Variable sexually dimorphic gene expression in laboratory strains of Drosophila melanogaster (original) (raw)
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Extensive Sex-Specific Nonadditivity of Gene Expression in Drosophila melanogaster
Genetics, 2004
Assessment of the degree to which gene expression is additive and heritable has important implications for understanding the maintenance of variation, adaptation, phenotypic divergence, and the mapping of genotype onto phenotype. We used whole-genome transcript profiling using Agilent long-oligonucleotide microarrays representing 12,017 genes to demonstrate that gene transcription is pervasively nonadditive in Drosophila melanogaster. Comparison of adults of two isogenic lines and their reciprocal F 1 hybrids revealed 5820 genes as significantly different between at least two of the four genotypes in either males or females or across both sexes. Strikingly, while 25% of all genes differ between the two parents, 33% differ between both F 1 's and the parents, averaged across sexes. However, only 5% of genes show overdominance, suggesting that heterosis for expression is rare.
Constraint and turnover in sex-biased gene expression in the genus Drosophila
Nature, 2007
Both genome content and deployment contribute to phenotypic differences between species 1-5. Sex is the most important difference between individuals in a species and has long been posited to be rapidly evolving. Indeed, in the Drosophila genus, traits such as sperm length, genitalia, and gonad size are the most obvious differences between species 6. Comparative analysis of sex-biased expression should deepen our understanding of the relationship between genome content and deployment during evolution. Using existing 7,8 and newly assembled genomes 9 , we designed species-specific microarrays to examine sex-biased expression of orthologues and species-restricted genes in D. melanogaster, D. simulans, D. yakuba, D. ananassae, D. pseudoobscura, D. virilis and D. mojavensis. We show that averaged sex-biased expression changes accumulate monotonically over time within the genus. However, different genes contribute to expression variance within species groups compared to between groups. We observed greater turnover of species-restricted genes with male-biased expression, indicating that gene formation and extinction may play a significant part in species differences. Genes with male-biased expression also show the greatest expression and DNA sequence divergence. This higher divergence and turnover of genes with male-biased expression may be due to high transcription rates in the male germline, greater functional pleiotropy of genes expressed in females, and/or sexual competition. There are numerous case studies demonstrating that orthologues with sex-biased function diverge more rapidly than genes with non-biased function 10. To determine systematically the relative contributions of gene content and expression divergence to sexual differences, we sampled sex-biased expression within the Drosophila genus using species-specific microarrays designed for the closely related D. melanogaster, D. simulans and D. yakuba group (common ancestor, 10-13 million years ago), and for the more distantly related D. ananassae, D. pseudoobscura, D. virilis and D. mojavensis (common ancestor, 40-65 million years ago) (Supplementary Table 1). The species-specific platform eliminated confounding effects of sequence divergence on hybridization and allowed us to assay the expression of lineagerestricted genes.
Sex-biased transcriptome evolution in Drosophila
Genome biology and evolution, 2012
Sex-biased genes are thought to drive phenotypic differences between males and females. The recent availability of high-throughput gene expression data for many related species has led to a burst of investigations into the genomic and evolutionary properties of sex-biased genes. In Drosophila, a number of studies have found that X chromosomes are deficient in male-biased genes (demasculinized) and enriched for female-biased genes (feminized) and that male-biased genes evolve faster than female-biased genes. However, studies have yielded vastly different conclusions regarding the numbers of sex-biased genes and forces shaping their evolution. Here, we use RNA-seq data from multiple tissues of Drosophila melanogaster and D. pseudoobscura, a species with a recently evolved X chromosome, to explore the evolution of sex-biased genes in Drosophila. First, we compare several independent metrics for classifying sex-biased genes and find that the overlap of genes identified by different metrics is small, particularly for female-biased genes. Second, we investigate genome-wide expression patterns and uncover evidence of demasculinization and feminization of both ancestral and new X chromosomes, demonstrating that gene content on sex chromosomes evolves rapidly. Third, we examine the evolutionary rates of sex-biased genes and show that male-biased genes evolve much faster than female-biased genes, which evolve at similar rates to unbiased genes. Analysis of gene expression among tissues reveals that this trend may be partially due to pleiotropic effects of female-biased genes, which limits their evolutionary potential. Thus, our findings illustrate the importance of accurately identifying sex-biased genes and provide insight into their evolutionary dynamics in Drosophila.
Genetics, 2009
Upon mating, Drosophila melanogaster females undergo numerous alterations in their behavior and reproductive physiology that are accompanied by small-magnitude transcript-level changes in up to 1700 genes. Many of these postmating transcriptome changes are the direct result of the sperm and seminal fluid proteins (Acps) that females receive from their mates. To begin to determine if the genetic background of the female's mate contributes to the previously described gene expression changes, we assessed whether interactions between the genotypes of two commonly used laboratory strains of D. melanogaster (Canton-S and Oregon R) influence the female's postmating transcriptome as well as several pre- and postcopulatory phenotypes. We find negligible differences in the female's transcriptome at 1–3 hr postmating regardless of the strain of the male with whom she mated. However, a male × female genotype interaction significantly influenced mate selection, and, in some cases, fe...
G3 (Bethesda, Md.), 2014
Here, we provide revised gene models for D. ananassae, D. yakuba, and D. simulans, which include untranslated regions and empirically verified intron-exon boundaries, as well as ortholog groups identified using a fuzzy reciprocal-best-hit blast comparison. Using these revised annotations, we perform differential expression testing using the cufflinks suite to provide a broad overview of differential expression between reproductive tissues and the carcass. We identify thousands of genes that are differentially expressed across tissues in D. yakuba and D. simulans, with roughly 60% agreement in expression patterns of orthologs in D. yakuba and D. simulans. We identify several cases of putative polycistronic transcripts, pointing to a combination of transcriptional read-through in the genome as well as putative gene fusion and fission events across taxa. We furthermore identify hundreds of lineage specific genes in each species with no blast hits among transcripts of any other Drosophi...
BMC Genomics, 2011
Background: Understanding animal development and physiology at a molecular-biological level has been advanced by the ability to determine at high resolution the repertoire of mRNA molecules by whole transcriptome resequencing. This includes the ability to detect and quantify rare abundance transcripts and isoform-specific mRNA variants produced from a gene. The sex hierarchy consists of a pre-mRNA splicing cascade that directs the production of sex-specific transcription factors that specify nearly all sexual dimorphism. We have used deep RNA sequencing to gain insight into how the Drosophila sex hierarchy generates somatic sex differences, by examining gene and transcript isoform expression differences between the sexes in adult head tissues.
Simpler mode of inheritance of transcriptional variation in male Drosophila melanogaster
Proceedings of the National Academy of Sciences, 2007
Sexual selection drives faster evolution in males. The X chromosome is potentially an important target for sexual selection, because hemizygosity in males permits accumulation of alleles, causing tradeoffs in fitness between sexes. Hemizygosity of the X could cause fundamentally different modes of inheritance between the sexes, with more additive variation in males and more nonadditive variation in females. Indeed, we find that genetic variation for the transcriptome is primarily additive in males but nonadditive in females. As expected, these differences are more pronounced on the X chromosome than the autosomes, but autosomal loci are also affected, possibly because of X-linked transcription factors. These differences may be of evolutionary significance because additive variation responds quickly to selection, whereas nonadditive genetic variation does not. Thus, hemizygosity of the X may underlie much of the faster male evolution of the transcriptome and potentially other phenotypes. Consistent with this prediction, genes that are additive in males and nonadditive in females are overrepresented among genes responding to selection for increased mating speed. microarray ͉ sexual antagonism ͉ sexual conflict ͉ sexual selection ͉ transcription Author contributions: M.L.W.
A survey of ovary-, testis-, and soma-biased gene expression in Drosophila melanogaster adults
Genome Biology, 2004
Background Sexual dimorphism results in the formation of two types of individuals with specialized reproductive roles and is most evident in the germ cells and gonads. Results We have undertaken a global analysis of transcription between the sexes using a 31,464 element FlyGEM microarray to determine what fraction of the genome shows sex-biased expression, what tissues express these genes, the predicted functions of these genes, and where these genes map onto the genome. Females and males (both with and without gonads), dissected testis and ovary, females and males with genetically ablated germlines, and sex-transformed flies were sampled. Conclusions Using any of a number of criteria, we find extensive sex-biased expression in adults. The majority of cases of sex differential gene expression are attributable to the germ cells. There is also a large class of genes with soma-biased expression. There is little germline-biased expression indicating that nearly all genes with germline expression also show sex-bias. Monte Carlo simulations show that some genes with sex-biased expression are non-randomly distributed in the genome.
G3 Genes|Genomes|Genetics
Sexual dimorphism occurs widely throughout insects and has profound influences on evolutionary path. Sex-biased genes are considered to account for most of phenotypic differences between sexes. In order to explore the sex-biased genes potentially associated with sexual dimorphism and sexual development in Drosophila suzukii, a major devastating and invasive crop pest, we conducted whole-organism transcriptome profiling and sex-biased gene expression analysis on adults of both sexes. We identified transcripts of genes involved in several sex-specific physiological and functional processes, including transcripts involved in sex determination, reproduction, olfaction, and innate immune signals. A total of 11,360 differentially expressed genes were identified in the comparison, and 1,957 differentially expressed genes were female-biased and 4,231 differentially expressed genes were male-biased. The pathway predominantly enriched for differentially expressed genes was related to spliceos...