The genetic factors of bilaterian evolution

  1. Peter Heger  Is a corresponding author
  2. Wen Zheng
  3. Anna Rottmann
  4. Kristen A Panfilio
  5. Thomas Wiehe
  1. Universitaet zu Koeln, Germany
  2. Sichuan University, China
  3. University of Cologne, Germany

Abstract

The Cambrian explosion was a unique animal radiation ~540 million years ago that produced the full range of body plans across bilaterians. The genetic mechanisms underlying these events are unknown, leaving a fundamental question in evolutionary biology unanswered. Using large-scale comparative genomics and advanced orthology evaluation techniques, we identified 157 bilaterian-specific genes. They include the entire Nodal pathway, a key regulator of mesoderm development and left-right axis specification; components for nervous system development, including a suite of G protein-coupled receptors that control physiology and behaviour, the Robo-Slit midline repulsion system, and the neurotrophin signalling system; a high number of zinc finger transcription factors; and novel factors that previously escaped attention. Contradicting the current view, our study reveals that genes with bilaterian origin are robustly associated with key features in extant bilaterians, suggesting a causal relationship.

Data availability

Accession numbers and/or URLs for previously published transcriptome datasets are listed in Supplementary file 3. Download links for previously published genomic sequences are listed in Supplementary File 1-Supplementary Table S7.Orthology datasets generated in this study have been deposited to Dryad, under the doi:10.5061/dryad.4qf7168

The following data sets were generated

Article and author information

Author details

  1. Peter Heger

    Institute for Genetics, Universitaet zu Koeln, Cologne, Germany
    For correspondence
    peter.heger@uni-koeln.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2583-2981
  2. Wen Zheng

    West China-Washington Mitochondria and Metabolism Research Center, Sichuan University, Chengdu, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Anna Rottmann

    Institute for Genetics, Universitaet zu Koeln, Cologne, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Kristen A Panfilio

    Institute for Zoology/Developmental Biology, University of Cologne, Köln, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6417-251X
  5. Thomas Wiehe

    Institut fuer Genetik, Universitaet zu Koeln, Koeln, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8932-2772

Funding

Deutsche Forschungsgemeinschaft (CRC~680 and CRC~1211)

  • Thomas Wiehe

Deutsche Forschungsgemeinschaft (CRC~680)

  • Kristen A Panfilio

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

Reviewing Editor

  1. Patricia J Wittkopp, University of Michigan, United States

Version history

  1. Received: January 31, 2019
  2. Accepted: July 3, 2020
  3. Accepted Manuscript published: July 16, 2020 (version 1)
  4. Version of Record published: October 5, 2020 (version 2)

Copyright

© 2020, Heger 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

  • 6,460
    views
  • 783
    downloads
  • 49
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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. Peter Heger
  2. Wen Zheng
  3. Anna Rottmann
  4. Kristen A Panfilio
  5. Thomas Wiehe
(2020)
The genetic factors of bilaterian evolution
eLife 9:e45530.
https://doi.org/10.7554/eLife.45530

Share this article

https://doi.org/10.7554/eLife.45530

Further reading

    1. Biochemistry and Chemical Biology
    2. Evolutionary Biology
    Foteini Karapanagioti, Úlfur Águst Atlason ... Sebastian Obermaier
    Research Article

    The emergence of new protein functions is crucial for the evolution of organisms. This process has been extensively researched for soluble enzymes, but it is largely unexplored for membrane transporters, even though the ability to acquire new nutrients from a changing environment requires evolvability of transport functions. Here, we demonstrate the importance of environmental pressure in obtaining a new activity or altering a promiscuous activity in members of the amino acid-polyamine-organocation (APC)-type yeast amino acid transporters family. We identify APC members that have broader substrate spectra than previously described. Using in vivo experimental evolution, we evolve two of these transporter genes, AGP1 and PUT4, toward new substrate specificities. Single mutations on these transporters are found to be sufficient for expanding the substrate range of the proteins, while retaining the capacity to transport all original substrates. Nonetheless, each adaptive mutation comes with a distinct effect on the fitness for each of the original substrates, illustrating a trade-off between the ancestral and evolved functions. Collectively, our findings reveal how substrate-adaptive mutations in membrane transporters contribute to fitness and provide insights into how organisms can use transporter evolution to explore new ecological niches.

    1. Evolutionary Biology
    2. Genetics and Genomics
    Yannick Schäfer, Katja Palitzsch ... Jaanus Suurväli
    Research Article Updated

    Copy number variation in large gene families is well characterized for plant resistance genes, but similar studies are rare in animals. The zebrafish (Danio rerio) has hundreds of NLR immune genes, making this species ideal for studying this phenomenon. By sequencing 93 zebrafish from multiple wild and laboratory populations, we identified a total of 1513 NLRs, many more than the previously known 400. Approximately half of those are present in all wild populations, but only 4% were found in 80% or more of the individual fish. Wild fish have up to two times as many NLRs per individual and up to four times as many NLRs per population than laboratory strains. In contrast to the massive variability of gene copies, nucleotide diversity in zebrafish NLR genes is very low: around half of the copies are monomorphic and the remaining ones have very few polymorphisms, likely a signature of purifying selection.