Department of Organismic and Evolutionary Biology, Harvard University, 16 Divinity Avenue, Cambridge, MA, 02138, USA.
Department of Molecular and Cellular Biology, Harvard University, 16 Divinity Avenue, Cambridge, MA, 02138, USA.
BMC Evol Biol. 2019 Feb 20;19(1):60. doi: 10.1186/s12862-019-1377-4.
Sex-biased gene expression is thought to drive the phenotypic differences in males and females in metazoans. Drosophila has served as a primary model for studying male-female differences in gene expression, and its effects on protein sequence divergence. However, the forces shaping evolution of sex-biased expression remain largely unresolved, including the roles of selection and pleiotropy. Research on sex organs in Drosophila, employing original approaches and multiple-species contrasts, provides a means to gain insights into factors shaping the turnover and magnitude (fold-bias) of sex-biased expression.
Here, using recent RNA-seq data, we studied sex-biased gonadal expression in 10,740 protein coding sequences in four species of Drosophila, D. melanogaster, D. simulans, D. yakuba and D. ananassae (5 to 44 My divergence). Using an approach wherein we identified genes with lineage-specific transitions (LSTs) in sex-biased status (amongst testis-biased, ovary-biased and unbiased; thus, six transition types) standardized to the number of genes with the ancestral state (S-LSTs), and those with clade-wide expression bias status, we reveal several key findings. First, the six categorical types of S-LSTs in sex-bias showed disparate rates of turnover, consistent with differential selection pressures. Second, the turnover in sex-biased status was largely unrelated to cross-tissue expression breadth, suggesting pleiotropy does not restrict evolution of sex-biased expression. Third, the fold-sex-biased expression, for both testis-biased and ovary-biased genes, evolved directionally over time toward higher values, a crucial finding that could be interpreted as a selective advantage of greater sex-bias, and sexual antagonism. Fourth, in terms of protein divergence, genes with LSTs to testis-biased expression exhibited weak signals of elevated rates of evolution (than ovary-biased) in as little as 5 My, which strengthened over time. Moreover, genes with clade-wide testis-specific expression (44 My), a status not observed for any ovary-biased genes, exhibited striking acceleration of protein divergence, which was linked to low pleiotropy.
By studying LSTs and clade-wide sex-biased gonadal expression in a multi-species clade of Drosophila, we describe evidence that interspecies turnover and magnitude of sex-biased expression have been influenced by selection. Further, whilst pleiotropy was not connected to turnover in sex-biased gonadal expression, it likely explains protein sequence divergence.
性别偏向基因表达被认为是驱动后生动物中雄性和雌性表型差异的原因。果蝇一直是研究性别表达差异和对蛋白质序列分化影响的主要模式生物。然而，塑造性别偏向表达进化的力量在很大程度上仍未得到解决，包括选择和多效性的作用。利用原始方法和多物种对比研究果蝇性器官的研究为深入了解塑造性别偏向表达的周转率和幅度（倍偏）的因素提供了一种手段。
在这里，我们使用最近的 RNA-seq 数据，研究了四个果蝇物种（黑腹果蝇、拟果蝇、黑腹果蝇和 D. ananassae（5 到 44 My 分歧）中 10740 个蛋白质编码序列的性器官偏向表达。我们采用一种方法，其中我们鉴定了在性别偏向状态（睾丸偏向、卵巢偏向和无偏向；因此，有六种转变类型）中具有谱系特异性转变（LSTs）的基因，并将其标准化为具有祖先状态的基因数量（S-LSTs），以及具有全谱系表达偏向状态的基因，我们揭示了几个关键发现。首先，六种 S-LST 类别在性别偏向中的转变率不同，这与不同的选择压力一致。其次，性别偏向状态的转变与跨组织表达广度基本无关，这表明多效性不会限制性别偏向表达的进化。第三，对于睾丸偏向和卵巢偏向基因，性别偏向的折叠表达随着时间的推移朝着更高的值方向进化，这是一个重要的发现，可以解释为更大的性别偏向和性拮抗的选择优势。第四，就蛋白质分化而言，具有向睾丸偏向表达转变的基因在短短 5 My 内表现出进化速率升高的微弱信号（比卵巢偏向），随着时间的推移而增强。此外，具有全谱系睾丸特异性表达（44 My）的基因（没有观察到任何卵巢偏向基因）表现出惊人的蛋白质分化加速，这与低多效性有关。
通过在一个多物种果蝇分支中研究 LSTs 和全谱系性器官偏向表达，我们描述了证据表明种间周转率和性别偏向表达的幅度受到了选择的影响。进一步，虽然多效性与性别偏向性腺表达的转变无关，但它可能解释了蛋白质序列的分化。
