Genetic diversity, pyrethroid resistance, and pathogen infection in populations of Rhipicephalus sanguineus sensu lato (Acari: Ixodidae) collected from dogs in Thailand

Abstract

Brown dog ticks, Rhipicephalus sanguineus sensu lato (tropical lineage), are one of the common ectoparasites infesting dogs in Thailand. Importantly, these ticks could harbor several animal-related and zoonotic pathogens affecting animal health, including Anaplasma spp., Ehrlichia spp., and Rickettsia spp. A wide range of acaricides, including pyrethroids, are used to manage infestation. Nevertheless, prolonged or preventive use of acaricides with similar mechanisms can promote the emergence of resistant tick populations. Reported resistance mechanisms of pyrethroid in Rhipicephalus ticks include target-site insensitivity caused by point mutations in the sodium channel gene. This study aimed to study the genetic diversity of Rh. sanguineus populations through morphological examination and molecular identification, to investigate the status of pyrethroid resistance using a PCR assay targeting the point mutation in the sodium channel gene of Rh. sanguineus, and to screen ticks for selected pathogens, including Anaplasma spp., Bartonella spp., Ehrlichia spp., Rickettsia spp., Babesia spp., and Hepatozoon spp., using PCR assays. A total of 1,071 ticks were collected from 122 dogs in 16 provinces in Thailand. For genetic diversity, 8.7% (45/520) of individual ticks and 3.9% (2/52) of tick pools were sequenced and shown as Rh. linnaei representative genome for 99.75–100%, suggesting that Rh. sanguineus in Thailand should be accurately classified as Rh. linnaei. Only individual ticks were screened for mutation. The results revealed 1.72% (9/520) of homozygous susceptible (SS) samples, 98.3% (511/520) of heterozygous (SR) samples, and no homozygous resistant (RR) sample. The presence of SR genotypes for 98.3% indicated the circulation of resistance-associated alleles, suggesting potentially partial or advanced pyrethroid resistance within this tick population. Pathogen screening showed 1.6% (9/572), 6.8% (39/572), 28.1% (161/572), 2.6% (15/572), and 2.6% (15/572) of individual ticks and tick pools tested positive for Babesia spp., Hepatoozoon spp., Anaplasmataceae family, Bartonella spp., and Rickettsia spp., respectively. Pathogen sequencing results showed that Babesia vogeli (n = 8), Hepatozoon canis (n = 17), Anaplasma platys (n = 5), Anaplasma bovis (n = 1), Ehrlichia canis (n = 13), Bartonella henselae (n = 4), and uncultured Rickettsia sp. (n = 12) were found in these tick samples. Notably, pathogens with zoonotic potential (i.e., Anaplasma bovis, Bartonella hensalae, and Rickettsia sp.) were present in ticks carrying the SR genotype. Altogether, our findings highlight the critical need for enhanced acaricide resistance monitoring, accurate tick species identification, and updated tick-control strategies. Addressing these issues is vital to protect both animal and human health from the growing threat posed by resistant tick populations capable of transmitting important vector-borne pathogens.