Genome of the green-head ant, Rhytidoponera metallica, reveals mechanisms of toxin evolution in a genetically hyper-diverse eusocial species

IF 10.1 1区 生物学 Q1 BIOTECHNOLOGY & APPLIED MICROBIOLOGY
Anders Isaksen, Pedro G. Nachtigall, Robin A. Araya, Jia Hao Beh, Samuel D. Robinson, Thomas F. Hansen, Eivind A. B. Undheim
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Abstract

While ants are textbook examples of eusocial animals in which altruistic behavior is maintained through kin selection, several ants form genetically diverse colonies that challenge this concept. One example is the Australian green-head ant (Rhytidoponera metallica) whose colonies harbor such extreme genetic variation that they have been speculated to represent an unstable form of eusociality. Yet, R. metallica is among the most successful ants on the Australian subcontinent. This success has been hypothesized to be partly due to the diverse venoms harbored within each colony. However, the genomic basis and evolutionary scenarios that maintain this toxin diversity remain unknown. To examine toxin genomic architecture, quantify individual-level genetic variation, and identify both proximate and ultimate mechanisms that have facilitated the toxin diversity in R. metallica, we generate a high-quality draft genome from a single worker. Most ectatotoxin genes are in clusters that contain evidence of multiple, complex gene-family expansions, some of which are likely explained by the presence of transposable elements. We also show that toxin regions of the genome exhibit elevated genetic variation despite being under strong selection and that this variation can translate to phenotypic diversity through toxin alleles with different functional properties. Taken together, our results point to classical gene duplication and diversification as the main evolutionary mechanism by which the main toxin family in ant venoms evolves, suggest toxin-gene functional diversification under frequency-dependent selection maintains colony-level venom hypervariability in R. metallica, and provide new insight into the role of multi-level selection in eusocial animals.
绿头蚁(Rhytidoponera metallica)的基因组揭示了一个遗传高度多样化的真社会物种的毒素进化机制
虽然蚂蚁是教科书上的社会性动物的例子,其中利他行为是通过近亲选择来维持的,但一些蚂蚁形成了基因多样化的群体,挑战了这一概念。其中一个例子是澳大利亚绿头蚁(Rhytidoponera metallica),它的种群有如此极端的遗传变异,以至于人们推测它们代表了一种不稳定的群居形式。然而,R. metallica是澳大利亚次大陆上最成功的蚂蚁之一。据推测,这种成功的部分原因是由于每个群体中隐藏着不同的毒液。然而,维持这种毒素多样性的基因组基础和进化情景仍然未知。为了检验毒素基因组结构,量化个体水平的遗传变异,并确定促进金属圆霉毒素多样性的近似和最终机制,我们从单个工蚁中生成了高质量的基因组草图。大多数膨胀毒素基因聚集在一起,包含多个复杂基因家族扩展的证据,其中一些可能是由转座因子的存在来解释的。我们还表明,尽管在强选择下,基因组的毒素区域表现出较高的遗传变异,这种变异可以通过具有不同功能特性的毒素等位基因转化为表型多样性。综上所述,我们的研究结果表明,经典的基因复制和多样化是蚂蚁毒液中主要毒素家族进化的主要进化机制,表明频率依赖选择下的毒素基因功能多样化维持了金属金蚁群体水平的毒液高度变异性,并为多层次选择在社会性动物中的作用提供了新的见解。
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来源期刊
Genome Biology
Genome Biology Biochemistry, Genetics and Molecular Biology-Genetics
CiteScore
21.00
自引率
3.30%
发文量
241
审稿时长
2 months
期刊介绍: Genome Biology stands as a premier platform for exceptional research across all domains of biology and biomedicine, explored through a genomic and post-genomic lens. With an impressive impact factor of 12.3 (2022),* the journal secures its position as the 3rd-ranked research journal in the Genetics and Heredity category and the 2nd-ranked research journal in the Biotechnology and Applied Microbiology category by Thomson Reuters. Notably, Genome Biology holds the distinction of being the highest-ranked open-access journal in this category. Our dedicated team of highly trained in-house Editors collaborates closely with our esteemed Editorial Board of international experts, ensuring the journal remains on the forefront of scientific advances and community standards. Regular engagement with researchers at conferences and institute visits underscores our commitment to staying abreast of the latest developments in the field.
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