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Occasional paternal inheritance of the germline-restricted chromosome in songbirds.

Authors
  • Pei, Yifan1
  • Forstmeier, Wolfgang1
  • Ruiz-Ruano, Francisco J2, 3
  • Mueller, Jakob C4
  • Cabrero, Josefa5
  • Camacho, Juan Pedro M5
  • Alché, Juan D6
  • Franke, Andre7
  • Hoeppner, Marc7
  • Börno, Stefan8
  • Gessara, Ivana9
  • Hertel, Moritz9
  • Teltscher, Kim4
  • Knief, Ulrich10
  • Suh, Alexander2, 3
  • Kempenaers, Bart4
  • 1 Department of Behavioral Ecology and Evolutionary Genetics, Max Planck Institute for Ornithology 82319 Seewiesen, Germany; [email protected] [email protected] [email protected] [email protected] , (Germany)
  • 2 School of Biological Sciences, University of East Anglia, Norwich NR4 7TU, United Kingdom; [email protected] [email protected] [email protected] [email protected] , (United Kingdom)
  • 3 Department of Organismal Biology, Evolutionary Biology Centre, Science for Life Laboratory, Uppsala University SE-752 36 Uppsala, Sweden. , (Sweden)
  • 4 Department of Behavioral Ecology and Evolutionary Genetics, Max Planck Institute for Ornithology 82319 Seewiesen, Germany. , (Germany)
  • 5 Department of Genetics, University of Granada E-18071 Granada, Spain. , (Spain)
  • 6 Department of Biochemistry, Cell and Molecular Biology of Plants, Estación Experimental del Zaidín, Spanish National Research Council E-18008 Granada, Spain. , (Spain)
  • 7 Institute of Clinical Molecular Biology, Christian-Albrechts-Universität zu Kiel 24118 Kiel, Germany. , (Germany)
  • 8 Sequencing Core Facility, Max Planck Institute for Molecular Genetics 14195 Berlin, Germany. , (Germany)
  • 9 Department of Behavioral Neurobiology, Max Planck Institute for Ornithology 82319 Seewiesen, Germany. , (Germany)
  • 10 Division of Evolutionary Biology, Faculty of Biology, Ludwig Maximilian University of Munich D-82152 Planegg-Martinsried, Germany. , (Germany)
Type
Published Article
Journal
Proceedings of the National Academy of Sciences
Publisher
Proceedings of the National Academy of Sciences
Publication Date
Jan 25, 2022
Volume
119
Issue
4
Identifiers
DOI: 10.1073/pnas.2103960119
PMID: 35058355
Source
Medline
Keywords
Language
English
License
Unknown

Abstract

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. Copyright © 2022 the Author(s). Published by PNAS.

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