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

Joseph D. Busch, Nathan E. Stone, Roxanne Nottingham, Ana Araya-Anchetta, Jillian Lewis, Christian Hochhalter, John R. Giles, Jeffrey Gruendike, Jeanne Freeman, Greta Buckmeier, Deanna Bodine, Roberta Duhaime, Robert J. Miller, Ronald B. Davey, Pia U. Olafson, Glen A. Scoles, David M Wagner

Research output: Contribution to journalArticle

32 Citations (Scopus)

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.

Original languageEnglish (US)
Article number188
JournalParasites and Vectors
Volume7
Issue number1
DOIs
StatePublished - Apr 17 2014

Fingerprint

Rhipicephalus
Deer
Ticks
Fever
Acaricides
Quarantine
Tick Infestations
Population Genetics
Mexico
Babesia bovis
Tick Control
Permethrin
Babesia
Gene Pool
Emigration and Immigration
Microsatellite Repeats
Population
Disease Outbreaks
Parasites

Keywords

  • Bovine babesiosis
  • Cattle fever ticks
  • Eradication
  • Population genetics
  • Rhipicephalus (Boophilus) microplus

ASJC Scopus subject areas

  • Parasitology
  • Infectious Diseases
  • Medicine(all)

Cite this

Widespread movement of invasive cattle fever ticks (Rhipicephalus microplus) in southern Texas leads to shared local infestations on cattle and deer. / Busch, Joseph D.; Stone, Nathan E.; Nottingham, Roxanne; Araya-Anchetta, Ana; Lewis, Jillian; Hochhalter, Christian; Giles, John R.; Gruendike, Jeffrey; Freeman, Jeanne; Buckmeier, Greta; Bodine, Deanna; Duhaime, Roberta; Miller, Robert J.; Davey, Ronald B.; Olafson, Pia U.; Scoles, Glen A.; Wagner, David M.

In: Parasites and Vectors, Vol. 7, No. 1, 188, 17.04.2014.

Research output: Contribution to journalArticle

Busch, JD, Stone, NE, Nottingham, R, Araya-Anchetta, A, Lewis, J, Hochhalter, C, Giles, JR, Gruendike, J, Freeman, J, Buckmeier, G, Bodine, D, Duhaime, R, Miller, RJ, Davey, RB, Olafson, PU, Scoles, GA & Wagner, DM 2014, 'Widespread movement of invasive cattle fever ticks (Rhipicephalus microplus) in southern Texas leads to shared local infestations on cattle and deer', Parasites and Vectors, vol. 7, no. 1, 188. https://doi.org/10.1186/1756-3305-7-188
Busch, Joseph D. ; Stone, Nathan E. ; Nottingham, Roxanne ; Araya-Anchetta, Ana ; Lewis, Jillian ; Hochhalter, Christian ; Giles, John R. ; Gruendike, Jeffrey ; Freeman, Jeanne ; Buckmeier, Greta ; Bodine, Deanna ; Duhaime, Roberta ; Miller, Robert J. ; Davey, Ronald B. ; Olafson, Pia U. ; Scoles, Glen A. ; Wagner, David M. / Widespread movement of invasive cattle fever ticks (Rhipicephalus microplus) in southern Texas leads to shared local infestations on cattle and deer. In: Parasites and Vectors. 2014 ; Vol. 7, No. 1.
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T1 - Widespread movement of invasive cattle fever ticks (Rhipicephalus microplus) in southern Texas leads to shared local infestations on cattle and deer

AU - Busch, Joseph D.

AU - Stone, Nathan E.

AU - Nottingham, Roxanne

AU - Araya-Anchetta, Ana

AU - Lewis, Jillian

AU - Hochhalter, Christian

AU - Giles, John R.

AU - Gruendike, Jeffrey

AU - Freeman, Jeanne

AU - Buckmeier, Greta

AU - Bodine, Deanna

AU - Duhaime, Roberta

AU - Miller, Robert J.

AU - Davey, Ronald B.

AU - Olafson, Pia U.

AU - Scoles, Glen A.

AU - Wagner, David M

PY - 2014/4/17

Y1 - 2014/4/17

N2 - 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.

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KW - Cattle fever ticks

KW - Eradication

KW - Population genetics

KW - Rhipicephalus (Boophilus) microplus

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