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Legrand, D.

Publications and source records attributed to Legrand, D..

8 recordsLinked to original sources

Intraspecific variation at the free-living stage of a soil-borne pathogen is organized into an exploration syndrome associated with infectivity

Many pathogens spend a substantial portion of their life cycle outside the host tissues. During its free-living stage, the root legume-plant pathogen Aphanomyces euteiches persists in soil either as non-motile resting oospores or actively explores the environment through mycelium and motile zoospores. These two latter stages are critical for survival, dispersal and host encounter. However, the extent of intraspecific variation during these phases remains poorly explored, and it is still unknown whether they are organized into phenotypic syndromes contributing to infection success. Here, we measured eight free-living phenotypic traits associated with mycelial and zoospore stages across 23 A. euteiches strains from distinct geographic regions (USA, Europe) whose genomes were sequenced. We tested whether traits are organized into a phenotypic syndrome linked to either geographic origin, genomic diversity or infectivity. The microbial strains exhibited substantial intraspecific phenotypic variation that we proposed as an 'exploration syndrome' linked to host search. Beyond this general syndrome, we detected sub-structure according to strains' infectivity, geographic origin and genetic group. This suggests that the free-living stage of pathogens may contribute to disease potential. Our results highlight the importance of integrating functional trait approaches into plant pathology and suggest that the identified "exploration syndrome" may serve as a predictor of infectivity in soilborne oomycete pathogens.

ecology↗

Environmental complexity constrains evolutionary adaptation across taxa

Complex environments combining multiple stressors are the new norm worldwide. Adaptive evolution will be critical to population persistence under these combined challenges, but how environmental complexity affects the pace of evolution remains poorly understood. Using a meta-experimental evolution approach, we exposed 14 species, from bacteria to unicellular eukaryotes and plants, to single stressors and their pairwise combinations for multiple generations, while keeping the overall stress level comparable. Populations evolving under combined stressors tended to have lower fitness increase in the selective environments, higher fitness reductions in the control environment, and shallower relation between initial maladaptation and fitness gain, than under single stressors. However, these responses varied with species and stressor type. Accounting for such constraints on evolutionary dynamics should prove crucial for the management of biodiversity. Significance StatementA pressing challenges for modern science and society in the face of ongoing global change is understanding what limits the capacity of living organisms to adapt to complex environments combining multiple stressors. To answer to this question, we conducted a large-scale meta-experimental evolution design across a diversity of organisms, exposing them for multiple generations to either single or combined-stress treatments. Combined stressors led to less adaptive fitness gain than single stressors, and imposed additional costs through reduced fitness in non-stressful conditions. This unique combination of meta-experimental approach with a careful distinction between environmental complexity and overall stress allowed us to gain robust quantitative evidence on how environmental complexity can impact the pace of evolution.

evolutionary biology↗

GENETIC DIVERSITY AFFECTS ECOSYSTEM FUNCTIONS ACROSS TROPHIC LEVELS AS MUCH AS SPECIES DIVERSITY, BUT IN AN OPPOSITE DIRECTION

Understanding the relationships between biodiversity and ecosystem functioning stands as a cornerstone in ecological research. Extensive evidence now underscores the profound impact of species loss on the stability and dynamics of ecosystem functions. However, it remains unclear whether the loss of genetic diversity within key species yield similar consequences. Here, we delve into the intricate relationship between species diversity, genetic diversity, and ecosystem functions across three trophic levels --primary producers, primary consumers, and secondary consumers-- in natural aquatic ecosystems. Our investigation involves estimating species diversity and genome-wide diversity -gauged within three pivotal species-within each trophic level, evaluating seven key ecosystem functions, and analyzing the magnitude of the relationships between biodiversity and ecosystem functions (BEFs). We found that, overall, the absolute effect size of genetic diversity on ecosystem functions mirrors that of species diversity in natural ecosystems. We nonetheless unveil a striking dichotomy: while genetic diversity was positively correlated with various ecosystem functions, species diversity displays a negative correlation with these functions. These intriguing antagonist effects of species and genetic diversity persists across the three trophic levels (underscoring its systemic nature), but were apparent only when BEFs were assessed within trophic levels rather than across them. This study reveals the complexity of predicting the consequences of genetic and species diversity loss under natural conditions, and emphasizes the need for further mechanistic models integrating these two facets of biodiversity.

ecology↗

The macronuclear genomic landscape within Tetrahymena thermophila

The extent of intraspecific genomic variation is key to understanding species evolutionary history, including recent adaptive shifts. Intraspecific genomic variation remains poorly explored in eukaryotic microorganisms, especially in the nuclear dimorphic ciliates, despite their fundamental role as laboratory model systems and their ecological importance in many ecosystems. We sequenced the macronuclear genome of 22 laboratory strains of the oligohymenophoran Tetrahymena thermophila, a model species in both cellular biology and evolutionary ecology. We explored polymorphisms at the junctions of programmed eliminated sequences, and reveal their utility to barcode very closely related cells. As for other species of the genus Tetrahymena, we confirm micronuclear centromeres as gene diversification centres in T. thermophila, but also reveal a two-speed evolution in these regions. In the rest of the genome, we highlight recent diversification of genes encoding for extracellular proteins and cell adhesion. We discuss all these findings in relation with ciliates ecology and cellular characteristics. Impact StatementThis is the first study of population genomics in the ciliate Tetrahymena thermophila. This bacterivore species plays an important role in aquatic trophic chains and is widely used as a model in cell and molecular biology, ecology, evolution or toxicology. As all ciliates, it contains a germline micronucleus and a somatic macronucleus. Sequencing of the macronucleus reveals that the centromeric region of the micronucleus are simultaneously a region of new gene diversification, as observed in other Tetrahymena species, and a region containing highly conserved genes. The results also confirm that the formation of the macronucleus from the micronucleus is highly imprecise. Interestingly, this process generates a genomic barcode that can discriminate cells derived from a given sexual reproduction event, allowing to study more finely population dynamics/history in nature. Data summaryAll data are fully provided in Supplementary Materials. The raw data of the 22 Tetrahymena genomes have been deposited in the Sequence Read Archive (https://www-ncbi-nlm-nih-gov.inee.bib.cnrs.fr/bioproject/PRJNA1012331). Accession numbers are listed in Table S1 (available in the online version of this article).

genomics↗

Plastic cell morphology changes during dispersal

Dispersal is the movement of organisms from one habitat to another that potentially results in gene flow. It is often found to be plastic, allowing organisms to adjust dispersal movements depending on environmental conditions. A fundamental aim in ecology is to understand the determinants underlying dispersal and its plasticity. We utilized 22 strains of the ciliate Tetrahymena thermophila to determine if different phenotypic dispersal strategies co-exist within a species and which mechanisms underlie this variability. We quantified the cell morphologies impacting cell motility and dispersal. Distinct differences in innate cellular morphology and dispersal rates were detected, but no universally utilized combinations of morphological parameters correlate with dispersal. Rather, multiple distinct and plastic morphological changes impact cilia-dependent motility during dispersal, especially in proficient dispersing strains facing challenging environmental conditions. Combining ecology and cell biology experiments, we show that dispersal can be promoted through a panel of plastic motility-associated changes to cell morphology and motile cilia. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=152 SRC="FIGDIR/small/448130v1_ufig1.gif" ALT="Figure 1"> View larger version (45K): org.highwire.dtl.DTLVardef@1aad069org.highwire.dtl.DTLVardef@158adbdorg.highwire.dtl.DTLVardef@f6570forg.highwire.dtl.DTLVardef@cdc249_HPS_FORMAT_FIGEXP M_FIG C_FIG HighlightsO_LITetrahymena thermophila exhibits intra-specific diversity in morphology and dispersal. C_LIO_LICell motility behavior during dispersal changes with cilia length and cell shape. C_LIO_LICells from proficient dispersing strains transiently change basal body and cilia position. C_LIO_LIStarvation-induced dispersal triggers increased basal body and cilia density and caudal cilium formation in rapid-swimming cells. C_LI

cell biology↗

Dispersal syndromes affect ecosystem functioning in ciliate microcosms

Dispersal is a key process mediating ecological and evolutionary dynamics. Its effects on metapopulations dynamics, population genetics or species range distribution can depend on phenotypic differences between dispersing and non-dispersing individuals (i.e., dispersal syndromes). However, scaling up to the importance of dispersal syndromes for meta-ecosystems have rarely been considered, despite intraspecific phenotypic variability is now recognised as an important factor mediating ecosystem functioning. In this study, we characterised the intraspecific variability of dispersal syndromes in twenty isolated genotypes of the ciliate Tetrahymena thermophila to test their consequences for biomass productivity in communities composed of five Tetrahymena species. To do so, dispersers and residents of each genotype were introduced, each separately, in ciliate communities composed of four other competing species of the genus Tetrahymena to investigate the effects of dispersal syndromes. We found that introducing dispersers led to a lower biomass compared to introducing residents. This effect was highly consistent across the twenty T. thermophila genotypes despite their marked differences of dispersal syndromes. Finally, we found a strong genotypic effect on biomass production, confirming that intraspecific variability in general affected ecosystem functions in our system. Our study shows that intraspecific variability and the existence of dispersal syndromes can impact the functioning of spatially structured ecosystems in a consistent and therefore predictable way.

ecology↗

Transgenerational dispersal plasticity and its fitness consequences are under genetic control

Phenotypic plasticity, the ability of one genotype to produce different phenotypes in different environments, plays a central role in species response to environmental changes. Transgenerational plasticity (TGP) allows the transmission of this environmentally-induced phenotypic variation across generations, and can influence adaptation. To date, the genetic control of TGP, its long-term stability, and its potential costs remain largely unknown, mostly because empirical demonstrations of TGP across many generations in several genetic backgrounds are scarce. Here, we examined how genotype determines the TGP of dispersal, a fundamental process in ecology and evolution. We used an experimental approach involving ~200 clonal generations in a model-species of ciliate to determine if and how TGP influences the expression of dispersal-related traits in several genotypes. Our results show that morphological and movement traits associated with dispersal are plastic, and that these modifications are inherited over at least 35 generations. We also highlight that genotype modulates the fitness costs and benefits associated with plastic dispersal strategies. Our study suggests that genotype-dependent TGP could play a critical role in eco-evolutionary dynamics as dispersal determines gene flow and the long-term persistence of natural populations. More generally, it outlines the tremendous importance that genotype-dependent TGP could have in the ability of organisms to cope with current and future environmental changes.\n\nSignificanceThe genetic control of the transgenerational plasticity is still poorly understood despite its critical role in species responses to environmental changes. We examined how genotype determines transgenerational plasticity of a complex trait (i.e., dispersal) in a model-species of ciliate across ~200 clonal generations. Our results provide evidence that plastic phenotypic variation linked to dispersal is stably inherited over tens of generations and that cell genotype modulates the expression and fitness cost of transgenerational plasticity.

evolutionary biology↗

Bottom-up and top-down control of dispersal across major organismal groups: a coordinated distributed experiment

Organisms rarely experience a homogeneous environment. Rather, ecological and evolutionary dynamics unfold in spatially structured and fragmented landscapes, with dispersal as the central process linking these dynamics across spatial scales. Because dispersal is a multi-causal and highly plastic life-history trait, finding general drivers that are of importance across species is challenging but highly relevant for ecological forecasting.\n\nWe here tested whether two fundamental ecological forces and main determinants of local population dynamics, top-down and bottom-up control, generally explain dispersal in spatially structured communities. In a coordinated distributed experiment spanning a wide range of actively dispersing organisms, from protozoa to vertebrates, we show that bottom-up control, that is resource limitation, consistently increased dispersal. While top-down control, that is predation risk, was an equally important dispersal driver as bottom-up control, its effect depended on prey and predator space use and whether dispersal occurred on land, in water or in the air: species that routinely use more space than their predators showed increased dispersal in response to predation, specifically in aquatic environments. After establishing these general causes of dispersal, we used a metacommunity model to show that bottom-up and top-down control of dispersal has important consequences for local population fluctuations as well as cascading effects on regional metacommunity dynamics. Context-dependent dispersal reduced local population fluctuations and desynchronized dynamics between communities, two effects that increase population and community stability.\n\nOur study provides unprecedented insights into the generality of the positive resource dependency of dispersal as well as a robust experimental test of current theory predicting that predator-induced dispersal is modulated by prey and predator space use. Our experimental and theoretical work highlights the critical importance of the multi-causal nature of dispersal as well as its cascading effects on regional community dynamics, which are specifically relevant to ecological forecasting.

ecology↗