Genomic signatures of endosymbiosis: altered mitogenomic compositions
and relaxed selection pressure in mitochondrial protein-coding genes of
endosymbiotic rhabdocoels (Platyhelminthes)
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.