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Immunogenetic losses co-occurred with seahorse male pregnancy and mutation in tlx1 accompanied functional asplenia

Yali Liu, Meng Qu, Han Jiang, Ralf Schneider, Geng Qin, Wei Luo, Haiyan Yu, Bo Zhang, Xin Wang, Yanhong Zhang, Huixian Zhang, Zhixin Zhang, Yongli Wu, Yingyi Zhang, Jianping Yin, Si Zhang, Byrappa Venkatesh, Olivia Roth (), Axel Meyer () and Qiang Lin ()
Additional contact information
Yali Liu: Chinese Academy of Sciences
Meng Qu: Chinese Academy of Sciences
Han Jiang: Chinese Academy of Sciences
Ralf Schneider: Kiel University
Geng Qin: Chinese Academy of Sciences
Wei Luo: Chinese Academy of Sciences
Haiyan Yu: Chinese Academy of Sciences
Bo Zhang: Chinese Academy of Sciences
Xin Wang: Chinese Academy of Sciences
Yanhong Zhang: Chinese Academy of Sciences
Huixian Zhang: Chinese Academy of Sciences
Zhixin Zhang: Chinese Academy of Sciences
Yongli Wu: Chinese Academy of Sciences
Yingyi Zhang: Chinese Academy of Sciences
Jianping Yin: Chinese Academy of Sciences
Si Zhang: Chinese Academy of Sciences
Byrappa Venkatesh: Institute of Molecular and Cell Biology, A*STAR
Olivia Roth: Kiel University
Axel Meyer: University of Konstanz
Qiang Lin: Chinese Academy of Sciences

Nature Communications, 2022, vol. 13, issue 1, 1-12

Abstract: Abstract In the highly derived syngnathid fishes (pipefishes, seadragons & seahorses), the evolution of sex-role reversed brooding behavior culminated in the seahorse lineage’s male pregnancy, whose males feature a specialized brood pouch into which females deposit eggs during mating. Then, eggs are intimately engulfed by a placenta-like tissue that facilitates gas and nutrient exchange. As fathers immunologically tolerate allogenic embryos, it was suggested that male pregnancy co-evolved with specific immunological adaptations. Indeed, here we show that a specific amino-acid replacement in the tlx1 transcription factor is associated with seahorses’ asplenia (loss of spleen, an organ central in the immune system), as confirmed by a CRISPR-Cas9 experiment using zebrafish. Comparative genomics across the syngnathid phylogeny revealed that the complexity of the immune system gene repertoire decreases as parental care intensity increases. The synchronous evolution of immunogenetic alterations and male pregnancy supports the notion that male pregnancy co-evolved with the immunological tolerance of the embryo.

Date: 2022
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DOI: 10.1038/s41467-022-35338-7

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