Department of Ecology and Evolutionary Biology, University of Toronto, ON, Canada.
Genome Biol Evol. 2023 Apr 6;15(4). doi: 10.1093/gbe/evad055.
The world's astounding biodiversity results from speciation, the process of formation of distinct species. Hybrids between species often have reduced fitness due to negative epistatic interactions between divergent genetic factors, as each lineage accumulated substitutions independently in their evolutionary history. Such negative genetic interactions can manifest as gene misexpression due to divergence in gene regulatory controls from mutations in cis-regulatory elements and trans-acting factors. Gene misexpression due to differences in regulatory controls can ultimately contribute to incompatibility within hybrids through developmental defects such as sterility and inviability. We sought to quantify the contributions of regulatory divergence to postzygotic reproductive isolation using sterile interspecies hybrids of two Caenorhabditis nematodes: Caenorhabditis briggsae and Caenorhabditis nigoni. We analyzed previous transcriptome profiles for two introgression lines with distinct homozygous X-linked fragments from C. briggsae in a C. nigoni genomic background that confers male sterility, owing to defects in spermatogenesis (Li R, et al. 2016. Specific down-regulation of spermatogenesis genes targeted by 22G RNAs in hybrid sterile males associated with an X-chromosome introgression. Genome Res. 26:1219-1232). Our analysis identified hundreds of genes that show distinct classes of nonadditive expression inheritance and regulatory divergence. We find that these nonoverlapping introgressions affect many of the same genes in the same way and demonstrate that the preponderance of transgressive gene expression is due to regulatory divergence involving compensatory and joint effects of cis- and trans-acting factors. The similar transcriptomic responses to nonoverlapping genetic perturbations of the X-chromosome implicate multiway incompatibilities as an important feature contributing to hybrid male sterility in this system.
世界上令人惊叹的生物多样性是由物种形成（形成不同物种的过程）产生的。由于物种间杂交的负上位性相互作用，不同遗传因素之间的差异，以及每个谱系在其进化历史中独立积累替代，杂交种的适应性通常会降低。这种负遗传相互作用可能表现为由于顺式调控元件和反式作用因子突变导致基因调控控制的差异而导致基因表达错误。由于调控控制的差异导致的基因表达错误最终可能导致杂种的不兼容性，例如不育和不能存活。我们试图使用两种秀丽隐杆线虫 Caenorhabditis briggsae 和 Caenorhabditis nigoni 的不育种间杂种来量化调节分歧对合子后生殖隔离的贡献。我们分析了先前的转录组图谱，这些图谱是两个具有不同纯合性 X 连锁片段的导入系的图谱，这些片段来自 C. briggsae 在 C. nigoni 基因组背景中，由于精子发生缺陷而导致雄性不育（Li R，等。2016 年。杂种不育雄性中 22G RNA 靶向的精子发生基因的特异性下调与 X 染色体导入有关。基因组研究。26：1219-1232）。我们的分析确定了数百个表现出不同类别的非加性表达遗传和调节分歧的基因。我们发现这些不重叠的导入以相同的方式影响许多相同的基因，并证明大多数基因的转录超过是由于涉及顺式和反式作用因子的补偿和联合效应的调节分歧。X 染色体非重叠遗传扰动的相似转录组反应表明多方式不兼容性是导致该系统杂种雄性不育的一个重要特征。
