Divergent molecular signatures in fish Bouncer proteins define cross-fertilization boundaries

Abstract 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....

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Main Authors: Krista R. B. Gert, Karin Panser, Joachim Surm, Benjamin S. Steinmetz, Alexander Schleiffer, Luca Jovine, Yehu Moran, Fyodor Kondrashov, Andrea Pauli
Format: Article
Language:English
Published: Nature Portfolio 2023-06-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-023-39317-4
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author Krista R. B. Gert
Karin Panser
Joachim Surm
Benjamin S. Steinmetz
Alexander Schleiffer
Luca Jovine
Yehu Moran
Fyodor Kondrashov
Andrea Pauli
author_facet Krista R. B. Gert
Karin Panser
Joachim Surm
Benjamin S. Steinmetz
Alexander Schleiffer
Luca Jovine
Yehu Moran
Fyodor Kondrashov
Andrea Pauli
author_sort Krista R. B. Gert
collection DOAJ
description Abstract 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.
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spelling doaj.art-145bb6c80580420988cfedaedfd84a842023-06-18T11:19:13ZengNature PortfolioNature Communications2041-17232023-06-0114111410.1038/s41467-023-39317-4Divergent molecular signatures in fish Bouncer proteins define cross-fertilization boundariesKrista R. B. Gert0Karin Panser1Joachim Surm2Benjamin S. Steinmetz3Alexander Schleiffer4Luca Jovine5Yehu Moran6Fyodor Kondrashov7Andrea Pauli8Research Institute of Molecular Pathology (IMP), Vienna BioCenter (VBC)Research Institute of Molecular Pathology (IMP), Vienna BioCenter (VBC)Department of Ecology, Evolution and Behavior, Alexander Silberman Institute of Life Sciences, The Hebrew University of JerusalemResearch Institute of Molecular Pathology (IMP), Vienna BioCenter (VBC)Research Institute of Molecular Pathology (IMP), Vienna BioCenter (VBC)Department of Biosciences and Nutrition, Karolinska InstitutetDepartment of Ecology, Evolution and Behavior, Alexander Silberman Institute of Life Sciences, The Hebrew University of JerusalemInstitute of Science and Technology AustriaResearch Institute of Molecular Pathology (IMP), Vienna BioCenter (VBC)Abstract 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.https://doi.org/10.1038/s41467-023-39317-4
spellingShingle Krista R. B. Gert
Karin Panser
Joachim Surm
Benjamin S. Steinmetz
Alexander Schleiffer
Luca Jovine
Yehu Moran
Fyodor Kondrashov
Andrea Pauli
Divergent molecular signatures in fish Bouncer proteins define cross-fertilization boundaries
Nature Communications
title Divergent molecular signatures in fish Bouncer proteins define cross-fertilization boundaries
title_full Divergent molecular signatures in fish Bouncer proteins define cross-fertilization boundaries
title_fullStr Divergent molecular signatures in fish Bouncer proteins define cross-fertilization boundaries
title_full_unstemmed Divergent molecular signatures in fish Bouncer proteins define cross-fertilization boundaries
title_short Divergent molecular signatures in fish Bouncer proteins define cross-fertilization boundaries
title_sort divergent molecular signatures in fish bouncer proteins define cross fertilization boundaries
url https://doi.org/10.1038/s41467-023-39317-4
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