Convergent Degenerated Regulatory Elements Associated with Limb Loss in Limbless Amphibians and Reptiles
Limbs are a defining characteristic of tetrapods, yet numerous taxa, primarily among amphibians and reptiles, have independently lost limbs as an adaptation to new ecological niches. To elucidate the genetic factors contributing to this convergent limb loss, we present a 12 Gb chromosome-level assembly of the Banna caecilian (Ichthyophis bannanicus), a limbless amphibian. Our comparative analysis, which includes the reconstruction of amphibian karyotype evolution, reveals constrained gene length evolution in a subset of developmental genes across 3 large genomes. Investigation of limb development genes uncovered the loss of Grem1 in caecilians and Tulp3 in snakes. Interestingly, caecilians and snakes share a significantly larger number of convergent degenerated conserved noncoding elements than limbless lizards, which have a shorter evolutionary history of limb loss. These convergent degenerated conserved noncoding elements overlap significantly with active genomic regions during mouse limb development and are conserved in limbed species, suggesting their essential role in limb patterning in the tetrapod common ancestor. While most convergent degenerated conserved noncoding elements emerged in the jawed vertebrate ancestor, coinciding with the origin of paired appendage, more recent degenerated conserved noncoding elements also contribute to limb development, as demonstrated through functional experiments. Our study provides novel insights into the regulatory elements associated with limb development and loss, offering an evolutionary perspective on the genetic basis of morphological specialization.
Authors
- Jinghui Huang (ORCID: https://orcid.org/0000-0002-0991-0591)
- Chenglong Zhu (ORCID: https://orcid.org/0000-0003-4013-1825)
- Shengyou Li (ORCID: https://orcid.org/0000-0003-3739-2477)
- Baoming Ge (ORCID: https://orcid.org/0000-0002-3328-4498)
- Dai-Zhen Zhang (ORCID: https://orcid.org/0009-0006-0746-4061)
- Jiangmin Zheng (ORCID: https://orcid.org/0000-0002-3384-8708)
- Qiang Qiu (ORCID: https://orcid.org/0000-0002-9874-271X)
- Zhengfei Wang (ORCID: https://orcid.org/0000-0003-1918-6282)
- Botong Zhou (ORCID: https://orcid.org/0000-0002-1091-5867)
- Huixian Zhang (ORCID: https://orcid.org/0000-0002-6031-2247)
- Xueli Gao
- Kun Wang (ORCID: https://orcid.org/0000-0001-6059-6529)
- Chunhui Li (ORCID: https://orcid.org/0000-0002-8093-1600)
- Tingfeng Xue
- Wenjie Xu (ORCID: https://orcid.org/0000-0001-6240-8472)
- Qiuning Liu (ORCID: https://orcid.org/0000-0002-1373-2425)
- Boping Tang (ORCID: https://orcid.org/0000-0002-3241-7914)
- Gang Wang (ORCID: https://orcid.org/0000-0002-3124-7968)
- Jin-Jin Zhang (ORCID: https://orcid.org/0000-0001-9261-6571)
- Huabin Zhang (ORCID: https://orcid.org/0000-0002-5170-2753)
- Yuxuan Liu (ORCID: https://orcid.org/0009-0008-6732-7717)
Institutions
- Northwestern Polytechnical University (CN)
- Kunming Institute of Zoology (CN)
- Chinese Academy of Sciences (CN)
- Institute of Oceanology (CN)
- South China Sea Institute Of Oceanology (CN)
- Yancheng Teachers University (CN)
- Xijing Hospital (CN)
- Air Force Medical University (CN)
Publication Details
- Journal
- Molecular Biology and Evolution
- Published
- 2024-11-01
- DOI
- https://doi.org/10.1093/molbev/msae239
- Citations
- 3
- Primary Topic
- Chromosomal and Genetic Variations
- Type
- article
- Field-Weighted Citation Impact
- 1.80
Funders
- National Natural Science Foundation of China
- Government of Jiangsu Province
- Jiangsu Key Laboratory for Bioresources of Saline Soils
- National Key Research and Development Program of China