The males and females of many dioecious plants differ in morphological (Dawson and Geber 1999; Barrett and Hough 2013; Tonnabel et al. 2017), physiological (Juvany and Munne-Bosch 2015), life-history (Delph 1999), and defence traits (Cornelissen and Stiling 2005). Ultimately, such sexual dimorphism must largely be due to differential gene expression between the sexes (Ellegren and Parsch 2007), but little is known about how sex-biased genes are recruited and how their expression evolves over time. We measured gene expression in leaves of males and females of ten species sampled across the South African Cape genus Leucadendron, which shows repeated changes in sexual dimorphism and includes the most extreme differences between males and females in flowering plants (Midgley 2010; Barrett and Hough 2013; Tonnabel et al. 2014). Even in the most dimorphic species in our sample, fewer than 2% of genes showed sex-biased gene expression (SBGE) in vegetative tissue, with surprisingly little correspondence between SBGE and vegetative dimorphism across species. The identity of sex-biased genes in Leucadendron was highly species-specific, with a rapid turnover among species. In animals, sex-biased genes often evolve more quickly than unbiased genes in their sequences and expression levels (Ranz et al. 2003; Khaitovich et al. 2005; Ellegren and Parsch 2007; Voolstra et al. 2007; Harrison et al. 2015; Naqvi et al. 2019), consistent with hypotheses invoking rapid evolution due to sexual selection. Our phylogenetic analysis in Leucadendron, however, clearly indicates that sex-biased genes are recruited from a class of genes with ancestrally rapid rates of expression evolution, perhaps due to low evolutionary or pleiotropic constraints. Nevertheless, we also find evidence for adaptive evolution of expression levels once sex bias evolves. Thus, although the expression of sex-biased genes is ultimately responsive to selection, high rates of expression evolution might usually predate the evolution of sex bias.

中文翻译：

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在进化性最高的两性被子植物Leucadendron中，向性别偏向的基因表达转变之前，进化率很高。

许多雌雄异株植物的雄性和雌性在形态（Dawson和Geber 1999； Barrett和Hough 2013； Tonnabel等人2017），生理（Juvany和Munne-Bosch 2015），生活史（Delph 1999）和防御性状上有所不同。 （Cornelissen and Stiling 2005）。最终，这种性别二态性很大程度上必须归因于性别之间的差异基因表达（Ellegren and Parsch 2007），但是人们对性别歧视基因的招募方式以及其表达随着时间的演变却知之甚少。我们测量了南非海角属Leucadendron采样的十个物种的雄性和雌性叶片中的基因表达，这表明性二态性反复变化，其中包括开花植物中雌雄之间的最极端差异（Midgley 2010； Barrett和Hough 2013； Tonnabel等人2014）。即使在我们样本中最双态的物种中，也只有不到2％的基因在营养组织中显示出性别偏向的基因表达（SBGE），而跨物种的SBGE与植物性二态性之间的对应关系却出乎意料地很少。Leucadendron中性别偏向基因的身份具有高度的物种特异性，物种间的周转速度很快。在动物中，性别偏向的基因在序列和表达水平上的进化往往比非偏向的基因更快（Ranz等，2003； Khaitoovich等，2005； Ellegren和Parsch 2007； Voolstra等，2007； Harrison等，2015； Herson等，2015）。 Naqvi et al.2019），与假设因性选择而导致快速进化的假设一致。我们在Leucadendron中的系统发育分析然而，清楚地表明，性别偏向的基因是从一类具有祖先快速的表达进化速率的基因中募集的，这可能是由于低进化或多效性限制所致。然而，我们也发现一旦性别偏见进化出适应性表达水平的证据。因此，尽管性别偏向基因的表达最终对选择产生响应，但高表达进化率通常可能早于性别偏向的进化。