Zhang, Y., Sturgill, D., Parisi, M., Kumar, S. & Oliver, B. Constraint and turnover in sex-biased gene expression in the genus Drosophila. Nature 450, 233-237

Laboratory of Cellular and Developmental Biology, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Department of Health and Human Services, Bethesda, Maryland 20892, USA.
Nature (Impact Factor: 41.46). 12/2007; 450(7167):233-7. DOI: 10.1038/nature06323
Source: PubMed


Both genome content and deployment contribute to phenotypic differences between species. 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. Comparative analysis of sex-biased expression should deepen our understanding of the relationship between genome content and deployment during evolution. Using existing and newly assembled genomes, 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.

Download full-text


Available from: Michael Parisi
  • Source
    • "To enhance predictions of functional binding sites, we used comparative genomics to analyze DSX binding site conservation among 20 species of Drosophila (Adams et al., 2000; Chen et al., 2014; Drosophila 12 Genomes Consortium et al., 2007; Richards et al., 2005). While conservation is not always predictive of function (Villar et al., 2014), and some nonconserved sites may be interesting species-specific targets, evolutionarily conserved sites are likely to regulate the vast array of genes showing sexbiased expression in the genus (Chen et al., 2014; Zhang et al., 2007). The dsx sex-specific splicing pattern and encoded DNA binding domain was highly conserved across $34 million years of Drosophila evolution (Figure S2). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Primary sex-determination ''switches'' evolve ra-pidly, but Doublesex (DSX)-related transcription fac-tors (DMRTs) act downstream of these switches to control sexual development in most animal species. Drosophila dsx encodes female-and male-specific isoforms (DSX F and DSX M), but little is known about how dsx controls sexual development, whether DSX F and DSX M bind different targets, or how DSX proteins direct different outcomes in diverse tissues. We undertook genome-wide analyses to identify DSX targets using in vivo occupancy, binding site predic-tion, and evolutionary conservation. We find that DSX F and DSX M bind thousands of the same targets in multiple tissues in both sexes, yet these targets have sex-and tissue-specific functions. Interestingly, DSX targets show considerable overlap with targets identified for mouse DMRT1. DSX targets include transcription factors and signaling pathway compo-nents providing for direct and indirect regulation of sex-biased expression. INTRODUCTION
    Full-text · Article · Dec 2014 · Developmental Cell
  • Source
    • "However, results from early microarray expression profiling studies demonstrated that transcribed elements were unannotated (Andrews et al. 2000; Hild et al. 2003; Stolc et al. 2004). Evolutionary conservation in the genus has been important for improving annotation of D. melanogaster (Pollard et al. 2006; Drosophila 12 Genomes Consortium 2007; Stark et al. 2007; Zhang et al. 2007). As part of a major effort to improve the annotation, expression profiles provided in the first phase of modENCODE (Cherbas et al. 2011; Graveley et al. 2011) and by complementary studies (Daines et al. 2011) added thousands of new exons to the annotation, especially untranslated 59 and 39 regions and noncoding RNAs, as well as confirming the expression of most of the previously annotated transcripts (McQuilton et al. 2012). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Accurate gene model annotation of reference genomes is critical for making them useful. The modENCODE project has improved the D. melanogaster genome annotation by using deep and diverse high-throughput data. Since transcriptional activity that has been evolutionarily conserved is likely to have an advantageous function, we have performed large-scale interspecific comparisons to increase confidence in predicted annotations. To support comparative genomics, we filled in divergence gaps in the Drosophila phylogeny by generating draft genomes for eight new species. For comparative transcriptome analysis, we generated mRNA expression profiles on 81 samples from multiple tissues and developmental stages of 15 Drosophila species, and we performed cap analysis of gene expression in D. melanogaster and D. pseudoobscura. We also describe conservation of four distinct core promoter structures composed of combinations of elements at three positions. Overall, each type of genomic feature shows a characteristic divergence rate relative to neutral models, highlighting the value of multispecies alignment in annotating a target genome that should prove useful in the annotation of other high priority genomes, especially human and other mammalian genomes that are rich in noncoding sequences. We report that the vast majority of elements in the annotation are evolutionarily conserved, indicating that the annotation will be an important springboard for functional genetic testing by the Drosophila community.
    Preview · Article · Sep 2014
  • Source
    • "This can create a link between rate of sequence evolution and biased gene expression if genes that are under weak selection with respect to sequence are also under weak selection in terms of expression, and consequently more likely to have a drifted toward biased expression pattern than constrained genes. This is likely to often be the case given the observed correlations between gene essentiality and expression noise (Fraser et al., 2004), and expression divergence and sequence divergence among species (Lemos et al., 2005b; Zhang et al., 2007; Mcmanus et al., 2010). This process should result in the pattern observed in S. invicta (Hunt et al., 2011), where genes that presently exhibit morphbiased expression evolved faster even before the evolution of morphs or before morph biased expression pattern arose (Figure 1). "
    [Show abstract] [Hide abstract]
    ABSTRACT: The castes of social insects provide outstanding opportunities to address the causes and consequences of evolution of discrete phenotypes, i.e., polymorphisms. Here we focus on recently described patterns of a positive association between the degree of caste-specific gene expression and the rate of sequence evolution. We outline how neutral and adaptive evolution can cause genes that are morph-biased in their expression profiles to exhibit historical signatures of faster or slower sequence evolution compared to unbiased genes. We conclude that evaluation of different hypotheses will benefit from (i) reconstruction of the phylogenetic origin of biased expression and changes in rates of sequence evolution, and (ii) replicated data on gene expression variation within versus between morphs. Although the data are limited at present, we suggest that the observed phylogenetic and intra-population variation in gene expression lends support to the hypothesis that the association between caste-biased expression and rate of sequence evolution largely is a result of neutral processes.
    Full-text · Article · Aug 2014 · Frontiers in Genetics
Show more