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Occasional paternal inheritance of the germline-restricted chromosome in songbirds

Songbirds have one special accessory chromosome, the so-called germline-restricted chromosome (GRC), which is only present in germline cells and absent from all somatic tissues. Earlier work on the zebra finch (Taeniopygia guttata castanotis) showed that the GRC is inherited only through the female...

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Autores principales: Pei, Yifan, Forstmeier, Wolfgang, Ruiz-Ruano, Francisco J., Mueller, Jakob C., Cabrero, Josefa, Camacho, Juan Pedro M., Alché, Juan D., Franke, Andre, Hoeppner, Marc, Börno, Stefan, Gessara, Ivana, Hertel, Moritz, Teltscher, Kim, Knief, Ulrich, Suh, Alexander, Kempenaers, Bart
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8794876/
https://www.ncbi.nlm.nih.gov/pubmed/35058355
http://dx.doi.org/10.1073/pnas.2103960119
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author Pei, Yifan
Forstmeier, Wolfgang
Ruiz-Ruano, Francisco J.
Mueller, Jakob C.
Cabrero, Josefa
Camacho, Juan Pedro M.
Alché, Juan D.
Franke, Andre
Hoeppner, Marc
Börno, Stefan
Gessara, Ivana
Hertel, Moritz
Teltscher, Kim
Knief, Ulrich
Suh, Alexander
Kempenaers, Bart
author_facet Pei, Yifan
Forstmeier, Wolfgang
Ruiz-Ruano, Francisco J.
Mueller, Jakob C.
Cabrero, Josefa
Camacho, Juan Pedro M.
Alché, Juan D.
Franke, Andre
Hoeppner, Marc
Börno, Stefan
Gessara, Ivana
Hertel, Moritz
Teltscher, Kim
Knief, Ulrich
Suh, Alexander
Kempenaers, Bart
author_sort Pei, Yifan
collection PubMed
description Songbirds have one special accessory chromosome, the so-called germline-restricted chromosome (GRC), which is only present in germline cells and absent from all somatic tissues. Earlier work on the zebra finch (Taeniopygia guttata castanotis) showed that the GRC is inherited only through the female line—like the mitochondria—and is eliminated from the sperm during spermatogenesis. Here, we show that the GRC has the potential to be paternally inherited. Confocal microscopy using GRC-specific fluorescent in situ hybridization probes indicated that a considerable fraction of sperm heads (1 to 19%) in zebra finch ejaculates still contained the GRC. In line with these cytogenetic data, sequencing of ejaculates revealed that individual males from two families differed strongly and consistently in the number of GRCs in their ejaculates. Examining a captive-bred male hybrid of the two zebra finch subspecies (T. g. guttata and T. g. castanotis) revealed that the mitochondria originated from a castanotis mother, whereas the GRC came from a guttata father. Moreover, analyzing GRC haplotypes across nine castanotis matrilines, estimated to have diverged for up to 250,000 y, showed surprisingly little variability among GRCs. This suggests that a single GRC haplotype has spread relatively recently across all examined matrilines. A few diagnostic GRC mutations that arose since this inferred spreading suggest that the GRC has continued to jump across matriline boundaries. Our findings raise the possibility that certain GRC haplotypes could selfishly spread through the population via occasional paternal transmission, thereby outcompeting other GRC haplotypes that were limited to strict maternal inheritance, even if this was partly detrimental to organismal fitness.
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spelling pubmed-87948762022-02-03 Occasional paternal inheritance of the germline-restricted chromosome in songbirds Pei, Yifan Forstmeier, Wolfgang Ruiz-Ruano, Francisco J. Mueller, Jakob C. Cabrero, Josefa Camacho, Juan Pedro M. Alché, Juan D. Franke, Andre Hoeppner, Marc Börno, Stefan Gessara, Ivana Hertel, Moritz Teltscher, Kim Knief, Ulrich Suh, Alexander Kempenaers, Bart Proc Natl Acad Sci U S A Biological Sciences Songbirds have one special accessory chromosome, the so-called germline-restricted chromosome (GRC), which is only present in germline cells and absent from all somatic tissues. Earlier work on the zebra finch (Taeniopygia guttata castanotis) showed that the GRC is inherited only through the female line—like the mitochondria—and is eliminated from the sperm during spermatogenesis. Here, we show that the GRC has the potential to be paternally inherited. Confocal microscopy using GRC-specific fluorescent in situ hybridization probes indicated that a considerable fraction of sperm heads (1 to 19%) in zebra finch ejaculates still contained the GRC. In line with these cytogenetic data, sequencing of ejaculates revealed that individual males from two families differed strongly and consistently in the number of GRCs in their ejaculates. Examining a captive-bred male hybrid of the two zebra finch subspecies (T. g. guttata and T. g. castanotis) revealed that the mitochondria originated from a castanotis mother, whereas the GRC came from a guttata father. Moreover, analyzing GRC haplotypes across nine castanotis matrilines, estimated to have diverged for up to 250,000 y, showed surprisingly little variability among GRCs. This suggests that a single GRC haplotype has spread relatively recently across all examined matrilines. A few diagnostic GRC mutations that arose since this inferred spreading suggest that the GRC has continued to jump across matriline boundaries. Our findings raise the possibility that certain GRC haplotypes could selfishly spread through the population via occasional paternal transmission, thereby outcompeting other GRC haplotypes that were limited to strict maternal inheritance, even if this was partly detrimental to organismal fitness. National Academy of Sciences 2022-01-20 2022-01-25 /pmc/articles/PMC8794876/ /pubmed/35058355 http://dx.doi.org/10.1073/pnas.2103960119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Pei, Yifan
Forstmeier, Wolfgang
Ruiz-Ruano, Francisco J.
Mueller, Jakob C.
Cabrero, Josefa
Camacho, Juan Pedro M.
Alché, Juan D.
Franke, Andre
Hoeppner, Marc
Börno, Stefan
Gessara, Ivana
Hertel, Moritz
Teltscher, Kim
Knief, Ulrich
Suh, Alexander
Kempenaers, Bart
Occasional paternal inheritance of the germline-restricted chromosome in songbirds
title Occasional paternal inheritance of the germline-restricted chromosome in songbirds
title_full Occasional paternal inheritance of the germline-restricted chromosome in songbirds
title_fullStr Occasional paternal inheritance of the germline-restricted chromosome in songbirds
title_full_unstemmed Occasional paternal inheritance of the germline-restricted chromosome in songbirds
title_short Occasional paternal inheritance of the germline-restricted chromosome in songbirds
title_sort occasional paternal inheritance of the germline-restricted chromosome in songbirds
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8794876/
https://www.ncbi.nlm.nih.gov/pubmed/35058355
http://dx.doi.org/10.1073/pnas.2103960119
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