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.

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.

Reviewing Editor

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

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.

Metrics

  • 3,278
    Page views
  • 382
    Downloads
  • 17
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Further reading

    1. Evolutionary Biology
    2. Neuroscience
    Katja Heuer, Nicolas Traut ... Roberto Toro
    Research Article

    The process of brain folding is thought to play an important role in the development and organisation of the cerebrum and the cerebellum. The study of cerebellar folding is challenging due to the small size and abundance of its folia. In consequence, little is known about its anatomical diversity and evolution. We constituted an open collection of histological data from 56 mammalian species and manually segmented the cerebrum and the cerebellum. We developed methods to measure the geometry of cerebellar folia and to estimate the thickness of the molecular layer. We used phylogenetic comparative methods to study the diversity and evolution of cerebellar folding and its relationship with the anatomy of the cerebrum. Our results show that the evolution of cerebellar and cerebral anatomy follows a stabilising selection process. We observed 2 groups of phenotypes changing concertedly through evolution: a group of 'diverse' phenotypes - varying over several orders of magnitude together with body size, and a group of 'stable' phenotypes varying over less than 1 order of magnitude across species. Our analyses confirmed the strong correlation between cerebral and cerebellar volumes across species, and showed in addition that large cerebella are disproportionately more folded than smaller ones. Compared with the extreme variations in cerebellar surface area, folial anatomy and molecular layer thickness varied only slightly, showing a much smaller increase in the larger cerebella. We discuss how these findings could provide new insights into the diversity and evolution of cerebellar folding, the mechanisms of cerebellar and cerebral folding, and their potential influence on the organisation of the brain across species.

    1. Developmental Biology
    2. Evolutionary Biology
    Salvatore D'Aniello, Stephanie Bertrand, Hector Escriva
    Feature Article

    Cephalochordates and tunicates represent the only two groups of invertebrate chordates, and extant cephalochordates – commonly known as amphioxus or lancelets – are considered the best proxy for the chordate ancestor, from which they split around 520 million years ago. Amphioxus has been an important organism in the fields of zoology and embryology since the 18th century, and the morphological and genomic simplicity of cephalochordates (compared to vertebrates) makes amphioxus an attractive model for studying chordate biology at the cellular and molecular levels. Here we describe the life cycle of amphioxus, and discuss the natural histories and habitats of the different species of amphioxus. We also describe their use as laboratory animal models, and discuss the techniques that have been developed to study different aspects of amphioxus.