State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, College of Plant Protection, Fujian Agriculture and Forestry University, Fuzhou, China.
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.
Mol Ecol Resour. 2024 Nov;24(8):e14019. doi: 10.1111/1755-0998.14019. Epub 2024 Sep 12.
The origin of sociality represents one of the most important evolutionary transitions. Insect sociality evolved in some hemipteran aphids, which can produce soldiers and normal nymphs with distinct morphology and behaviour through parthenogenesis. The lack of genomic data resources has hindered the investigations into molecular mechanisms underlying their social evolution. Herein, we generated the first chromosomal-level genome of a social hemipteran (Pseudoregma bambucicola) with highly specialized soldiers and performed comparative genomic and transcriptomic analyses to elucidate the molecular signatures and regulatory mechanisms of caste differentiation. P. bambucicola has a larger known aphid genome of 582.2 Mb with an N50 length of 11.24 Mb, and about 99.6% of the assembly was anchored to six chromosomes with a scaffold N50 of 98.27 Mb. A total of 14,027 protein-coding genes were predicted and 37.33% of the assembly were identified as repeat sequences. The social evolution is accompanied by a variety of changes in genome organization, including expansion of gene families related to transcription factors, transposable elements, as well as species-specific expansions of certain sugar transporters and UGPases involved in carbohydrate metabolism. We also characterized large candidate gene sets linked to caste differentiation and found evidence of expression regulation and positive selection acting on energy metabolism and muscle structure, explaining the soldier-specific traits including morphological and behavioural specialization, developmental arrest and infertility. Overall, this study offers new insights into the molecular basis of social aphids and the evolution of insect sociality and also provides valuable data resources for further comparative and functional studies.
社会性的起源代表了最重要的进化转变之一。昆虫的社会性起源于某些半翅目蚜虫中，它们可以通过孤雌生殖产生形态和行为明显不同的兵蚁和正常若虫。缺乏基因组数据资源阻碍了对其社会进化的分子机制的研究。在此，我们生成了第一个具有高度专业化兵蚁的社会性半翅目昆虫（Pseudoregma bambucicola）的染色体水平基因组，并进行了比较基因组和转录组分析，以阐明分群分化的分子特征和调控机制。P. bambucicola 具有已知的较大蚜虫基因组，大小为 582.2Mb，N50 长度为 11.24Mb，约 99.6%的组装被锚定到 6 条染色体上，支架 N50 为 98.27Mb。共预测到 14027 个蛋白质编码基因，组装的 37.33%被鉴定为重复序列。社会进化伴随着基因组组织的多种变化，包括与转录因子、转座元件相关的基因家族的扩张，以及参与碳水化合物代谢的某些糖转运体和 UGPase 的物种特异性扩张。我们还对与分群分化相关的大量候选基因集进行了特征描述，并发现了对能量代谢和肌肉结构有表达调控和正选择作用的证据，解释了兵蚁特有的特征，包括形态和行为专业化、发育停滞和不育。总的来说，这项研究为社会性蚜虫和昆虫社会性进化的分子基础提供了新的见解，并为进一步的比较和功能研究提供了有价值的数据集。
