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 11;19(1):53. doi: 10.1186/s12862-019-1363-x.
Germ lines are the cell lineages that give rise to the sperm and eggs in animals. The germ lines first arise from primordial germ cells (PGCs) during embryogenesis: these form from either a presumed derived mode of preformed germ plasm (inheritance) or from an ancestral mechanism of inductive cell-cell signalling (induction). Numerous genes involved in germ line specification and development have been identified and functionally studied. However, little is known about the molecular evolutionary dynamics of germ line genes in metazoan model systems.
Here, we studied the molecular evolution of germ line genes within three metazoan model systems. These include the genus Drosophila (N=34 genes, inheritance), the fellow insect Apis (N=30, induction), and their more distant relative Caenorhabditis (N=23, inheritance). Using multiple species and established phylogenies in each genus, we report that germ line genes exhibited marked variation in the constraint on protein sequence divergence (dN/dS) and codon usage bias (CUB) within each genus. Importantly, we found that de novo lineage-specific inheritance (LSI) genes in Drosophila (osk, pgc) and in Caenorhabditis (pie-1, pgl-1), which are essential to germ plasm functions under the derived inheritance mode, displayed rapid protein sequence divergence relative to the other germ line genes within each respective genus. We show this may reflect the evolution of specialized germ plasm functions and/or low pleiotropy of LSI genes, features not shared with other germ line genes. In addition, we observed that the relative ranking of dN/dS and of CUB between genera were each more strongly correlated between Drosophila and Caenorhabditis, from different phyla, than between Drosophila and its insect relative Apis, suggesting taxonomic differences in how germ line genes have evolved.
Taken together, the present results advance our understanding of the evolution of animal germ line genes within three well-known metazoan models. Further, the findings provide insights to the molecular evolution of germ line genes with respect to LSI status, pleiotropy, adaptive evolution as well as PGC-specification mode.
生殖细胞系是产生动物精子和卵子的细胞谱系。生殖细胞系最初是在胚胎发生过程中从原始生殖细胞（PGC）中产生的：这些细胞要么来自假定的预先形成的生殖质的衍生模式（遗传），要么来自诱导细胞-细胞信号的祖先机制（诱导）。已经鉴定出许多参与生殖系指定和发育的基因，并对其进行了功能研究。然而，关于后生动物模型系统中生殖系基因的分子进化动态知之甚少。
在这里，我们研究了三个后生动物模型系统中生殖系基因的分子进化。这些包括果蝇属（N=34 个基因，遗传）、同种昆虫蜜蜂（N=30 个，诱导）及其更远的亲缘关系秀丽隐杆线虫（N=23 个，遗传）。我们使用多个物种和每个属中的已建立的系统发育，报告说生殖系基因在每个属内的蛋白质序列分歧（dN/dS）和密码子使用偏性（CUB）的约束方面表现出明显的变化。重要的是，我们发现果蝇中的从头谱系特异性遗传（LSI）基因（osk、pgc）和秀丽隐杆线虫中的（pie-1、pgl-1），它们是衍生遗传模式下生殖质功能所必需的，与各自属内的其他生殖系基因相比，蛋白质序列迅速进化。我们表明，这可能反映了专门的生殖质功能的进化和/或 LSI 基因的低多效性，这些特征与其他生殖系基因不同。此外，我们观察到，在不同门的果蝇和秀丽隐杆线虫之间，dN/dS 和 CUB 的相对排名比在果蝇和其昆虫亲缘关系蜜蜂之间更为相关，这表明生殖系基因进化的分类学差异。
总之，目前的结果提高了我们对三个著名后生动物模型中动物生殖系基因进化的理解。此外，这些发现为 LSI 状态、多效性、适应性进化以及 PGC 特异性模式的生殖系基因的分子进化提供了见解。
