Phylogeny and origin of diversification of Amblyomma (Acari: Ixodidae)

Abstract

Abstract Background Amblyomma is the second most diversified genus of Ixodidae that is distributed across the Indomalayan, Afrotropical, Australasian (IAA), Nearctic, and Neotropical biogeographic ecoregions, reaching in the Neotropic its higher diversity. There have been hints in previously published phylogenetic trees from mitochondrial (mt) genome, nuclear rRNA, from combinations of both and morphology that the Australasian Amblyomma or the Australasian Amblyomma plus the Amblyomma species from the southern cone of South America, might be the sister-group to the Amblyomma of the rest of the world. However, a stable phylogenetic framework of Amblyommafor a better understanding of the biogeographic patterns underpinning its diversification is lacking. Methods We used genomic techniques to sequence complete and nearly complete mt genomes –ca. 15 kbp– as well as the ribosomal operons –ca. 8 kbp– for 17 Amblyomma ticks in order to study the phylogeny and biogeographic pattern of the genus Amblyomma, with particular emphasis on the Neotropical region. The new genomic information generated here together with genomic information available of 43 ticks (22 other Amblyommaspecies and 21 other hard ticks –as outgroup–) were used to perform probabilistic methods of phylogenetic and biogeographic inferences and time-tree estimation using biogeographic dates. Results In the present paper, we present the strongest evidence yet that Australasian Amblyomma may indeed be the sister group to the Amblyomma of the rest of the world (species that occur mainly in the Neotropical and Afrotropical zoogeographic regions). Our results showed that all Amblyomma subgenera included, but Walkeriana and Amblyomma, are not monophyletic, as in the cases of Cernyomma, Anastosiella, Xiphiastor, Adenopleura, Aponomma, and Dermiomma. Likewise, our best biogeographic scenario supports the origin of Amblyomma and its posterior diversification in the southern hemisphere at 47.8 and 36.8 Mya, respectively. This diversification could be associated with the end of the connection of Australasia and Neotropical ecoregions by the Antarctic land bridge. Also, the biogeographic analyses let us see the colonization patterns of some neotropical Amblyomma species to the Nearctic. Conclusions We found strong evidence that the main theatre of diversification of Amblyomma was the southern hemisphere, potentially driven by the Antarctic Bridge's intermittent connection in the late Eocene. In addition, the subgeneric classification of Amblyomma lacks evolutionary support. Future studies using denser taxonomic sampling may take us to new findings on the phylogenetic relationships and biogeographic history of Amblyommagenus.