Ant phylogenomics reveals a natural selection hotspot preceding the origin of complex eusociality

Ant phylogenomics reveals a natural selection hotspot preceding the origin of complex eusociality
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DOI:
10.1016/j.cub.2022.05.001
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发表时间:
2022-07-11
期刊:
影响因子:
9.2
通讯作者:
Keller, Laurent
Keller, Laurent
中科院分区:
生物学1区
文献类型:
--
作者:
Romiguier, Jonathan;Borowiec, Marek L.;Keller, Laurent

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群居性的进化使蚂蚁成为世界上最引人注目和生态优势的生物群体之一。目前的14000种蚂蚁中,绝大多数属于蚁类,(1)一个由9个亚科组成的分支,表现出最极端的生殖劳动分工、大的群体规模、(2)工蚁多态性、(3)和延长的蚁后寿命。(4)其余8个非蚁类亚科的研究较少,迄今为止基因组测序较少,系统发育关系不明确。(5)通过对65个基因组进行测序,我们提供了17个蚂蚁亚科的强大系统发育,为有争议的瘦蚁进化支(Leptanillinae和Martialinae)作为所有其他现存蚂蚁的姐妹群获得了高度支持。此外,我们的基因组分析显示,类甲酸虫的出现伴随着积极选择事件的增加。重要的是,在选择过程中,前三种基因功能与复杂的群居性的关键特征有关,组蛋白乙酰化与种姓分化有关,RNA基因沉默与工蜂不育有关,自噬与长寿有关。这些结果表明,与真社会性相关的关键途径在白垩纪经历了强烈的选择,表明复杂的真社会性的分子基础可能在不到20 Ma的时间内迅速进化。
The evolution of eusociality has allowed ants to become one of the most conspicuous and ecologically dominant groups of organisms in the world. A large majority of the current similar to 14,000 ant species belong to the formicoids,(1) a clade of nine subfamilies that exhibit the most extreme forms of reproductive division of labor, large colony size,(2) worker polymorphism,(3) and extended queen longevity.(4) The eight remaining non-formicoid subfamilies are less well studied, with few genomes having been sequenced so far and unclear phylogenetic relationships.(5) By sequencing 65 genomes, we provide a robust phylogeny of the 17 ant subfamilies, retrieving high support to the controversial leptanillomorph clade (Leptanillinae and Martialinae) as the sister group to all other extant ants. Moreover, our genomic analyses revealed that the emergence of the formicoids was accompanied by an elevated number of positive selection events. Importantly, the top three gene functions under selection are linked to key features of complex eusociality, with histone acetylation being implicated in caste differentiation, gene silencing by RNA in worker sterility, and autophagy in longevity. These results show that the key pathways associated with eusociality have been under strong selection during the Cretaceous, suggesting that the molecular foundations of complex eusociality may have evolved rapidly in less than 20 Ma.