Molecular evolution in rhabdocoel flatworms as a case study on the acquistion of endosymbiosis

Abstract

The transition from a free-living lifestyle to a permanent association with a non-related species comprises a large evolutionary step for any organism. This is reflected by extensive alterations in body plan and genetic makeup. However, it remains unknown whether such changes occur uniformly across all symbiotic lineages alike. Here, we analyzed mitogenomic evolution in three closely related families of endosymbiotic flatworms infecting marine invertebrates: Umagillidae, Pterastericolidae, and Graffillidae (all belonging to Rhabdocoela).

Our study adds over 50 new rhabdocoel mitochondrial genomes, increasing the current mitogenomic database for these animals by more than 10-fold. A high variation in rhabdocoel gene order was inferred, including over 20 distinct gene orders and rearrangements occurring within and between species. Base composition and GC skew are demonstrated to be correlated with endosymbiosis, and trends linking divergence rate with lifestyle are discussed. Inferred interrelationships based on these new data are not fully reflected in the current classification of these animals, demonstrating the need for systematic revision. Co-phylogenetic analyses suggest a host switch from sea urchins to sea cucumbers in umagillid flatworms. Selection pressure was tested in this new phylogenomic framework and, for several protein-coding genes, was shown to be significantly relaxed in endosymbiotic rhabdocoels as compared to their free-living counterparts.

Our study reveals an overall large degree of undiscovered (mito)genomic plasticity in rhabdocoels, indicating that this phenomenon is widespread in flatworms as a whole and not exclusive to the better-studied neodermatans. We also discuss various aspects of mitogenomic content and architecture, such as evolutionary rate, nucleotide composition, and gene order, in relation to these animals' lifestyle. The availability of lineage-specific reference sequences, combined with the assessment of rapidly evolving and conservative mitogenomic regions, will facilitate future molecular work in rhabdocoels, allowing for further study of their evolutionary history and, in particular, the molecular changes accompanying the transition to an obligate symbiotic lifestyle.