Biology subjects

Estoup, A.

Publications and source records attributed to Estoup, A..

11 recordsLinked to original sources

bioRxiv2026

Genome-Environment Associations reveal shared and unique adaptive loci across multiple pollutants and populations of the eastern mosquitofish Gambusia holbrooki

Rapid adaptation to human-induced stressors is commonplace in the context of global change, including during biological invasions. Identifying the genomic bases and associated biological functions underlying such adaptation is hence crucial to understand and anticipate the response of populations and species to changing conditions. In particular, the extent to which genetic responses to multiple anthropogenic stressors vary between populations in the wild has been relatively unexplored. We addressed this question by leveraging whole-genome sequence data (both PoolSeq and IndSeq) in invasive populations of Gambusia holbrooki - a widespread invasive fish species - collected from 14 locations with different multi-pollutants exposure. We sought to identify adaptive loci associated with pollution tolerance by conducting Genome-Environment Association (GEA) analyses. Additionally, we investigated the degree of adaptive loci reuse between pollutants and their combinations as well as across populations. We found strong signals of association between allele frequency changes and pollutant exposure at several genomic locations, often overlapping with genes known for their functions in detoxification and immune response. We further showed that most adaptive loci are not shared among all populations, suggesting heterogeneous genomic response to each local selection. Interestingly, multiple tests looking for footprints of selection and association to pollutants yielded consistent results. Our results shed new light on the extent of genetic convergence in the genomic bases of rapid adaptation to different cocktails of human-induced pollution, and are important to our understanding of the fate of wild populations facing increasingly complex and stressful environments.

genomics↗

bioRxiv2024

Better confidence intervals in simulation-based inference

Simulation-based methods such as approximate Bayesian computation (ABC) are widely used to infer the evolutionary history of populations from molecular genetic data. We describe and evaluate a new iterative method of statistical inference about model parameters, which revisits the idea of inferring a likelihood surface using simulation when the likelihood function cannot be evaluated. It is based on combining the random forest machine learning method, and multivariate Gaussian mixture (MGM) models, in an effective inference workflow, here used to fit models with up to 15 variable parameters. In addition to the traditional assessment of precision in terms of bias and mean square error, we also evaluate the coverage of confidence intervals. The method is compared with approximate Bayesian computation using random forests (ABC-RF), a non-iterative method sharing some technical features with the proposed approach, across scenarios of historical demographic inference from population genetic data. It is also compared to another iterative method, sequential neural likelihood estimation (SNLE). These comparisons highlight the importance of an iterative workflow for exploring the parameter space efficiently. For equivalent simulation effort of the data-generating process, the new summary-likelihood method provides intervals whose coverage is better controlled than the marginal coverage of intervals provided by ABC with random forests, and than generally reported for ABC methods. The iterative workflow can also yield greater improvements in estimator precision when larger datasets are used.

bioinformatics↗

bioRxiv2022

Rapid and transient evolution of local adaptation to seasonal host fruits in an invasive fly

Both local adaptation and adaptive phenotypic plasticity can influence the match between phenotypic traits and local environmental conditions. Theory predicts that environments stable for multiple generations promote local adaptation, while highly heterogeneous environments favor adaptive phenotypic plasticity. However, when environments have periods of stability mixed with heterogeneity, the relative importance of local adaptation and adaptive phenotypic plasticity is unclear. Here, we used Drosophila suzukii as a model system to evaluate the relative influence of genetic and plastic effects on the match of populations to environments with periods of stability from three to four generations. This invasive pest insect can develop within different fruits, and persists throughout the year in a given location on a succession of distinct host fruits, each one being available for only a few generations. Using reciprocal common environment experiments of natural D. suzukii populations collected from cherry, strawberry and blackberry, we found that both oviposition preference and offspring performance were higher on medium made with the fruit from which the population originated, than on media made with alternative fruits. This pattern, which remained after two generations in the laboratory, was analyzed using a statistical method we developed to quantify the contributions of local adaptation and adaptive plasticity in determining fitness. Altogether, we found that genetic effects (local adaptation) dominate over plastic effects (adaptive phenotypic plasticity). Our study demonstrates that spatially and temporally variable selection does not prevent the rapid evolution of local adaptation in natural populations. The speed and strength of adaptation may be facilitated by several mechanisms including a large effective population size and strong selective pressures imposed by host plants. Impact SummaryNatural populations often exhibit good "fit" to the environment they are in. However, environments change over time and space, and following change, the fit between a population and its environment may be poor. A question of long-standing interest is how do populations track changing environments to maintain fitness? Two main mechanisms are known: (i) genetic shifts in the form of local adaptation, in which traits evolve over time through differences in fitness of individuals harboring different genetic variants, and (ii) plastic shifts, or adaptive phenotypic plasticity, in which traits immediately change in response to environmental change. Adaptation is common when environments change over multiple generations, while plasticity is common when environments change over an individuals lifetime. However, it remains unclear whether plasticity or adaptation is more vital to maintaining fitness when environments change at an intermediate pace. Drosophila suzukii is well-suited to evaluating the relative importance of plasticity and adaptation in response to an intermediate pace of environmental change. This invasive pest species experiences an environment that shifts every 1-4 generations as host fruits change over time and space. Here, we studied natural populations of D. suzukii collected from different hosts. Using reciprocal common environment experiments, we evaluated their fitness on their source and alternative hosts. Drosophila suzukii populations were most fit on their source host, successfully tracking an intermediate pace of environmental change. We developed a statistical method to quantify the contributions of adaptive plasticity and local adaptation in determining fitness. We found that fitness was mainly maintained through local adaptation to each new host in succession. This study highlights that spatially and temporally variable selection does not prevent local adaptation and, on the contrary, illustrates how rapid the adaptive process can be. It also provides a novel statistical tool that can be applied to other systems

evolutionary biology↗

bioRxiv2021

f-statistics estimation and admixture graph construction with Pool-Seq or allele count data using the R package poolfstat

By capturing various patterns of the structuring of genetic variation across populations, f -statistics have proved highly effective for the inference of demographic history. Such statistics are defined as covariance of SNP allele frequency differences among sets of populations without requiring haplotype information and are hence particularly relevant for the analysis of pooled sequencing (Pool-Seq) data. We here propose a reinterpretation of the F (and D) parameters in terms of probability of gene identity and derive from this unified definition unbiased estimators for both Pool-Seq and standard allele count data obtained from individual genotypes. We implemented these estimators in a new version of the R package poolfstat, which now includes a wide range of inference methods: (i) three-population test of admixture; (ii) four-population test of treeness; (iii) F4-ratio estimation of admixture rates; and (iv) fitting, visualization and (semi-automatic) construction of admixture graphs. A comprehensive evaluation of the methods implemented in poolfstat on both simulated Pool-Seq (with various sequencing coverages and error rates) and allele count data confirmed the accuracy of these approaches, even for the most cost-effective Pool-Seq design involving low sequencing coverages. We further analyzed a real Pool-Seq data made of 14 populations of the invasive species Drosophila suzukii which allowed refining both the demographic history of native populations and the invasion routes followed by this emblematic pest. Our new package poolfstat provides the community with a user-friendly and efficient all-in-one tool to unravel complex population genetic histories from large-size Pool-Seq or allele count SNP data.

evolutionary biology↗

bioRxiv2020

The worldwide invasion of Drosophila suzukii isaccompanied by a large increase of transposable elementload and a small number of putatively adaptive insertions

Transposable Elements (TEs) are ubiquitous and mobile repeated sequences. They are major determinants of host fitness. Here, we portrayed the TE content of the spotted wing fly Drosophila suzukii. Using a recently improved genome assembly, we reconstructed TE sequences de novo, and found that TEs occupy 47% of the genome and are mostly located in gene poor regions. The majority of TE insertions segregate at low frequencies, indicating a recent and probably ongoing TE activity. To explore TE dynamics in the context of biological invasions, we studied variation of TE abundance in genomic data from 16 invasive and six native populations (of D. suzukii). We found a large increase of the TE load in invasive populations correlated with a reduced Watterson estimate of genetic diversity [Formula] a proxy of effective population size. We did not find any correlation between TE contents and bio-climatic variables, indicating a minor effect of environmentally induced TE activity. A genome-wide association study revealed that ca. 5,000 genomic regions are associated with TE abundance. We did not find, however, any evidence in such regions of an enrichment for genes known to interact with TE activity (e.g. transcription factor encoding genes or genes of the piRNA pathway). Finally, the study of TE insertion frequencies revealed 15 putatively adaptive TE insertions, six of them being likely associated with the recent invasion history of the species.

evolutionary biology↗

bioRxiv2020

Near-chromosome level genome assembly of the fruit pest Drosophila suzukii using long-read sequencing

Over the past decade, the spotted wing Drosophila, Drosophila suzukii, has invaded Europe and America and has become a major agricultural pest in these areas, thereby prompting intense research activities to better understand its biology. Two draft genome assemblies based on short-read sequencing were released in 2013 for this species. Although valuable, these resources contain pervasive assembly errors and are highly fragmented, two features limiting their values. Our purpose here was to improve the assembly of the D. suzukii genome. For this, we generated PacBio long-read sequencing data at 160X sequence coverage and assembled a novel, contiguous D. suzukii genome. We obtained a high-quality assembly of 270 Mb (with 546 contigs, a N50 of 2.6Mb, a L50 of 15, and a BUSCO score of 95%) that we called WT3-2.0. We found that despite 16 rounds of full-sib crossings the D. suzukii strain that we sequenced has maintained high levels of polymorphism in some regions of its genome (ca. 19Mb). As a consequence, the quality of the assembly of these regions was reduced. We explored possible origins of this high residual diversity, including the presence of structural variants and a possible heterogeneous admixture pattern of North American and Asian ancestry. Overall, our WT3-2.0 assembly provides a higher quality genomic resource compared to the previous one in terms of general assembly statistics, sequence quality and gene annotation. This new D. suzukii genome assembly is therefore an improved resource for high-throughput sequencing approaches, as well as manipulative genetic technologies to study D. suzukii.

ecology↗

bioRxiv2019

How do invasion syndromes evolve? An experimental evolution approach using the ladybug Harmonia axyridis

Experiments comparing native to introduced populations or distinct introduced populations to each other show that phenotypic evolution is common and often involves a suit of interacting phenotypic traits. We define such sets of traits that evolve in concert and contribute to the success of invasive populations as an invasion syndrome. The invasive Harlequin ladybird Harmonia axyridis displays such an invasion syndrome with, for instance, females from invasive populations being larger and heavier than individuals from native populations, allocating more resources to reproduction, and spreading reproduction over a longer lifespan. Invasion syndromes could emerge due to selection acting jointly and directly on a multitude of traits, or due to selection on one or a few key traits that drive correlated indirect responses in other traits. Here, we investigated the degree to which the H. axyridis invasion syndrome would emerge in response to artificial selection on either female body mass or on age at first reproduction, two traits involved in their invasion syndrome. To further explore the interaction between environmental context and evolutionary change in molding the phenotypic response, we phenotyped the individuals from the selection experiments in two environments, one with abundant food resources and one with limited resources. The two artificial selection experiments show that the number of traits showing a correlated response depends upon the trait undergoing direct selection. Artificial selection on female body mass resulted in few correlated responses and hence poorly reproduced the invasion syndrome. In contrast, artificial selection on age at first reproduction resulted in more widespread phenotypic changes, which nevertheless corresponded only partly to the invasion syndrome. The artificial selection experiments also revealed a large impact of diet on the traits, with effects dependent on the trait considered and the selection regime. Overall, our results indicate that direct selection on multiple traits was likely necessary in the evolution of the H. axyridis invasion syndrome. Furthermore, they show the strength of using artificial selection to identify the traits that are correlated in different selective contexts, which represents a crucial first step in understanding the evolution of complex phenotypic patterns, including invasion syndromes.

evolutionary biology↗

bioRxiv2019

A whole-genome scan for association with invasion success in the fruit fly Drosophila suzukii using contrasts of allele frequencies corrected for population structure

Evidence is accumulating that evolutionary changes are not only common during biological invasions but may also contribute directly to invasion success. The genomic basis of such changes is still largely unexplored. Yet, understanding the genomic response to invasion may help to predict the conditions under which invasiveness can be enhanced or suppressed. Here we characterized the genome response of the spotted wing drosophila Drosophila suzukii during the worldwide invasion of this pest insect species, by conducting a genome-wide association study to identify genes involved in adaptive processes during invasion. Genomic data from 22 population samples were analyzed to detect genetic variants associated with the status (invasive versus native) of the sampled populations based on a newly developed statistic, we called C2, that contrasts allele frequencies corrected for population structure. This new statistical framework has been implemented in an upgraded version of the program BO_SCPLOWAYC_SCPLOWPO_SCPLOWASSC_SCPLOW. We identified a relatively small set of single nucleotide polymorphisms (SNPs) that show a highly significant association with the invasive status of populations. In particular, two genes RhoGEF64C and cpo, the latter contributing to natural variation in several life-history traits (including diapause) in Drosophila melanogaster, contained SNPs significantly associated with the invasive status in the two separate main invasion routes of D. suzukii. Our methodological approaches can be applied to any other invasive species, and more generally to any evolutionary model for species characterized by non-equilibrium demographic conditions for which binary covariables of interest can be defined at the population level.

evolutionary biology↗

bioRxiv2019

Evolution of trade-offs across environments following experimental evolution of the generalist Drosophila suzukii to different fruit media

The process of local adaptation involves differential changes in fitness over time across different environments. While experimental evolution studies have extensively tested for patterns of local adaptation at a single time point, there is relatively little research that examines fitness more than once during the time course of adaptation. We allowed replicate populations of the fruit pest Drosophila suzukii to evolve in one of eight different fruit media. After five generations, populations with the highest initial levels of maladaptation had mostly gone extinct, whereas experimental populations evolving on cherry, strawberry and cranberry media had survived. We measured the fitness of each surviving population in each of the three fruit media after five and after 26 generations of evolution. After five generations, adaptation to each medium was associated with increased fitness in the two other media. This was also true after 26 generations, except when populations that evolved on cranberry medium developed on cherry medium. These results suggest that, in the theoretical framework of a fitness landscape, the fitness optima of cherry and cranberry media are the furthest apart. Our results show that studying how fitness changes across several environments and across multiple generations provides insights into the dynamics of local adaptation that would not be evident if fitness were analyzed at a single point in time. By allowing a qualitative mapping of an experimental fitness landscape, our approach will improve our understanding of the ecological factors that drive the evolution of local adaptation in D. suzukii.

evolutionary biology↗

bioRxiv2019

A young age of subspecific divergence in the desert locust Schistocerca gregaria

AO_SCPLOWBSTRACTC_SCPLOWDating population divergence within species from molecular data and relating such dating to climatic and biogeographic changes is not trivial. Yet it can help formulating evolutionary hypotheses regarding local adaptation and future responses to changing environments. Key issues include statistical selection of a demographic and historical scenario among a set of possible scenarios, and estimation of the parameter(s) of interest under the chosen scenario. Such inferences greatly benefit from new statistical approaches including approximate Bayesian computation - Random Forest (ABC-RF), the latter providing reliable inference at a low computational cost, with the possibility to take into account prior knowledge on both biogeographical history and genetic markers. Here, we used ABC-RF, including independent information on evolutionary rate and pattern at microsatellite markers, to decipher the evolutionary history of the African arid-adapted pest locust, Schistocerca gregaria. We found that the evolutionary processes that have shaped the present geographical distribution of the species in two disjoint northern and southern regions of Africa were recent, dating back 2.6 Ky (90% CI: 0.9 - 6.6 Ky). ABC-RF inferences also supported a southern colonization of Africa from a low number of founders of northern origin. The inferred divergence history is better explained by the peculiar biology of S. gregaria, which involves a density-dependent swarming phase with some exceptional spectacular migrations, rather than a continuous colonization resulting from the continental expansion of open vegetation habitats during more ancient Quaternary glacial climatic episodes.

evolutionary biology↗

bioRxiv2018

The genomic basis of colour pattern polymorphism in the harlequin ladybird

Many animal species are comprised of discrete phenotypic forms. Understanding the genetic mechanisms generating and maintaining such phenotypic variation within species is essential to comprehending morphological diversity. A common and conspicuous example of discrete phenotypic variation in natural populations of insects is the occurrence of different colour patterns, which has motivated a rich body of ecological and genetic research1-6. The occurrence of dark, i.e. melanic, forms, displaying discrete colour patterns, is found across multiple taxa, but the underlying genomic basis remains poorly characterized. In numerous ladybird species (Coccinellidae), the spatial arrangement of black and orange patches on adult elytra varies wildly within species, forming strikingly different complex colour patterns7,8. In the harlequin ladybird Harmonia axyridis, more than 200 distinct colour forms have been described, which classic genetic studies suggest result from allelic variation at a single, unknown, locus9,10. Here, we combined whole-genome sequencing, population genomics, gene expression and functional analyses, to establish that the gene pannier controls melanic pattern polymorphism in H. axyridis. We show that pannier, which encodes an evolutionary conserved transcription factor, is necessary for the formation of melanic elements on the elytra. Allelic variation in pannier leads to protein expression in distinct domains on the elytra, and thus determines the distinct colour patterns in H. axyridis. Recombination between pannier alleles may be reduced by a highly divergent sequence of ca. 170 kb in the cis-regulatory regions of pannier with a 50 kb inversion between colour forms. This likely helps maintaining the distinct alleles found in natural populations. Thus we propose that highly variable discrete colour forms can arise in natural populations through cis-regulatory allelic variation of a single gene.

evolutionary biology↗