Biology subjects

Pool, J. E.

Publications and source records attributed to Pool, J. E..

18 recordsLinked to original sources

bioRxiv2026

Replication-Enhanced Detection of Quantitative Traits Evolving Adaptively (REDQuanTEA): an improved statistical framework to detect locally adaptive traits

Comparing quantitative trait differentiation (Q_ST) with neutral genetic differentiation (F_ST) is an established approach to detect locally adaptive trait differentiation, but empirical applications can lose power when Q_ST is deflated by extrinsic trait variance (i.e. from non-genetic sources such as environmental effects and measurement error). We present REDQuanTEA (Replication-Enhanced Detection of Quantitative Traits Evolving Adaptively), a ready-to-use computational workflow that leverages biologically replicated data to disentangle genetic and extrinsic trait variance, while using Approximate Bayesian Computation (ABC) to refine estimates of Q_ST. Instead of comparing all traits with a single F_ST-based cutoff, REDQuanTEA generates trait-specific dynamic outlier Q_ST thresholds from neutral F_ST distributions based on matching experimental properties and the trait-specific level of extrinsic variance. In addition to identification of candidate adaptive traits from empirical data, the package enables simulation-guided assessment of experimental design and statistical analysis options. Using a demographic benchmark based on Drosophila melanogaster, REDQuanTEA outperformed estimators based on analysis of variance (ANOVA), particularly when extrinsic variance was moderate to high, while controlling false positive rates (FPRs). Assuming fixed experimental effort, two replicates with more independent genotypes often outperformed three replicate designs when extrinsic variance was low, and performed similarly as extrinsic variance increased. REDQuanTEA therefore provides a framework for optimizing experimental plans and detecting adaptively differentiated traits with improved power.

evolutionary biology↗

bioRxiv2025

Gene flow weakens genomic clines while selection maintains adaptive loci: two decades of evolution in Drosophila melanogaster natural populations

Spatial genetic clines suggest local adaptation, but whether they persist or erode over evolutionary time remains largely unknown. Here, we use a unique genomic time series collected over several decades to quantify how gene flow and selection jointly shape spatial genomic structure. We analyzed pooled whole-genome sequencing from 16 natural populations of Drosophila melanogaster sampled along the North American east coast between 1997 and 2023, spanning hundreds of generations. We find pronounced homogenization of populations over time, accompanied by a genome-wide loss of clinal variants. Polymorphisms that remained clinal were less steep on chromosome 3R, reflecting declines in the frequency and clinality of major chromosomal inversions. Genomic context modulates this process: clinal SNPs are preferentially lost in regions of high recombination, whereas remaining clines are increasingly concentrated in coding and splice-associated sites. Despite widespread erosion of spatial structure, we detect signatures of selection shared across space at detoxification loci, including cytochrome P450 genes linked to insecticide resistance. Together, our results show widespread homogenization of neutral spatial variation consistent with gene flow, while spatially varying selection has preserved a subset of functionally important loci.

evolutionary biology↗

bioRxiv2024

The Precision and Power of Population Branch Statistics in Identifying the Genomic Signatures of Local Adaptation

Population branch statistics, which estimate the branch lengths of focal populations with respect to two outgroups, have been used as an alternative to FST-based genome-wide scans for identifying loci associated with local selective sweeps. In addition to the original population branch statistic (PBS), there are subsequently proposed branch rescalings: normalized population branch statistic (PBSn1), which adjusts focal branch length with respect to outgroup branch lengths at the same locus, and population branch excess (PBE), which also incorporates median branch lengths at other loci. PBSn1 and PBE have been proposed to be less sensitive to allele frequency divergence generated by background selection or geographically ubiquitous positive selection rather than local selective sweeps. However, the accuracy and statistical power of branch statistics have not been systematically assessed. To do so, we simulate genomes in representative large and small populations with varying proportions of sites evolving under genetic drift or background selection (approximated using variable Ne), local selective sweeps, and geographically parallel selective sweeps. We then assess the probability that local selective sweep loci are correctly identified as outliers by FST and by each of the branch statistics. We find that branch statistics consistently outperform FST at identifying local sweeps. When background selection and/or parallel sweeps are introduced, PBSn1 and especially PBE correctly identify local sweeps among their top outliers at a higher frequency than PBS. These results validate the greater specificity of rescaled branch statistics such as PBE to detect population-specific positive selection, supporting their use in genomic studies focused on local adaptation. Significance StatementPopulation branch statistics are widely used in genome-wide scans to identify loci associated with local adaptation. This study finds that branch statistics are more accurate than FST at identifying local selective sweeps under a wide range of demographic parameters and models of evolution. It also demonstrates that certain branch statistics have improved ability to distinguish local adaptation from other models of natural selection.

evolutionary biology↗

bioRxiv2024

Recombinant inbred line panels inform the genetic architecture and interactions of adaptive traits in Drosophila melanogaster

The distribution of allelic effects on traits, along with their gene-by-gene and gene-by-environment interactions, contributes to the phenotypes available for selection and the trajectories of adaptive variants. Nonetheless, uncertainty persists regarding the effect sizes underlying adaptations and the importance of genetic interactions. Herein, we aimed to investigate the genetic architecture and the epistatic and environmental interactions involving loci that contribute to multiple adaptive traits using two new panels of Drosophila melanogaster recombinant inbred lines (RILs). To better fit our data, we re-implemented functions from R/qtl (Broman et al. 2003) using additive genetic models. We found 14 quantitative trait loci (QTL) underlying melanism, wing size, song pattern, and ethanol resistance. By combining our mapping results with population genetic statistics, we identified potential new genes related to these traits. None of the detected QTLs showed clear evidence of epistasis, and our power analysis indicated that we should have seen at least one significant interaction if sign epistasis or strong positive epistasis played a pervasive role in trait evolution. In contrast, we did find roles for gene-by-environment interactions involving pigmentation traits. Overall, our data suggest that the genetic architecture of adaptive traits often involves alleles of detectable effect, that strong epistasis does not always play a role in adaptation, and that environmental interactions can modulate the effect size of adaptive alleles.

evolutionary biology↗

bioRxiv2024

Courtship song differs between African and European populations of Drosophila melanogaster and involves a strong effect locus

The courtship song of Drosophila melanogaster has long served as an excellent model system for studies of animal communication and differences in courtship song have been demonstrated among populations and between species. Here, we report that flies of African and European origin, which diverged approximately 13,000 years ago, show significant genetic differentiation in the use of slow versus fast pulse song. Using a combination of quantitative trait mapping and population genetic analysis we detected a single strong QTL underlying this trait and we identified candidate genes that may contribute to the evolution of this trait. Song trait variation between parental strains of our recombinant inbred panel enabled detection of genomic intervals associated with six additional song traits, some of which include known courtship-related genes. These findings improve the prospects for further genetic insights into the evolution of reproductive behavior and the biology underlying courtship song.

evolutionary biology↗

bioRxiv2024

Polygenic architecture of adaptation to a high-altitude environment for Drosophila melanogaster wing shape and size.

As is typical of small insects, populations of Drosophila melanogaster adapted to high altitude environments evolved increased body size, disproportionality large wings, and differing wing shape compared to low-altitude ancestors. In one instance the colonization of high-altitude environments in Ethiopia is recent (2000-3000 years ago), and is a useful system to study alleles contributing to adaptive divergence. Unlike predictions derived from formulations Fisher-Kimura-Orr geometric model based on de novo mutations concurrent with selection, recent models predict segregating alleles in a population are more likely to contribute to adaptation on short time scales, particularly when populations are large and genetically diverse, like D. melanogaster. Strains derived from lowland ([~]500m above sea level - ASL) and highland ([~]3000m ASL) populations were used to generate F20 advanced-intercrosses. From each cross, phenotypically extreme individuals for size and shape were pool-sequenced, and genetic differentiation among pools of individuals demonstrated a polygenic architecture of divergence for size and shape. We identified one QTL of large effect, contributing to adaptive divergence in shape. This QTL is not observed in all crosses, pointing to the importance of examining independent genetic backgrounds when mapping alleles contributing to adaptation. Despite the intrinsic links between shape and size, we find a unique genetic basis of adaptation for these traits. This work demonstrates that many alleles, throughout the genome, rather than single, large effect alleles, contribute to adaption for Drosophila wing shape and size, adding to the growing body of evidence for polygenic adaptation.

evolutionary biology↗

bioRxiv2023

Inversions Can Accumulate Balanced Sexual Antagonism: Evidence from Simulations and Drosophila Experiments

Chromosomal inversion polymorphisms can be common, but the causes of their persistence are often unclear. We propose a model for the maintenance of inversion polymorphism, which requires that some variants contribute antagonistically to two phenotypes, one of which has negative frequency-dependent fitness. These conditions yield a form of frequency-dependent disruptive selection, favoring two predominant haplotypes segregating alleles that favor opposing antagonistic phenotypes. An inversion associated with one haplotype can reduce the fitness load incurred by generating recombinant offspring, reinforcing its linkage to the haplotype and enabling both haplotypes to accumulate more antagonistic variants than expected otherwise. We develop and apply a forward simulator to examine these dynamics under a tradeoff between survival and male display. These simulations indeed generate inversion-associated haplotypes with opposing sex-specific fitness effects. Antagonism strengthens with time, and can ultimately yield karyotypes at surprisingly predictable frequencies, with striking genotype frequency differences between sexes and between developmental stages. To test whether this model may contribute to well-studied yet enigmatic inversion polymorphisms in Drosophila melanogaster, we track inversion frequencies in laboratory crosses to test whether they influence male reproductive success or survival. We find that two of the four tested inversions show significant evidence for the tradeoff examined, with In(3R)K favoring survival and In(3L)Ok favoring male reproduction. In line with the apparent sex-specific fitness effects implied for both of those inversions, In(3L)Ok was also found to be less costly to the viability and/or longevity of males than females, whereas In(3R)K was more beneficial to female survival. Based on this work, we expect that balancing selection on antagonistically pleiotropic traits may provide a significant and underappreciated contribution to the maintenance of natural inversion polymorphism.

evolutionary biology↗

bioRxiv2023

Genomic Diversity Illuminates the Species History and Environmental Adaptation of Drosophila suzukii

Biological invasions carry substantial practical and scientific importance, and represent natural evolutionary experiments on contemporary timescales. Here, we investigated genomic diversity and environmental adaptation of the crop pest Drosophila suzukii using whole-genome sequencing data and environmental metadata for 29 population samples from its native and invasive range. Through a multifaceted analysis of this population genomic data, we increase our understanding of the D. suzukii genome, its diversity and its evolution, and we identify an appropriate genotype-environment association pipeline for our data set. Using this approach, we detect genetic signals of local adaptation associated with nine distinct environmental factors related to altitude, wind speed, precipitation, temperature, and human land use. We uncover unique functional signatures for each environmental variable, such as a prevalence of cuticular genes associated with annual precipitation. We also infer biological commonalities in the adaptation to diverse selective pressures, particularly in terms of the apparent contribution of nervous system evolution to enriched processes (ranging from neuron development to circadian behavior) and to top genes associated with all nine environmental variables. Our findings therefore depict a finer-scale adaptive landscape underlying the rapid invasion success of this agronomically important species.

evolutionary biology↗

bioRxiv2023

Genomes From 25 Historical Drosophila melanogaster Specimens Illuminate Adaptive and Demographic Changes Across More Than 200 Years of Evolution

The ability to perform genomic sequencing on long-dead organisms is opening new frontiers in evolutionary research. These opportunities are especially profound in the case of museum collections, from which countless documented specimens may now be suitable for genomic analysis. Here, we report 25 newly sequenced genomes from museum specimens of the model organism Drosophila melanogaster, including the oldest extant specimens of this species. By comparing historical samples ranging from the early 1800s to 1933 against modern day genomes, we document evolution across thousands of generations, including time periods that encompass the species initial occupation of northern Europe and an era of rapidly increasing human activity. At the genome-wide level, we find that historical flies from the same time and place show much greater evidence for relatedness than flies from modern collections, and some show evidence of inbreeding as well, potentially reflecting either much smaller local population sizes in the past or else the specific circumstances of the collections. We also find that the Lund, Sweden population underwent local genetic differentiation during the early 1800s to 1933 interval (potentially due to accelerated drift) but then became more similar to other European populations thereafter (potentially due to increased migration). Within each time period, our temporal sampling allows us to document compelling candidates for recent natural selection. In some cases, we gain insights regarding previously implicated selection candidates, such as ChKov1, for which our inferred timing of selection favors the hypothesis of antiviral resistance over insecticide resistance. Other candidates are novel, such as the circadian-related gene Ahcy, which yields a selection signal that rivals that of the DDT resistance gene Cyp6g1. These insights deepen our understanding of recent evolution in a model system, and highlight the potential of future museomic studies.

evolutionary biology↗

bioRxiv2022

Hybrid Breakdown in Male Reproduction Between Recently-Diverged Drosophila melanogaster Populations Has a Complex and Variable Genetic Architecture

Populations no longer experiencing a sufficient rate of gene flow will accumulate genetic differences over time. One potential consequence of divergence between natural populations is hybrid breakdown, which can occur during secondary contact when untested allelic combinations in hybrids beyond the F1 generation are maladaptive and restrict gene flow. Hybrid breakdown is an important process in the development and maintenance of species boundaries, and has largely been studied between populations that are completely or nearly completely isolated. Here, we leverage the recent worldwide expansion of Drosophila melanogaster to investigate signatures of hybrid breakdown between populations that diverged within approximately the last 13,000 years. We did not find clear evidence for hybrid breakdown in viability or female reproductive performance. In contrast, we found that many but not all between-population crosses yielded an elevated fraction of second generation male offspring that were unable to reproduce. The frequency of non-reproducing F2 males varied among different crosses involving the same southern African and European populations, as did the qualitative effect of cross direction, implying a genetically variable basis of hybrid breakdown and a role for uniparentally inherited factors. The levels of male reproductive failure observed in F2 hybrids were not recapitulated in backcrossed individuals, suggesting the existence of incompatibilities with at least three partners. These results suggest that some of the very first steps toward reproductive isolation may involve incompatibilities with complex and variable genetic architectures, and they support the prediction that hybrid breakdown affects the heterogametic sex first. Collectively, our findings on polymorphic incompatibilities within D. melanogaster emphasize this systems potential for future studies on the genetic and organismal basis of early-stage reproductive isolation. IMPACT SUMMARYThe biological diversity that exists around the world is an emergent property of the generation of forms, which are commonly grouped into units we call species. The rate at which new species form can be influenced by the evolution of reproductive isolation, the inability of groups to interbreed. When reproductive isolation is studied in its nascent stages, researchers can gain critical insights into the genetic architectures and evolutionary forces underlying the earliest steps toward speciation. One process that may contribute to early-stage reproductive isolation is hybrid breakdown, when genetic incompatibilities in the offspring of hybrid individuals reduce their fitness. Here, we illuminate a complex pattern of hybrid breakdown among natural populations of Drosophila flies that diverged within the past 13,000 years. We find signals of hybrid breakdown involving male reproduction, between some but not all population pairs, whereas we find no clear evidence for hybrid breakdown impacting female reproduction or developmental survival. These findings are in agreement with Haldanes Rule, which posits that hybrid incompatibilities are more likely to affect the sex that carries distinct sex chromosomes (here, XY males). From certain crosses between African and European fly strains, we find strongly elevated rates of reproductive failure in second generation hybrid males, but outcomes vary dramatically depending on the individual strains crossed. We also provide evidence of incompatibilities underlying male reproductive failure that involve three or more genes, including uniparental factors such as the Y chromosome or mitochondrial genome. Our results highlight a complex and variable basis of hybrid breakdown during the earliest stages of reproductive isolation, in contrast to commonly envisioned scenarios that focus on two-locus incompatibilities caused by fixed genetic differences between groups. These findings also suggest that recently diverged populations of D. melanogaster provide notable opportunities for future studies of the genetic basis of early-stage reproductive isolation.

evolutionary biology↗

bioRxiv2022

Gene regulatory evolution in cold-adapted fly populations neutralizes plasticity and may undermine genetic canalization

The relationships between adaptive evolution, phenotypic plasticity, and canalization remain incompletely understood. Theoretical and empirical studies have made conflicting arguments on whether adaptive evolution may enhance or oppose the plastic response. Gene regulatory traits offer excellent potential to study the relationship between plasticity and adaptation, and they can now be studied at the transcriptomic level. Here we take advantage of three closely-related pairs of natural populations of Drosophila melanogaster from contrasting thermal environments that reflect three separate instances of cold tolerance evolution. We measure the transcriptome-wide plasticity in gene expression levels and alternative splicing (intron usage) between warm and cold laboratory environments. We find that suspected adaptive changes in both gene expression and alternative splicing tend to neutralize the ancestral plastic response. Further, we investigate the hypothesis that adaptive evolution can lead to decanalization of selected gene regulatory traits. We find strong evidence that suspected adaptive gene expression (but not splicing) changes in cold-adapted populations are more vulnerable to the genetic perturbation of inbreeding than putatively neutral changes. We find some evidence that these patterns may reflect a loss of genetic canalization accompanying adaptation, although other processes including hitchhiking recessive deleterious variants may contribute as well. Our findings augment our understanding of genetic and environmental effects on gene regulation in the context of adaptive evolution. Significance StatementIt is unclear whether adaptive evolution is concordant or discordant with regulatory plasticity, especially for splicing plasticity which is rarely studied. Here we analyzed RNA-seq data from three pairs of natural fly populations that represent separate adaptive evolution to cold climate. We found that adaptive evolution is generally discordant with the ancestral plasticity between cold and warm temperatures for gene expression abundance and splicing. We also investigate the hypothesis that adaptation leads to decanalization of the selected traits. By comparing the expression variance between inbred and outbred samples, we found evidence that adaptation may lead to genetic decanalization for expression abundance but not for splicing. Our study reveals the relationship between adaptation, plasticity and canalization in three instances in nature.

evolutionary biology↗

bioRxiv2022

SNP-level FST outperforms window statistics for detecting soft sweeps in local adaptation

Local adaptation can lead to elevated genetic differentiation at the targeted genetic variant and nearby sites. Selective sweeps come in different forms, and depending on the initial and final frequencies of a favored variant, very different patterns of genetic variation may be produced. If local selection favors an existing variant that had already recombined onto multiple genetic backgrounds, then the width of elevated genetic differentiation (high FST) may be too narrow to detect using a typical windowed genome scan, even if the targeted variant becomes highly differentiated. We therefore used a simulation approach to investigate the power of SNP-level FST (specifically, the maximum SNP FST value within a window) to detect diverse scenarios of local adaptation, and compared it against whole-window FST and the Comparative Haplotype Identity statistic. We found that SNP FST had superior power to detect complete or mostly complete soft sweeps, but lesser power than window-wide statistics to detect partial hard sweeps. To investigate the relative enrichment and nature of SNP FST outliers from real data, we applied the two FST statistics to a panel of Drosophila melanogaster populations. We found that SNP FST had a genome-wide enrichment of outliers compared to demographic expectations, and though it yielded a lesser enrichment than window FST, it detected mostly unique outlier genes and functional categories. Our results suggest that SNP FST is highly complementary to typical window-based approaches for detecting local adaptation, and merits inclusion in future genome scans and methodologies. Significance statementStudies that use genetic variation to search for genes evolving under population-specific natural selection tend to analyze data at the level of genomic windows that may each contain hundreds of variable sites. However, some models of natural selection (e.g. favoring an existing genetic variant) may result in genetic signals of local adaptation that are too narrow to be detected by such approaches. Here we use both simulations and empirical data analysis to show that searching for a site-specific signal of elevated genetic differentiation can find instances of local adaptation that other approaches miss, and therefore the integration of this signal into future studies may significantly improve our understanding of adaptive evolution and its genetic targets.

evolutionary biology↗

bioRxiv2021

A Population Genomic Assessment of Three Decades of Evolution in a Natural Drosophila Population

Population genetics seeks to illuminate the forces shaping genetic variation, often based on a single snapshot of genomic variation. However, utilizing multiple sampling times to study changes in allele frequencies can help clarify the relative roles of neutral and non-neutral forces on short time scales. This study compares whole-genome sequence variation of recently collected natural population samples of Drosophila melanogaster against a collection made approximately 35 years prior from the same locality - encompassing roughly 500 generations of evolution. The allele frequency changes between these time points would suggest a relatively small local effective population size on the order of 10,000, significantly smaller than the global effective population size of the species. Some loci display stronger allele frequency changes than would be expected anywhere in the genome under neutrality - most notably the tandem paralogs Cyp6a17 and Cyp6a23, which are impacted by structural variation associated with resistance to pyrethroid insecticides. We find a genome-wide excess of outliers for high genetic differentiation between old and new samples, but a larger number of adaptation targets may have affected SNP-level differentiation versus window differentiation. We also find evidence for strengthening latitudinal allele frequency clines: northern-associated alleles have increased in frequency by an average of nearly 2.5% at SNPs previously identified as clinal outliers, but no such pattern is observed at random SNPs. This project underscores the scientific potential of using multiple sampling time points to investigate how evolution operates in natural populations, by quantifying how genetic variation has changed over ecologically relevant timescales.

evolutionary biology↗

bioRxiv2021

Interactions between natural selection and recombination shape the genomic landscape of introgression

Hybridization between lineages that have not reached complete reproductive isolation appears more and more like a common phenomenon. Indeed, speciation genomics studies have now extensively shown that many species genomes have hybrid ancestry. However, genomic patterns of introgression are often heterogeneous across the genome. In many organisms, a positive correlation between introgression levels and recombination rate has been observed. It is usually explained by the purging of deleterious introgressed material due to incompatibilities. However, the opposite relationship was observed in a North American population of Drosophila melanogaster with admixed European and African ancestry. In order to explore how directional and epistatic selection can impact the relationship between introgression and recombination, we performed forward simulations of whole D. melanogaster genomes reflecting the North American populations history. Our results revealed that the simplest models of positive selection often yield negative correlations between introgression and recombination such as the one observed in D. melanogaster. We also confirmed that incompatibilities tend to produce positive introgression-recombination correlations. And yet, we identify parameter space under each model where the predicted correlation is reversed. These findings deepen our understanding of the evolutionary forces that may shape patterns of ancestry across genomes, and they strengthen the foundation for future studies aimed at estimating genome-wide parameters of selection in admixed populations.

evolutionary biology↗

bioRxiv2021

The Evolution of Larger Size in High Altitude Drosophila melanogaster has a Polymorphic Genetic Architecture

Important uncertainties persist regarding the genetic architecture of adaptive trait evolution in natural populations, including the number of genetic variants involved, whether they are drawn from standing genetic variation, and whether directional selection drives them to complete fixation. Here, we take advantage of a unique natural population of Drosophila melanogaster from the Ethiopian highlands, which has evolved larger body size than any other known population of this species. We apply a bulk segregant quantitative trait locus (QTL) mapping approach to four unique crosses between highland Ethiopian and lowland Zambian populations for both thorax length and wing length. Results indicated a persistently variable genetic basis for these evolved traits (with largely distinct sets of QTLs for each cross), and at least a moderately polygenic architecture with relatively strong effects present. We complemented these mapping experiments with population genetic analyses of QTL regions and gene ontology enrichment analysis, generating strong hypotheses for specific genes and functional processes that may have contributed to these adaptive trait changes. Finally, we find that the genetic architectures our QTL mapping results for size traits mirror those from similar experiments on other recently-evolved traits in this species. Collectively, these studies suggest a recurring pattern of polygenic adaptation in this species, in which causative variants do not approach fixation and moderately strong effect loci are present.

evolutionary biology↗

bioRxiv2019

Evolution of Gene Expression and Splicing in Parallel Cold-Adapted Fly Populations

Changes in gene regulation at multiple levels may comprise an important share of the molecular changes underlying adaptive evolution in nature. However, few studies have assayed within- and between-population variation in gene regulatory traits at a transcriptomic scale, and therefore inferences about the characteristics of adaptive regulatory changes have been elusive. Here, we assess quantitative trait differentiation in gene expression levels and alternative splicing (intron usage) between three closely-related pairs of natural populations of Drosophila melanogaster from contrasting thermal environments that reflect three separate instances of cold tolerance evolution. The cold-adapted populations were known to show population genetic evidence for parallel evolution at the SNP level, and here we find evidence for parallel expression evolution between them, with stronger parallelism at larval and adult stages than for pupae. We also implement a flexible method to estimate cis- versus trans-encoded contributions to expression or splicing differences at the adult stage. The apparent contributions of cis- versus trans-regulation to adaptive evolution vary substantially among population pairs. While two of three population pairs show a greater enrichment of cis-regulatory differences among adaptation candidates, trans-regulatory differences are more likely to be implicated in parallel expression changes between population pairs. Genes with significant cis-effects are enriched for signals of elevated genetic differentiation between cold- and warm-adapted populations, suggesting that they are potential targets of local adaptation. These findings expand our knowledge of adaptive gene regulatory evolution and our ability to make inferences about this important and widespread process.

evolutionary biology↗

bioRxiv2018

Discovery of Drosophila melanogaster from Wild African Environments and Genomic Insights into Species History

A long-standing enigma concerns the geographic and ecological origins of the intensively studied vinegar fly, Drosophila melanogaster, a globally widespread species [1] which \"has invariably appeared to be a strict human commensal\" [2]. In spite of its sub-Saharan origins, this species has never been reported from undisturbed wilderness environments that might reflect its pre-commensal niche [3]. Here, we document the collection of 288 D. melanogaster individuals from African wilderness areas in Zambia, Zimbabwe, and Namibia. After sequencing the genomes of 17 flies collected from Kafue National Park, Zambia, we found reduced genetic diversity relative to town populations, elevated chromosomal inversion frequencies, and strong differences at specific genes including known insecticide targets. Combining these new genomes with prior data enabled us to gain novel insights into the history of this species geographic expansion. Our demographic estimates indicated that an expansion from southern Africa began approximately 10,000 years ago, with a Saharan crossing soon after, but expansion from the Middle East into Europe did not begin until roughly 1,400 years ago. This improved model of demographic history will provide a critical resource for future evolutionary and genomic studies of this key model organism. Our results add historical context to the species human association, and the opportunity to study wilderness populations opens the door for future studies on the biological basis of its adaptation to human environments.

genomics↗

bioRxiv2017

Impacts of Recurrent Hitchhiking on Divergence and Demographic Inference in Drosophila

In species with large population sizes such as Drosophila, natural selection may have substantial effects on genetic diversity and divergence. However, the implications of this widespread nonneutrality for standard population genetic assumptions and practices remain poorly resolved. Here, we assess the consequences of recurrent hitchhiking (RHH), in which selective sweeps occur at a given rate randomly across the genome. We use forward simulations to examine two published RHH models for D. melanogaster, reflecting relatively common/weak and rare/strong selection. We find that unlike the rare/strong RHH model, the common/weak model entails a slight degree of Hill-Robertson interference in high recombination regions. We also find that the common/weak RHH model is more consistent with our genome-wide estimate of the proportion of substitutions fixed by natural selection between D. melanogaster and D. simulans (19%). Finally, we examine how these models of RHH might bias demographic inference. We find that these RHH scenarios can bias demographic parameter estimation, but such biases are weaker for parameters relating recently-diverged populations, and for the common/weak RHH model in general. Thus, even for species with important genome-wide impacts of selective sweeps, neutralist demographic inference can have some utility in understanding the histories of recently-diverged populations.

evolutionary biology↗