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

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Liu, Kaiqiang, Wang, Qian, Wang, Ning, Meng, Lingfeng, Li, Shuo, Wang, Hong‐Yan, Liu, Yuyan, Liu, Qian +15 more·2025·Advanced Science
DOI 10.1002/advs.202417251PMC PMC12520575
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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.

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  • Multiple loach (Cobitoidei) families have consistently small genome sizes, with several falling below or approaching the genome size of pufferfishes (346.5 to 385.0 Mb).

    “A particularly striking finding were the consistently small genome sizes observed across multiple loach (Cobitoidei) families (SI Appendix, Fig. S2): Balitoridae (347.9 to 537.5 Mb), Barbuccidae (379.5 Mb), Gastromyzontidae (411.6 to 474.3 Mb), Vaillantellidae (427.5 Mb), Serpenticobitidae (440.3 Mb), and Ellopostomatidae (452.7 Mb), with several falling below or approaching the genome size of puf”

    From Convergent genome streamlining accompanies independent miniaturization in the world’s smallest fishes (2026) · cites this paper as [31]

    The Results section (Genome Assembly, Annotation, and TAD Organization; page unavailable) reports pufferfish genome assemblies of 346.48–385.03 Mb, matching the comparison range. The paper does not report genome sizes for the listed loach families or establish that their genomes approach that range. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • Genome compaction has been documented across diverse vertebrate and invertebrate lineages irrespective of body size, with compact genomes consistently showing predictable signatures of repeat depletion and structural simplification.

    “Genome compaction has been documented across diverse vertebrate and invertebrate lineages irrespective of body size, with compact genomes consistently showing predictable signatures of repeat depletion and structural simplification (e.g., refs. 31, 55, and 56).”

    From Convergent genome streamlining accompanies independent miniaturization in the world’s smallest fishes (2026) · cites this paper as [31]

    The Results sections on functional composition and mechanisms preserving compactness (page not provided) report short introns in pufferfish and restrained transposable-element insertion in compact Takifugu genomes. They do not establish the claim across invertebrates, irrespective of body size, or show that repeat depletion and structural simplification are consistent signatures across compact genomes. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

  • Depletion of LTR elements and DNA transposons suggests either reduced transposition activity, increased elimination of newly inserted elements, or both, consistent with mechanisms proposed for genome compaction in other vertebrates with streamlined genomes.

    “Depletion of these elements suggests either reduced transposition activity, increased elimination of newly inserted elements, or both, consistent with mechanisms proposed for genome compaction in other vertebrates with streamlined genomes (31, 43, 53, 56).”

    From Convergent genome streamlining accompanies independent miniaturization in the world’s smallest fishes (2026) · cites this paper as [31]

    Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.

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  • Genome compaction in pufferfishes combines TE/repeat reduction via suppression of transposable-element activity along with genome-wide intron shortening rather than intron loss.

    “Genome compaction in pufferfishes likewise combines TE/repeat reduction via suppression of transposable-element activity (31) along with genome-wide intron shortening rather than intron loss (30, 31, 71)”

    From Convergent genome streamlining accompanies independent miniaturization in the world’s smallest fishes (2026) · cites this paper as [31]

    The Results sections on functional composition and genome compactness report that pufferfish have the shortest introns among vertebrates and that reduced TE propagation contributes to their compact genomes (page numbers unavailable). The copy does not establish that intron shortening occurred rather than intron loss. (LLM, conf=0.85)

    Experimental — accuracy not yet measured

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Authors
Liu, K., Wang, Q., Wang, N., Meng, L., Li, S., Wang, H., Liu, Y., Liu, Q., Zhang, Y., Doretto, L. B., Zhang, M., Qin, Y., Pan, S., Han, S., Li, W., Liu, S., Gao, F., Meyer, A., Taipale, J., Fan, G., Schartl, M., Zhang, J., & Shao, C.
Affiliations
  • Qingdao National Laboratory for Marine Science and Technology (CN)
  • Karolinska Institutet (SE)
  • BGI Group (China) (CN)
  • State Key Laboratory of Mariculture Biobreeding and Sustainable Goods Yellow Sea Fisheries Research Institute Chinese Academy of Fishery Sciences Qingdao Shandong 266071 China
  • BGI‐Qingdao BGI‐Shenzhen Qingdao Shandong 266555 China
  • Weifang University (CN)
  • Harvard University (US)
  • University of Cambridge (GB)
  • University of Würzburg (DE)
  • City University of Hong Kong (HK)
Corresponding author
  • Schartl, Manfred
  • Zhang, Jilin
  • Shao, Changwei
ORCID
Venue
Advanced Science
Publisher
Wiley
Published
2025-09-10
Volume
12
Issue
38
Pages
e17251-e17251
ISSN
2198-3844 (ISSN-L)
DOI
10.1002/advs.202417251
PMC
PMC12520575
OpenAlex
W4414083796
Cited by
3
References
0
Citations by year
2026: 3
FWCI
1.40
Type
journal article
Language
en
Open access
Licence
Locations
  • Advanced Science (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Apollo (University of Cambridge) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • KOPS (University of Konstanz) (submittedVersion, cc-by)
  • CityU Scholars (submittedVersion, cc-by)
Funders
  • City University of Hong Kong (9610580)
  • Karolinska Institutet
  • Knut och Alice Wallenbergs Stiftelse (2013.0088, KAW 2013.0088)
  • Natural Science Foundation of Shandong Province (ZR2024QC056)
  • National Key Research and Development Program of China (2023TD19, 2022YFD2400100, tstp20221149, 21326307D, 2022YFD2401500)
  • Central Public-interest Scientific Institution Basal Research Fund, Chinese Academy of Fishery Sciences (2023TD19, 2022YFD2400100, 2022XT0303, 21326307D)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genome Rearrangement Algorithms
Keywords
pufferfish, Takifugu, genome size reduction, genome compaction, transposable elements, transposon suppression, DNA methylation, DNA repair, comparative genomics, introgression, speciation, linked selection, positive selection, mechanotransduction, integrins, skin pigmentation, coloration, genome editing
MeSH terms
Animals, DNA Transposable Elements, Phylogeny, Selection, Genetic, Vertebrates, Genome, Evolution, Molecular, Genomics, Tetraodontiformes, Takifugu

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Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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