Widespread movement of invasive cattle fever ticks (Rhipicephalus microplus) in southern Texas leads to shared local infestations on cattle and deer

Abstract

BackgroundRhipicephalus (Boophilus) microplus is a highly-invasive tick that transmits the cattle parasites (Babesia bovis and B. bigemina) that cause cattle fever. R. microplus and Babesia are endemic in Mexico and ticks persist in the United States inside a narrow tick eradication quarantine area (TEQA) along the Rio Grande. This containment area is threatened by unregulated movements of illegal cattle and wildlife like white-tailed deer (WTD; Odocoileus virginianus).MethodsUsing 11 microsatellite loci we genotyped 1,247 R. microplus from 63 Texas collections, including outbreak infestations from outside the TEQA. We used population genetic analyses to test hypotheses about ecological persistence, tick movement, and impacts of the eradication program in southern Texas. We tested acaricide resistance with larval packet tests (LPTs) on 47 collections.ResultsLPTs revealed acaricide resistance in 15/47 collections (32%); 11 were outside the TEQA and three were resistant to multiple acaricides. Some collections highly resistant to permethrin were found on cattle and WTD. Analysis of genetic differentiation over time at seven properties revealed local gene pools with very low levels of differentiation (FST 0.00-0.05), indicating persistence over timespans of up to 29 months. However, in one neighborhood differentiation varied greatly over a 12-month period (FST 0.03-0.13), suggesting recurring immigration from distinct sources as another persistence mechanism. Ticks collected from cattle and WTD at the same location are not differentiated (FST = 0), implicating ticks from WTD as a source of ticks on cattle (and vice versa) and emphasizing the importance of WTD to tick control strategies. We identified four major genetic groups (K = 4) using Bayesian population assignment, suggesting multiple introductions to Texas.ConclusionsTwo dispersal mechanisms give rise to new tick infestations: 1) frequent short-distance dispersal from the TEQA; and 2) rare long-distance, human-mediated dispersal from populations outside our study area, probably Mexico. The threat of cattle fever tick transport into Texas is increased by acaricide resistance and the ability of R. microplus to utilize WTD as an alternate host. Population genetic analyses may provide a powerful tool for tracking invasions in other parts of the world where these ticks are established.

Multiple mutations in the para -sodium channel gene are associated with pyrethroid resistance in Rhipicephalus microplus from the United States and Mexico

“…microplus ticks obtained from three separate sources were used for this study: 1) 68 USDA-APHIS field collections from southern Texas, 2) nine Mexico field collections, and 3) four USDA-ARS laboratory strains (Additional file 1: Table S1). A tick collection is defined as a sample of ticks collected from a single property within a thirty day time window, as previously described by Busch et al [14]. The most important hosts for R. microplus in southern Texas are cattle (mixed Bos taurus/B.…”

“…The USDA-APHIS field collections were made from both hosts, but the other sampling sources (Mexico field collections and ARS laboratory strains) were from cattle only. All U.S. field collections (n = 68) were sampled by APHIS personnel at 51 properties in southern Texas, as described by Busch et al [14]. Our study utilized excess field ticks that were not needed for larval packet discriminating dose (DD) assays (see section below on acaricide testing) and had been stored frozen in an archive maintained by the USDA-ARS in Kerrville, TX.…”

“…Additionally, we genotyped and analyzed R. microplus (n = 114) from five U.S. (Rm64-Rm68) and nine Mexico (Rm69-Rm77) field collections to determine their probability of assignment to five major genetic groups using 11 microsatellite loci and Bayesian analysis in STRUCTURE as described by Busch et al [14]. These collections were acquired after the completion of these previous analyses, and in some cases, represent unique resistance MLGs that were not present in the 1247 ticks we previously described [14]. Furthermore, all of the ticks that exhibited resistant phenotypes in that previous study assigned to a single genetic group [14].…”

“…Following these procedures the cattle can then be transported beyond the TEQA to feedlots or slaughter facilities but are not allowed to remain within it. Despite rigorous efforts to prevent tick movements into southern Texas, new infestations are being discovered both in the TEQA and beyond it in temporary preventative quarantine areas (TPQAs) (Figure 1) [14,15].…”

“…This is highlighted by an increasing number of infestations in the TEQA and beyond that have been found in recent years to be resistant [19,20]. Nearly all resistant infestations discovered within the U.S. are associated with pyrethroid acaricides, however, resistance to multiple acaricide classes (including coumaphos) has been described in the U.S. [14,19] and Mexico [21,22]. Pyrethroid resistance was first discovered in Mexico in 1994, shortly after the introduction of pyrethroids into the Mexican cattle market in the 1980s [23].…”