Evolutionary dynamics of transposable elements in bdelloid rotifers
- University of Oxford, United Kingdom
- University College London, United Kingdom
- University of Cologne, Germany
- National Research Council of Italy, Italy
- University of Konstanz, Germany
- Marine Biological Laboratory, United States
Abstract
Transposable elements (TEs) are selfish genomic parasites whose ability to spread autonomously is facilitated by sexual reproduction in their hosts. If hosts become obligately asexual, TE frequencies and dynamics are predicted to change dramatically, but the long-term outcome is unclear. Here, we test current theory using whole-genome sequence data from eight species of bdelloid rotifers, a class of invertebrates in which males are thus far unknown. Contrary to expectations, we find a variety of active TEs in bdelloid genomes, at an overall frequency within the range seen in sexual species. We find no evidence that TEs are spread by cryptic recombination or restrained by unusual DNA repair mechanisms. Instead, we find that that TE content evolves relatively slowly in bdelloids and that gene families involved in RNAi-mediated TE suppression have undergone significant expansion, which might mitigate the deleterious effects of active TEs and compensate for the consequences of long-term asexuality.
Data availability
All raw sequencing data have been deposited in the relevant International Nucleotide Sequence Database Collaboration (INSDC) databases under the Study ID PRJEB39843. Genome assemblies and gene predictions have been deposited at DDBJ/ENA/GenBank with the same Study ID. Figure 2--source data 2 has been uploaded to Dryad Digital Repository (doi:10.5061/dryad.fbg79cnsr).
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Evolutionary dynamics of transposable elements in bdelloid rotifersEuropean Nucleotide Archive (ENA), PRJEB39843.
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Figure 2--source data 2. Reference and maxhap assembly RepeatMasker output filesDryad Digital Repository, doi:10.5061/dryad.fbg79cnsr.
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Comparative genomics of bdelloid rotifers: evaluating the effects of asexuality and desiccation tolerance on genome evolutionEuropean Nucleotide Archive (ENA), PRJEB23547.
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Genome sequencing of Adineta vagaEuropean Nucleotide Archive (ENA), PRJEB1171.
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Brachionus plicatilis species complex Genome sequencing and assemblyEuropean Nucleotide Archive (ENA), PRJNA541909.
Article and author information
Author details
Philipp H Schiffer
Funding
Natural Environment Research Council (NE/M01651X/1)
- Timothy G Barraclough
Natural Environment Research Council (NE/S010866/2)
- Christopher G Wilson
- Timothy G Barraclough
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Antonis Rokas, Vanderbilt University, United States
Version history
- Received: September 17, 2020
- Accepted: February 4, 2021
- Accepted Manuscript published: February 5, 2021 (version 1)
- Accepted Manuscript updated: February 11, 2021 (version 2)
- Version of Record published: March 8, 2021 (version 3)
Copyright
© 2021, Nowell 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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Evolutionary dynamics of transposable elements in bdelloid rotifers
eLife 10:e63194.
https://doi.org/10.7554/eLife.63194
Further reading
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- Evolutionary Biology
Understanding how plants adapt to changing environments and the potential contribution of transposable elements (TEs) to this process is a key question in evolutionary genomics. While TEs have recently been put forward as active players in the context of adaptation, few studies have thoroughly investigated their precise role in plant evolution. Here, we used the wild Mediterranean grass Brachypodium distachyon as a model species to identify and quantify the forces acting on TEs during the adaptation of this species to various conditions, across its entire geographic range. Using sequencing data from more than 320 natural B. distachyon accessions and a suite of population genomics approaches, we reveal that putatively adaptive TE polymorphisms are rare in wild B. distachyon populations. After accounting for changes in past TE activity, we show that only a small proportion of TE polymorphisms evolved neutrally (<10%), while the vast majority of them are under moderate purifying selection regardless of their distance to genes. TE polymorphisms should not be ignored when conducting evolutionary studies, as they can be linked to adaptation. However, our study clearly shows that while they have a large potential to cause phenotypic variation in B. distachyon, they are not favored during evolution and adaptation over other types of mutations (such as point mutations) in this species.
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Biologically-controlled mineralization producing organic-inorganic composites (hard skeletons) by metazoan biomineralizers has been an evolutionary innovation since the earliest Cambrian. Among them, linguliform brachiopods are one of the key invertebrates that secrete calcium phosphate minerals to build their shells. One of the most distinct shell structures is the organo-phosphatic cylindrical column exclusive to phosphatic-shelled brachiopods, including both crown and stem groups. However, the complexity, diversity, and biomineralization processes of these microscopic columns are far from clear in brachiopod ancestors. Here, exquisitely well-preserved columnar shell ultrastructures are reported for the first time in the earliest eoobolids Latusobolus xiaoyangbaensis gen. et sp. nov. and Eoobolus acutulus sp. nov. from the Cambrian Series 2 Shuijingtuo Formation of South China. The hierarchical shell architectures, epithelial cell moulds, and the shape and size of cylindrical columns are scrutinised in these new species. Their calcium phosphate-based biomineralized shells are mainly composed of stacked sandwich columnar units. The secretion and construction of the stacked sandwich model of columnar architecture, which played a significant role in the evolution of linguliforms, is highly biologically controlled and organic-matrix mediated. Furthermore, a continuous transformation of anatomic features resulting from the growth of diverse columnar shells is revealed between Eoobolidae, Lingulellotretidae, and Acrotretida, shedding new light on the evolutionary growth and adaptive innovation of biomineralized columnar architecture among early phosphatic-shelled brachiopods during the Cambrian explosion.
