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Abstract Prezygotic isolation is often stronger between sympatric as opposed to allopatric taxa, but the underlying cause can be difficult to infer from comparative studies alone. Experimental evolution, where evolutionary responses to treatments manipulating the presence/absence of heterospecific individuals are tracked, can provide a powerful complementary approach. We used experimental evolution to investigate a naturally occurring pattern of reproductive character displacement in the mushroom-feeding fly, Drosophila subquinaria. In nature, female D. subquinaria from populations sympatric with the closely related Drosophila recens discriminate more strongly against heterospecific males than do females from allopatric populations. Starting with 16 replicate allopatric populations of D. subquinaria, we manipulated the presence/absence of D. recens during mating (experimental sympatry vs. control) and, when present, we allowed hybrids to live or kill them each generation. Across 12 generations, heterospecific offspring production from no-choice mating trials between D. subquinaria females and D. recens males declined in both experimental sympatry treatments relative to the control, suggesting increased sexual isolation. Male cuticular hydrocarbon profiles also evolved, but only in the hybrids killed treatment. Our results strongly imply that the existing reproductive character displacement in wild D. subquinaria populations was an evolutionary response to selection arising from secondary contact with D. recens. 

Abstract Understanding how and when key novel adaptations evolved is a central goal of evolutionary biology. Within theimmigrans‐tripunctataradiation ofDrosophila, many mushroom‐feeding species are tolerant of host toxins, such as cyclopeptides, that are lethal to nearly all other eukaryotes. In this study, we used phylogenetic and functional approaches to investigate the evolution of cyclopeptide tolerance in theimmigrans‐tripunctataradiation ofDrosophila. First, we inferred the evolutionary relationships among 48 species in this radiation using 978 single copy orthologs. Our results resolved previous incongruities within species groups across the phylogeny. Second, we expanded on previous studies of toxin tolerance by assaying 16 of these species for tolerance to α‐amanitin and found that six of them could develop on diet with toxin. Finally, we asked how α‐amanitin tolerance might have evolved across theimmigrans‐tripunctataradiation, and inferred that toxin tolerance was ancestral in mushroom‐feedingDrosophilaand subsequently lost multiple times. Our findings expand our understanding of toxin tolerance across theimmigrans‐tripunctataradiation and emphasize the uniqueness of toxin tolerance in this adaptive radiation and the complexity of biochemical adaptations. 

Abstract Inferring evolutionary relationships among recently diverged lineages is necessary to understand how isolating barriers produce independent lineages. Here, we investigate the phylogenetic relationships between three incompletely isolated and closely related mushroom‐feedingDrosophilaspecies. These species form theDrosophila subquinariaspecies complex and consist of one Eurasian species (D. transversa) and two widespread North American species (D. subquinariaandD. recens) that are sympatric in central Canada. Although patterns of pre‐ and post‐mating isolation among these species are well characterized, previous work on their phylogenetic relationships is limited and conflicting. In this study, we generated a multi‐locus data set of 29 loci from across the genome sequenced in a population sample from each species, and then, we inferred species relationships and patterns of introgression. We find strong statistical support thatD. subquinariais paraphyletic, showing that samples from the geographic region sympatric withD. recensare most closely related toD. recens, whereas samples from the geographic region allopatric withD. recensare most closely related toD. transversa. We present several lines of evidence that both incomplete lineage sorting and gene flow are causing phylogenetic discordance. We suggest that ongoing gene flow primarily fromD. recensintoD. subquinariain the sympatric part of their ranges causes phylogenetic uncertainty in the evolutionary history of these species. Our results highlight how population genetic data can be used to disentangle the sources of phylogenetic discordance among closely related species. 

Abstract Selfish genetic elements that manipulate gametogenesis to achieve a transmission advantage are known as meiotic drivers.Sex‐ratioX chromosomes (SR) are meiotic drivers that prevent the maturation of Y‐bearing sperm in male carriers to result in the production of mainly female progeny. The spread of an SR chromosome can affect host genetic diversity and genome evolution, and can even cause host extinction if it reaches sufficiently high prevalence. Meiotic drivers have evolved independently many times, though only in a few cases is the underlying genetic mechanism known. In this study we use a combination of transcriptomics and population genetics to identify widespread expression differences between the standard (ST) andsex‐ratio(SR) X chromosomes of the flyDrosophila neotestacea.We found the X chromosome is enriched for differentially expressed transcripts and that many of these X‐linked differentially expressed transcripts had elevatedK_a/K_svalues between ST and SR, indicative of potential functional differences. We identified a set of candidate transcripts, including a testis‐specific, X‐linked duplicate of the nuclear transport geneimportin‐α2that is overexpressed in SR.We find suggestions of positive selection in the lineage leading to the duplicate and that its molecular evolutionary patterns are consistent with relaxed purifying selection in ST. As these patterns are consistent with involvement in the mechanism of drive in this species, this duplicate is a strong candidate worthy of further functional investigation. Nuclear transport may be a common target for genetic conflict, as the mechanism of the autosomalSegregation Distorterdrive system inD. melanogasterinvolves the same pathway. 

Abstract Drosophila melanogaster is a leading model in population genetics and genomics, and a growing number of whole-genome data sets from natural populations of this species have been published over the last years. A major challenge is the integration of disparate data sets, often generated using different sequencing technologies and bioinformatic pipelines, which hampers our ability to address questions about the evolution of this species. Here we address these issues by developing a bioinformatics pipeline that maps pooled sequencing (Pool-Seq) reads from D. melanogaster to a hologenome consisting of fly and symbiont genomes and estimates allele frequencies using either a heuristic (PoolSNP) or a probabilistic variant caller (SNAPE-pooled). We use this pipeline to generate the largest data repository of genomic data available for D. melanogaster to date, encompassing 271 previously published and unpublished population samples from over 100 locations in >20 countries on four continents. Several of these locations have been sampled at different seasons across multiple years. This data set, which we call Drosophila Evolution over Space and Time (DEST), is coupled with sampling and environmental metadata. A web-based genome browser and web portal provide easy access to the SNP data set. We further provide guidelines on how to use Pool-Seq data for model-based demographic inference. Our aim is to provide this scalable platform as a community resource which can be easily extended via future efforts for an even more extensive cosmopolitan data set. Our resource will enable population geneticists to analyze spatiotemporal genetic patterns and evolutionary dynamics of D. melanogaster populations in unprecedented detail. 

To advance our understanding of adaptation to temporally varying selection pressures, we identified signatures of seasonal adaptation occurring in parallel among Drosophila melanogaster populations. Specifically, we estimated allele frequencies genome-wide from flies sampled early and late in the growing season from 20 widely dispersed populations. We identified parallel seasonal allele frequency shifts across North America and Europe, demonstrating that seasonal adaptation is a general phenomenon of temperate fly populations. Seasonally fluctuating polymorphisms are enriched in large chromosomal inversions, and we find a broad concordance between seasonal and spatial allele frequency change. The direction of allele frequency change at seasonally variable polymorphisms can be predicted by weather conditions in the weeks prior to sampling, linking the environment and the genomic response to selection. Our results suggest that fluctuating selection is an important evolutionary force affecting patterns of genetic variation in Drosophila . 

Understanding the pleiotropic consequences of gene drive systems on host fitness is essential to predict their spread through a host population. Here, we study sex-ratio (SR) X-chromosome drive in the fly Drosophila recens , where SR causes the death of Y-bearing sperm in male carriers. SR males only sire daughters, which all carry SR, thus giving the chromosome a transmission advantage. The prevalence of the SR chromosome appears stable, suggesting pleiotropic costs. It was previously shown that females homozygous for SR are sterile, and here, we test for additional fitness costs of SR. We found that females heterozygous for SR have reduced fecundity and that male SR carriers have reduced fertility in conditions of sperm competition. We then use our fitness estimates to parametrize theoretical models of SR drive and show that the decrease in fecundity and sperm competition performance can account for the observed prevalence of SR in natural populations. In addition, we found that the expected equilibrium frequency of the SR chromosome is particularly sensitive to the degree of multiple mating and performance in sperm competition. Together, our data suggest that the mating system of the organism should be carefully considered during the development of gene drive systems.