Occasional paternal inheritance of the germline-restricted chromosome in songbirds

Pei, Yifan, Forstmeier, Wolfgang, Ruiz-Ruano, Francisco J. ORCID: https://orcid.org/0000-0002-5391-301X, 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 ORCID: https://orcid.org/0000-0002-8979-9992 and Kempenaers, Bart (2022) Occasional paternal inheritance of the germline-restricted chromosome in songbirds. Proceedings of the National Academy of Sciences, 119 (4). ISSN 0027-8424

[thumbnail of Published_Version]
Preview
PDF (Published_Version) - Published Version
Available under License Creative Commons Attribution Non-commercial No Derivatives.

Download (2MB) | Preview

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 out-competing other GRC haplotypes that were limited to strict maternal inheritance, even if this was partly detrimental to organismal fitness.

Item Type: Article
Additional Information: Data Accessibility: All sequencing data have been deposited in the Sequence Read Archive (BioProject accession number PRJNA741250) (50). All alignments have been deposited in Figshare (https://figshare.com/articles/dataset/Additional_datasets_for_Occasional_paternal_inheritance_of_the_germline-restricted_chromosome_in_songbirds_/14845026). Additional supporting data have been deposited in the Open Science Framework (https://doi.org/10.17605/OSF.IO/N9X2G) (52). Previously published data were used for this work. All supporting pipelines and scripts have been deposited in the Open Science Framework (https://doi.org/10.17605/OSF.IO/N9X2G) and in GitHub https://github.com/fjruizruano/In_Silico_SeqCap_10xG. Author acknowledgements: We thank Melanie Schneider and Christine Baumgart-ner for support with molecular work, Martin Irestedt for help with DNA extractions for the 10X samples, Shouwen Ma for discussion on microscopic image processing, Keren Sadanandan for discussion on tanglegram analysis, and Katrin Martin, Isabel Schmelcher, Claudia Scheicher, Sonja Bauer, Edith Bodendorfer, Jane Didsbury, Annemarie Groetsch, Andrea Kortner, Petra Neubauer, Frances Weigel, and Barbara Woerle for animal care and help with breeding zebra finches. We thank Frank Roeßler for providing the castanotis x guttata hybrid male, and Leo Joseph and the Australian National Wildlife Collection for providing testis and liver samples from a wild T. g. castanotis individual. We thank Leo Joseph, Julie Blommaert, Octavio Palacios, Simone Fouché, and three anonymous reviewers for comments on the manuscript. Some of the computations were performed on resources provided by the Swedish National Infrastructure for Computing through the Uppsala Multidisciplinary Center for Advanced Computational Science. We acknowledge support from the National Genomics Infrastructure in Stockholm funded by Science for Life Laboratory, the Knut and Alice Wallenberg Foundation, and the Swedish Research Council. This research was supported by the Max Planck Society (to B.K.), the Swedish Research Council Formas (2017-01597 and 2020-04436 to A.S.), and the Swedish Research Council Vetenskapsradet (2016-05139 to A.S.). Y.P. was part of the International Max Planck Research School for Organismal Biology. F.J.R.-R. was supported by a postdoctoral fellowship from Sven och Lilly Lawskis fond and a Marie Curie Individual Fellowship (875732).
Uncontrolled Keywords: elimination efficiency,germline-restricted chromosome,paternal spillover,selfish dna,zebra finch,general ,/dk/atira/pure/subjectarea/asjc/1000
Faculty \ School: Faculty of Science > School of Biological Sciences
Related URLs:
Depositing User: LivePure Connector
Date Deposited: 16 Feb 2022 15:30
Last Modified: 29 Oct 2022 17:33
URI: https://ueaeprints.uea.ac.uk/id/eprint/83532
DOI: 10.1073/pnas.2103960119

Actions (login required)

View Item View Item