An Ancient and Eroded Social Supergene Is Widespread across Formica Ants

An Ancient and Eroded Social Supergene Is Widespread across Formica Ants
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DOI:
10.1016/j.cub.2019.11.032
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发表时间:
2020-01-20
期刊:
影响因子:
9.2
通讯作者:
Chapuisat, Michel
Chapuisat, Michel
中科院分区:
生物学1区
文献类型:
--
作者:
Brelsford, Alan;Purcell, Jessica;Chapuisat, Michel

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超基因,紧密连接的基因簇,在复杂适应性变异的进化中起着关键作用[1,2]。虽然在许多物种中已经发现了超基因,但我们对它们的起源、进化和持久性仍缺乏了解。在这里,我们发现了一个与多态社会组织相关的20-40 Ma的超基因进化史。我们发现,5个福米卡物种在3号染色体上表现出跨越11 Mbp的同源发散单倍型。尽管超基因的大小,只有142个单核苷酸多态性(SNPs)在所有五个物种中一致地区分不同的超基因单倍型。这些保守的跨物种snp定位在分布在超基因上的少数不相交的簇中。这种意想不到的分化模式表明,福米卡表基因并不遵循性染色体进化的标准模型,在标准模型中,不同的进化层反映了一个扩大的抑制重组[5]区域。我们提出了另一种“侵蚀地层模型”,其中保守的跨物种snp集群代表了在面对祖先单倍型之间罕见的重组时通过选择维持的功能重要区域。对另外10个福米卡物种的全基因组序列的比较表明,该超基因最保守的区域包含一个对果蝇[6]运动神经元发育至关重要的转录因子。这个庞大而古老的超基因中有一小部分含有与群体社会组织有关的保守的跨物种单倍型,这一发现表明,祖先的单倍型已经被重组所侵蚀,选择保留了一个或几个基因的分化,产生了替代的社会组织。
Supergenes, clusters of tightly linked genes, play a key role in the evolution of complex adaptive variation [1, 2]. Although supergenes have been identified in many species, we lack an understanding of their origin, evolution, and persistence [3]. Here, we uncover 20-40 Ma of evolutionary history of a supergene associated with polymorphic social organization in Formica ants [4]. We show that five Formica species exhibit homologous divergent haplotypes spanning 11 Mbp on chromosome 3. Despite the supergene's size, only 142 single nucleotide polymorphisms (SNPs) consistently distinguish alternative supergene haplotypes across all five species. These conserved trans-species SNPs are localized in a small number of disjunct clusters distributed across the supergene. This unexpected pattern of divergence indicates that the Formica supergene does not follow standard models of sex chromosome evolution, in which distinct evolutionary strata reflect an expanding region of suppressed recombination [5]. We propose an alternative "eroded strata model'' in which clusters of conserved trans-species SNPs represent functionally important areas maintained by selection in the face of rare recombination between ancestral haplotypes. The comparison of whole-genome sequences across 10 additional Formica species reveals that the most conserved region of the supergene contains a transcription factor essential for motor neuron development in Drosophila [6]. The discovery that a very small portion of this large and ancient supergene harbors conserved trans-species SNPs linked to colony social organization suggests that the ancestral haplotypes have been eroded by recombination, with selection preserving differentiation at one or a few genes generating alternative social organization.