Adaptive Bird-like Genome Miniaturization During the Evolution of Scallop Swimming Lifestyle
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...
| Main Authors: | , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2022-12-01
|
| Series: | Genomics, Proteomics & Bioinformatics |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S1672022922000857 |
| _version_ | 1797328341442756608 |
|---|---|
| author | Yuli Li Yaran Liu Hongwei Yu Fuyun Liu Wentao Han Qifan Zeng Yuehuan Zhang Lingling Zhang Jingjie Hu Zhenmin Bao Shi Wang |
| author_facet | Yuli Li Yaran Liu Hongwei Yu Fuyun Liu Wentao Han Qifan Zeng Yuehuan Zhang Lingling Zhang Jingjie Hu Zhenmin Bao Shi Wang |
| author_sort | Yuli Li |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-03-08T06:49:30Z |
| format | Article |
| id | doaj.art-cae53f85d2164ab4899eec6687432b38 |
| institution | Directory Open Access Journal |
| issn | 1672-0229 |
| language | English |
| last_indexed | 2024-03-08T06:49:30Z |
| publishDate | 2022-12-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Genomics, Proteomics & Bioinformatics |
| spelling | doaj.art-cae53f85d2164ab4899eec6687432b382024-02-03T07:18:52ZengElsevierGenomics, Proteomics & Bioinformatics1672-02292022-12-0120610661077Adaptive Bird-like Genome Miniaturization During the Evolution of Scallop Swimming LifestyleYuli Li0Yaran Liu1Hongwei Yu2Fuyun Liu3Wentao Han4Qifan Zeng5Yuehuan Zhang6Lingling Zhang7Jingjie Hu8Zhenmin Bao9Shi Wang10Sars-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, ChinaSars-Fang Centre & MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaSars-Fang Centre & MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaSars-Fang Centre & MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaSars-Fang Centre & MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaSars-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 Fisheries Science and Food Production Processes, Pilot Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China; Key Laboratory of Tropical Aquatic Germplasm of Hainan Province, Sanya Oceanographic Institution, Ocean University of China, Sanya 572000, ChinaCAS Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, ChinaSars-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, ChinaSars-Fang Centre & MOE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of China, Qingdao 266003, China; Key Laboratory of Tropical Aquatic Germplasm of Hainan Province, Sanya Oceanographic Institution, Ocean University of China, Sanya 572000, ChinaSars-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 Fisheries Science and Food Production Processes, Pilot Qingdao National Laboratory for Marine Science and Technology, Qingdao 266237, China; Key Laboratory of Tropical Aquatic Germplasm of Hainan Province, Sanya Oceanographic Institution, Ocean University of China, Sanya 572000, ChinaSars-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; Key Laboratory of Tropical Aquatic Germplasm of Hainan Province, Sanya Oceanographic Institution, Ocean University of China, Sanya 572000, China; Corresponding author.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.http://www.sciencedirect.com/science/article/pii/S1672022922000857Genome sizeLifestyle evolutionGenome sequencingScallopBird |
| spellingShingle | Yuli Li Yaran Liu Hongwei Yu Fuyun Liu Wentao Han Qifan Zeng Yuehuan Zhang Lingling Zhang Jingjie Hu Zhenmin Bao Shi Wang Adaptive Bird-like Genome Miniaturization During the Evolution of Scallop Swimming Lifestyle Genomics, Proteomics & Bioinformatics Genome size Lifestyle evolution Genome sequencing Scallop Bird |
| title | Adaptive Bird-like Genome Miniaturization During the Evolution of Scallop Swimming Lifestyle |
| title_full | Adaptive Bird-like Genome Miniaturization During the Evolution of Scallop Swimming Lifestyle |
| title_fullStr | Adaptive Bird-like Genome Miniaturization During the Evolution of Scallop Swimming Lifestyle |
| title_full_unstemmed | Adaptive Bird-like Genome Miniaturization During the Evolution of Scallop Swimming Lifestyle |
| title_short | Adaptive Bird-like Genome Miniaturization During the Evolution of Scallop Swimming Lifestyle |
| title_sort | adaptive bird like genome miniaturization during the evolution of scallop swimming lifestyle |
| topic | Genome size Lifestyle evolution Genome sequencing Scallop Bird |
| url | http://www.sciencedirect.com/science/article/pii/S1672022922000857 |
| work_keys_str_mv | AT yulili adaptivebirdlikegenomeminiaturizationduringtheevolutionofscallopswimminglifestyle AT yaranliu adaptivebirdlikegenomeminiaturizationduringtheevolutionofscallopswimminglifestyle AT hongweiyu adaptivebirdlikegenomeminiaturizationduringtheevolutionofscallopswimminglifestyle AT fuyunliu adaptivebirdlikegenomeminiaturizationduringtheevolutionofscallopswimminglifestyle AT wentaohan adaptivebirdlikegenomeminiaturizationduringtheevolutionofscallopswimminglifestyle AT qifanzeng adaptivebirdlikegenomeminiaturizationduringtheevolutionofscallopswimminglifestyle AT yuehuanzhang adaptivebirdlikegenomeminiaturizationduringtheevolutionofscallopswimminglifestyle AT linglingzhang adaptivebirdlikegenomeminiaturizationduringtheevolutionofscallopswimminglifestyle AT jingjiehu adaptivebirdlikegenomeminiaturizationduringtheevolutionofscallopswimminglifestyle AT zhenminbao adaptivebirdlikegenomeminiaturizationduringtheevolutionofscallopswimminglifestyle AT shiwang adaptivebirdlikegenomeminiaturizationduringtheevolutionofscallopswimminglifestyle |