Gert, Krista R.B.; Panser, Karin; Surm, Joachim; Steinmetz, Benjamin S.; Schleiffer, Alexander; Jovine, Luca; Moran, Yehu; Kondrashov, FyodorISTA ; Pauli, Andrea
Molecular compatibility between gametes is a prerequisite for successful fertilization. As long as a sperm and egg can recognize and bind each other via their surface proteins, gamete fusion may occur even between members of separate species, resulting in hybrids that can impact speciation. The egg membrane protein Bouncer confers species specificity to gamete interactions between medaka and zebrafish, preventing their cross-fertilization. Here, we leverage this specificity to uncover distinct amino acid residues and N-glycosylation patterns that differentially influence the function of medaka and zebrafish Bouncer and contribute to cross-species incompatibility. Curiously, in contrast to the specificity observed for medaka and zebrafish Bouncer, seahorse and fugu Bouncer are compatible with both zebrafish and medaka sperm, in line with the pervasive purifying selection that dominates Bouncer’s evolution. The Bouncer-sperm interaction is therefore the product of seemingly opposing evolutionary forces that, for some species, restrict fertilization to closely related fish, and for others, allow broad gamete compatibility that enables hybridization.
We thank Manfred Schartl for sharing RNA-seq data from medaka ovaries and testes prior to publication; Maria Novatchkova for help with RNA-seq analysis; Katharina Lust for advice on medaka techniques; Milan Malinsky for input on Lake Malawi cichlid Bouncer sequences; Felicia Spitzer, Mirjam Binner, and Anna Bandura for help with genotyping; Friedrich Puhl, Kerstin Rattner, Julia Koenig, and Dijana Sunjic for taking care of zebrafish and medaka; and the Pauli lab for helpful discussions about the project and feedback on the manuscript. K.R.B.G. was supported by a DOC Fellowship from the Austrian Academy of Sciences. Work in the Pauli lab was supported by the FWF START program (Y 1031-B28 to A.P.), the ERC CoG 101044495/GaMe, the HFSP Career Development Award (CDA00066/2015 to A.P.), a HFSP Young Investigator Award (RGY0079/2020 to A.P.) and the FWF SFB RNA-Deco (project number F80). The IMP receives institutional funding from Boehringer Ingelheim and the Austrian Research Promotion Agency (Headquarter grant FFG-852936). Work by J.S. and Y.M. in this project was supported by the Israel Science Foundation grant 636/21 to Y.M. Work by L.J. was supported by the Swedish Research Council grant 2020-04936 and the Knut and Alice Wallenberg Foundation grant 2018.0042. For the purpose of Open Access, the author has applied a CC BY public copyright license to any Author Accepted Manuscript (AAM) version arising from this submission.
Gert KRB, Panser K, Surm J, et al. Divergent molecular signatures in fish Bouncer proteins define cross-fertilization boundaries. Nature Communications. 2023;14. doi:10.1038/s41467-023-39317-4
Gert, K. R. B., Panser, K., Surm, J., Steinmetz, B. S., Schleiffer, A., Jovine, L., … Pauli, A. (2023). Divergent molecular signatures in fish Bouncer proteins define cross-fertilization boundaries. Nature Communications. Springer Nature. https://doi.org/10.1038/s41467-023-39317-4
Gert, Krista R.B., Karin Panser, Joachim Surm, Benjamin S. Steinmetz, Alexander Schleiffer, Luca Jovine, Yehu Moran, Fyodor Kondrashov, and Andrea Pauli. “Divergent Molecular Signatures in Fish Bouncer Proteins Define Cross-Fertilization Boundaries.” Nature Communications. Springer Nature, 2023. https://doi.org/10.1038/s41467-023-39317-4.
K. R. B. Gert et al., “Divergent molecular signatures in fish Bouncer proteins define cross-fertilization boundaries,” Nature Communications, vol. 14. Springer Nature, 2023.
Gert KRB, Panser K, Surm J, Steinmetz BS, Schleiffer A, Jovine L, Moran Y, Kondrashov F, Pauli A. 2023. Divergent molecular signatures in fish Bouncer proteins define cross-fertilization boundaries. Nature Communications. 14, 3506.
Gert, Krista R. B., et al. “Divergent Molecular Signatures in Fish Bouncer Proteins Define Cross-Fertilization Boundaries.” Nature Communications, vol. 14, 3506, Springer Nature, 2023, doi:10.1038/s41467-023-39317-4.
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