Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-26T13:07:07.330Z Has data issue: false hasContentIssue false
  • English
  • Français

Population genetic structure of the prairie dog flea and plague vector, Oropsylla hirsuta

Published online by Cambridge University Press:  10 August 2010

R. JORY BRINKERHOFF ,
ANDREW P. MARTIN ,
RYAN T. JONES  and
SHARON K. COLLINGE
R. JORY BRINKERHOFF*
Affiliation:
Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, 80309-0334, USA
ANDREW P. MARTIN
Affiliation:
Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, 80309-0334, USA
RYAN T. JONES
Affiliation:
Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, 80309-0334, USA
SHARON K. COLLINGE
Affiliation:
Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, 80309-0334, USA Environmental Studies Program, University of Colorado, 334 UCB, Boulder, CO, 80309-0334, USA
*
*Corresponding author: Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, 80309-0334, USA. Tel: +203 785 2272. Fax: +203 785 3604. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Oropsylla hirsuta is the primary flea of the black-tailed prairie dog and is a vector of the plague bacterium, Yersinia pestis. We examined the population genetic structure of O. hirsuta fleas collected from 11 prairie dog colonies, 7 of which had experienced a plague-associated die-off in 1994. In a sample of 332 O. hirsuta collected from 226 host individuals, we detected 24 unique haplotype sequences in a 480 nucleotide segment of the cytochrome oxidase II gene. We found significant overall population structure but we did not detect a signal of isolation by distance, suggesting that O. hirsuta may be able to disperse relatively quickly at the scale of this study. All 7 colonies that were recently decimated by plague showed signs of recent population expansion, whereas 3 of the 4 plague-negative colonies showed haplotype patterns consistent with stable populations. These results suggest that O. hirsuta populations are affected by plague-induced prairie dog die-offs and that flea dispersal among prairie dog colonies may not be dependent exclusively on dispersal of prairie dogs. Re-colonization following plague events from plague-free refugia may allow for rapid flea population expansion following plague epizootics.

Keywords

disease ecologydispersalpathogen transmissionreservoir hostSiphonapteraYersinia pestis
Type
Research Article
Information
Parasitology , Volume 138 , Issue 1 , January 2011 , pp. 71 - 79
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Brinkerhoff, R. J. (2008). Mammal and flea occurrence in association with black-tailed prairie dog (Cynomys ludovicianus) colonies: implications for interspecific plague transmission. Ph.D. Dissertation, University of Colorado, Boulder, CO, USA.Google Scholar
Brinkerhoff, R. J., Markeson, A. B., Knouft, J. H., Gage, K. L. and Montenieri, J. A. (2006). Abundance patterns of two Oropsylla (Siphonaptera: Ceratophylidae) species on black-tailed prairie dog (Cynomys ludovicianus) hosts. Journal of Vector Ecology 31, 355–363.CrossRefGoogle Scholar
Chao, A. (1984). Nonparametric estimation of the number of classes in a population. Scandanavian Journal of Statistics 11, 265–270.Google Scholar
Collinge, S. K., Johnson, W. C., Ray, C., Matchett, R., Grensten, J., Cully, J. F., Gage, K. L., Kosoy, M. Y., Loye, J. E. and Martin, A. P. (2005). Landscape structure and plague occurrence in black-tailed prairie dogs on grasslands of the western USA. Landscape Ecology 20, 941–955.CrossRefGoogle Scholar
Conlin, D. B. (2005). Abundance of rodents on grasslands characterized by patchy distribution of prairie dogs and urban development. Master's Thesis, University of Colorado, Boulder, CO, USA.Google Scholar
Criscione, C. D., Poulin, R. and Blouin, N. S. (2005). Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Molecular Ecology 14, 2247–2257.CrossRefGoogle ScholarPubMed
Cully, J. F. and Williams, E. S. (2001). Interspecific comparisons of sylvatic plague in prairie dogs. Journal of Mammalogy 82, 894–905.2.0.CO;2>CrossRefGoogle Scholar
de la Cruz, K. D. and Whiting, M. F. (2003). Genetic and phylogeographic structure of populations of Pulex simulans (Siphonaptera) in Peru inferred from two genes (CytB and CoII). Parasitology Research 91, 55–59.CrossRefGoogle ScholarPubMed
Dryden, M. W. (1989). Biology of the cat flea, Ctenocephalides felis felis. Companion Animal Practice 19, 23–27.Google Scholar
Eisen, R. J., Bearden, S. W., Wilder, A. P., Montenieri, J. A., Antolin, M. F. and Gage, K. L. (2006). Early-phase transmission of Yersinia pestis by unblocked fleas as a mechanism for explaining rapidly spreading plague epizootics. Proceedings of the National Academy of Sciences, USA 103, 15380–15385.CrossRefGoogle ScholarPubMed
Furman, D. P. and Catts, E. P. (1982). Manual of Medical Entomology. 4th Edn.Cambridge University Press, New York, USA.Google Scholar
Gage, K. L. and Kosoy, M. Y. (2005). Natural history of plague: perspectives from more than a century of research. Annual Review of Entomology 50, 505–528.CrossRefGoogle ScholarPubMed
Garrett, M. G. and Franklin, W. L. (1981). Prairie dog dispersal in Wind Cave National Park: possibilities for control. Great Plains Wildlife Damage Control Proceedings 5, 185–188.Google Scholar
Hubbard, C. A. (1968). Fleas of Western North America. Iowa State College Press, Iowa, USA.Google Scholar
Jones, P. H. and Britten, H. B. (2010). The absence of concordant population genetic structure in the black-tailed prairie dog and the flea, Oropsylla hirsuta, with implications for the spread of Yersinia pestis. Molecular Ecology 19, 2039–2049.CrossRefGoogle ScholarPubMed
Kartman, L., Quan, S. F. and Lechleinter, B. R. (1962). Die-off of a Gunnison's prairie dog colony in central Colorado II. Retrospective determination of plague infection in flea vectors. Zoonoses Research 1, 201–224.Google ScholarPubMed
Krasnov, B. R., Khokhlova, I. S., Fielden, L. J. and Burdelova, N. V. (2001). Effect of air temperature and humidity on the survival of pre-imaginal stages of two flea species. Journal Medical Entomology 38, 630–637.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Khokhlova, I. S., Fielden, L. J. and Burdelova, N. I. (2002). Time of survival under starvation in two flea species (Siphonaptera : Pulicidae) at different air temperatures and relative humidities. Journal of Vector Ecology 27, 70–81.Google ScholarPubMed
Krasnov, B. R., Shenbrot, G. I., Mouillot, D., Khokhlova, I. S. and Poulin, R. (2006). Ecological characteristics of flea species relate to their suitability as plague vectors. Oecologia 149, 474–481.CrossRefGoogle ScholarPubMed
Lorange, E. A., Race, B. L., Sebbane, F. and Hinnebusch, B. J. (2005). Poor vector competence of fleas and the evolution of hypervirulence in Yersinia pestis. Journal of Infectious Diseases 191, 1907–1912.CrossRefGoogle ScholarPubMed
Magle, S. B., Theobald, D. M. and Crooks, K. R. (2009). A comparison of metrics predicting landscape connectivity for a highly interactive species along an urban gradient in Colorado, USA. Landscape Ecology 24, 267–280.CrossRefGoogle Scholar
Markeson, A. B. (2005). Spatial and seasonal patterns of pathogen prevalence in grassland rodents of Boulder County, Colorado. Master's Thesis, University of Colorado, Boulder, CO, USA.Google Scholar
Marshall, A. G. (1981). The Ecology of Ectoparasitic Insects. Academic Press, London, UK.Google Scholar
McCoy, K. D., Boulinier, T. and Tirard, C. (2005). Comparative host-parasite population structures: disentangling prospecting and dispersal in the black-legged kittiwake Rissa tridactyla. Molecular Ecology 14, 2825–2838.CrossRefGoogle ScholarPubMed
McGee, B. K., Butler, M. J., Pence, D. B., Alexander, J. L., Nissen, J. B., Ballard, W. B. and Nicholson, K. L. (2006). Possible vector dissemination by swift foxes following a plague epizootic in black-tailed prairie dogs in northwestern Texas. Journal of Wildlife Diseases 42, 415–420.CrossRefGoogle ScholarPubMed
Perkins, S. L. (2001). Phylogeography of Caribbean lizard malaria: tracing the history of vector-borne parasites. Journal of Evolutionary Biology 14, 34–45.CrossRefGoogle ScholarPubMed
Perry, R. D. and Fetherston, J. D. (1997). Yersinia pestis – etiologic agent of plague. Clinical Microbiology Reviews 10, 36–66.CrossRefGoogle ScholarPubMed
Salkeld, D. J. and Stapp, P. (2008). No evidence of deer mouse involvement in plague (Yersinia pestis) epizootics in prairie dogs. Vector-borne and Zoonotic Diseases 8, 331–337.CrossRefGoogle ScholarPubMed
Salkeld, D. J., Eisen, R. J., Stapp, P., Wilder, A. P., Lowell, J., Tripp, D. W., Albertson, D. and Antolin, M. F. (2007). The role of swift foxes (Vulpes velox) and their fleas in plague (Yersinia pestis) outbreaks. Journal of Wildlife Diseases 42, 425–431.CrossRefGoogle Scholar
Schneider, S., Roessli, D. and Excoffier, L. (2000). Arlequin: a Software for Population Genetics Data Analysis. Ver 2.000. Genetics and Biometry Laboratory, Department of Anthropology, University of Geneva, Geneva, Switzerland.Google Scholar
Traub, R. (1985). Coevolution of fleas and mammals. In Coevolution of Parasitic Arthropods and Mammals (ed. Kim, , , K. C.), pp. 95–437. John Wiley and Sons, Inc., New York, NY, USA.Google Scholar
Walker, S. M., Prodohl, P. A., Fletcher, H. L., Hanna, R. E.B., Kantzoura, V., Hoey, E. M. and Trudgett, A. (2007). Evidence for multiple mitochondrial lineages of Fasciola hepatica (liver fluke) within infrapopulations from cattle and sheep. Parasitology Research 101, 117–125.CrossRefGoogle ScholarPubMed
Webb, C. T., Brooks, C. P., Gage, K. L. and Antolin, M. F. (2006). Classic flea-borne transmission does not drive plague epizootics in prairie dogs. Proceedings of the National Academy of Sciences, USA 103, 6236–6241.CrossRefGoogle Scholar
Whiteman, N. K. and Parker, P. G. (2005). Using parasites to infer host population history: a new rationale for parasite conservation. Animal Conservation 8, 175–181.CrossRefGoogle Scholar
Whiting, M. F. (2002). Mecoptera is paraphyletic: multiple genes and phylogeny of Mecoptera and Siphonaptera. Zoologica Scripta 31, 93–105.CrossRefGoogle Scholar
Wilder, A. P., Eisen, R. J., Bearden, S. J., Montenieri, J. A., Tripp, D. W., Brinkerhoff, R. J., Gage, K. L. and Antolin, M. F. (2008). Transmission efficiency of two flea species (Oropsylla tuberculata cynomuris and Oropsylla hirsuta) involved in plague epizootics among prairie dogs. EcoHealth 5, 205–212.CrossRefGoogle ScholarPubMed