Department of Biological Sciences, Texas Tech University, Lubbock, TX, USA.
Department of Cell Biology and Biochemistry, Texas Tech University Health Sciences Center, Lubbock, TX, USA.
Genome Biol. 2022 Jul 11;23(1):155. doi: 10.1186/s13059-022-02721-y.
Speciation genes contribute disproportionately to species divergence, but few examples exist, especially in vertebrates. Here we test whether Zan, which encodes the sperm acrosomal protein zonadhesin that mediates species-specific adhesion to the egg's zona pellucida, is a speciation gene in placental mammals.
Genomic ontogeny reveals that Zan arose by repurposing of a stem vertebrate gene that was lost in multiple lineages but retained in Eutheria on acquiring a function in egg recognition. A 112-species Zan sequence phylogeny, representing 17 of 19 placental Orders, resolves all species into monophyletic groups corresponding to recognized Orders and Suborders, with <5% unsupported nodes. Three other rapidly evolving germ cell genes (Adam2, Zp2, and Prm1), a paralogous somatic cell gene (TectA), and a mitochondrial gene commonly used for phylogenetic analyses (Cytb) all yield trees with poorer resolution than the Zan tree and inferior topologies relative to a widely accepted mammalian supertree. Zan divergence by intense positive selection produces dramatic species differences in the protein's properties, with ordinal divergence rates generally reflecting species richness of placental Orders consistent with expectations for a speciation gene that acts across a wide range of taxa. Furthermore, Zan's combined phylogenetic utility and divergence exceeds those of all other genes known to have evolved in Eutheria by positive selection, including the only other mammalian speciation gene, Prdm9.
Species-specific egg recognition conferred by Zan's functional divergence served as a mode of prezygotic reproductive isolation that promoted the extraordinary adaptive radiation and success of Eutheria.
物种形成基因在物种分化中起着不成比例的作用，但很少有例子存在，尤其是在脊椎动物中。在这里，我们测试了 Zan 是否是胎盘哺乳动物中的一个物种形成基因，Zan 编码的精子顶体蛋白 zonadhesin 介导了与卵透明带的种间特异性结合。
基因组发生揭示了 Zan 是通过重新利用一个在多个谱系中丢失但在获得卵识别功能的 Eutheria 中保留的脊椎动物基因产生的。代表 19 个胎盘类中的 17 个的 112 种 Zan 序列系统发育树，将所有物种解析为与公认的类群和亚类相对应的单系群，无支持的节点<5%。其他三个快速进化的生殖细胞基因（Adam2、Zp2 和 Prm1）、一个同源体细胞基因（TectA）和一个常用于系统发育分析的线粒体基因（Cytb），其生成的树的分辨率均低于 Zan 树，并且相对于广泛接受的哺乳动物超级树，拓扑结构较差。Zan 的强烈正选择导致其蛋白性质发生了显著的物种差异，其进化率通常反映了胎盘类的物种丰富度，这与作为一个在广泛的分类群中起作用的物种形成基因的预期一致。此外，Zan 的综合系统发育功能和进化速度超过了通过正选择在 Eutheria 中进化的所有其他已知基因，包括唯一的另一个哺乳动物物种形成基因 Prdm9。
Zan 的功能分化导致的物种特异性卵识别作为一种种间生殖隔离的模式，促进了 Eutheria 的非凡适应性辐射和成功。
