Evolution of Sex-Dependent Gene Expression in Three Recently Diverged Species of Drosophila

Jiang, Zhi‐Yun; Machado, Carlos A.

doi:10.1534/genetics.109.105775

Cited by 50 publications

(87 citation statements)

References 69 publications

(97 reference statements)

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“…These results are similar to those observed in D. pulex , where 25% of the genes are classified as sex-biased with a P value cut-off of 0.05, and 10% are classified as sex-biased with a fold-change cut-off of 2 (supplementary table S4, Supplementary Material online). The proportion of sex-biased genes is much less than that reported for Drosophila species where as many as two-thirds of all genes can show sex-biased expression when whole animals are assayed (Gnad and Parsch 2006; Jiang and Machado 2009; Meisel et al 2012). However, in D. melanogaster , the proportion of genes showing sex-biased expression can vary greatly among tissues (Huylmans and Parsch 2015).…”

Section: Discussionmentioning

confidence: 64%

De Novo Transcriptome Assembly and Sex-Biased Gene Expression in the Cyclical ParthenogeneticDaphnia galeata

et al. 2016

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Daphnia species have become models for ecological genomics and exhibit interesting features, such as high phenotypic plasticity and a densely packed genome with many lineage-specific genes. They are also cyclic parthenogenetic, with alternating asexual and sexual cycles and environmental sex determination. Here, we present a de novo transcriptome assembly of over 32,000 D. galeata genes and use it to investigate gene expression in females and spontaneously produced males of two clonal lines derived from lakes in Germany and the Czech Republic. We find that only a low percentage (18%) of genes shows sex-biased expression and that there are many more female-biased gene (FBG) than male-biased gene (MBG). Furthermore, FBGs tend to be more conserved between species than MBGs in both sequence and expression. These patterns may be a consequence of cyclic parthenogenesis leading to a relaxation of purifying selection on MBGs. The two clonal lines show considerable differences in both number and identity of sex-biased genes, suggesting that they may have reproductive strategies differing in their investment in sexual reproduction. Orthologs of key genes in the sex determination and juvenile hormone pathways, which are thought to be important for the transition from asexual to sexual reproduction, are present in D. galeata and highly conserved among Daphnia species.

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Section: Discussionmentioning

confidence: 64%

De Novo Transcriptome Assembly and Sex-Biased Gene Expression in the Cyclical ParthenogeneticDaphnia galeata

et al. 2016

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“…Instead, we found that male-biased genes tend to have higher expression divergence in females, and female-biased genes have higher expression divergence in males. This suggests that sex-biased genes experience high selective pressure in the opposite sex (Jiang and Machado 2009). …”

Section: Better Conservation Of Male-biased Gene Expression On the Nementioning

confidence: 99%

Sex-Biased Gene Expression and Evolution of the X Chromosome in Nematodes

et al. 2014

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Studies of X chromosome evolution in various organisms have indicated that sex-biased genes are nonrandomly distributed between the X and autosomes. Here, to extend these studies to nematodes, we annotated and analyzed X chromosome gene content in four Caenorhabditis species and in Pristionchus pacificus. Our gene expression analyses comparing young adult male and female mRNAseq data indicate that, in general, nematode X chromosomes are enriched for genes with high female-biased expression and depleted of genes with high male-biased expression. Genes with low sex-biased expression do not show the same trend of X chromosome enrichment and depletion. Combined with the observation that highly sex-biased genes are primarily expressed in the gonad, differential distribution of sex-biased genes reflects differences in evolutionary pressures linked to tissue-specific regulation of X chromosome transcription. Our data also indicate that X dosage imbalance between males (XO) and females (XX) is influential in shaping both expression and gene content of the X chromosome. Predicted upregulation of the single male X to match autosomal transcription (Ohno's hypothesis) is supported by our observation that overall transcript levels from the X and autosomes are similar for highly expressed genes. However, comparison of differentially located one-to-one orthologs between C. elegans and P. pacificus indicates lower expression of X-linked orthologs, arguing against X upregulation. These contradicting observations may be reconciled if X upregulation is not a global mechanism but instead acts locally on a subset of tissues and X-linked genes that are dosage sensitive. IN an XY sex-determination system, male and female genomes are identical with the exception of the male-specific Y chromosome, which bears few genes (Charlesworth et al. 2005). This is particularly true when the Y chromosome is thought to be completely lost, as is the case for C. elegans and many other nematodes (Walton 1940). Because gene content is the same, phenotypic differences between males and females, termed "sexual dimorphisms," must be caused by differential gene expression between the two sexes (Connallon and Knowles 2005;Ellegren and Parsch 2007). Throughout the article, such differentially expressed genes are referred to as "sex biased." As males and females have different fitness optima, a trait that is beneficial to one sex can be harmful to the other (termed sexual antagonism) (Rice and Chippindale 2001;Arnqvist 2004;Connallon and Knowles 2005;Ellegren and Parsch 2007;Mank et al. 2008a;Rice 1984). The evolution of sex-biased gene expression is thought to mediate the effects of sexual antagonism and allow for achievement of sex-specific fitness. Previous studies have indicated that anywhere between 30 and 60% of metazoan genes may be sex biased Parisi et al. 2004;Reinke et al. 2004;Yang et al. 2006;Reinius et al. 2008;Small et al. 2009;Innocenti and Morrow 2010;Assis et al. 2012;Reinius et al. 2012;Thomas et al. 2012). Genes with sex-biased exp...

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“…In line with this, studies in a wide array of organisms have attempted to determine the differences in gene expression between males and females (Parsch and Ellegren 2013), including Drosophila (Assis et al 2012; Perry et al 2014), birds (Pointer et al 2013), nematodes (Albritton et al 2014), and brown alga (Lipinska et al 2015). These works have revealed that a significant fraction of genes in the genome exhibit differential expression between males and females (Rinn and Snyder 2005; Mank, Hultin-Rosenberg, Webster, et al 2008; Reinius et al 2008; Jiang and Machado 2009), which suggests that the expression of sexual dimorphism is related to marked genetic reprogramming (Lipinska et al 2015). …”

Section: Introductionmentioning

confidence: 99%

Both Male-Biased and Female-Biased Genes Evolve Faster in Fish Genomes

Yang

Zhang

2016

Genome Biol Evol

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Males and females often display extensive phenotypic differences, and many of these sexual dimorphisms are thought to result from differences between males and females in expression of genes present in both sexes. Sex-biased genes have been shown to exhibit accelerated rates of evolution in a wide array of species, however the cause of this remains enigmatic. In this study, we investigate the extent and evolutionary dynamics of sex-biased gene expression in zebrafish. Our results indicate that both male-biased genes and female-biased genes exhibit accelerated evolution at the protein level. In order to differentiate between adaptive and nonadaptive causes, we tested for codon usage bias and signatures of different selective regimes in our sequence data. Our results show that both male- and female-biased genes show signatures consistent with adaptive evolution. In order to test the generality of our findings across fish, we also analyzed publicly available data on sticklebacks, and found results consistent with our findings in zebrafish.

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Evolution of Sex-Dependent Gene Expression in Three Recently Diverged Species of Drosophila

Cited by 50 publications

References 69 publications

De Novo Transcriptome Assembly and Sex-Biased Gene Expression in the Cyclical ParthenogeneticDaphnia galeata

De Novo Transcriptome Assembly and Sex-Biased Gene Expression in the Cyclical ParthenogeneticDaphnia galeata

Sex-Biased Gene Expression and Evolution of the X Chromosome in Nematodes

Both Male-Biased and Female-Biased Genes Evolve Faster in Fish Genomes

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