Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Bunkyo-ku, Tokyo, 113-0032, Japan.
Fisheries Laboratory, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Hamamatsu, Shizuoka, 431-0214, Japan.
Evolution. 2021 Jan;75(1):176-194. doi: 10.1111/evo.14120. Epub 2020 Nov 30.
Hybridization between divergent lineages generates new allelic combinations. One mechanism that can hinder the formation of hybrid populations is mitonuclear incompatibility, that is, dysfunctional interactions between proteins encoded in the nuclear and mitochondrial genomes (mitogenomes) of diverged lineages. Theoretically, selective pressure due to mitonuclear incompatibility can affect genotypes in a hybrid population in which nuclear genomes and mitogenomes from divergent lineages admix. To directly and thoroughly observe this key process, we de novo sequenced the 747-Mb genome of the coastal goby, Chaenogobius annularis, and investigated its integrative genomic phylogeographics using RNA-sequencing, RAD-sequencing, genome resequencing, whole mitogenome sequencing, amplicon sequencing, and small RNA-sequencing. Chaenogobius annularis populations have been geographically separated into Pacific Ocean (PO) and Sea of Japan (SJ) lineages by past isolation events around the Japanese archipelago. Despite the divergence history and potential mitonuclear incompatibility between these lineages, the mitogenomes of the PO and SJ lineages have coexisted for generations in a hybrid population on the Sanriku Coast. Our analyses revealed accumulation of nonsynonymous substitutions in the PO-lineage mitogenomes, including two convergent substitutions, as well as signals of mitochondrial lineage-specific selection on mitochondria-related nuclear genes. Finally, our data implied that a microRNA gene was involved in resolving mitonuclear incompatibility. Our integrative genomic phylogeographic approach revealed that mitonuclear incompatibility can affect genome evolution in a natural hybrid population.
杂交种形成新的等位基因组合。一种可以阻碍杂种群体形成的机制是线粒体核不兼容，即来自不同谱系的核基因组和线粒体基因组（线粒体基因组）编码的蛋白质之间的功能失调相互作用。从理论上讲，由于线粒体核不兼容而产生的选择压力会影响来自不同谱系的核基因组和线粒体基因组混合的杂种群体中的基因型。为了直接和彻底地观察这一关键过程，我们从头测序了沿海虾虎鱼 Chaenogobius annularis 的 747-Mb 基因组，并使用 RNA-seq、RAD-seq、基因组重测序、全线粒体基因组测序、扩增子测序和小 RNA-seq 研究了其综合基因组系统地理学。过去，由于日本群岛周围的隔离事件，Chaenogobius annularis 种群在地理上已分为太平洋（PO）和日本海（SJ）两个谱系。尽管这些谱系之间存在分化历史和潜在的线粒体核不兼容，但 PO 和 SJ 谱系的线粒体基因组已经在三陆海岸的一个杂种群体中共存了几代。我们的分析揭示了 PO 谱系线粒体基因组中非同义替换的积累，包括两个趋同替换，以及线粒体相关核基因的线粒体谱系特异性选择的信号。最后，我们的数据表明一个 microRNA 基因参与了解决线粒体核不兼容。我们的综合基因组系统地理学方法表明，线粒体核不兼容会影响自然杂种群体中的基因组进化。
