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Genomic signatures of endosymbiosis: altered mitogenomic compositions and relaxed selection pressure in mitochondrial protein-coding genes of endosymbiotic rhabdocoels (Platyhelminthes)
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  • Marlies Monnens,
  • Tom Artois,
  • Andrew Briscoe,
  • Yander Diez,
  • Keiron Fraser,
  • Brian Leander,
  • T. Littlewood,
  • Maria Santos,
  • Karen Smeets,
  • Niels Van Steenkiste,
  • Maarten Vanhove
Marlies Monnens
Hasselt University

Corresponding Author:marlies.monnens@uhasselt.be

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Tom Artois
Hasselt University
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Andrew Briscoe
Natural History Museum
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Yander Diez
Hasselt University
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Keiron Fraser
University of Plymouth
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Brian Leander
The University of British Columbia
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T. Littlewood
Natural History Museum
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Maria Santos
Universidade do Porto
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Karen Smeets
Hasselt University
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Niels Van Steenkiste
The University of British Columbia
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Maarten Vanhove
Hasselt University
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Abstract

The transition from a free-living lifestyle to endosymbiosis represents a large evolutionary shift, impacting various aspects of any organism’s biology, including its molecular basis. So far, it has been impossible to generalise the impact this lifestyle shift has on genomic architecture. This study explores this phenomenon using a new model system: neodalyellid flatworms (Rhabdocoela), a diverse assemblage of free-living and independently evolved endosymbiotic lineages. A uniquely comprehensive mitochondrial genomic dataset, consisting of 50 complete or partial mitogenome sequences (47 of which are new to science), is constructed, increasing the genomic resources available for rhabdocoel flatworms over tenfold. A robust phylogenomic framework is built, enabling an in-depth exploration of the molecular-genetic signatures associated with evolutionary shifts towards endosymbiosis. To understand speciation influenced by host phylogeny, first steps are taken to unravel the host-switching history of the largest endosymbiotic group of neodalyellids. We test several hypotheses regarding the potential consequences of a symbiotic lifestyle, and find heightened AT content, more pronounced AT skew, and relaxed selection on specific protein-coding genes in endosymbionts compared to their free-living counterparts. Numerous substitutions have accumulated in certain endosymbiotic lineages; however, the correlation with lifestyle remains uncertain. A high frequency of genetic rearrangements across all studied lineages is observed. Our findings affirm the variable nature of rhabdocoel mitogenomes and, for the first time, reveal distinct signatures of an endosymbiotic lifestyle in neodalyellid flatworms. This effort lays the groundwork for future research into the evolutionary and genomic consequences of a symbiotic lifestyle in this and other animal systems.
22 Jul 2024Submitted to Molecular Ecology
23 Jul 2024Submission Checks Completed
23 Jul 2024Assigned to Editor
23 Jul 2024Review(s) Completed, Editorial Evaluation Pending
26 Aug 2024Reviewer(s) Assigned