A transcriptome-based phylogenetic study of hard ticks (Ixodidae)

Hard ticks are widely distributed across temperate regions, show strong variation in host associations, and are potential vectors of a diversity of medically important zoonoses, such as Lyme disease. To address unresolved issues with respect to the evolutionary relationships among certain species or genera, we produced novel RNA-Seq data sets for nine different Ixodes species. We combined this new data with 18 data sets obtained from public databases, both for Ixodes and non-Ixodes hard tick species, using soft ticks as an outgroup. We assembled transcriptomes (for 27 species in total), predicted coding sequences and identified single copy orthologues (SCO). Using Maximum-likelihood and Bayesian frameworks, we reconstructed a hard tick phylogeny for the nuclear genome. We also obtained a mitochondrial DNA-based phylogeny using published genome sequences and mitochondrial sequences derived from the new transcriptomes. Our results confirm previous studies showing that the Ixodes genus is monophyletic and clarify the relationships among Ixodes sub-genera. This work provides a baseline for studying the evolutionary history of ticks: we indeed found an unexpected acceleration of substitutions for mitochondrial sequences of Prostriata, and for nuclear and mitochondrial genes of two species of Rhipicephalus, which we relate with patterns of genome architecture and changes of life-cycle, respectively.We thank Olivier Lambert and Philippe Gourlay from the Centre Veterinaire de la Faune Sauvage et des Ecosystemes des Pays de la Loire (Oniris, Nantes, France), for providing biological material (I. frontalis and I. hexagonus). We are grateful to the Genotoul bioinformatics platform Toulouse Midi-Pyrenees (Bioinfo Genotoul) and to the Bordeaux Bioinformatics Center (CbiB) for providing support and computing resources. Funding for I. acuminatus was provided by the ANR grant OSCAR (ANR-13-BSV7-0018) to O.P. Funding for the transcriptome sequencing of I. uriae was provided by the ANR grant ESPEVEC (ANR-13-BSV7-0018) and French Polar Institute (IPEV, programme no 333 PARASITO-ARCTIQUE) to K.D.M. D.H. was funded by the Marie Sklodowska-Curie Actions (EU-Horizon 2020, Individual Global Fellowship, project no 799609) and the Fund for Scientific Research -Flanders (FWO)