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Accelerated evolution of an Lhx2 enhancer shapes mammalian social hierarchies.
Cell Research ( IF 28.1 ) Pub Date : 2020-04-01 , DOI: 10.1038/s41422-020-0308-7 Yuting Wang 1, 2 , Guangyi Dai 1 , Zhili Gu 1 , Guopeng Liu 1, 2 , Ke Tang 3 , Yi-Hsuan Pan 4 , Yujie Chen 5 , Xin Lin 1, 2 , Nan Wu 4 , Haoshan Chen 2, 6 , Su Feng 2, 7 , Shou Qiu 2, 6 , Hongduo Sun 1, 2 , Qian Li 1 , Chuan Xu 1 , Yanan Mao 2, 8 , Yong Edward Zhang 2, 8, 9 , Philipp Khaitovich 1, 9 , Yan-Ling Wang 10 , Qunxiu Liu 11 , Jing-Dong Jackie Han 1 , Zhen Shao 1 , Gang Wei 1 , Chun Xu 6 , Naihe Jing 7 , Haipeng Li 1, 9
Cell Research ( IF 28.1 ) Pub Date : 2020-04-01 , DOI: 10.1038/s41422-020-0308-7 Yuting Wang 1, 2 , Guangyi Dai 1 , Zhili Gu 1 , Guopeng Liu 1, 2 , Ke Tang 3 , Yi-Hsuan Pan 4 , Yujie Chen 5 , Xin Lin 1, 2 , Nan Wu 4 , Haoshan Chen 2, 6 , Su Feng 2, 7 , Shou Qiu 2, 6 , Hongduo Sun 1, 2 , Qian Li 1 , Chuan Xu 1 , Yanan Mao 2, 8 , Yong Edward Zhang 2, 8, 9 , Philipp Khaitovich 1, 9 , Yan-Ling Wang 10 , Qunxiu Liu 11 , Jing-Dong Jackie Han 1 , Zhen Shao 1 , Gang Wei 1 , Chun Xu 6 , Naihe Jing 7 , Haipeng Li 1, 9
Affiliation
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Social hierarchies emerged during evolution, and social rank influences behavior and health of individuals. However, the evolutionary mechanisms of social hierarchy are still unknown in amniotes. Here we developed a new method and performed a genome-wide screening for identifying regions with accelerated evolution in the ancestral lineage of placental mammals, where mammalian social hierarchies might have initially evolved. Then functional analyses were conducted for the most accelerated region designated as placental-accelerated sequence 1 (PAS1, P = 3.15 × 10-18). Multiple pieces of evidence show that PAS1 is an enhancer of the transcription factor gene Lhx2 involved in brain development. PAS1s isolated from various amniotes showed different cis-regulatory activity in vitro, and affected the expression of Lhx2 differently in the nervous system of mouse embryos. PAS1 knock-out mice lack social stratification. PAS1 knock-in mouse models demonstrate that PAS1s determine the social dominance and subordinate of adult mice, and that social ranks could even be turned over by mutated PAS1. All homozygous mutant mice had normal huddled sleeping behavior, motor coordination and strength. Therefore, PAS1-Lhx2 modulates social hierarchies and is essential for establishing social stratification in amniotes, and positive Darwinian selection on PAS1 plays pivotal roles in the occurrence of mammalian social hierarchies.
中文翻译：
Lhx2 增强子的加速进化塑造了哺乳动物的社会等级制度。
社会等级制度在进化过程中出现，社会等级影响个人的行为和健康。然而，羊膜动物的社会等级进化机制仍然未知。在这里，我们开发了一种新方法，并进行了全基因组筛选，以识别胎盘哺乳动物祖先谱系中加速进化的区域，哺乳动物的社会等级制度可能最初是在这些区域进化的。然后对指定为胎盘加速序列 1 (PAS1, P = 3.15 × 10-18) 的加速最快区域进行功能分析。多项证据表明，PAS1 是参与大脑发育的转录因子基因 Lhx2 的增强子。从不同羊膜动物中分离的PAS1在体外表现出不同的顺式调节活性，并且对小鼠胚胎神经系统中Lhx2的表达产生不同的影响。PAS1 基因敲除小鼠缺乏社会分层。PAS1敲入小鼠模型表明，PAS1决定成年小鼠的社会支配地位和从属地位，甚至突变的PAS1还可以改变社会地位。所有纯合突变小鼠均具有正常的蜷缩睡眠行为、运动协调性和力量。因此，PAS1-Lhx2调节社会等级，对于羊膜动物社会分层的建立至关重要，而PAS1的正向达尔文选择在哺乳动物社会等级的发生中起着关键作用。
更新日期：2020-04-24
中文翻译：
Lhx2 增强子的加速进化塑造了哺乳动物的社会等级制度。
社会等级制度在进化过程中出现，社会等级影响个人的行为和健康。然而，羊膜动物的社会等级进化机制仍然未知。在这里，我们开发了一种新方法，并进行了全基因组筛选，以识别胎盘哺乳动物祖先谱系中加速进化的区域，哺乳动物的社会等级制度可能最初是在这些区域进化的。然后对指定为胎盘加速序列 1 (PAS1, P = 3.15 × 10-18) 的加速最快区域进行功能分析。多项证据表明，PAS1 是参与大脑发育的转录因子基因 Lhx2 的增强子。从不同羊膜动物中分离的PAS1在体外表现出不同的顺式调节活性，并且对小鼠胚胎神经系统中Lhx2的表达产生不同的影响。PAS1 基因敲除小鼠缺乏社会分层。PAS1敲入小鼠模型表明，PAS1决定成年小鼠的社会支配地位和从属地位，甚至突变的PAS1还可以改变社会地位。所有纯合突变小鼠均具有正常的蜷缩睡眠行为、运动协调性和力量。因此，PAS1-Lhx2调节社会等级，对于羊膜动物社会分层的建立至关重要，而PAS1的正向达尔文选择在哺乳动物社会等级的发生中起着关键作用。
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