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Simon, J.-C.

Publications and source records attributed to Simon, J.-C..

16 recordsLinked to original sources

Morph-specific plasticity drives divergent host-shift and acclimation strategies in aphids

Understanding how organisms cope with environmental change is central to eco-evolutionary theory, yet a key unresolved challenge is distinguishing anticipatory plasticity, where phenotypes are pre-configured using predictive cues, from responsive plasticity, where phenotypes are adjusted after environmental exposure. Empirically testing these strategies is challenging because phenotypes measured after environmental transitions integrate both prior cue-dependent state configuration and post-exposure adjustment, obscuring when plastic responses are initiated. Systems with predictable environmental transitions and discrete life-history stages provide a powerful opportunity to resolve this challenge. Here, we use host-alternating aphids to test how plasticity strategies are organized across morphs experiencing the same seasonal host shift but facing different ecological constraints. We quantified fitness, transcriptomic responses, and host chemical landscapes across three morphs transferred among secondary hosts differing in phloem composition. Migratory spring morphs maintained uniformly high survival and showed minimal transcriptional change, consistent with anticipatory plasticity mediated by pre-configured metabolic and detoxification programs. In contrast, summer morphs exhibited host-dependent survival costs and extensive regulatory remodeling, indicating responsive plasticity. By integrating fitness, transcriptomics, and metabolomics, we show that predictable environmental transitions can favor the evolution and partitioning of plasticity strategies across life-history stages. More broadly, our results provide mechanistic evidence linking environmental predictability, regulatory architecture, and the evolution of plastic responses to heterogeneous environments.

evolutionary biology↗

The dynamics of barrier locus accumulation during speciation with gene flow

Understanding how reproductive isolation (RI) evolves in the context of gene flow is central to explaining how new species arise. Theory predicts that the accumulation of barrier loci depends on the interplay between divergent selection, recombination, and genomic architecture. However, empirical tests that track these processes across multiple stages of divergence within species remain scarce. The pea aphid complex, which comprises sympatric host-specialised biotypes spanning a continuum of divergence, provides a powerful opportunity to examine how ecological adaptation drives reproductive isolation despite ongoing gene flow. Using whole-genome sequencing data from 13 sympatric European biotypes, we constructed a dense, reference-anchored view of genomic divergence that controls for shared genetic background and recombination landscape. Joint analyses of genetic differentiation, absolute divergence, genetic diversity, recombination, and introgression rates reveal a consistent signature of divergence with gene flow and enable robust identification of barrier loci. Across the divergence continuum, RI is highly polygenic, but barrier loci are clustered and enriched in low-recombination regions and large chromosomal rearrangements, which are expected to strengthen linkage disequilibrium and promote the coupling of barrier effects. While genome-wide differentiation and the number of barrier loci increase gradually with divergence, differentiation within barrier loci displays patterns consistent with non-continuous dynamics, which could reflect threshold effects predicted by theory. Barrier loci contain excesses of salivary effector, detoxification and chemosensory genes, highlighting their central role in host plant specialisation and RI. The representation of these gene categories varies across divergence levels, and some loci are shared among independent biotype comparisons, suggesting common functional routes to specialisation via parallel evolution or introgression. Together, our results provide a comprehensive view of the genomic architecture and evolutionary dynamics underlying speciation with gene flow, illustrating how tightly linked, polygenic architectures can facilitate adaptation and diversification in natural populations.

evolutionary biology↗

Plant and Aphid Genotypes Modulate Legume Rhizobium-Induced Defense Against Aphids

Sustainable protein production is needed to ensure food security while mitigating climate change. Leguminous crops contribute to these goals by providing protein-rich seeds and improving soil fertility through nitrogen-fixing symbiosis (NFS) with rhizobia. Beyond their nutritional and agronomic benefits, legumes face major challenges from insect herbivores such as the pea aphid, Acyrthosiphon pisum. While NFS can enhance plant defences against aphids, the influence of plant and aphid genotypic variation on these rhizobia-mediated effects remains poorly understood. Here, we investigated how genotype interactions influence rhizobia-mediated defence priming by using two Medicago truncatula genotypes (A17 and R108) grown under NFS with Sinorhizobium meliloti 2011 or nitrate (NI) feeding conditions and infested with three clonal lines representing two pea aphid biotypes. We analysed aphid performance, plant fitness, and plant leaf expression of defence genes associated with the jasmonic acid (JA) and salicylic acid (SA) signalling pathways over a 12-day period following aphid infestation. Aphid fitness varied significantly with both plant and aphid genotypes and was further modulated by rhizobia inoculation. Expression of defence marker genes involved in SA and JA pathway was dependent on specific plant-aphid genotype combinations and was significantly modulated by rhizobia inoculation. This pattern suggests that both SA- and JA-mediated plant defences contribute to regulating aphid weight, possibly through different mechanisms or in response to different plant-aphid interactions. Our study shows that plant and aphid genotypes, rhizobia inoculation and interactions (G x G x R) are thus central components driving plantaphid-rhizobia interaction dynamics. Our study highlights importance of genetic context and microbial symbiosis in structuring multitrophic interactions and suggests new opportunities to optimize pest resistance using plant-beneficial microbial associations.

plant biology↗

RNA editing fine-tunes transcriptional plasticity and enhances the adaptability of Myzus persicae to diverse host plants

Parthenogenetic organisms can adapt to diverse and rapidly changing environments despite limited standing genetic variation, but the molecular mechanisms enabling such adaptability remain unclear. Here, we investigate this question in the green peach aphid (Myzus persicae, GPA), an asexual generalist herbivore capable of colonizing a wide range of host plants without underlying genetic change. By integrating RNA-seq and DNA-seq from genetically identical clones reared on different hosts, we identified 1,368 high-confidence RNA editing sites (RES), many of which exhibited strong host-dependent differences in editing levels. These RES encompassed all 12 possible nucleotide substitutions, with A-to-I, C-to-U, and U-to-C conversions being particularly prevalent. Editing at several sites shifted dynamically within 48 hours of host transfer and often coincided with changes in transcript abundance. Functional knockdown of the editing genes ADAR1 and ADAR2 reduced editing at specific sites, diminished fecundity, and abolished aphid survival on new hosts. Comparative analyses across aphid species reveal that although the biochemical signatures of A-to-I editing are deeply conserved, the genomic locations and functional roles of edited transcripts are species specific, reflecting lineage-specific adaptive strategies. Together, our findings demonstrate that RNA editing provides a rapid, reversible mechanism for environmental acclimation in GPA, enabling adaptive phenotypic plasticity even in the absence of genetic variation. This work establishes RNA editing as a key molecular basis for the remarkable ecological generalism of clonal organisms. Significance statementA major question in evolutionary biology is how clonal organisms with little genetic variation rapidly adapt to diverse, changing environments. Here we show that RNA editing provides a mechanism enabling the parthenogenetic green peach aphid (Myzus persicae) to colonize a wide range of host plants. RNA editing generates transcriptomic diversity, responds quickly to host shifts, and is essential for adaptation, as silencing ADAR genes disrupts A-to-I editing, reduces fitness, and prevents survival on new hosts. Comparative analyses across aphid species reveal that although the biochemical features of A-to-I editing are conserved, its genomic deployment and functional outcomes differ among species, reflecting lineage-specific strategies. These findings demonstrate that RNA editing creates a dynamic regulatory layer that offsets constraints of asexual reproduction.

molecular biology↗

Disc-Toroid Hybrid Lipid Nanoparticles for Efficient Drug Encapsulation and Subcutaneous Delivery

The development of an effective for subcutaneous or intradermal injection drug delivery requires systems with improved bioavailability and biocompatibility. Systematic physicochemical and biological interrogation of carnauba-wax/red-palm-oil lipid nanoparticles (LNPs) stabilised with d--tocopheryl-PEG-1000-succinate and polysorbate-40 shows that purposeful matrix engineering yields a robust sub-50 nm carrier for under-skin delivery. Cryo-TEM and SAXS uncover a disc-toroid hybrid morphology dominated by 30-40 nm particles with toroidal/disc shape - an advantageous biconcave geometry to enhance surface-to-volume ratio and is expected to accelerate enzymatic erosion after injection. Orthogonal analytics (AF4-MD, DLS, MALS, WAXS) confirmed that loading with quinine or dihydroartemisinin leaves size and crystallinity unchanged while delivering encapsulation efficiencies of approximately 90 % and long-term particle stability up to 18 months at 4 {degrees}C. Red-palm oil and the dual-surfactant corona act synergistically to suppress bimodality and narrow size distribution compared with single-component controls. Short-term viability assays in keratinocytes, fibroblasts and macrophages showed no cytotoxicity even at [≥]1 % (w/v) lipid, underscoring excellent biocompatibility. Fluorescein-labelled LNPs injected into ex vivo human skin traversed the dermis and hypodermis, while only nanomolar lipid concentrations appeared in the receiver medium, indicating a sustained local depot. Collectively, these insights link composition, structure and performance, positioning wax-based disc-toroid LNPs as a flexible platform for high-load delivery of small-molecule or biopharmaceutical therapeutics via minimally invasive under-skin administration.

biochemistry↗

Plant-induced transcriptional plasticity diverges between generalist and specialist herbivores

Most herbivores are specialized on particular host plants but some are generalists that can exploit distinct hosts. Generalists may have evolved adaptive transcriptional plasticity to cope with the defenses of the different hosts. However, the fundamental differences in plant-induced transcriptional plasticity between generalists and specialists remain poorly understood. Here, we investigated transcriptional plasticity of the generalist aphid Myzus persicae and two specialist aphids, Brevicoryne brassicae and Rhopalosiphum padi, by transferring them between Brassica napus (a host for B. brassicae but not for R. padi) and Zea mays (a host for R. padi but not for B. brassicae), both suitable hosts for M. persicae. Generalist and specialist aphids exhibited transcriptional plasticity coordinately in response to different plant species, but their gene expression patterns often diverged. Generalists suppressed plant-defense salicylic acid (SA) signaling in the host plants, while specialist aphids provoked it in nonhost plants. SA signaling had limited effects on gene expression in the generalist aphids, but significantly shaped transcriptional responses of the specialists. These findings underscore the fundamental differences in plant-induced transcriptional plasticity between generalists and specialists and highlight the critical role of plasticity directionality in insect adaptation. Significance statementMost insects specialize in feeding on just a few specific plants, but some generalists can thrive on many plant species. This study compares the gene expression of green peach aphid Myzus persicae, a generalist, with two specialist aphids in response to different types of plants. Generalists showed adaptive plasticity in their gene responses, while specialists often exhibited opposite gene expression changes. Interestingly, generalists appeared to suppress plant defense signals like salicylic acid, while specialists tended to trigger them. These findings highlight how gene expression plasticity enables generalists to adapt and survive, providing new insights into the evolution of insect-plant interactions.

plant biology↗

Insights into the triggering factors and determination mechanisms of host alternation in aphids

The bird cherry-oat aphid Rhopalosiphum padi, is one of the ten percent of aphids that are host alternating. The annual life cycle of R. padi entails an obligatory migration between a primary woody host, Prunus padus (Rosaceae), where sexual reproduction occurs, and many secondary hosts of the Poaceae family, where successive generations reproduce parthenogenetically. Migration between the two types of host plants is achieved by specialized migrant morphs. Very little is known about the cues that trigger migrant development, host alternation establishment and the underlying mechanisms. In this study, we aimed to elucidate the key steps involved in migrant induction and determination of host alternation, and to shed light on these intricate processes. We showed that a specific stage of leaf maturity triggers the development into a migrant morph when presented to R. padi at the first or second larval instar stages. We also demonstrated the gradual establishment of acclimation to the secondary hosts that precedes the migration step. Finally, we showed that the switch to feeding on the alternative hosts is irreversible once emigrants have reached adulthood. These results not only allowed us to define the critical periods of the leaf stage associated with morph induction and determination, but also to pinpoint the emigrants developmental stages when acclimation to secondary hosts begins. These novel insights of these critical periods will facilitate the investigation of molecular changes associated with host alternation in aphids.

ecology↗

Multi-omics approaches define novel aphid effector candidates associated with virulence and avirulence phenotypes

BackgroundCompatibility between plant parasites and their hosts is genetically determined by both interacting organisms. For example, plants may carry resistance (R) genes or deploy chemical defences. Aphid saliva contains many proteins that are secreted into host tissues. Subsets of these proteins are predicted to act as effectors, either subverting or triggering host immunity. However, associating particular effectors with virulence or avirulence outcomes presents challenges due to the combinatorial complexity. Here we use defined aphid and host genetics to test for co-segregation of expressed aphid transcripts and proteins with virulent or avirulent phenotypes. ResultsWe compared virulent and avirulent pea aphid parental genotypes, and their bulk segregant F1 progeny on Medicago truncatula genotypes carrying or lacking the RAP1 resistance quantitative trait locus. Differential gene expression analysis of whole body and head samples, in combination with proteomics of saliva and salivary glands, enabled us to pinpoint proteins associated with virulence/avirulence phenotypes. There was relatively little impact of host genotype, whereas large numbers of transcripts and proteins were differentially expressed between parental aphids, likely a reflection of their classification as divergent biotypes within the pea aphid species complex. Many fewer transcripts intersected with the equivalent differential expression patterns in the bulked F1 progeny, providing an effective filter for removing genomic background effects. Overall, there were more upregulated genes detected in the F1 avirulent dataset compared with the virulent one. Some genes were differentially expressed both in the transcriptome and in the proteome datasets, with aminopeptidase N proteins being the most frequent differentially expressed family. In addition, a substantial proportion (27%) of salivary proteins lack annotations, suggesting that many novel functions remain to be discovered. ConclusionsEspecially when combined with tightly controlled genetics of both insect and host, multi-omics approaches are powerful tools for revealing and filtering candidate lists down to plausible genes for further functional analysis as putative aphid effectors.

genomics↗

A quarter-million-year-old polymorphism drives reproductive mode variation in the pea aphid

Although asexual linages evolved from sexual lineages in many different taxa, the genetics of sex loss remains poorly understood. We addressed this issue in the pea aphid Acyrthosiphon pisum, whose natural populations encompass lineages performing cyclical parthenogenesis (CP) and producing one sexual generation per year, as well as obligate parthenogenetic (OP) lineages that can no longer produce sexual females but can still produce males. A SNP-based, whole-genome scan of CP and OP populations sequenced in pools (103 individuals from six populations) showed that a single X-linked region controls the variation in reproductive mode. This 840-kb region is highly divergent between CP and OP populations (FST = 34.9%), with >2000 SNPs or short Indels showing a high degree of association with the phenotypic trait. Comparison of de novo genome assemblies built from long reads did not reveal large structural rearrangements between CP and OP lineages within the candidate region. This reproductive polymorphism still appears relatively ancient, as we estimated its age at ~0.25 million years from the divergence between cp and op alleles. The low genetic differentiation between CP and OP populations at the rest of the genome (FST = 2.4%) suggests gene flow between them. Males from OP lineages thus likely transmit their op allele to new genomic backgrounds. This "contagious asexuality", combined with environment-induced selection (each reproductive mode being favored under different climates) probably contributes to the long-term persistence of the cp and op alleles. SignificanceAsexual taxa occur in all major clades of Eukaryotes and derive from related sexual species. Yet, the genetic basis for these transitions is poorly known because crosses cannot generally be performed to genetically map the ability to propagate asexually. As a result, only one gene responsible for sex loss has been identified in one animal species. Here, using pooled genome sequencing, we identified an 840kb region (carrying 32 genes) that controls the transition to permanent asexuality in the pea aphid. We also revealed that sexual and asexual alleles diverged 0.25 million years ago and that asexual lineages likely persist through contagious asexuality, providing new insights into the mechanisms of coexistence of sexual and asexual lineages.

evolutionary biology↗

Pea-adapted biotype of the aphid Acyrthosiphon pisum induces susceptibility of pea to non-adapted biotype enabling improved feeding and performance

Most insect herbivores are adapted to feed on a few host plants only, but the mechanisms underlying plant specialization are poorly understood. One of the dominant hypotheses is that insects inject an oral secretion into the plant that manipulates the plants defences resulting in induced susceptibility. We tested this hypothesis on the pea aphid (Acyrthosiphon pisum), which forms multiple biotypes, each specialized on specific legume hosts. In particular, we tested whether a pea-adapted biotype can induce host susceptibility on pea, which should positively affect the fitness of a non-pea-adapted biotype. We found that survival and fecundity of an alfalfa-adapted biotype on pea were enhanced by co-infestation but not pre-infestation with a pea-adapted biotype. The electrical penetration graph (EPG) method was then used to dissect the components of alfalfa biotype feeding behaviour on pea with and without co-infestation by the pea biotype. While probing time did not differ between these two conditions, differences were observed in most other EPG parameters. When co-infested with the pea-adapted biotype, the alfalfa-adapted biotype was more likely to establish a phloem feeding and exhibited a longer ingestion time on pea. Our results clearly indicated that the pea-adapted biotype induced pea susceptibility by increasing the accessibility of non-pea-adapted aphids to the host phloem sap, and as a result, the alfalfa biotype increased its survival rate and fecundity. These results contribute to understanding how aphids manipulate their specific host plants.

ecology↗

Masculinization of the X-chromosome in aphid soma and gonads

Males and females share essentially the same genome but differ in their optimal values for many phenotypic traits, which can result in intra-locus conflict between the sexes. Aphids display XX/X0 sex chromosomes and combine unusual X chromosome inheritance with cyclical parthenogenesis. Theoretical and empirical works support the hypothesis that the large excess of male-biased genes observed on the aphid X chromosome compared to autosomes evolved in response to sexual conflicts, by restricting the products of sexually antagonistic alleles to the sex they benefits. However, whether such masculinization of the X affects all tissues (as expected if it evolved in response to sexual conflicts) or is limited to specific tissues remains an open question. Here, we measured gene expression in three different somatic and gonadic tissues of males, sexual females and parthenogenetic females of the pea aphid. We observed a masculinization of the X in each of the studied tissues, with male-biased genes being 2.5 to 3.5 more frequent on the X than expected. We also tested the hypothesis that gene duplication can facilitate the attenuation of conflicts by allowing gene copies to neo- or sub-functionalize and reach sex-specific optima. As predicted, X-linked copies of duplicated genes having their other copies on autosomes were more frequently male-biased (40.5% of the genes) than duplicated autosomal genes (6.6%) or X-linked single-copy genes (32.5%). These results highlight a peculiar pattern of expression of X-linked genes in aphids at the tissue level and provide further support for sex-biased expression as a mechanism to attenuate intra-locus sexual conflicts.

evolutionary biology↗

MinYS: Mine Your Symbiont by targeted genome assembly in symbiotic communities

Most metazoans are associated with symbionts. Characterizing the effect of a particular symbiont often requires to get access to its genome, which is usually done by sequencing the whole community. We present MinYS, a targeted assembly approach to assemble one particular genome of interest from such metagenomic data. First, taking advantage of a reference genome, a subset of the reads is assembled into a set of backbone contigs. Then, this draft assembly is completed using the whole metagenomic readset in a de novo manner. The resulting assembly is output as a genome graph, allowing to distinguish different strains with potential structural variants coexisting in the sample. MinYS was applied to 50 pea aphid re-sequencing samples, with low and high diversity, in order to recover the genome sequence of its obligatory bacterial symbiont, Buchnera aphidicola. It was able to return high quality assemblies (one contig assembly in 90% of the samples), even when using increasingly distant reference genomes, and to retrieve large structural variations in the samples. Due to its targeted essence, it outperformed standard metagenomic assemblers in terms of both time and assembly quality.

bioinformatics↗

Functional insights from the GC-poor genomes of two aphid parasitoids, Aphidius ervi and Lysiphlebus fabarum

BackgroundParasitoid wasps have fascinating life cycles and play an important role in trophic networks, yet little is known about their genome content and function. Parasitoids that infect aphids are an important group with the potential for biocontrol, and infecting aphids requires overcoming both aphid defenses and their defensive endosymbionts. ResultsWe present the de novo genome assemblies, detailed annotation, and comparative analysis of two closely related parasitoid wasps that target pest aphids: Aphidius ervi and Lysiphlebus fabarum (Hymenoptera: Braconidae: Aphidiinae). The genomes are small (139 and 141 Mbp), highly syntenic, and the most AT-rich reported thus far for any arthropod (GC content: 25.8% and 23.8%). This nucleotide bias is accompanied by skewed codon usage, and is stronger in genes with adult-biased expression. AT-richness may be the consequence of reduced genome size, a near absence of DNA methylation, and age-specific energy demands. We identify expansions of F-box/Leucine-rich-repeat proteins, suggesting that diversification in this gene family may be associated with their broad host range or with countering defenses from aphids endosymbionts. The absence of some immune genes (Toll and Imd pathways) resembles similar losses in their aphid hosts, highlighting the potential impact of symbiosis on both aphids and their parasitoids. ConclusionsThese findings are of fundamental interest for insect evolution and beyond. This will provide a strong foundation for further functional studies including coevolution with respect to their hosts, the basis of successful infection, and biocontrol. Both genomes are available at https://bipaa.genouest.org.

genomics↗

Herbivore intraspecific variation and evolutionary divergence drive trophic cascade strength

AO_SCPLOWBSTRACTC_SCPLOWTrophic cascades--the indirect effect of predators on non-adjacent lower trophic levels--are important drivers of the structure and dynamics of ecological communities. However, the influence of intraspecific trait variation on the strength of trophic cascade remains largely unexplored, which limits our understanding of the mechanisms underlying ecological networks. Here we experimentally investigated how intraspecific difference among herbivore lineages specialized on different host plants influences the strength of trophic cascade in a terrestrial tritrophic system. We found that the occurrence and strength of the trophic cascade are strongly influenced by herbivores lineage and host-plant specialization but are not associated with density-dependent effects mediated by the growth rate of herbivore populations. Our findings stress the importance of intraspecific heterogeneities and evolutionary specialization as drivers of the strength of trophic cascades and underline that intraspecific variation should not be overlooked to decipher the joint influence of evolutionary and ecological factors on the functioning of multi-trophic interactions.

ecology↗

Unravelling the genomic basis and evolution of the pea aphid male wing dimorphism

Wing dimorphisms have long served as models for examining the ecological and evolutionary tradeoffs associated with alternative morphologies [1], yet the mechanistic basis of morph determination remains largely unknown. Here we investigate the genetic basis of the pea aphid (Acyrthosiphon pisum) wing dimorphism, wherein males exhibit one of two alternative morphologies that differ dramatically in a set of correlated traits that inclused the presence or absence of wings [2-4]. Unlike the environmentally-induced asexual female aphid wing polyphenism [5], the male wing polymorphism is genetically determined by a single uncharacterized locus on the X chromosome called aphicarus (\"aphid\" plus \"Icarus\", api) [6, 7]. Using recombination and association mapping, we localized api to a 130kb region of the pea aphid genome. No nonsynonymous variation in coding sequences strongly associated with the winged and wingless phenotypes, indicating that api is likely a regulatory change. Gene expression level profiling revealed an aphid-specific gene from the region expressed at higher levels in winged male embryos, coinciding with the expected stage of api action. Comparison of the api region across biotypes (pea aphid populations specialized to different host plants that began diverging ~16,000 years ago [8, 9]) revealed that the two alleles were likely present prior to biotype diversification. Moreover, we find evidence for a recent selective sweep of a wingless allele since the biotypes diversified. In sum, this study provides insight into how adaptive, complex traits evolve within and across natural populations.

evolutionary biology↗

Disentangling The Causes For Faster-X Evolution In Aphids

Faster evolution of X chromosomes has been documented in several species and results from the increased efficiency of selection on recessive alleles in hemizygous males and/or from increased drift due to the smaller effective population size of X chromosomes. Aphids are excellent models for evaluating the importance of selection in faster-X evolution, because their peculiar life-cycle and unusual inheritance of sex-chromosomes lead to equal effective population sizes for X and autosomes. Because we lack a high-density genetic map for the pea aphid whose complete genome has been sequenced, we assigned its entire genome to the X and autosomes based on ratios of sequencing depth in males and females. Unexpectedly, we found frequent scaffold misassembly, but we could unambiguously locate 13,726 genes on the X and 19,263 on autosomes. We found higher non-synonymous to synonymous substitutions ratios (dN/dS) for X-linked than for autosomal genes. Our analyses of substitution rates together with polymorphism and expression data showed that relaxed selection is likely to contribute predominantly to faster-X as a large fraction of X-linked genes are expressed at low rates and thus escape selection. Yet, a minor role for positive selection is also suggested by the difference between substitution rates for X and autosomes for male-biased genes (but not for asexual female-biased genes) and by lower Tajimas D for X-linked than for autosomal genes with highly male-biased expression patterns. This study highlights the relevance of organisms displaying alternative inheritance of chromosomes to the understanding of forces shaping genome evolution.

evolutionary biology↗