Molecular evolution of wound healing-related genes during cetacean secondary aquatic adaptation

Jieqiong KANG , Long GU , Boxiong GUO , Wenqi RONG , Shixia XU , Guang YANG , Wenhua REN

Integrative Zoology ›› 2024, Vol. 19 ›› Issue (5) : 898 -912.

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Integrative Zoology ›› 2024, Vol. 19 ›› Issue (5) : 898 -912. DOI: 10.1111/1749-4877.12781
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Molecular evolution of wound healing-related genes during cetacean secondary aquatic adaptation

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Abstract

The marine environment presents challenges for wound healing in cetaceans, despite their remarkable recovery abilities with minimal infections or complications. However, the molecular mechanism underlying this efficient wound healing remains underexplored. To better understand the molecular mechanisms behind wound healing in cetaceans, we investigated the evolutionary patterns of 37 wound healing-related genes in representative mammals. We found wound healing-related genes experience adaptive evolution in cetaceans: (1) Three extrinsic coagulation pathway-related genes—tissue factor (F3), coagulation factor VII (F7), and coagulation factor X (F10)—are subject to positive selection in cetaceans, which might promote efficient hemostasis after injury; positive selection in transforming growth factor-beta 2 (TGF-β2), transforming growth factor-beta 3 (TGF-β3), and platelet-derived growth factor D (PDGFD), which play immunological roles in wound healing, may help cetaceans enhance inflammatory response and tissue debridement. (2) Coagulation factor XII (F12) is the initiation factor in the intrinsic coagulation pathway. It had a premature stop codon mutation and was subjected to selective stress relaxation in cetaceans, suggesting that the early termination of F12 may help cetaceans avoid the risk of vascular blockage during diving. (3) Fibrinogen alpha chain (FGA) and FIII, which were detected to contain the specific amino acid substitutions in marine mammals, indicating similar evolutionary mechanisms might exist among marine mammals to maintain strong wound-healing ability. Thus, our research provides further impetus to study the evolution of the wound healing system in cetaceans and other marine mammals, extending knowledge of preventing coagulation disorder and atherosclerosis in humans.

Keywords

adaptive evolution / coagulation / habitat differences / marine mammals / wound healing

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Jieqiong KANG, Long GU, Boxiong GUO, Wenqi RONG, Shixia XU, Guang YANG, Wenhua REN. Molecular evolution of wound healing-related genes during cetacean secondary aquatic adaptation. Integrative Zoology, 2024, 19(5): 898-912 DOI:10.1111/1749-4877.12781

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2023 International Society of Zoological Sciences, Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd.

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