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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. 

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.