Patterns and Processes of Genomic Evolution Inferred From the Ten Smallest Vertebrate Genomes

Pufferfish exhibit the smallest vertebrate genomes, making them ideal models for investigating evolutionary patterns and processes that affect genome size. While the Takifugu rubripes genome was fully sequenced two decades ago, key evolutionary drivers remain elusive. We sequenced 10 pufferfish genomes and generated 35 transcriptomes and 13 methylomes to understand genomic evolutionary mechanisms. Comparative genomics revealed that transposable element suppression-rather than lineage-specific conserved element loss-primarily underlies genome compaction. This is mediated by reductions in transposon-associated enzymes that limit transposable element propagation and modify DNA repair mechanisms that promote genomic streamlining. Based on resolved phylogeny among nine Takifugu, it is found that introgression drives speciation of T. niphobles and T. oblongus, while long-term linked selection dominates divergence in other species. Positive selection analyses highlighted mechanotransduction pathway genes (integrins, ion channel transport) that are functionally convergent with mammalian lung cell mechanisms, potentially supporting inflation-based anti-predatory strategies. Additionally, positive selection variants in genes that control lineage-specific skin patterning and coloration, which are either selected for or are rewired in regulatory processes, might suggest a role for pigmentation during the rapid speciation of this lineage. This findings shed light on mechanisms enabling extreme vertebrate genome compaction and provide insights for genome engineering applications.

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Publication Details

Journal
Advanced Science
Published
2025-09-10
DOI
https://doi.org/10.1002/advs.202417251
Citations
1
Primary Topic
Genomics and Phylogenetic Studies
Type
article
Field-Weighted Citation Impact
0.81

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Patterns and Processes of Genomic Evolution Inferred From the Ten Smallest Vertebrate Genomes

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Patterns and Processes of Genomic Evolution Inferred From the Ten Smallest Vertebrate Genomes

Lingfeng Meng, Minna Taipale, Yangqing Zhang, Lucas Benites Doretto, Manfred Schartl, Yating Qin, Changwei Shao, Guangyi Fan, Kaiqiang Liu, Qian Wang, Qian Liu, Hongyan Wang, Shuo Li, Jilin Zhang, Yuyan Liu, Weijing Li, Shan-Shan Pan, Mengqi Zhang, Shanshan Liu, Ning Wang, Axel Meyer, Shenglei Han, Fengtao Gao
article en
1 citations

Abstract

Pufferfish exhibit the smallest vertebrate genomes, making them ideal models for investigating evolutionary patterns and processes that affect genome size. While the Takifugu rubripes genome was fully sequenced two decades ago, key evolutionary drivers remain elusive. We sequenced 10 pufferfish genomes and generated 35 transcriptomes and 13 methylomes to understand genomic evolutionary mechanisms. Comparative genomics revealed that transposable element suppression-rather than lineage-specific conserved element loss-primarily underlies genome compaction. This is mediated by reductions in transposon-associated enzymes that limit transposable element propagation and modify DNA repair mechanisms that promote genomic streamlining. Based on resolved phylogeny among nine Takifugu, it is found that introgression drives speciation of T. niphobles and T. oblongus, while long-term linked selection dominates divergence in other species. Positive selection analyses highlighted mechanotransduction pathway genes (integrins, ion channel transport) that are functionally convergent with mammalian lung cell mechanisms, potentially supporting inflation-based anti-predatory strategies. Additionally, positive selection variants in genes that control lineage-specific skin patterning and coloration, which are either selected for or are rewired in regulatory processes, might suggest a role for pigmentation during the rapid speciation of this lineage. This findings shed light on mechanisms enabling extreme vertebrate genome compaction and provide insights for genome engineering applications.

Advanced ScienceVol. 12(38)
BGI Group (China) (CN), Tung Wah College (HK), Harvard University (US), City University of Hong Kong (HK), University of Konstanz (DE), Chinese Academy of Sciences (CN), University of Cambridge (GB), University of Würzburg (DE), Karolinska Institutet (SE), Institute of Oceanology (CN), South China Sea Institute Of Oceanology (CN), City University of Hong Kong, Shenzhen Research Institute (CN), Qingdao National Laboratory for Marine Science and Technology (CN), Weifang University of Science and Technology (CN), Qingdao Center of Resource Chemistry and New Materials (CN), Chinese Academy of Fishery Sciences (CN), Weifang University (CN)
City University of Hong Kong, Karolinska Institutet, Knut och Alice Wallenbergs Stiftelse, Natural Science Foundation of Shandong Province, National Key Research and Development Program of China, Central Public-interest Scientific Institution Basal Research Fund, Chinese Academy of Fishery Sciences
Openalex Percentile: Top 24%
Genomics and Phylogenetic Studies
0.81
DOIOpen Access PDFOpenAlex
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