Department of Evolutionary Biology, Uppsala University, Uppsala, Sweden.
Mol Biol Evol. 2013 Nov;30(11):2435-46. doi: 10.1093/molbev/mst143. Epub 2013 Aug 20.
Differential gene expression is believed to largely explain sexually dichotomous phenotypes. This phenomenon is especially significant in hermaphrodites, in which male and female sexual tissues have identical genotypes. Sex differences in transcription have been linked to molecular evolution: genes with higher expression in male compared with female sexual tissues (i.e., male-biased genes) have been associated with rapid gene divergence in various animals and plants, implying that selective differences exist among the sexual structures. In the present investigation, we examined expressed sequence tags, microarrays, and gene sequence data from the hermaphroditic fungus Neurospora crassa and confirmed selective differences of genes with disparate expression among male versus female sexual structures in this organism. The results held across various genotypes and stages of sexual development. Furthermore, our data showed that N. crassa comprises a rare example of an organism where female-biased genes evolve rapidly; they exhibited faster evolution at the protein level and reduced optimal codon usage compared with male-biased genes, sexually unbiased genes, and vegetative genes. Female-biased genes also had a greater portion of sites that experienced positive selection and showed stronger signals of selective sweeps than male-biased genes, suggesting that the rapid evolution is at least partly driven by adaptive evolution. Distinctive aspects of the reproductive biology of N. crassa which might explain the rapid evolution of female-biased genes are discussed, particularly the propensity for female-female competition during mating, as well as the multifunctional nature of male structures. The present findings open new opportunities to test hypotheses about sex-biased gene expression and molecular evolution.
差异基因表达被认为在很大程度上解释了两性异形表型。这种现象在雌雄同体中尤为显著，因为雄性和雌性生殖组织具有相同的基因型。转录中的性别差异与分子进化有关：与雌性生殖组织相比，在雄性中表达更高的基因（即雄性偏性基因）与各种动植物中快速的基因分化有关，这意味着性结构之间存在选择差异。在本研究中，我们检查了两性真菌 Neurospora crassa 的表达序列标签、微阵列和基因序列数据，并证实了在该生物体中，雄性与雌性生殖结构之间表达差异的基因存在选择差异。这些结果在各种基因型和性发育阶段都得到了验证。此外，我们的数据表明，Neurospora crassa 是一个罕见的快速进化的生物体，其中雌性偏性基因进化迅速；与雄性偏性基因、两性偏性基因和营养性基因相比，它们在蛋白质水平上的进化更快，最优密码子使用频率更低。雌性偏性基因中经历正选择的位点比例也更大，并且比雄性偏性基因表现出更强的选择清除信号，这表明快速进化至少部分是由适应性进化驱动的。我们讨论了 Neurospora crassa 生殖生物学的独特方面，这些方面可能解释了雌性偏性基因的快速进化，特别是在交配期间雌性之间竞争的倾向，以及雄性结构的多功能性。这些发现为测试关于性别偏性基因表达和分子进化的假设提供了新的机会。
