Rapid evolution of male-biased genes in Drosophila

Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 09/2003; 100(17):9894-9. DOI: 10.1073/pnas.1630690100
Source: PubMed


A number of genes associated with sexual traits and reproduction evolve at the sequence level faster than the majority of genes coding for non-sex-related traits. Whole genome analyses allow this observation to be extended beyond the limited set of genes that have been studied thus far. We use cDNA microarrays to demonstrate that this pattern holds in Drosophila for the phenotype of gene expression as well, but in one sex only. Genes that are male-biased in their expression show more variation in relative expression levels between conspecific populations and two closely related species than do female-biased genes or genes with sexually monomorphic expression patterns. Additionally, elevated ratios of interspecific expression divergence to intraspecific expression variation among male-biased genes suggest that differences in rates of evolution may be due in part to natural selection. This finding has implications for our understanding of the importance of sexual dimorphism for speciation and rates of phenotypic evolution.

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Available from: Jose Ranz, Aug 01, 2014
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    • "In support of this theory, genes that are male-biased in their expression show greater divergence between species compared to female-biased and non-biased genes (Civetta and Singh, 1995; Meiklejohn et al., 2003; Hearty et al., 2007, but see Metta et al., 2006 for a counter example). In addition, spermatogenesis is considered to be more easily disrupted by mutations than oogenesis , leading to more male than female hybrid sterility (Wu and Davis, 1993). "
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    Frontiers in Genetics 05/2015; 6. DOI:10.3389/fgene.2015.00140
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    • "Sex-biased gene expression is a common phenomenon in both dioecious plant and animal species, as documented in humans (Dimas & Nica, 2012), Drosophila (Zhang et al., 2007), emus (Vicoso et al., 2013) and Silene latifolia (Zemp et al., 2014), among others. Genes that exhibit sex-biased expression might be under unique evolutionary constraints, evolving more rapidly in terms of both sequence and expression (Meiklejohn et al., 2003). "
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    ABSTRACT: Sex chromosomes have evolved independently in phylogenetically diverse flowering plant lineages. The genes governing sex determination in dioecious species remain unknown, but theory predicts that the linkage of genes influencing male and female function will spur the origin and early evolution of sex chromosomes. For example, in an XY system, the origin of an active Y may be spurred by the linkage of female suppressing and male promoting genes. Garden asparagus (Asparagus officinalis) serves as a model for plant sex chromosome evolution, given that it has recently evolved an XX/XY sex chromosome system. In order to elucidate the molecular basis of gender differences and sex determination, we used RNA-sequencing (RNA-Seq) to identify differentially expressed genes between female (XX), male (XY) and supermale (YY) individuals. We identified 570 differentially expressed genes, and showed that significantly more genes exhibited male-biased than female-biased expression in garden asparagus. In the context of anther development, we identified genes involved in pollen microspore and tapetum development that were specifically expressed in males and supermales. Comparative analysis of genes in the Arabidopsis thaliana, Zea mays and Oryza sativa anther development pathways shows that anther sterility in females probably occurs through interruption of tapetum development before microspore meiosis. © 2015 The Authors. New Phytologist © 2015 New Phytologist Trust.
    New Phytologist 03/2015; 207(3). DOI:10.1111/nph.13389 · 7.67 Impact Factor
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    • "Divergence of the regulatory networks controlling gene expression can cause misexpression in F 1 hybrids that can contribute to speciation (Meiklejohn et al. 2003; Michalak and Noor 2004; Ranz et al. 2004; Haerty and Singh 2006; Moehring et al. 2007; Maheshwari and Barbash 2012). This can occur, for example, when proteins and/or DNA with sequence-specific interactions coevolve such that divergent alleles of the interacting molecules do not function properly together in F 1 hybrids. "
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    ABSTRACT: Genetic changes affecting gene expression contribute to phenotypic divergence, thus understanding how regulatory networks controlling gene expression change over time is critical for understanding evolution. Prior studies of expression differences within and between species have identified properties of regulatory divergence, but technical and biological differences among these studies make it difficult to assess the generality of these properties or to understand how regulatory changes accumulate with divergence time. Here, we address these issues by comparing gene expression among strains and species of Drosophila with a range of divergence times and use F1 hybrids to examine inheritance patterns and disentangle cis- and trans-regulatory changes. We find that the fixation of compensatory changes has caused the regulation of gene expression to diverge more rapidly than gene expression itself. Specifically, we observed that the proportion of genes with evidence of cis-regulatory divergence has increased more rapidly with divergence time than the proportion of genes with evidence of expression differences. Surprisingly, the amount of expression divergence explained by cis-regulatory changes did not increase steadily with divergence time, as was previously proposed. Rather, one species (D. sechellia) showed an excess of cis-regulatory divergence that we argue most likely resulted from positive selection in this lineage. Taken together, this work reveals not only the rate at which gene expression evolves, but also the molecular and evolutionary mechanisms responsible for this evolution.
    Genome Research 02/2014; 24(5). DOI:10.1101/gr.163014.113 · 14.63 Impact Factor
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