Gene Duplication and Gain in the Trematode Atriophallophorus winterbourni Contributes to Adaptation to Parasitism

Abstract

Gene duplications and novel genes have been shown to play a major role in helminth adaptation to a parasitic lifestyle because they providethenoveltynecessaryforadaptationtoachangingenvironment,suchaslivinginmultiplehosts.Herewepresentthedenovo sequenced and annotated genome of the parasitic trematodeAtriophallophorus winterbourni and its comparative genomic analysis to other major parasitic trematodes. First, we reconstructed the species phylogeny, and dated the split of A. winterbourni from the Opisthorchiata suborder to approximately 237.4 Ma (6120.4 Myr). We then addressed the question of which expanded gene families and gained genes are potentially involved inadaptation to parasitism. To do this, we usedhierarchical orthologous groups to reconstructthreeancestralgenomesonthephylogenyleadingtoA. winterbourni andperformeda GO (GeneOntology)enrichment analysisofthegenecompositionofeachancestralgenome,allowingustocharacterizethesubsequentgenomicchanges.Outofthe 11,499 genes in the A. winterbourni genome, as much as 24% have arisen through duplication events since the speciation of A. winterbourni from the Opisthorchiata, and as much as 31.9% appear to be novel, that is, newly acquired. We found 13 gene families in A. winterbourni to have had more than ten genes arising through these recent duplications; all of which have functions potentially relating to host behavioral manipulation, host tissue penetration, and hiding from host immunity through antigen presentation. We identified several families with genes evolving under positive selection. Our results provide a valuable resource for future studies on the genomic basis of adaptation to parasitism and point to specific candidate genes putatively involved in antagonistic host-parasite adaptation.