Sars-Fang Centre & MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China; Laboratory for Marine Biology and Biotechnology, Pilot Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China.
Sars-Fang Centre & MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China.
Genomics Proteomics Bioinformatics. 2022 Dec;20(6):1066-1077. doi: 10.1016/j.gpb.2022.07.001. Epub 2022 Jul 26.
Genome miniaturization drives key evolutionary innovations of adaptive traits in vertebrates, such as the flight evolution of birds. However, whether similar evolutionary processes exist in invertebrates remains poorly understood. Derived from the second-largest animal phylum, scallops are a special group of bivalve molluscs and acquire the evolutionary novelty of the swimming lifestyle, providing excellent models for investigating the coordinated genome and lifestyle evolution. Here, we show for the first time that genome sizes of scallops exhibit a generally negative correlation with locomotion activity. To elucidate the co-evolution of genome size and swimming lifestyle, we focus on the Asian moon scallop (Amusium pleuronectes) that possesses the smallest known scallop genome while being among scallops with the highest swimming activity. Whole-genome sequencing of A. pleuronectes reveals highly conserved chromosomal macrosynteny and microsynteny, suggestive of a highly contracted but not degenerated genome. Genome reduction of A. pleuronectes is facilitated by significant inactivation of transposable elements, leading to reduced gene length, elevated expression of genes involved in energy-producing pathways, and decreased copy numbers and expression levels of biomineralization-related genes. Similar evolutionary changes of relevant pathways are also observed for bird genome reduction with flight evolution. The striking mimicry of genome miniaturization underlying the evolution of bird flight and scallop swimming unveils the potentially common, pivotal role of genome size fluctuation in the evolution of novel lifestyles in the animal kingdom.
基因组小型化驱动了脊椎动物适应性状的关键进化创新，如鸟类的飞行进化。然而，无脊椎动物是否存在类似的进化过程还知之甚少。扇贝起源于第二大动物门，是双壳类软体动物中的一个特殊群体，它们获得了游泳生活方式的进化新颖性，为研究协调的基因组和生活方式进化提供了极好的模型。在这里，我们首次表明，扇贝的基因组大小与运动活性呈普遍负相关。为了阐明基因组大小和游泳生活方式的协同进化，我们专注于亚洲日月贝（Amusium pleuronectes），它拥有已知最小的扇贝基因组，同时也是扇贝中游泳活性最高的一种。A. pleuronectes 的全基因组测序揭示了高度保守的染色体宏同线性和微同线性，表明基因组高度收缩但没有退化。A. pleuronectes 的基因组减少是由转座元件的显著失活促成的，导致基因长度缩短，参与能量产生途径的基因表达水平升高，以及与生物矿化相关的基因的拷贝数和表达水平降低。在鸟类飞行进化导致的鸟类基因组减少中，也观察到了相关途径的类似进化变化。鸟类飞行进化和扇贝游泳进化所涉及的基因组小型化的惊人相似性揭示了基因组大小波动在动物王国中新型生活方式进化中的潜在共同关键作用。
