Inflammation and convergent placenta gene co-option contributed to a novel reproductive tissue

• Published in: Current biology 2022-02, Vol.32 (3), p.715-724.e4
• Main Authors: Hilgers, Leon, Roth, Olivia, Nolte, Arne W., Schüller, Alina, Spanke, Tobias, Flury, Jana M., Utama, Ilham V., Altmüller, Janine, Wowor, Daisy, Misof, Bernhard, Herder, Fabian, Böhne, Astrid, Schwarzer, Julia
• Format: Article
• Language: English
• Subjects: Animals; convergent evolution; Embryo, Mammalian; Eutheria; evolutionary innovation; Female; gene co-option; gene expression; inflammation; Inflammation - genetics; maternal-embryonic contact; pelvic brooding; Placenta; Pregnancy; Reproduction; ricefish
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2021.12.004

The evolution of pregnancy exposes parental tissues to new, potentially stressful conditions, which can trigger inflammation.1 Inflammation is costly2,3 and can induce embryo rejection, which constrains the evolution of pregnancy.1 In contrast, inflammation can also promote morphological innovation at the maternal-embryonic interface as exemplified by co-option of pro-inflammatory signaling for eutherian embryo implantation.1,4,5 Given its dual function, inflammation could be a key process explaining how innovations such as pregnancy and placentation evolved many times convergently. Pelvic brooding ricefishes evolved a novel “plug” tissue,6,7 which forms inside the female gonoduct after spawning, anchors egg-attaching filaments, and enables pelvic brooders to carry eggs externally until hatching.6,8 Compared to pregnancy, i.e., internal bearing of embryos, external bearing should alleviate constraints on inflammation in the reproductive tract. We thus hypothesized that an ancestral inflammation triggered by the retention of attaching filaments gave rise to pathways orchestrating plug formation. In line with our hypothesis, histological sections of the developing plug revealed signs of gonoduct injuries by egg-attaching filaments in the pelvic brooding ricefish Oryzias eversi. Tissue-specific transcriptomes showed that inflammatory signaling dominates the plug transcriptome and inflammation-induced genes controlling vital processes for plug development such as tissue growth and angiogenesis were overexpressed in the plug. Finally, mammalian placenta genes were enriched in the plug transcriptome, indicating convergent gene co-option for building, attaching, and sustaining a transient tissue in the female reproductive tract. This study highlights the role of gene co-option and suggests that recruiting inflammatory signaling into physiological processes provides a fast-track to evolutionary innovation. [Display omitted] •Pelvic brooding induces tissue-specific changes in gene expression•Inflammatory signaling characterizes transcriptome of the egg-anchoring plug•Similar to embryo implantation, the plug likely evolved from an inflammatory response•Mammalian placenta genes were independently co-opted into the plug Hilgers et al. combine tissue-specific transcriptomes with morphological data to investigate the evolution of a novel egg-anchoring tissue in ricefishes. Their data show convergent co-option of mammalian placenta genes and indicate that recruiting infl