology↗

bioRxiv2021

I alternate therefore I generalize: how the intrinsic resistance risk of fungicides counterbalances their durability

The evolution of resistance to pesticides is a major burden in agriculture. Resistance management involves maximizing selection pressure heterogeneity, particularly by combining active ingredients with different modes of action. We tested the hypothesis that alternation may delay the build-up of resistance not only by spreading selection pressure over longer periods, but also by decreasing the rate of evolution of resistance to alternated fungicides, by applying an experimental evolution approach to the economically important crop pathogen Zymoseptoria tritici. Our results show that alternation is either neutral or slows the overall resistance evolution rate, relative to continuous fungicide use, but results in higher levels of generalism in evolved lines. We demonstrate that the nature of the fungicides, and therefore their relative intrinsic risk of resistance may underly this trade-off, more so than the number of fungicides and the rhythm of alternation. This trade-off is also dynamic over the course of resistance evolution. These findings open up new possibilities for tailoring resistance management effectively while optimizing interplay between alternation components.

evolutionary biology↗

bioRxiv2020

Large-scale study reveals regional fungicide applications as a major determinant of resistance evolution in the wheat pathogen Zymoseptoria tritici in France.

O_LIResearch rationale: In modern cropping systems, the near-universal use of plant protection products selects for resistance in pest populations. The emergence and evolution of this adaptive trait threaten treatment efficacy. We identified determinants of fungicide resistance evolution and quantified their effects at a large spatiotemporal scale. C_LIO_LIMethods: We focused on Zymoseptoria tritici, which causes leaf blotch in wheat. Phenotypes of qualitative or quantitative resistance to various fungicides were monitored annually, from 2004 to 2017, at about 70 sites throughout 22 regions of France (territorial units of 25 000km2 on average). We modelled changes in resistance frequency with regional anti-Septoria fungicide use, yield losses due to the disease and the regional area under organic wheat. C_LIO_LIKey results: The major driver of resistance dynamics was fungicide use at the regional scale. We estimated its effect on the increase in resistance and relative apparent fitness of each resistance phenotype. The predictions of the model replicated the spatiotemporal patterns of resistance observed in field populations (R2 from 0.56 to 0.82). C_LIO_LIMain conclusion: The evolution of fungicide resistance is mainly determined at the regional scale. This study therefore showed that collective management at the regional scale could effectively complete local actions. C_LI

evolutionary biology↗

bioRxiv2019

The polyphagous plant pathogenic fungus Botrytis cinerea encompasses host-specialized and generalist populations

The host plant is often the main variable explaining population structure in fungal plant pathogens, because specialization contributes to reduce gene flow between populations associated with different hosts. Previous population genetic analysis revealed that French populations of the grey mould pathogen Botrytis cinerea were structured by hosts tomato and grapevine, suggesting host specialization in this highly polyphagous pathogen. However, these findings raised questions about the magnitude of this specialization and the possibility of specialization to other hosts. Here we report specialization of B. cinerea populations to tomato and grapevine hosts but not to other tested plants. Population genetic analysis revealed two pathogen clusters associated with tomato and grapevine, while the other clusters co-occurred on hydrangea, strawberry and bramble. Measurements of quantitative pathogenicity were consistent with host specialization of populations found on tomato, and to a lesser extent, populations found on grapevine. Pathogen populations from hydrangea and strawberry appeared to be generalist, while populations from bramble may be weakly specialized. Our results suggest that the polyphagous B. cinerea is more accurately described as a collection of generalist and specialist individuals in populations. This work opens new perspectives for grey mold management, while suggesting spatial optimization of crop organization within agricultural landscapes.

microbiology↗

bioRxiv2019

SILand: an R package for estimating the spatial influence of landscape

ContextThe spatial distributions of species and populations are both influenced by local variables and by characteristics of surrounding landscapes. Understanding how landscape features spatially structure the frequency of a trait in a population, the abundance of a species or the species richness remains difficult specially because the spatial scale effects of the landscape variables are often unknown. ObjectivesHere, we present "siland", an R package for analyzing the effect of landscape features on georeferenced point observations (described in a Geographic Information System shapefile format). Methods & Results"siland" simultaneously estimates the spatial scales and intensities of landscape variable effects. It does not require any information about the scale of effect. Two methods are available: one is based on focal sample site (Bsiland method, b for buffer) and one is distance weighted using Spatial Influence Function (Fsiland method, f for function). siland allows for effects tests, effects maps and models comparison. ConclusionsAdaptable and user-friendly, the "siland" package is a very practical tool to perform landscape analysis.

ecology↗

bioRxiv2019

Differential gene expression is associated with degeneration of mating-type chromosomes in the absence of sexual antagonism

In animals and plants, differential expression of genes on sex chromosomes is widespread and it is usually considered to result from sexually antagonistic selection; however differential expression can also be caused by asymmetrical sequence degeneration in non-recombining sex chromosomes, which has been very little studied. The anther-smut fungus Microbotryum lychnidis-dioicae is ideal to investigate the extent to which differential gene expression is associated with sequence degeneration because: 1) separate haploid cultures of opposite mating types help identify differential expression, 2) its mating-type chromosomes display multiple evolutionary strata reflecting successive events of gene linkage to the mating-type loci, and 3) antagonistic selection is unlikely between isogamous haploid mating types. We therefore tested the hypothesis that differential gene expression between mating types resulted from sequence degeneration. We found that genes showing differential expression between haploid mating types were enriched only on the oldest evolutionary strata of the mating-type chromosomes and were associated with multiple signatures of sequence degeneration. We found that differential expression between mating types was associated with elevated differences between alleles in non-synonymous substitution rates, indels and premature stop codons, transposable element insertions, and altered intron and GC content. Our findings strongly suggest that degenerative mutations are important in the evolution of differential expression in non-recombining regions. Our results are relevant for a broad range of taxa where mating compatibility or sex is determined by genes located in large regions of recombination suppression, showing that differential expression should not be taken as necessarily arising from antagonistic selection.\n\nAuthor SummaryDifferences between males and females, from morphology to behavior and physiology, are considered to largely reflect differential expression of genes that maximize fitness benefits relative to costs that are specific to one sex. However, there is an unexplored alternative to such sexually antagonistic selection to explain differential expression. Reproductive compatibility is often determined by genes located in large non-recombining chromosomal regions, where degenerative mutations are expected to accumulate and may separately affect the expression of alternate alleles of genes. We tested the role of genetic degeneration in determining differential expression between the isogamous haploid mating types of the anther-smut fungus, Microbotryum lychnidis-dioicae, where sexually antagonistic selection is not a confounding factor. We show that differentially expressed genes are highly enriched in the non-recombining mating-type chromosomes, and that they are associated with various forms of degenerative mutations, some of which indicate that the less expressed allele suffers greater mutational effects. Our finding of the role for degenerative mutations in the evolution of differential expression is relevant for a broad range of organisms where reproductive compatibility or sex is determined by genes in regions of suppressed recombination, and shows that differential expression should not be taken as necessarily arising from antagonistic selection.

evolutionary biology↗

bioRxiv2017

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

This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100039). The efficiency of plant resistance to fungal pathogen populations is expected to decrease over time, due to its evolution with an increase in the frequency of virulent or highly aggressive strains. This dynamics may differ depending on the scale investigated (annual or pluriannual), particularly for annual crop pathogens with both sexual and asexual reproduction cycles. We assessed this time-scale effect, by comparing aggressiveness changes in a local Zymoseptoria tritici population over an eight-month cropping season and a six-year period of wheat monoculture. We collected two pairs of subpopulations to represent the annual and pluriannual scales: from leaf lesions at the beginning and end of a single annual epidemic, and from crop debris at the beginning and end of a six-year period. We assessed two aggressiveness traits - latent period and lesion size - on sympatric and allopatric host varieties. A trend toward decreased latent period concomitant with a significant loss of variability was established during the course of the annual epidemic, but not over the six-year period. Furthermore, a significant cultivar effect (sympatric vs. allopatric) on the average aggressiveness of the isolates revealed host adaptation, arguing that the observed patterns could result from selection. We thus provide an experimental body of evidence of an epidemiological trade-off between the intra- and inter-annual scales in the evolution of aggressiveness in a local plant pathogen population. More aggressive isolates were collected from upper leaves, on which disease severity is usually lower than on the lower part of the plants left in the field as crop debris after harvest. We suggest that these isolates play little role in sexual reproduction, due to an Allee effect (difficulty finding mates at low pathogen densities), particularly as the upper parts of the plant are removed from the field, explaining the lack of transmission of increases in aggressiveness between epidemics.

epidemiology↗