A de novo evolved gene in the house mouse regulates female pregnancy cycles

  1. Chen Xie
  2. Cemalettin Bekpen
  3. Sven Künzel
  4. Maryam Keshavarz
  5. Rebecca Krebs-Wheaton
  6. Neva Skrabar
  7. Kristian Karsten Ullrich
  8. Diethard Tautz  Is a corresponding author
  1. Max-Planck Institute for Evolutionary Biology, Germany
  2. Max-Planck Institute of Evolutionary Biology, Germany

Abstract

The de novo emergence of new genes has been well documented through genomic analyses. However, a functional analysis, especially of very young protein-coding genes, is still largely lacking. Here, we identify a set of house mouse-specific protein-coding genes and assess their translation by ribosome profiling and mass spectrometry data. We functionally analyze one of them, Gm13030, which is specifically expressed in females in the oviduct. The interruption of the reading frame affects the transcriptional network in the oviducts at a specific stage of the estrous cycle. This includes the upregulation of Dcpp genes, which are known to stimulate the growth of preimplantation embryos. As a consequence, knockout females have their second litters after shorter times and have a higher infanticide rate. Given that Gm13030 shows no signs of positive selection, our findings support the hypothesis that a de novo evolved gene can directly adopt a function without much sequence adaptation.

Data availability

The ENA BioProject accession number for the sequencing data reported in this study is PRJEB28348

The following data sets were generated

Article and author information

Author details

  1. Chen Xie

    Department Evolutionary Genetics, Max-Planck Institute for Evolutionary Biology, Plön, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6183-7301
  2. Cemalettin Bekpen

    Department Evolutionary Genetics, Max-Planck Institute for Evolutionary Biology, Plön, Germany
    Competing interests
    No competing interests declared.
  3. Sven Künzel

    Department Evolutionary Genetics, Max-Planck Institute of Evolutionary Biology, Plön, Germany
    Competing interests
    No competing interests declared.
  4. Maryam Keshavarz

    Department Evolutionary Genetics, Max-Planck Institute for Evolutionary Biology, Plön, Germany
    Competing interests
    No competing interests declared.
  5. Rebecca Krebs-Wheaton

    Department Evolutionary Genetics, Max-Planck Institute for Evolutionary Biology, Plön, Germany
    Competing interests
    No competing interests declared.
  6. Neva Skrabar

    Department Evolutionary Genetics, Max-Planck Institute for Evolutionary Biology, Plön, Germany
    Competing interests
    No competing interests declared.
  7. Kristian Karsten Ullrich

    Department Evolutionary Genetics, Max-Planck Institute for Evolutionary Biology, Plön, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4308-9626
  8. Diethard Tautz

    Department Evolutionary Genetics, Max-Planck Institute for Evolutionary Biology, Plön, Germany
    For correspondence
    tautz@evolbio.mpg.de
    Competing interests
    Diethard Tautz, Senior editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0460-5344

Funding

H2020 European Research Council (NewGenes - 322564)

  • Chen Xie

Max-Planck Institut fuer Evolutionsbiologie (Open-access funding)

  • Diethard Tautz

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. George H Perry, Pennsylvania State University, United States

Ethics

Animal experimentation: The behavioral studies were approved by the supervising authority (Ministerium für Energiewende, Landwirtschaftliche Räume und Umwelt, Kiel) under the registration numbers V244-71173/2015, V244-4415/2017 and V244-47238/17. Animals were kept according to FELASA (Federation of European Laboratory Animal Science Association) guidelines, with the permit from the Veterinäramt Kreis Plön: 1401-144/PLÖ-004697. The respective animal welfare officer at the University of Kiel was informed about the sacrifice of the animals for this study.

Version history

  1. Received: December 13, 2018
  2. Accepted: August 21, 2019
  3. Accepted Manuscript published: August 22, 2019 (version 1)
  4. Version of Record published: September 25, 2019 (version 2)

Copyright

© 2019, Xie et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Chen Xie
  2. Cemalettin Bekpen
  3. Sven Künzel
  4. Maryam Keshavarz
  5. Rebecca Krebs-Wheaton
  6. Neva Skrabar
  7. Kristian Karsten Ullrich
  8. Diethard Tautz
(2019)
A de novo evolved gene in the house mouse regulates female pregnancy cycles
eLife 8:e44392.
https://doi.org/10.7554/eLife.44392

Share this article

https://doi.org/10.7554/eLife.44392

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