Biology subjects

Battlay, P.

Publications and source records attributed to Battlay, P..

15 recordsLinked to original sources

bioRxiv2026

Historical genomes reveal scale-dependent predictability of climate adaptation

Predicting evolution remains a central challenge in biology. Contemporary spatial patterns are increasingly used as space-for-time proxies to forecast evolutionary responses to environmental change, yet the reliability of such predictions--and whether it varies among biological scales--remains unclear. Using historical and contemporary genomes of the invasive weed Ambrosia artemisiifolia--spanning the species' native range, invasions on two continents and nearly two centuries--we show that genomically predicted flowering-time clines remained stable in the native range while introduced populations re-evolved them. Haploblocks--likely structural variants--were likewise temporally stable in the native range, and two showed striking parallel evolution across all three ranges. Climate-associated SNPs with the strongest contemporary clines showed the greatest temporal change, with limited and variable parallelism among introduced ranges. Together, these results suggest adaptive evolution is partly predictable even when individual genomic trajectories remain flexible and contingent, with predictability emerging most clearly at the level of polygenic traits and large structural variants.

evolutionary biology↗

bioRxiv2026

Selection shapes the evolution of genome size in a globally invasive plant

O_LIBiological invasions provide powerful natural experiments for understanding how genome architecture responds to novel climatic environments. Transposable elements (TEs) can rapidly restructure genomes, yet their role in adaptive genome size evolution during invasion remains poorly understood. C_LIO_LIHere, we examined genome size and TE abundance in 439 individuals of globally invasive common ragweed (Ambrosia artemisiifolia L.) across native (North American) and invasive (European, Australian) ranges. By integrating whole-genome resequencing, flow cytometry, and trait versus genetic differentiation comparison (QST-FST), we tested whether genome size evolution is shaped by selection, climate, and life-history traits. C_LIO_LIGenome size was significantly larger in Australian genotypes, driven by increased TE and rRNA (ribosomal RNA) abundance. Crucially, trait versus genetic differentiation comparison provided evidence of divergent selection on genome size in North American and European populations, but not in Australia. Genome size was correlated with mean annual temperature (MAT) across all ranges, linking genomic traits to environmental variables. C_LIO_LIGenome size evolution during invasion can be rapid, adaptive, and range-specific, with TE-driven genome expansion emerging as a potential genomic response to the demographic and environmental pressures accompanying colonization of novel environments. C_LI

evolutionary biology↗

bioRxiv2024

Rapid parallel adaptation in distinct invasions of Ambrosia artemisiifolia is driven by large-effect structural variants

When introduced to multiple distinct ranges, invasive species provide a compelling natural experiment for understanding the repeatability of adaptation. Ambrosia artemisiifolia is an invasive, noxious weed and chief cause of hay fever. Leveraging over 400 whole-genome sequences spanning the native range in North America and two invasions in Europe and Australia, we inferred demographically distinct invasion histories on each continent. Despite substantial differences in genetic source and effective population size changes during introduction, scans of both local climate adaptation and divergence from the native range revealed genomic signatures of parallel adaptation between invasions. Disproportionately represented among these parallel signatures are 37 large haploblocks - indicators of structural variation - that cover almost 20% of the genome and exist as standing genetic variation in the native range. Many of these haploblocks are associated with traits important for adaptation to local climate, like size and the timing of flowering, and have rapidly reformed native range clines in invasive ranges. Others show extreme frequency divergence between ranges, consistent with a response to divergent selection on different continents. Our results demonstrate the key role of large-effect standing variants in rapid adaptation during range expansion, a pattern that is robust to diverse invasion histories.

genomics↗

bioRxiv2024

Structural variants underlie parallel adaptation following global invasion

Rapid adaptation during invasion has historically been considered limited and unpredictable. We leverage whole-genome sequencing of >2600 plants across six continents to investigate the relative roles of colonization history and adaptation during the worldwide invasion of Trifolium repens. Introduced populations contain high levels of genetic variation with independent colonization histories evident on different continents. Five large structural variants on three chromosomes exist as standing genetic variation within the native range, and exhibit strong signatures of parallel climate-associated adaptation across continents. Common gardens in the native and introduced ranges demonstrate that three structural variants exhibit patterns of selection consistent with local adaptation across each range. Our results provide strong evidence that rapid and parallel adaptation during invasion is caused by large-effect structural variants introduced throughout the world. Significance StatementBiological invasions occur over short timescales and introductions are often hypothesized to include limited genetic diversity, making the role of adaptation in invasion success controversial. We demonstrate that the invasion of a human-commensal species, Trifolium repens, likely stems from multiple, diverse introductions with significant evidence of climate-associated adaptation following introduction. The genetic basis of adaptation is most strongly linked to five chromosomal rearrangements that each span hundreds of genes - matching theoretical predictions that large-effect variants are key to the initial stages of adaptation to novel environments. Chromosomal rearrangements have remarkably parallel signatures of adaptation across different introductions despite initial colonization from different areas of Europe. Our study highlights the impact of globalization and rapid adaptation for the invasion success of human commensal species.

evolutionary biology↗

bioRxiv2024

Copy number variation contributes to parallel local adaptation in an invasive plant

Adaptation is a critical determinant of the diversification, persistence, and geographic range limits of species. Yet the genetic basis of adaptation is often unknown and potentially underpinned by a wide range of mutational types - from single nucleotide changes to large-scale alterations of chromosome structure. Copy number variation (CNV) is thought to be an important source of adaptive genetic variation, as indicated by decades of candidate gene studies that point to CNVs underlying rapid adaptation to strong selective pressures. Nevertheless, population- genomic studies of CNVs face unique logistical challenges not encountered by other forms of genetic variation. Consequently, few studies have systematically investigated the contributions of CNVs to adaptation at a genome-wide scale. We present a genome-wide analysis of CNV contributing to the adaptation of an invasive weed, Ambrosia artemisiifolia - the first such study in an invasive pest. CNVs show clear signatures of parallel local adaptation between North American (native) and European (invaded) ranges, implying widespread reuse of CNVs during adaptation to shared heterogeneous patterns of selection. We used a local principal component analysis to genotype CNV regions in whole-genome sequences of samples collected over the last two centuries. We identified 16 large CNV regions of up to 11.85 megabases in length, six of which show signals of rapid evolutionary change, with pronounced frequency shifts between historic and modern populations. Our results provide compelling genome-wide evidence that copy number variation underlies rapid adaptation over contemporary timescales of natural populations. Significance StatementUsing a population-genomic approach, we identified copy number variants - stretches of DNA that can be either present, absent, or in multiple copies - displaying parallel signatures of local adaptation across the native and introduced ranges of the invasive weed Ambrosia artemisiifolia. We further identified 16 large copy number variants, some associated with ecologically important traits including sex allocation and height, that show strong signatures of selection over space, along with dramatic temporal changes over the past several decades. These results highlight the importance of an often-overlooked form of genomic variation in both local adaptation and rapid adaptation of invasive species.

evolutionary biology↗

bioRxiv2023

Haplotype-resolved, chromosome-level assembly of white clover (Trifolium repens L., Fabaceae)

BackgroundWhite clover (Trifolium repens L.; Fabaceae) is an important forage and cover crop in agricultural pastures around the world, and is increasingly used in evolutionary ecology and genetics to understand the genetic basis of adaptation. Historically, improvements in white clover breeding practices and assessments of genetic variation in nature have been hampered by a lack of high-quality genomic resources for this species, owing in part to its high heterozygosity and allotetraploid hybrid origin. FindingsHere, we use PacBio HiFi and chromosome conformation capture (Omni-C) technologies to generate a chromosome-level, haplotype-resolved genome assembly for white clover totaling 998 Mbp (scaffold N50 = 59.3 Mbp) and 1 Gbp (scaffold N50 = 58.6 Mbp) for haplotypes 1 and 2, respectively, with each haplotype arranged into 16 chromosomes (8 per subgenome). We additionally provide a functionally annotated haploid mapping assembly (968 Mbp, scaffold N50 = 59.9 Mbp), which drastically improves on the existing reference assembly in both contiguity and assembly accuracy. We annotated 78,174 protein-coding genes, resulting in protein BUSCO completeness scores of 99.6% and 99.3% against the embryophyta_odb10 and fabales_odb10 lineage datasets, respectively. ConclusionsWe provide two white clover genome assemblies as part of this project: (1) a haplotype-resolved, chromosome-level assembly, and (2) a functionally annotated haploid mapping assembly. These assemblies place white clover among the best sequenced legumes to date, and one of the best assemblies for a plant of recent polyploid origins. This work promises to facilitate ongoing and future work in agricultural and evolutionary genetics in this agronomically and ecologically important species.

genomics↗

bioRxiv2022

Large haploblocks underlie rapid adaptation in an invasive weed

Adaptation is the central feature and leading explanation for the evolutionary diversification of life. Adaptation is also notoriously difficult to study in nature, owing to its complexity and logistically prohibitive timescale. We leverage extensive contemporary and historical collections of Ambrosia artemisiifolia--an aggressively invasive weed and primary cause of pollen-induced hayfever--to track the phenotypic and genetic causes of recent local adaptation across its native and invasive ranges in North America and Europe, respectively. Large haploblocks-- indicative of chromosomal inversions--contain a disproportionate share (26%) of genomic regions conferring parallel adaptation to local climates between ranges, are associated with rapidly adapting traits, and exhibit dramatic frequency shifts over space and time. These results highlight the importance of large-effect standing variants in rapid adaptation, which have been critical to A. artemisiifolias global spread across vast climatic gradients.

evolutionary biology↗

bioRxiv2022

QTL analysis reveals an oligogenic architecture of a rapidly adapting trait during the European invasion of common ragweed

Biological invasions offer a unique opportunity to investigate evolution over contemporary time-scales. Rapid adaptation to local climates during range expansion can be a major determinant of invasion success, yet fundamental questions remain about its genetic basis. This study sought to investigate the genetic basis of climate adaptation in invasive common ragweed (Ambrosia artemisiifolia). Flowering time adaptation is key to this annual species invasion success, so much so that it has evolved repeated latitudinal clines in size and phenology across its native and introduced ranges despite high gene flow among populations. Here, we produced a high-density linkage map (4,493 SNPs) and paired this with phenotypic data from an F2 mapping population (n=336) to identify one major and two minor quantitative trait loci (QTL) underlying flowering time and height differentiation in this species. Within each QTL interval, several candidate flowering time genes were also identified. Notably, the major flowering time QTL detected in this study was found to overlap with a previously identified haploblock (putative inversion). Multiple genetic maps of this region identified evidence of suppressed recombination in specific genotypes, consistent with inversions. These discoveries support the expectation that a concentrated genetic architecture with fewer, larger and more tightly-linked alleles should underlie rapid local adaptation during invasion, particularly when divergently-adapting populations experience high-levels of gene flow.

evolutionary biology↗

bioRxiv2022

Uncovering the hologenomic basis of an extraordinary plant invasion

While invasive species are a key driver of the global biodiversity crisis, the drivers of invasiveness remain debated. To investigate the genomic basis of invasiveness in plants, we use the invasive weed Ambrosia artemisiifolia, introduced to Europe in the late 19th century, resequencing 655 ragweed genomes, including 308 herbarium specimens collected up to 190 years ago. In introduced European populations, we report selection signatures in defense genes and lower prevalence of particular plant pathogens in the invasive range. Together with temporal changes in population structure associated with introgression from closely related Ambrosia species, escape from microbial enemies likely favoured the plants remarkable success as an invasive species. One-Sentence SummaryThe invasive success of European ragweed was facilitated by release from enemy microbes and inter-species hybridization.

genomics↗

bioRxiv2021

Local adaptation and spatiotemporal patterns of genetic diversity revealed by repeated sampling of Caenorhabditis elegans across the Hawaiian Islands

The nematode Caenorhabditis elegans is among the most widely studied organisms, but relatively little is known about its natural ecology. Wild C. elegans have been isolated from both temperate and tropical climates, where they feed on bacteria associated with decomposing plant material. Genetic diversity is low across much of the globe but high in the Hawaiian Islands and across the Pacific Rim. The high genetic diversity found there suggests that: (1) the origin of the species lies in Hawaii or the surrounding Pacific Rim; and (2) the ancestral niche of the species is likely similar to the Hawaiian niche. A recent study of the Hawaiian niche found that genetically distinct groups appeared to correlate with elevation and temperature, but the study had a limited sample size. To better characterize the niche and genetic diversity of C. elegans on the Hawaiian Islands and to explore how genetic diversity might be influenced by local adaptation, we repeatedly sampled nematodes over a three-year period, measured various environmental parameters at each sampling site, and whole-genome sequenced the C. elegans isolates that we identified. We found that the typical Hawaiian C. elegans niche is moderately moist native forests at high elevations (500 to 1500 meters) where temperatures are cool (15 to 20{degrees}C). We measured levels of genetic diversity and differentiation among Hawaiian strains and found evidence of seven genetically distinct groups distributed across the islands. Then, we scanned these genomes for signatures of local adaptation and identified 18 distinct regions that overlap with hyperdivergent regions, which are likely maintained by balancing selection and enriched for genes related to environmental sensing, xenobiotic detoxification, and pathogen resistance. These results provide strong evidence of local adaptation among Hawaiian C. elegans and a possible genetic basis for this adaptation.

ecology↗

bioRxiv2021

Pleiotropy drives repeatability in the genetic basis of adaptation

Observations of genetically repeated evolution (repeatability) in complex organisms are incongruent with the Fisher-Orr model, which implies that repeated use of the same gene should be rare when mutations are pleiotropic (i.e., affect multiple traits). When spatially divergent selection occurs in the presence of migration, mutations of large effect are more strongly favoured, and hence repeatability is more likely, but it is unclear whether this observation is limited by pleiotropy. Here, we explore this question using individual-based simulations of a two-patch model incorporating multiple quantitative traits governed by mutations with pleiotropic effects. We explore the relationship between fitness trade-offs and repeatability by varying the alignment between mutation effect and spatial variation in trait optima. While repeatability decreases with increasing trait dimensionality, trade-offs in mutation effects on traits do not strongly limit the contribution of a locus of large effect to repeated adaptation, particularly under increased migration. These results suggest that repeatability will be more pronounced for local rather than global adaptation. Whereas pleiotropy limits repeatability in a single-population model, when there is local adaptation with gene flow, repeatability can occur if some loci are able to produce alleles of large effect, even when there are pleiotropic trade-offs. Article summaryClassical evolutionary theory predicts that genetically repeated evolution should be vanishingly rare in organisms where mutations affect multiple traits. In this article, we use simulations to study such pleiotropic mutations, and explore their effects on local adaptation in two patches under divergent selection. We find that migration between patches increases the likelihood of repeated evolution, even when there are fitness trade-offs imposed by pleiotropy.

genetics↗

bioRxiv2020

Identifying candidate detoxification genes in the ecdysteroid kinase-like (EcKL) and cytochrome P450 gene families in Drosophila melanogaster by integrating evolutionary and transcriptomic data

The capacity to detoxify toxic compounds is essential for adaptation to the ecological niches of many organisms, especially insects. However, detoxification in insects is often viewed through the lens of mammalian detoxification research, even though the organ and enzyme systems involved have diverged for over half a billion years. Phosphorylation is a non-canonical phase II detoxification reaction that, among animals, occurs near exclusively in insects, but the enzymes responsible have never been cloned or otherwise identified. We propose the hypothesis that members of the arthropod-specific ecdysteroid kinase-like (EcKL) gene family encode detoxicative kinases. To test this hypothesis, we annotated the EcKL gene family in 12 species of Drosophila and explored their evolution within the genus. Many ancestral EcKL clades are evolutionarily unstable and have experienced repeated gene gain and loss events, while others are conserved as single copy orthologs. Leveraging multiple published gene expression datasets from D. melanogaster, and using the cytochrome P450s--a canonical detoxification family--as a test case, we demonstrate relationships between xenobiotic induction, detoxification tissue-enriched expression and evolutionary instability in the EcKLs and the P450s. We also found previously unreported genomic and transcriptomic variation in a number of EcKLs and P450s associated with toxic stress phenotypes using a targeted phenome-wide association study (PheWAS) approach. Lastly, we devised a systematic method for identifying candidate detoxification genes in large gene families that is concordant with experimentally determined functions of P450 genes in D. melanogaster. Applying this method to the EcKLs suggested a significant proportion of these genes play roles in detoxification, and that the EcKLs may constitute a detoxification gene family in insects. Additionally, we estimate that between 11-16 uncharacterised D. melanogaster P450s are strong detoxification candidates. HighlightsO_LIThe poorly characterised ecdysteroid kinase-like (EcKL) gene family is hypothesised to encode enzymes responsible for detoxification by phosphorylation in insects. C_LIO_LIAn integrative detoxification score method accurately categorises the known functions of a canonical detoxification family, the cytochrome P450s, and suggests many EcKLs are also involved in detoxification. C_LIO_LIA targeted phenome-wide association study finds novel associations between EcKL/P450 variation and a number of toxic stress phenotypes, such as two unlinked EcKL paralogs that are both associated with developmental methylmercury resistance. C_LI

genetics↗

bioRxiv2019

The spread of resistance to imidacloprid is restricted by thermotolerance in natural populations of Drosophila melanogaster

Imidacloprid, the worlds most utilised insecticide1, has raised considerable controversy due to its harmful effects on non-pest species2-6 and there is increasing evidence showing that insecticides have become the primary selective force in many insect species7-14. The genetic response to insecticides is heterogeneous across population and environment15-17, leading to more complex patterns of genetic variation than previously thought. This motivated the investigation of imidacloprid resistance at different temperatures in natural populations of Drosophila melanogaster originating from four climate extremes replicated across two continents. Population and quantitative genomic analysis, supported by functional tests, demonstrated a polygenic basis to resistance and a major trade-off with thermotolerance. Reduced genetic differentiation at resistance-associated loci indicate enhanced gene flow at these loci. Resistance alleles showed stronger evidence of positive selection in temperate populations compared to tropical populations. Polygenic architecture and ecological factors should be considered when developing sustainable management strategies for both pest and beneficial insects.

evolutionary biology↗

bioRxiv2018

Cis and trans-acting variants contribute to survivorship in a naive Drosophila melanogaster population exposed to ryanoid insecticides

Insecticide resistance is a paradigm of microevolution and insecticides are responsible for the strongest cases of recent selection in the genome of Drosophila melanogaster. Here we use a naive population and a novel insecticide class to examine the ab initio genetic architecture of a potential selective response. Genome wide association studies of chlorantraniliprole susceptibility reveal variation in a gene of major effect, Stretchin Myosin light chain kinase (Strn-Mlck), which we validate with linkage mapping and transgenic manipulation of gene expression. We propose that allelic variation in Strn-Mlck alters sensitivity to the calcium depletion attributable to chlorantraniliproles mode of action. Genome-wide association studies also reveal a network of genes involved in neuromuscular biology. In contrast, phenotype to transcriptome associations identify differences in constitutive levels of multiple transcripts regulated by cnc, the homologue of mammalian Nrf2. This suggests that genetic variation acts in trans to regulate multiple metabolic enzymes in this pathway. The most outstanding association is with the transcription level of Cyp12d1 which is also affected in cis by copy number variation. Transgenic overexpression of Cyp12d1 reduces susceptibility to both chlorantraniliprole and the closely related insecticide cyantraniliprole. This systems genetics study reveals multiple allelic variants segregating at intermediate frequency in a population that is completely naive to this new insecticide chemistry and it adumbrates a selective response among natural populations to these chemicals.\n\nSignificanceAround the world insecticides are being deregistered and banned, as their environmental costs are deemed too great or their efficacy against pest insects is reduced through the evolution of insecticide resistance. With the introduction of replacement insecticides comes the responsibility to assess the way new insecticides perturb various levels of biological systems; from insect physiology to ecosystems. We used a systems genetics approach to identify genetic variants affecting survivorship of Drosophila melanogaster exposed to chlorantraniliprole. The study population was completely naive to this insecticide chemistry and yet we find associations with variants in neuromuscular genes and co-regulated detoxification genes. We predict that these variants will increase in populations of this sentinel species as these insecticides are applied in the environment.

genetics↗

bioRxiv2017

Multiple P450s And Variation In Neuronal Genes Underpins The Response To The Insecticide Imidacloprid In A Population Of Drosophila melanogaster

Insecticide resistance is an economically important example of evolution in response to intense selection pressure. Here, the genetics of resistance to the neonicotinoid insecticide imidacloprid is explored using the Drosophila Genetic Reference Panel, a collection of inbred Drosophila melanogaster genotypes derived from a single population in North Carolina. Imidacloprid resistance varied substantially among genotypes, and more resistant genotypes tended to show increased capacity to metabolize and excrete imidacloprid. Variation in resistance level was then associated with genomic and transcriptomic variation, implicating several candidate genes involved in central nervous system function and the cytochrome P450s Cyp6g1 and Cyp6g2. CRISPR-Cas9 mediated removal of Cyp6g1 suggested that it contributed to imidacloprid resistance only in backgrounds where it was already highly expressed. Cyp6g2, previously implicated in juvenile hormone synthesis via expression in the ring gland, was shown to be expressed in metabolically relevant tissues of resistant genotypes. Cyp6g2 overexpression was shown to both metabolize imidacloprid and confer resistance. These data collectively suggest that imidacloprid resistance is influenced by a variety of previously known and unknown genetic factors.

genetics↗