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

Abstract

Background: Rhipicephalus (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).

Methods: Using 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.

Results: LPTs 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.

Conclusions: Two 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.

Figure 1

Map of sampling locations for Rhipicephalus microplus ticks in southern Texas. The tick eradication quarantine area (TEQA) lies between the international border between Texas and Mexico (the Rio Grande River) and the pink line. This genetic study used 63 tick collections made at 46 properties during 2005–2010 (see Table 1 for sample sizes and dates of collection). Each location is color-coded to represent the four main genetic groups (see Additional file 3: Figure S1) that were found with Bayesian assignment testing using STRUCTURE software [19]. The light blue symbols represent highly admixed collections along the Rio Grande River that do not assign to any single genetic group. The green group in eastern Zapata Co. (Rm20-Rm32) includes pyrethroid-resistant tick collections. The two temporary preventative quarantine areas (TPQAs or blanket quarantine zones) represented by light green polygons were enforced during 2007–2012 to address new infestations outside of the TEQA; the maximum extent of these TPQAs is shown (year 2009). The blue triangles from the inset map mark three livestock feedyards where traceback ticks from Prop37 (Rm43) were transported in April of 2008 and later eradicated.

Figure 2

Isolation over time in Texas collections of Rhipicephalus microplus. Tick samples include collections from cattle and white-tailed deer. Panel a) pairwise F_ST comparisons over time within seven individual properties (see Table 1, collection subset “T_A”). Each individual point is a pairwise θ value between two collections at a single property, which controls for spatial variation. Filled pink triangles denote pairwise comparisons within Prop11 in Zapata Co.; filled blue squares denote pairwise comparisons within Prop34 in Starr Co.; open circles represent pairwise comparisons within five other properties sampled over shorter time intervals. Panel b) pairwise F_ST comparisons for collections sampled within a 4 km neighborhood around Prop11 (Zapata Co.) or Prop34 (Starr Co.) (see Table 1, collection subset “T_B”). Symbol definitions are the same as for Panel a, with the following additions: open pink triangles denote all pairwise θ values among collections near Prop11; open blue squares denote all pairwise θ values among collections near Prop34.

Figure 3

Isolation by distance in Texas populations of Rhipicephalus microplus ticks collected during two years of high infestation rates, a) 2008 and b) 2009. Open grey circles denote all possible pairwise comparisons of ticks from all hosts (cattle and white-tailed deer [WTD]). Closed red triangles denote comparisons among ticks from WTD only. Pairwise F_ST estimates from FSTAT (θ) were transformed to F_ST /(1- F_ST) according to the method of Rousset [39]. The regression line (solid black line) and bootstrapped 95% confidence limits for slope (dashed lines) were calculated using reduced major axis (RMA) regression in the IBD program [36]. The regression equation is only provided for “all” comparisons.