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Title: Widespread Movement of Invasive Cattle Fever Ticks (Rhipicephalus microplus) in Southern Texas Leads to Shared Local Infestations on Cattle and Deer

Author
item BUSCH, JOSEPH - Northern Arizona University
item STONE, NATHAN - Northern Arizona University
item NOTTINGHAM, ROXANNE - Northern Arizona University
item ARAYA-ANCHETTA, A - Northern Arizona University
item LEWIS, J - Northern Arizona University
item HOCHHALTER, C - Northern Arizona University
item GILES, JOHN - Northern Arizona University
item FREEMAN, J - Former ARS Employee
item Buckmeier, Beverly - Greta
item Bodine, Deanna
item DUHAIME, ROBERTA - Animal And Plant Health Inspection Service (APHIS)
item Miller, Robert
item DAVEY, RONALD - Former ARS Employee
item Olafson, Pia
item Scoles, Glen
item WAGNER, DAVE - Northern Arizona University

Submitted to: Parasites & Vectors
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/12/2014
Publication Date: 4/17/2014
Citation: Busch, J.D., Stone, N.E., Nottingham, R., Araya-Anchetta, A., Lewis, J., Hochhalter, C., Giles, J.R., Freeman, J.M., Buckmeier, B.G., Bodine, D.L., Duhaime, R.A., Miller, R., Davey, R.B., Olafson, P.U., Scoles, G.A., Wagner, D.M. 2014. Widespread movement of invasive cattle fever ticks (Rhipicephalus microplus) in southern Texas leads to shared local infestations on cattle and deer. Parasites & Vectors. 7:188.

Interpretive Summary: Rhipicephalus microplus is a highly-invasive tick that vectors cattle fever parasites (Babesia bovis and B. bigemina). In North America, ticks and Babesia are endemic in Mexico and ticks persist in the United States inside a narrow permanent quarantine zone (PQZ) along the Rio Grande. This containment area is threatened by importation of cattle from Mexico (1-2 million annually), unregulated movement of cattle, and movements of infested white-tailed deer and other wildlife. Molecular tools were used to analyze 1,247 R. microplus ticks from 63 Texas collections, including new infestations from "tick-free" areas north of the PQZ. Using population genetic analyses we deduced that two dispersal mechanisms give rise to new tick infestations: 1) frequent short-distance dispersal from the PQZ; and 2) rare long-distance, human-mediated dispersal from populations outside our study area, probably Mexico. We also assessed acaricide susceptibility for 47 collections and found that 15/47 collections (32%) displayed resistance; 11 were located outside of the PQZ and 3 were resistant to multiple acaricides. Some tick collections highly resistant to permethrin were found on cattle and WTD. We found that ticks collected from cattle and WTD at the same location are not genetically differentiated, implicating ticks from WTD as a source of ticks on cattle and emphasizing the importance of WTD in implementing tick control strategies. 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 cattle fever ticks have invaded.

Technical Abstract: Background: Rhipicephalus microplus is a highly-invasive tick that vectors cattle fever parasites (Babesia bovis and B. bigemina). In North America, ticks and Babesia are endemic in Mexico and ticks persist in the United States inside a narrow permanent quarantine zone (PQZ) along the Rio Grande. This containment area is threatened by importation of cattle from Mexico (1-2 million annually), unregulated movement of cattle, and movements of infested white-tailed deer (WTD; Odocoileus virginianus) and other wildlife. Methods: Using 11 microsatellite loci we genotyped 1,247 R. microplus from 63 Texas collections, including new infestations from "tick-free" areas north of the PQZ. We used population genetic analyses to test hypotheses about ecological persistence, tick movement, and impacts of the eradication program in southern Texas. We also performed larval packet tests (LPTs) on 47 collections to test acaricide resistance. Results: LPTs revealed acaricide resistance in 15/47 collections (32%); 11 were located outside of the PQZ and 3 were resistant to multiple acaricides. Some tick collections highly resistant to permethrin were found on cattle and WTD. Analysis of genetic differentiation over time at seven properties revealed local tick gene pools with very low levels of differentiation (FST 0.00-0.05), indicating persistence over timespans of up to 29 months. In one neighborhood, however, differentiation varied greatly over a 12-month period (FST 0.03-0.13), suggesting recurring immigration from distinct sources as another mechanism of persistence. We found that 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 emphasizing the importance of WTD to tick control strategies. We also identified four major genetic groups (K=4) using Bayesian population assignment, suggesting multiple tick introductions to Texas. Conclusions: Two dispersal mechanisms give rise to new tick infestations: 1) frequent short-distance dispersal from the PQZ; 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 cattle fever ticks have invaded.