First glimpse into the origin and spread of the Asian longhorned tick, Haemaphysalis longicornis, in the United States

Abstract

Established populations of Asian longhorned ticks (ALT), Haemaphysalis longicornis, were first identified in the United States (US) in 2017 by sequencing the mitochondrial cytochrome c oxidase subunit I (cox1) ‘barcoding’ locus followed by morphological confirmation. Subsequent investigations detected ALT infestations in 12, mostly eastern, US states. To gain information on the origin and spread of US ALT, we (1) sequenced cox1 from ALT populations across 9 US states and (2) obtained cox1 sequences from potential source populations [China, Japan and Republic of Korea (ROK) as well as Australia, New Zealand and the Kingdom of Tonga (KOT)] both by sequencing and by downloading publicly available sequences in NCBI GenBank. Additionally, we conducted epidemiological investigations of properties near its initial detection locale in Hunterdon County, NJ, as well as a broader risk analysis for importation of ectoparasites into the area. In eastern Asian populations (China/Japan/ROK), we detected 35 cox1 haplotypes that neatly clustered into two clades with known bisexual versus parthenogenetic phenotypes. In Australia/New Zealand/KOT, we detected 10 cox1 haplotypes all falling within the parthenogenetic cluster. In the United States, we detected three differentially distributed cox1 haplotypes from the parthenogenetic cluster, supporting phenotypic evidence that US ALT are parthenogenetic. While none of the source populations examined had all three US cox1 haplotypes, a phylogeographic network analysis supports a northeast Asian source for the US populations. Within the United States, epidemiological investigations indicate ALT can be moved long distances by human transport of animals, such as horses and dogs, with smaller scale movements on wildlife. These results have relevant implications for efforts aimed at minimizing the spread of ALT in the United States and preventing additional exotic tick introductions.

Comparison of Habitat Suitability Models for Haemaphysalis longicornis Neumann in North America to Determine Its Potential Geographic Range

“…In New Jersey, among more than the 1100 ticks collected from the index site, only one male specimen was found, indicating that the invasive population was parthenogenetic [16]. This was supported by a genetic analysis, which indicated H. longicornis ticks in the United States are more similar to those of parthenogenetic populations than those of bisexual populations [24]. The parthenogenetic populations are distributed in Australia, New Zealand, New Caledonia, Fiji, New Hebrides, Tonga, northeastern Russia, northern Japan, Kyushu and Yakushima in southern Japan, and Sichuan and Shanghai in China [1,25,26].…”

“…Haemaphysalis longicornis has most likely come to North America from East Asia [24]. Companion animals (particularly dogs) entering the United States are thought to be the source [24]. Based on our habitat suitability models, the geographic distribution of the H. longicornis will likely continue to expand in North America.…”

“…Previously, specimens of H. longicornis were misidentified as the native rabbit tick, Haemaphysalis leporispalustris [18], resulting in a delay in an appropriate response to the incursion of this exotic tick. Haemaphysalis longicornis has most likely come to North America from East Asia [24]. Companion animals (particularly dogs) entering the United States are thought to be the source [24].…”

A U.S. Isolate of Theileria Orientalis, Ikeda Genotype, is Transmitted to Cattle by the Invasive Asian Longhorned Tick, Haemaphysalis Longicornis

“…The previous detection of T. orientalis Ikeda in H. longicornis, but not native ticks, from the same area in VA provides further support for this hypothesis [33]. H. longicornis has already spread to at least fourteen U.S. states [27,28,35], survives well in varied environmental conditions [24,27,28,35], and exhibits a wide array of host feeding preference [24], including deer and avian species [25,27,28,35]. Given the cosmopolitan nature of the tick vector, there is signi cant potential for extensive, rapid spread of T. orientalis Ikeda throughout the U.S. due to movement of infected, asymptomatic cattle.…”

“…In conclusion, we have demonstrated that a U.S. population of the invasive Asian longhorned tick, H. longicornis, is a competent vector of the T. orientalis Ikeda genotype isolated from a beef herd outbreak in VA, U.S. in 2017 [23]. Since the Asian longhorned tick has become established in fourteen U.S. states [25,28,35], and many T. orientalis-infected cattle exhibit only mild, intermittent clinical signs, there is signi cant potential for T. orientalis Ikeda to spread widely within the expanding North American range of H. longicornis in the absence of surveillance and livestock tick control measures throughout this and neighboring regions. Furthermore, the development and implementation of improved diagnostic assays for T. orientalis surveillance may be needed to reduce losses incurred by the U.S. cattle industry.…”