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Parsch, J.

Publications and source records attributed to Parsch, J..

6 recordsLinked to original sources

Conservation and divergence of sex-biased gene expression across 50 million years of Drosophila evolution

In sexually dimorphic species, sex-biased gene expression plays an important role in driving morphological, physiological, and behavioral differences between males and females. Here, we examined patterns of sex-biased gene expression within and among 6 Drosophila species with divergence times ranging from 2-50 million years. We detected contrasting patterns of sex bias conservation and turnover between heads and bodies, with more extensive sex-biased expression and greater conservation of sex-biased expression in the body, but more species-specific turnover of sex-biased expression in the head, where conserved, unbiased expression was common. Interestingly, lineage-specific gains of sex-biased expression occurred most often via concordant expression changes in both sexes that differed only in their magnitude, with this pattern being particularly strong in the head, suggesting that the majority of lineage-specific sex bias gains do not represent a resolution of sexual antagonism, but instead reflect regulatory changes shared between the sexes. We detected an enrichment of putatively positively selected expression changes among sex-biased genes in both body parts. Altogether, our findings suggest that sex-biased expression changes are often facilitated by selection, including selection acting on the sex with lower expression, which is especially common for male expression of female-biased genes. We also detected differences in the proportion of sex-biased genes located on the X chromosome depending on sex bias and body part. Overall, our results provide novel insights into the dynamics of sex-biased gene expression, as well as the molecular mechanisms and selective forces underlying its turnover, across short and long evolutionary timescales.

evolutionary biology↗

Pervasive tissue-, genetic background-, and allele-specific gene expression effects in Drosophila melanogaster

The pervasiveness of gene expression variation and its contribution to phenotypic variation and evolution is well known. This gene expression variation is context dependent, with differences in regulatory architecture often associated with intrinsic and environmental factors, and is modulated by regulatory elements that can act in cis (linked) or in trans (unlinked) relative to the genes they affect. So far, little is known about how this genetic variation affects the evolution of regulatory architecture among closely related tissues during population divergence. To address this question, we analyzed gene expression in the midgut, hindgut, and Malpighian tubule as well as microbiome composition in the two gut tissues in four Drosophila melanogaster strains and their F1 hybrids from two divergent populations: one from the derived, European range and one from the ancestral, African range. In both the transcriptome and microbiome data, we detected extensive tissue- and genetic background-specific effects, including effects of genetic background on overall tissue specificity. Tissue-specific effects were typically stronger than genetic background-specific effects, although the two gut tissues were not more similar to each other than to the Malpighian tubules. An examination of allele specific expression revealed that, while both cis and trans effects were more tissue-specific in genes expressed differentially between populations than genes with conserved expression, trans effects were more tissue-specific than cis effects. Despite there being highly variable regulatory architecture, this observation was robust across tissues and genetic backgrounds, suggesting that the expression of trans variation can be spatially fine-tuned as well as or better than cis variation during population divergence and yielding new insights into cis and trans regulatory evolution. Author SummaryGenetic variants regulating gene expression can act in cis (linked) or in trans (unlinked) relative to the genes they affect and are thought to be important during adaptation because they can spatially and temporally fine-tune gene expression. In this study, we used the fruit fly Drosophila melanogaster to compare gene expression between inbred parental strains and their offspring in order to characterize the basis of gene expression regulation and inheritance. We examined gene expression in three tissues (midgut, hindgut, and Malpighian tubule) and four genetic backgrounds stemming from Europe and the ancestral range in Africa. Additionally, we characterized the bacterial community composition in the two gut tissues. We detected extensive tissue- and genetic background-specific effects on gene expression and bacterial community composition, although tissue-specific effects were typically stronger than genetic background effects. Genes with cis and trans regulatory effects were more tissue-specific than genes with conserved expression, while those with trans effects were more tissue-specific than those with cis effects. These results suggest that the expression of trans variation can be spatially fine-tuned as well as (or better than) cis variation as populations diverge from one another. Our study yields novel insight into the genetic basis of gene regulatory evolution.

evolutionary biology↗

Population genomics reveals mechanisms and dynamics of de novo proto-gene emergence in Drosophila melanogaster

Scientific AbstractNovel genes are essential for evolutionary innovations and differ substantially even between closely related species. Recently, multiple studies across many taxa have suggested that some novel genes arise de novo, i.e. from previously non-coding DNA. In order to characterise the underlying mutations that allowed de novo gene emergence and their order of occurrence, homologous regions must be detected within non-coding sequences in closely related sister genomes. So far, most studies do not detect non-coding homologs of de novo genes due to inconsistent data and long evolutionary distances separating genomes. Here we overcome these issues by searching for proto-genes, the not-yet fixed precursors of de novo genes that emerged within a single species. We sequenced and assembled genomes with long-read technology and the corresponding transcriptomes from inbred lines of Drosophila melanogaster, derived from seven geographically diverse populations. We found line-specific proto-genes in abundance but few proto-genes shared by lines, suggesting a rapid turnover. Gain and loss of transcription is more frequent than the creation of Open Reading Frames (ORFs), e.g. by forming new START- and STOP-codons. Consequently, the gain of ORFs becomes rate limiting and is frequently the initial step in proto-gene emergence. Furthermore, Transposable Elements (TEs) are major drivers for intra genomic duplications of proto-genes, yet TE insertions are less important for the emergence of proto-genes. However, highly mutable genomic regions around TEs provide new features that enable gene birth. In conclusion, proto-genes have a high birth-death rate, are rapidly purged, but surviving proto-genes spread neutrally through populations and within genomes.

genomics↗

Drosophila Evolution over Space and Time (DEST) - A New Population Genomics Resource

Drosophila melanogaster is a leading model in population genetics and genomics, and a growing number of whole-genome datasets from natural populations of this species have been published over the last 20 years. A major challenge is the integration of these disparate datasets, often generated using different sequencing technologies and bioinformatic pipelines, which hampers our ability to address questions about the evolution and population structure 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 population samples from over 100 locations in >20 countries on four continents based on a combination of 121 unpublished and 150 previously published genomic datasets. Several of these locations have been sampled at different seasons across multiple years. This dataset, which we call Drosophila Evolution over Space and Time (DEST), is coupled with sampling and environmental meta-data. A web-based genome browser and web portal provide easy access to the SNP dataset. 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 dataset. Our resource will enable population geneticists to analyze spatio-temporal genetic patterns and evolutionary dynamics of D. melanogaster populations in unprecedented detail.

genomics↗

The discovery, distribution and diversity of DNA viruses associated with Drosophila melanogaster in Europe

Drosophila melanogaster is an important model for antiviral immunity in arthropods, but very few DNA viruses have been described from the family Drosophilidae. This deficiency limits our opportunity to use natural host-pathogen combinations in experimental studies, and may bias our understanding of the Drosophila virome. Here we report fourteen DNA viruses detected in a metagenomic analysis of approximately 6500 pool-sequenced Drosophila, sampled from 47 European locations between 2014 and 2016. These include three new Nudiviruses, a new and divergent Entomopox virus, a virus related to Leptopilina boulardi filamentous virus, and a virus related to Musca domestica salivary gland hypertrophy virus. We also find an endogenous genomic copy of Galbut virus, a dsRNA Partitivirus, segregating at very low frequency. Remarkably, we find that Drosophila Vesanto virus, a small DNA virus previously described as a Bidnavirus, may be composed of up to 12 segments and represent a new lineage of segmented DNA viruses. Two of the DNA viruses, Drosophila Kallithea nudivirus and Drosophila Vesanto virus are relatively common, found in 2% or more of wild flies. The others are rare, with many likely to be represented by a single infected fly. We find that virus prevalence in Europe reflects the prevalence seen in publicly-available datasets, with Drosophila Kallithea nudivirus and Drosophila Vesanto virus the only ones commonly detectable in public data from wild-caught flies and large population cages, and the other viruses being rare or absent. These analyses suggest that DNA viruses are at lower prevalence than RNA viruses in D. melanogaster, and may be less likely to persist in laboratory cultures. Our findings go some way to redressing an earlier bias toward RNA virus studies in Drosophila, and lay the foundation needed to harness the power of Drosophila as a model system for the study of DNA viruses.

microbiology↗

Genomic analysis of European Drosophila melanogaster populations on a dense spatial scale reveals longitudinal population structure and continent-wide selection

Genetic variation is the fuel of evolution, with standing genetic variation especially important for short-term evolution and local adaptation. To date, studies of spatio-temporal patterns of genetic variation in natural populations have been challenging, as comprehensive sampling is logistically difficult, and sequencing of entire populations costly. Here, we address these issues using a collaborative approach, sequencing 48 pooled population samples from 32 locations, and perform the first continent-wide genomic analysis of genetic variation in European Drosophila melanogaster. Our analyses uncover longitudinal population structure, provide evidence for continent-wide selective sweeps, identify candidate genes for local climate adaptation, and document clines in chromosomal inversion and transposable element frequencies. We also characterise variation among populations in the composition of the fly microbiome, and identify five new DNA viruses in our samples.

evolutionary biology↗