The genetic factors of bilaterian evolution
- Universitaet zu Koeln, Germany
- Sichuan University, China
- 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
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Data from: The genetic factors of bilaterian evolutionDryad Digital Repository, doi:10.5061/dryad.4qf7168.
Article and author information
Author details
Kristen A Panfilio
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
- Patricia J Wittkopp, University of Michigan, United States
Version history
- Received: January 31, 2019
- Accepted: July 3, 2020
- Accepted Manuscript published: July 16, 2020 (version 1)
- 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.
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The genetic factors of bilaterian evolution
eLife 9:e45530.
https://doi.org/10.7554/eLife.45530
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As the genome encodes the information crucial for cell growth, a sizeable genomic deficiency often causes a significant decrease in growth fitness. Whether and how the decreased growth fitness caused by genome reduction could be compensated by evolution was investigated here. Experimental evolution with an Escherichia coli strain carrying a reduced genome was conducted in multiple lineages for approximately 1000 generations. The growth rate, which largely declined due to genome reduction, was considerably recovered, associated with the improved carrying capacity. Genome mutations accumulated during evolution were significantly varied across the evolutionary lineages and were randomly localized on the reduced genome. Transcriptome reorganization showed a common evolutionary direction and conserved the chromosomal periodicity, regardless of highly diversified gene categories, regulons, and pathways enriched in the differentially expressed genes. Genome mutations and transcriptome reorganization caused by evolution, which were found to be dissimilar to those caused by genome reduction, must have followed divergent mechanisms in individual evolutionary lineages. Gene network reconstruction successfully identified three gene modules functionally differentiated, which were responsible for the evolutionary changes of the reduced genome in growth fitness, genome mutation, and gene expression, respectively. The diversity in evolutionary approaches improved the growth fitness associated with the homeostatic transcriptome architecture as if the evolutionary compensation for genome reduction was like all roads leading to Rome.
