An exceptional case of mitochondrial tRNA duplication-deletion events in blood-feeding leeches

With few exceptions, animal mitochondrial genomes are impressively conserved with regard to gene arrangement (synteny). For certain taxonomic groups, specific genomic “hotspot” regions present high levels of gene rearrangements. This is the case for the region between the mitochondrial genes cox2 and atp8 across Annelida, particularly in members of the blood-feeding leeches of the genus Placobdella, for which duplications and deletions of trnD have been detected. Analyses of the intergenic region between cox2 and atp8 of 21 species of Placobdella broadly collected in Canada, Mexico, Portugal, and the USA revealed numerous instances of trnD duplication restricted to the species of Placobdella, and it can be inferred based on the phylogenetic position of samples with a single trnD copy that the duplicated condition is independently lost on five occasions. In species with the duplicated trnD, great variation in the size of insertions between both copies, in the secondary structure of the trnD products, and in their respective anticodon were found. For each of three species (Placobdella rugosa, P. ringueleti, and P. lamothei), samples collected from different localities exhibit different gene arrangements, revealing an unexpected amount of intraspecific variation. The rate at which rearrangements are occurring in this mitogenome region within Placobdella has no known equivalent in the animal kingdom and we propose it as a hotspot for tRNA genes duplication-deletion. Our findings are partially compatible with a “tandem duplication and random loss” model of evolution, however in species with just one trnD, it is the second copy the one that we inferred is eliminated. This is, to our knowledge, the first study where such changes are mapped in a phylogeny looking to reveal the state of the ancestor of the group.