Sequencing of complete mitochondrial genomes confirms synonymization of Hyalomma asiaticum asiaticum and kozlovi, and advances phylogenetic hypotheses for the Ixodidae

Abstract

Phylogeny of hard ticks (Ixodidae) remains unresolved. Mitochondrial genomes (mitogenomes) are increasingly used to resolve phylogenetic controversies, but remain unavailable for the entire large Hyalomma genus. Hyalomma asiaticum is a parasitic tick distributed throughout the Asia. As a result of great morphological variability, two subspecies have been recognised historically; until a morphological data-based synonymization was proposed. However, this hypothesis was never tested using molecular data. Therefore, objectives of this study were to: 1. sequence the first Hyalomma mitogenome; 2. scrutinise the proposed synonymization using molecular data, i.e. complete mitogenomes of both subspecies: H. a. asiaticum and kozlovi; 3. conduct phylogenomic and comparative analyses of all available Ixodidae mitogenomes. Results corroborate the proposed synonymization: the two mitogenomes are almost identical (99.6%). Genomic features of both mitogenomes are standard for Metastriata; which includes the presence of two control regions and all three "Tick-Box" motifs. Gene order and strand distribution are perfectly conserved for the entire Metastriata group. Suspecting compositional biases, we conducted phylogenetic analyses (29 almost complete mitogenomes) using homogeneous and heterogeneous (CAT) models of substitution. The results were congruent, apart from the deep-level topology of prostriate ticks (Ixodes): the homogeneous model produced a monophyletic Ixodes, but the CAT model produced a paraphyletic Ixodes (and thereby Prostriata), divided into Australasian and non-Australasian clades. This topology implies that all metastriate ticks have evolved from the ancestor of the non-Australian branch of prostriate ticks. Metastriata was divided into three clades: 1. Amblyomminae and Rhipicephalinae (Rhipicephalus, Hyalomma, Dermacentor); 2. Haemaphysalinae and Bothriocrotoninae, plus Amblyomma sphenodonti; 3. Amblyomma elaphense, basal to all Metastriata. We conclude that mitogenomes have the potential to resolve the long-standing debate about the evolutionary history of ticks, but heterogeneous evolutionary models should be used to alleviate the effects of compositional heterogeneity on deep-level relationships.

Tick mitochondrial genomes: structural characteristics and phylogenetic implications

“…In recent years, phylogenetic studies based on mt-genome sequences have been effectively carried out for many tick species [21, 28–30, 36, 40]. These achievements are also essential for understanding the genetic differentiation and phylogeny of ticks [31–34]. However, the genera Anomalohimalaya , Compluriscutula , Margaropus and Nosomma still lack complete mt-genome information, and most species were sampled in a limited geographical area [45].…”

The Complete Mitochondrial Genome and Expression Profile of Mitochondrial Protein-Coding Genes in the Bisexual and Parthenogenetic Haemaphysalis longicornis

“…The minor rearrangement type was relatively common and occurred only in exchanges of the tRNA position (Cameron et al, 2007). This kind of rearrangement was common in Ixodes genus, but the rearrangement degree was significantly lower than that observed in other genera of ticks (Liu et al, 2018). The major gene rearrangement referred to the rearrangement or inversion of PCG or rRNA genes and infrequently occurred in insects.…”

“…The heavy strand contains 9 genes ( cox1 , cox2 , cox3 , cytb , nad2 , nad3 , nad6 , atp6 , and atp8 ), and the light strand contains 4 genes ( nad1 , nad4 , nad4l , and atp8 ). Mitochondrial genes of H. longicornis displayed distinct rearrangement characteristics from Haemaphysalis genus (Liu et al, 2018), and the arrangement and distribution of 13 PCGs were completely consistent in the two reproductive populations. Four start codons (ATA, ATT, ATG, and ATC) were detected in H. longicornis .…”

“…The secondary structure of tRNA differs only at a few bases between the two reproductive populations. The DHU arms of trnC and trnS1 were absent in the two populations, which were common features in ticks and insects (Jühling et al, 2009; Cameron, 2014; Williamsnewkirk et al, 2015; Yuan et al, 2015; Liu et al, 2018). The base mismatch of mitochondrial tRNA genes is a common phenomenon (Jühling et al, 2012), which mainly appears in four tRNA structures: the amino acid acceptor arm (AA), the TΨC arm (T), the anticodon arm (AC) and the dihydrouridine arm (DHU) (Zhang et al, 2012).…”

“…The major gene rearrangement referred to the rearrangement or inversion of PCG or rRNA genes and infrequently occurred in insects. Liu et al reported the major gene rearrangement from some tick genera, such as Haemaphysalis , Amblyomma , and Rhipicephalus (Liu et al, 2018). There were three types of tRNA gene position changes: shuffling (local rearrangements), translocation (cross-gene displacement) and inversion (change the encoding or transcriptional direction) (Dowton and Austin, 1999).…”