Comparative mitogenomics elucidates the population genetic structure of Amblyomma testudinarium in Japan and a closely related Amblyomma species in Myanmar

Abstract

Ticks are the second most important vector capable of transmitting diseases affecting the health of both humans and animals. Amblyomma testudinarium Koch 1844 (Acari: Ixodidae), is a hard tick species having a wide geographic distribution in Asia.In this study, we analyzed the composition of A. testudinarium whole mitogenomes from various geographical regions in Japan and investigated the population structure, demographic patterns, and phylogeographic relationship with other ixodid species. In addition, we characterized a potentially novel tick species closely related to A. testudinarium from Myanmar. Phylogeographic inference and evolutionary dynamics based on the 15 mitochondrial coding genes supported that A. testudinarium population in Japan is resolved into a star-like haplogroup and suggested a distinct population structure of A. testudinarium from Amami island in Kyushu region. Correlation analysis using Mantel test statistics showed that no significant correlation was observed between | INTRODUC TI ONTicks are obligatory ectoparasites that feed on the blood of various vertebrate species including mammals, birds, and reptiles (Brites-Neto et al., 2015). There are three major tick families described, namely, Ixodidae, Argasidae, and Nuttalliellidae (Horak et al., 2002). Some species of Ixodidae (hard ticks) and Argasidae (soft ticks) are implicated in the transmission of several bacterial, viral, and protozoan pathogens to humans and animals. Ticks are widely distributed around the world, especially in warm humid regions to remain hydrated and subsequently undergo metamorphosis (Vail & Smith, 1998).Amblyomma is the third biggest genus of Ixodidae ticks with more than 130 species (Guglielmone et al., 2014), some of which act as disease vectors of many pathogens, for instance Rickettsia tamurae and Rickettsia raoultii causing spotted fever (Fournier et al., 2006;Piotrowski & Rymaszewska, 2020), Ehrlichia chaffeensis causing ehrlichiosis (Cao et al., 2000), and severe fever with thrombocytopenia syndrome (SFTS) virus causing SFTS in humans (Suh et al., 2016). The geographical distribution of Amblyomma species is expanding due to anthropogenic activities, climate change, and increased geographical ranges of animal hosts (Childs & Paddock, 2003). In the United States, Amblyomma americanum populations have been constantly enlarging that contributed to change in the epidemiology of spotted fever group rickettsiosis in the country (Dahlgren et al., 2016;Sagurova et al., 2019). In Africa, Amblyomma species transmit Ehrlichia ruminantium and Rickettsia africae that cause heartwater disease and African tick-bite fever in animals and humans, respectively (Kelly et al., 1996;Yunker, 1996). Furthermore, although very little is known about the diseases caused by pathogens transmitted by this group of ticks (Jabin et al., 2019), there are 14 Amblyomma species in Asia (Voltzit, 2002), and at least three species, including

Complete Mitogenomes of Ticks Ixodes acutitarsus and Ixodes ovatus Parasitizing Giant Panda: Deep Insights into the Comparative Mitogenomic and Phylogenetic Relationship of Ixodidae Species

“…Ticks, which are common hematophagous ectoparasites, are capable of parasitizing almost all groups of terrestrial vertebrates, including mammals, birds, lizards, snakes, and toads [ 1 , 2 , 3 ]. Ticks rank second in the world as vectors of disease, and they can harbor and transmit a great variety of pathogens, including virus, bacteria, fungi, protozoa, and nematode, to humans, livestock, and wildlife [ 2 , 4 , 5 , 6 ]. More than 28 species of ticks are known to cause a variety of human diseases [ 5 , 7 ].…”

First mitochondrial genome of Amblyomma triste Koch, 1844 (Acari: Ixodidae): Evidence for studying species within the A. maculatum group</p >

“…Mitogenomes can provide a deeper understanding of tick systematics, allowing the resolution of phylogenetic relationships that are problematic when using partial genes (Wang et al 2019; Kelava et al 2021; Mohamed et al 2022). In this study, the interspecific distances of CDSs+rRNA genes between A. triste and A. maculatum were 4.2%, similar to the reported by Cotes-Perdomo et al (2023b) when comparing the complete genomes of two species of the A. marmoreum complex ( Amblyomma nuttalli and Amblyomma sparsum ) with an interspecific distance of 4.4%.…”

“…Currently, Ixodidae is the most diverse family with approximately 759 species and 15 genera, where Amblyomma is the third largest in terms of species number (136), surpassed by Ixodes and Haemaphysalis with 266 and 176 species, respectively (Guglielmone et al 2023). Amblyomma species have received special attention due to their involvement in pathogen transmission (e.g., Anaplasma , Ehrlichia , Hepatozoon , Rickettsia ) and by the presence of cryptic species (complexes or groups) in America, such as the Amblyomma cajennense , Amblyomma maculatum , and Amblyomma ovale (Dumler et al 2001; Demoner et al 2013; Rivera-Páez et al 2017; Suwanbongkot et al 2019), and the Amblyomma testudinarium and Amblyomma marmoreum complexes in Asia and Africa, respectively (Mohamed et al 2022; Cotes-Perdomo et al 2023b).…”

Nationwide survey of ticks on domesticated animals in Taiwan: Revealing the hidden threat to animal and public health

“…Third, A. testudinarium deserves further attention, although its numbers are relatively smaller than those of the other two dominant species. It is found in East and Southeast Asia (e.g., Malaysia, India, Japan, Korea, eastern China and Taiwan), and has been observed in wildlife species and occasionally in humans (Estrada‐Pena & Jongejan, 1999; Kang et al, 1981; Lim et al, 2018; Mohamed et al, 2022; Motoi et al, 2013; Nakao et al, 2021; Robbins, 2005; Suh et al, 2016; Tateno et al, 2015). This tick species is known to transmit numerous pathogens, including Borrelia , Rickettsia , Hepatozoon and tick‐borne viruses (Motoi et al, 2013; Suh et al, 2016; Sun et al, 2015; Tateno et al, 2015; Yun et al, 2016).…”