Hou Guan-Mei, Zhang Yao-Hua, Zhang Jian-Xu
The State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100101, China.
Curr Zool. 2022 Apr 22;69(2):143-155. doi: 10.1093/cz/zoac030. eCollection 2023 Apr.
Dominance relationships between males and their associated traits are usually heritable and have implications for sexual selection in animals. In particular, social dominance and its related male pheromones are heritable in inbred mice; thus, we wondered whether epigenetic changes due to altered levels of DNA methylation determine inheritance. Here, we used C57BL/6 male mice to establish a social dominance-subordination relationship through chronic dyadic encounters, and this relationship and pheromone covariation occurred in their offspring, indicative of heritability. Through transcriptome sequencing and whole-genome DNA methylation profiling of the sperm of both generations, we found that differential methylation of many genes was induced by social dominance-subordination in sires and could be passed on to the offspring. These methylated genes were mainly related to growth and development processes, neurodevelopment, and cellular transportation. The expression of the genes with similar functions in whole-genome methylation/bisulfite sequencing was also differentiated by social dominance-subordination, as revealed by RNA-seq. In particular, the gene , which regulates neural signaling, was differentially methylated and expressed in the sperm and medial prefrontal cortex in paired males before and after dominance-subordination establishment, suggesting the potential epigenetic control and inheritance of social dominance-related aggression. We suggest that social dominance might be passed on to male offspring through sperm DNA methylation and that the differences could potentially affect male competition in offspring by affecting the development of the nervous system.
雄性与其相关性状之间的优势关系通常是可遗传的，并且对动物的性选择有影响。特别是，社会优势及其相关的雄性信息素在近交系小鼠中是可遗传的；因此，我们想知道由于DNA甲基化水平改变而导致的表观遗传变化是否决定了遗传。在这里，我们使用C57BL/6雄性小鼠通过长期二元相遇建立社会优势-从属关系，并且这种关系和信息素协变在它们的后代中出现，表明具有遗传性。通过对两代小鼠精子进行转录组测序和全基因组DNA甲基化分析，我们发现许多基因的差异甲基化是由父代的社会优势-从属关系诱导产生的，并且可以传递给后代。这些甲基化基因主要与生长发育过程、神经发育和细胞运输有关。如RNA测序所示，在全基因组甲基化/亚硫酸氢盐测序中具有相似功能的基因的表达也因社会优势-从属关系而有所差异。特别是，调节神经信号的基因在优势-从属关系建立前后的配对雄性小鼠的精子和内侧前额叶皮质中存在差异甲基化和表达，这表明社会优势相关攻击行为存在潜在的表观遗传控制和遗传。我们认为社会优势可能通过精子DNA甲基化传递给雄性后代，并且这些差异可能通过影响神经系统的发育而潜在地影响后代中的雄性竞争。
