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Evolutionary traits and functional roles of chemokines and their receptors in the male pregnancy of the Syngnathidae

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Abstract

Vertebrates have developed various modes of reproduction, some of which are found in Teleosts. Over 300 species of the Syngnathidae (seahorses, pipefishes and seadragons) exhibit male pregnancies; the males have specialized brood pouches that provide immune protection, nourishment, and oxygen regulation. Chemokines play a vital role at the mammalian maternal–fetal interface; however, their functions in fish reproduction are unclear. This study revealed the evolutionary traits and potential functions of chemokine genes in 22 oviparous, ovoviviparous, and viviparous fish species through comparative genomic analyses. Our results showed that chemokine gene copy numbers and evolutionary rates vary among species with different modes of reproduction. Syngnathidae lost cxcl13 and cxcr5, which are involved in key receptor–ligand pairs for lymphoid organ development. Notably, Syngnathidae have site-specific mutations in cxcl12b and ccl44, suggesting immune function during gestation. Moreover, transcriptome analysis revealed that chemokine gene expression varies among Syngnathidae species with different types of brood pouches, suggesting adaptive variations in chemokine functions among seahorses and their relatives. Furthermore, challenge experiments on seahorse brood pouches revealed a joint immune function of chemokine genes during male pregnancy. This study provides insights into the evolutionary diversity of chemokine genes associated with different reproductive modes in fish.

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The authors declare that all data supporting the findings of this study are available within the article and its supplementary files.

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (41825013), the Marine Economic Development Project (GDNRC[2022]36), National Key R&D Program of China (2022YFC3102403), National Natural Science Foundation of China (42230409, 42276127), and Guangdong Basic and Applied Basic Research Foundation (2021A1515011380, 2021A1515011393).

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Authors and Affiliations

  1. CAS Key Laboratory of Tropical Marine Bio-Resources and Ecology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, 510301, China

    Han Jiang, Zhanwei Zhao, Haiyan Yu, Qiang Lin & Yali Liu

  2. Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, 510301, China

    Han Jiang, Zhanwei Zhao, Haiyan Yu, Qiang Lin & Yali Liu

  3. University of Chinese Academy of Sciences, Bei**g, 101400, China

    Han Jiang, Zhanwei Zhao, Qiang Lin & Yali Liu

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Contributions

QL and YL designed the study, HJ, HY and ZZ analyzed the data. HJ conducted the manuscript writing. All the authors have read and approved the final manuscript.

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Correspondence to Qiang Lin or Yali Liu.

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The authors declare no conflicts of interest. Author Qiang Lin is a member of the Editorial Board, but he was not involved in the journal’s review of, or decision related to this manuscript.

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All animal experiments were conducted in accordance with established guidelines and approved by the Chinese Academy of Sciences.

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Edited by Jiamei Li.

Special Topic: EvoDevo.

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Jiang, H., Zhao, Z., Yu, H. et al. Evolutionary traits and functional roles of chemokines and their receptors in the male pregnancy of the Syngnathidae. Mar Life Sci Technol 5, 500–510 (2023). https://doi.org/10.1007/s42995-023-00205-x

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