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Parasite epidemiology in a changing world: can molecular phylogeography help us tell the wood from the trees?

Published online by Cambridge University Press:  24 August 2012

E.R. MORGAN ,
E.L. CLARE ,
R. JEFFERIES  and
J. R. STEVENS
E.R. MORGAN*
Affiliation:
School of Biological Sciences, University of Bristol, Woodland Road, Bristol, BS8 1UG, UK
E.L. CLARE
Affiliation:
School of Biological Sciences, University of Bristol, Woodland Road, Bristol, BS8 1UG, UK
R. JEFFERIES
Affiliation:
Department of Anatomy and Neuroscience, University of Melbourne, Parkville, 3010, Australia
J. R. STEVENS
Affiliation:
Molecular Ecology and Evolution Group, School of Biosciences, Geoffrey Pope Building, University of Exeter, Stocker Road, Exeter EX4 4QD, UK
*
*Corresponding author:University of Bristol, School of Biological Sciences, Woodland Road, Bristol, BS8 1UG, UK. Tel. +44 (0)1179287485. Fax. +44 (0)1173317985 E-mail: [email protected]
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Summary

Molecular phylogeography has revolutionised our ability to infer past biogeographic events from cross-sectional data on current parasite populations. In ecological parasitology, this approach has been used to address fundamental questions concerning host-parasite co-evolution and geographic patterns of spread, and has raised many technical issues and problems of interpretation. For applied parasitologists, the added complexity inherent in adding population genetic structure to perceived parasite distributions can sometimes seem to cloud rather than clarify approaches to control. In this paper, we use case studies firstly to illustrate the potential extent of cryptic diversity in parasite and parasitoid populations, secondly to consider how anthropogenic influences including movement of domestic animals affect the geographic distribution and host associations of parasite genotypes, and thirdly to explore the applied relevance of these processes to parasites of socio-economic importance. The contribution of phylogeographic approaches to deeper understanding of parasite biology in these cases is assessed. Thus, molecular data on the emerging parasites Angiostrongylus vasorum in dogs and wild canids, and the myiasis-causing flies Lucilia spp. in sheep and Cochliomyia hominovorax in humans, lead to clear implications for control efforts to limit global spread. Broader applications of molecular phylogeography to understanding parasite distributions in an era of rapid global change are also discussed.

Keywords

Population geneticsglobal changebiological invasionlivestock movementwildlife diseasemyiasisAngiostrongylusBelvosiavampire bat
Type
Research Article
Information
Parasitology , Volume 139 , Issue 14: Dynamics of parasite distributions: modern analytical approaches , December 2012 , pp. 1924 - 1938
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Agosta, S. J., Janz, N. and Brooks, D. R. (2010). How specialists can be generalists: resolving the parasite paradox and implications for emerging infectious disease. Zoologia 27, 151–162.CrossRefGoogle Scholar
Almeida, M. F., Martorelli, L. F. A., Aires, C. C., Barros, R. F. and Massad, E. (2008). Vaccinating the vampire bat Desmodus rotundus against rabies. Virus Research 137, 275–277.CrossRefGoogle ScholarPubMed
Archie, E. A. and Ezenwa, V. O. (2011). Population genetic structure and history of a generalist parasite infecting multiple sympatric host species. International Journal for Parasitology 41, 89–98.CrossRefGoogle ScholarPubMed
Ballard, J. W. O. and Whitlock, M. C. (2004). The incomplete natural history of mitochondria. Molecular Ecology 13, 729–744.CrossRefGoogle ScholarPubMed
Balmer, O., Baedell, J. S., Gibson, W. and Caccone, A. (2011). Phylogeography and taxonomy of Trypanosoma brucei. PLOS Neglected Tropical Diseases 5, e961.CrossRefGoogle ScholarPubMed
Bertelsen, M. F., Meyland-Smith, F., Willesen, J. L., Jefferies, R., Morgan, E. R. and Monrad, J. (2010). Diversity and prevalence of metastrongyloid nematodes infecting the red panda (Ailurus fulgens) in European zoos. Veterinary Parasitology, 172, 299–304.CrossRefGoogle ScholarPubMed
Bisdorff, B. and Wall, R. (2008). Sheep blowfly strike and management in Great Britain: a survey of current practice. Medical and Veterinary Entomology 22, 303–308.CrossRefGoogle ScholarPubMed
Bishop, D. M. (1993). Early records (1984–1987) of the Australian green blowfly (Lucilia cuprina) in New Zealand. New Zealand Entomologist 16, 22–24.CrossRefGoogle Scholar
Blakeslee, A. M. H., Byers, J. E. and Lesser, M. P. (2008). Solving cryptogenic histories using host and parasite molecular genetics: the resolution of Littorina littorea's North American origin. Molecular Ecology 17, 3684–3696.CrossRefGoogle ScholarPubMed
Blouin, M. S., Dame, J. B., Tarrant, C. A. and Courtney, C. H. (1992). Unusual population genetics of a parasitic nematode: mtDNA variation within and among populations. Evolution 46, 470–476.CrossRefGoogle ScholarPubMed
Blouin, M. S., Yowell, C. A., Courtney, C. H. and Dame, J. B. (1995). Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141, 1007–1014.CrossRefGoogle ScholarPubMed
Bouzid, W., Stefka, J., Hypsa, V., Lek, S., Scholz, T., Legal, L., Ben Hassie, O. K. and Loot, G. (2008). Geography and host specificity: two forces behind the genetic structure of the freshwater fish parasite Ligula intestinalis (Cestoda: Diphyllobothriidae). International Journal for Parasitology 38, 1465–1479.CrossRefGoogle ScholarPubMed
Brooks, D. R. and Hoberg, E. P. (2007). How will global climate change affect parasite-host assemblages? Trends in Parasitology 23, 571–574.CrossRefGoogle ScholarPubMed
Brower, A. V. Z. (1994). Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial-DNA evolution. Proceedings of the National Academy of Sciences, USA 91, 6491–6495.CrossRefGoogle ScholarPubMed
Bruyndonckx, N., Biollaz, F., Dubey, S., Goudet, J. and Christie, P. (2010). Mites as biological tags of their hosts. Molecular Ecology 19, 2770–2778.CrossRefGoogle ScholarPubMed
Bruyndonckx, N., Dubey, S., Ruedi, M. and Christie, P. (2009 a). Molecular co-phylogenetic relationships between European bats and their ectoparasitic mites (Acari, Spinturnicidae). Molecular Phylogenetics and Evolution 51, 227–237.CrossRefGoogle Scholar
Bruyndonckx, N., Henry, I., Christie, P. and Kerth, G. (2009 b). Spatio-temporal population genetic structure of the parasitic mite Spinturnix bechsteini is shaped by its own demography and the social system of its bat host. Molecular Ecology 18, 3581–3592.CrossRefGoogle ScholarPubMed
Clare, E. (2011). Cryptic species? Patterns of maternal and paternal gene flow in eight neotropical bats. PLOS One 6, e21460.CrossRefGoogle ScholarPubMed
Clare, E. L., Lim, B. K., Fenton, M. B. and Hebert, P. D. N. (2011). Neotropical bats: Estimating species diversity with DNA barcodes. PLOS One 6, e22648.CrossRefGoogle ScholarPubMed
Coen, C. E. (2002). Comparative nutritional ecology of two genera of vampire bats: Desmodus rotundus and Diaemus youngi. Unpublished PhD thesis, Cornell University, USA.Google Scholar
Conboy, G. (2004). Natural infections of Crenosoma vulpis and Angiostrongylus vasorum in dogs in Atlantic Canada and their treatment with milbemycin oxime. Veterinary Record 155, 16–18.CrossRefGoogle ScholarPubMed
Conboy, G. A. (2011). Canine angiostrongylosis: the French heartworm: an emerging threat in North America. Veterinary Parasitology 176, 382–389.CrossRefGoogle ScholarPubMed
Criscione, C. D. (2008). Parasite co-structure: broad and local scale approaches. Parasite 15, 439–443.CrossRefGoogle ScholarPubMed
Criscione, C. D., Poulin, R. and Blouin, M. S. (2005). Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Molecular Ecology 14, 2247–2257.CrossRefGoogle ScholarPubMed
Criscione, C. D., Vilas, R., Paniagua, E. and Blouin, M. S. (2011). More than meets the eye: detecting cryptic microgeographic population structure in a parasite with a complex life cycle. Molecular Ecology 20, 2510–2524.CrossRefGoogle Scholar
De Leon, G. P. P. and Nadler, S. A. (2010). What we don't recognize can hurt us: a plea for awareness about cryptic species. Journal of Parasitology 96, 453–464.CrossRefGoogle Scholar
Detwiler, J. T., Bos, D. H., Minchella, D. J. (2010). Revealing the secret lives of cryptic species: examining the phylogenetic relationships of echinostome parasites in North America. Molecular Phylogenetics and Evolution 55, 611–620.CrossRefGoogle ScholarPubMed
Ditchfield, A. D. (2000). The comparative phylogeography of Neotropical mammals: patterns of intraspecific mitochondrial DNA variation among bats contrasts to nonvolant small mammals. Molecular Ecology 9, 1307–1318.CrossRefGoogle ScholarPubMed
Dowton, M. and Austin, A. D. (1995). Increased genetic diversity in mitochondrial genes is correlated with the evolution of parasitism in the Hymenoptera. Journal of Molecular Evolution 41, 958–965.CrossRefGoogle ScholarPubMed
Eamsobhana, P., Lim, P. E., Solano, G., Zhang., H. M., Gan, X. X. and Sen Yong, H. (2010 a). Molecular differentiation of Angiostrongylus taxa (Nematoda: Angiostrongylidae) by cytochrome c oxidase subunit I (COI) gene sequences. Acta Tropica 116, 152–156.CrossRefGoogle ScholarPubMed
Eamsobhana, P., Lim, P. E., Solano, G., Zhang., H. M., Gan, X. X. and Sen Yong, H. (2010 b). Molecular differentiation and phylogenetic relationships of three Angiostrongylus species and Angiostrongylus cantonensis geographical isolates based on a 66-kDa protein gene of A. cantonensis (Nematoda: Angiostrongylidae). Experimental Parasitology 126, 564–569.CrossRefGoogle ScholarPubMed
Edwards, S. V. (2009). Is a new and general theory of molecular systematics emerging? Evolution 63, 1–19.CrossRefGoogle ScholarPubMed
Faulkner, C. T., Patton, S., Munson, L., Johnson, E. M. and Coonan, T. J. (2001). Angiocaulus gubernaculatus in the Island Fox (Urocyon littoralis) from the California Channel Islands and comments on the diagnosis of Angiostrongylidae nematodes in canid and mustelid hosts. Journal of Parasitology 87, 1174–1176.CrossRefGoogle ScholarPubMed
Gerrikagoitia, X., Barral, M. and Juste, R. A. (2010). Angiostrongylus species in wild carnivores in the Iberian Peninsula. Veterinary Parasitology 174, 175–180.CrossRefGoogle ScholarPubMed
Gleeson, D. M. (1995). The effects on genetic variability following a recent colonization event: the Australian sheep blowfly, Lucilia cuprina arrives in New Zealand. Molecular Ecology 4, 699–708.CrossRefGoogle Scholar
Gleeson, D. M. and Sarre, S. (1997). Mitochondrial DNA variability and geographic origin of the sheep blowfly, Lucilia cuprina (Diptera: Calliphoridae), in New Zealand. Bulletin of Entomological Research 87, 265–272.CrossRefGoogle Scholar
Glennon, V., Perkins, E. M., Chisholm, L. A. and Whittington, I. D. (2008). Comparative phylogeography reveals host generalists, specialists and cryptic diversity: hexabothrid, microbothrid and monocotylid monogeneans from rhinobatid rays in southern Australia. International Journal for Parasitology 38, 1599–1612.CrossRefGoogle ScholarPubMed
Greenhall, A. M., Joermann, G. and Schmidt, U. (1983). Desmodus rotundus. Mammalian Species 202, 1–6.Google Scholar
Hall, M. and Wall, R. (1995). Myiasis of humans and domestic animals. Advances in Parasitology 35, 257–334.CrossRefGoogle ScholarPubMed
Hansen, H., Bakke, T. A. and Bachmann, L. (2007 a). Mitochondrial haplotype diversity of Gyrodactylus thymalli (Platyhelminthes: monogenea): extended geographic sampling in the United Kingdom, Poland and Norway reveals further lineages. Parasitology Research 100, 1389–1394.CrossRefGoogle ScholarPubMed
Hansen, H., Bakke, T. A. and Bachmann, L. (2007 b). DNA taxonomy and barcoding of monogenean parasites: lessons from Gyrodactylus. Trends in Parasitology 23, 363–367.CrossRefGoogle ScholarPubMed
Hartley, C. J., Newcomb, R. D., Russell, R. J., Yong, C. G., Stevens, J. R., Yeates, D. K., La Salle, J. and Oakeshott, J. G. (2006). Amplification of DNA from preserved specimens shows blowflies were pre-adapted for the rapid evolution of insecticide resistance. Proceedings of the National Academy of Sciences, USA 103, 8757–8762.CrossRefGoogle Scholar
Hebert, P. D. N., Cywinska, A., Ball, S. L. and deWaard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London Series B, Biological Sciences 270, 313–321.CrossRefGoogle ScholarPubMed
Hebert, P. D. N., Penton, E. H., Burns, J. M., Janzen, D. H. and Hallwachs, W. (2004). Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proceedings of the National Academy of Sciences, USA 101, 14812–14817.CrossRefGoogle ScholarPubMed
Helinski, M. E. H., Parker, A. G. and Knols, B. G. J. (2006). Radiation-induced sterility for pupal and adult stages of the malaria mosquito Anopheles arabiensis. Malaria Journal 5, 41.CrossRefGoogle ScholarPubMed
Helm, J., Gilleard, J., Jackson, M., Redman, E. and Bell, R. (2009). A case of canine Angiostrongylus vasorum in Scotland confirmed by PCR and sequence analysis. Journal of Small Animal Practice 50, 255–259.CrossRefGoogle ScholarPubMed
Helm, J. R., Morgan, E. R., Jackson, M. W., Wotton, P. and Bell, R. (2010). Canine angiostrongylosis: an emerging disease in Europe. Journal of Veterinary Emergency and Critical Care 20, 98–109.CrossRefGoogle ScholarPubMed
Hoberg, E. P. (2010). Invasive processes, mosaics and the structure of helminth parasite faunas. Revue Scientifique et Technique – Office International des Epizooties 29, 255–272.CrossRefGoogle ScholarPubMed
Hoberg, E. P. and Brooks, D. R. (2008). A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host-parasite systems. Journal of Biogeography 35, 1533–1550.CrossRefGoogle Scholar
Jefferies, R., Morgan, E. R., Helm, J., Robinson, M. and Shaw, S.E. (2011 a) Improved detection of canine Angiostrongylus vasorum infection using real-time PCR and indirect ELISA. Parasitology Research 109, 1577–1583.CrossRefGoogle ScholarPubMed
Jefferies, R., Morgan, E. R. and Shaw, S.E. (2009 b). A SYBR green real-time PCR assay for the detection of the nematode Angiostrongylus vasorum in definitive and intermediate hosts. Veterinary Parasitology 166, 112–118.CrossRefGoogle ScholarPubMed
Jefferies, R., Morgan, E. R., Shaw, S.E. and Heesom, K. (2011 b) Identification of immune-reactive adult Angiostrongylus vasorum proteinds using mass spectrometry. Molecular and Biochemical Parasitology 180, 56–61.CrossRefGoogle Scholar
Jefferies, R. J., Shaw, S.E., Viney, M. E. and Morgan, E. R. (2009 a). Angiostrongylus vasorum from South America and Europe represent distinct lineages. Parasitology 136, 107–115.CrossRefGoogle ScholarPubMed
Jefferies, R. J., Shaw, S.E., Willesen, J., Viney, M. E. and Morgan, E. R. (2010). Elucidating the spread of the emerging canid nematode Angiostrongylus vasorum between Palearctic and Nearctic ecozones. Infection Genetics and Evolution 10, 561–568.CrossRefGoogle Scholar
Kholodova, M. V. (2009). Comparative phylogeography: molecular methods, ecological interpretation. Molecular Biology 43, 847–854.CrossRefGoogle ScholarPubMed
Klassen, W. and Curtis, F. (2005). History of the sterile insect technique. In: Sterile Insect Technique (eds. Dyck, V. A., Hendrichs, J. & Robinson, A. S.), pp. 3–36. Springer, Dordrecht, Holland.CrossRefGoogle Scholar
Koch, J. and Willesen, J. L. (2009). Canine pulmonary angiostrongylosis: an update. Veterinary Journal 179, 348–359.CrossRefGoogle ScholarPubMed
Koehler, A. V. A., Hoberg, E. P., Dokuchev, N. E., Tranbenkova, N. A., Whitman, J. S., Nagorsen, D. W. and Cook, J. A. (2009). Phylogeography of a Holarctic nematode, Soboliphyme baturini, among mustelids: climate change, episodic colonization, and diversification in a complex host-parasite system. Biological Journal of the Linnean Society 96, 651–663.CrossRefGoogle Scholar
Krafsur, E. S. (1998). Sterile insect technique for suppressing and eradicating insect populations: 55 years and counting. Journal of Agricultural Entomology 15, 303–317.Google Scholar
Lam, T. T. Y., Hon, C. C. and Tang, J. W. (2010). Use of phylogenetics in the molecular epidemiology and evolutionary studies of viral infections. Critical Reviews in Clinical Laboratory Sciences 47, 5–49.CrossRefGoogle ScholarPubMed
Lawton, S. P., Hirai, H., Ironside, J. E., Johnston, D. A. and Rollinson, D. (2011). Genomes and geography: genomic insights into the evolution and phylogeography of the genus Schistosoma. Parasites and Vectors 4, 131.CrossRefGoogle ScholarPubMed
Lindquist, D. A., Abusowa, M. and Hall, M. J. R. (1992). The New World screwworm fly in Libya – a review of its introduction and eradication. Medical and Veterinary Entomology 6, 2–8.CrossRefGoogle ScholarPubMed
Lymbery, A. J. and Thompson, R. C. A. (2012). The molecular epidemiology of parasite infections: Tools and applications. Molecular and Biochemical Parasitology 181, 102–116.CrossRefGoogle ScholarPubMed
McDonagh, L., García, R. and Stevens, J. R. (2009). Phylogenetic analysis of New World screwworm fly, Cochliomyia hominivorax, suggests genetic isolation of some Caribbean island populations following colonization from South America. Medical and Veterinary Entomology 23, 14–22.CrossRefGoogle ScholarPubMed
McGarry, J. W. and Morgan, E. R. (2009). Identification of first-stage larvae of metastrongyles from dogs. Veterinary Record 165, 258–261.CrossRefGoogle ScholarPubMed
Martinez-Hernandez, F., Jimenez-Gonzales, D. E., Chenillo, P., Alonso-Fernandez, C., Maravilla, P. and Flisser, A. (2009). Geographical widespread of two lineages of Taenia solium due to human migrations: can population genetic analysis strengthen this hypothesis? Infection Genetics and Evolution 9, 1108–1114.CrossRefGoogle ScholarPubMed
Martinez-Sanchez, A., Smith, K. E., Rojo, S., Marcos-Garcia, M. A. and Wall, R. (2007). Geographic origin affects larval competitive ability in European populations of the blow fly, Lucilia sericata. Entomologia Experimentalis et Applicata 122, 93–98.CrossRefGoogle Scholar
Martins, F. M., Ditchfield, A. D., Meyer, D. and Morgante, J. S. (2007). Mitochondrial DNA phylogeography reveals marked population structure in the common vampire bat, Desmodus rotundus (Phyllostomidae). Journal of Zoological Systematics and Evolutionary Research 45, 372–378.CrossRefGoogle Scholar
Martins, F. M., Templeton, A. R., Pavan, A. C. O., Kohlback, B. C. and Morgante, J. S. (2009). Phylogeography of the common vampire bat (Desmodus rotundus): Marked population structure, Neotropical Pleistocene vicariance and incongruence between nuclear and mtDNA markers. BMC Evolutionary Biology 9, 294.CrossRefGoogle ScholarPubMed
Morgan, E. R., Jefferies, R., Krajewski, M., Ward, P. and Shaw, S. E. (2009). Canine pulmonary angiostrongylosis: The influence of climate on parasite distribution. Parasitology International 58, 406–410.CrossRefGoogle ScholarPubMed
Morgan, E. R., Jefferies, R., van Otterdijk, L., McEniry, R. B., Allen, F., Bakewell, M. and Shaw, S. E. (2011). Angiostrongylus vasorum infection in dogs: presentation and risk factors. Veterinary Parasitology 173, 255–261.CrossRefGoogle Scholar
Morgan, E. R., Milner-Gulland, E. J., Torgerson, P. R. and Medley, G. F. (2004). Ruminating on complexity: macroparasites of wildlife and livestock. Trends in Ecology and Evolution 19, 181–188.CrossRefGoogle ScholarPubMed
Morgan, E. R., Shaw, S. E., Brennan, S. F., De Waal, T., Jones, B. R. and Mulcahy, G. (2005). Angiostrongylus vasorum: a real heartbreaker. Trends in Parasitology 21, 49–51.CrossRefGoogle ScholarPubMed
Morgan, E. R., Tomlinson, A., Hunter, S., Nichols, T., Roberts, E., Fox, M. T. and Taylor, M. A. (2008). Angiostrongylus vasorum and Eucoleus aerophilus in foxes (Vulpes vulpes) in Great Britain. Veterinary Parasitology 154, 48–57.CrossRefGoogle ScholarPubMed
Morgan, E. R. and Wall, R. (2009). Climate change and parasitic disease: farmer mitigation? Trends in Parasitology 25, 308–313.CrossRefGoogle ScholarPubMed
Nadler, S. A. and De Leon, G. P. P. (2011). Integrating molecular and morphological approaches for characterizing parasite cryptic species: implications for parasitology. Parasitology 138, 1688–1709.CrossRefGoogle ScholarPubMed
Nakao, M., Xiao, N., Okamoto, M., Yanagida, T., Sako, Y. and Ito, A. (2009). Geographic pattern of genetic variation in the fox tapeworm Echinococcus multilocularis. Parasitology International 58, 384–389.CrossRefGoogle ScholarPubMed
Nickrent, D. L. and Starr, E. M. (1994). High rates of nucleotide substitution in nuclear small-subunit (18S) rDNA from holoparasitic flowering plants. Journal of Molecular Evolution 39, 62–70.CrossRefGoogle ScholarPubMed
Nieberding, C. M., Durette-Desset, M. C., Vanderpoorten, A., Casanova, J. C., Ribas, A., Deffontaine, V., Feliu, C., Morand, S., Libois, R. and Michaux, J. R. (2008). Geography and host biogeography matter for understanding the phylogeography of a parasite. Molecular Phylogenetics and Evolution 47, 538–554.CrossRefGoogle ScholarPubMed
Nieberding, C., Morand, S., Libois, R. and Michaux, J. R. (2004). A parasite reveals cryptic phylogeographic history of its host. Proceedings of the Royal Society of London Series B – Biological Sciences 271, 2559–2568.CrossRefGoogle ScholarPubMed
Nieberding, C. M. and Olivieri, I. (2007). Parasites: proxies for host genealogy and ecology? Trends in Ecology and Evolution 22, 156–165.CrossRefGoogle ScholarPubMed
Oliveira, S. D., Barcante, J. M. P., Barcante, T. A., Dias, S. R. C., Lima, W. S. (2006). Larval output of infected and re-infected dogs with Angiostrongylus vasorum (Baillet, 1866) Kamensky, 1905. Veterinary Parasitology 141, 101–106.CrossRefGoogle Scholar
Otranto, D. and Stevens, J. R. (2002). Molecular approaches to the study of myiasis-causing larvae. International Journal for Parasitology 32, 1345–1360.CrossRefGoogle Scholar
Patterson-Kane, J. C., Gibbons, L. M., Jefferies, R., Morgan, E. R., Wenzlow, N. and Redrobe, S. P. (2009). Pneumonia from Angiostrongylus vasorum infection in a red panda (Ailurus fulgens fulgens). Journal of Veterinary Diagnostic Investigation 21, 270–273.CrossRefGoogle Scholar
Picard, C. J. and Wells, J. D. (2009). Survey of the Genetic Diversity of Phormia regina (Diptera: Calliphoridae) Using Amplified Fragment Length Polymorphisms. Journal of Medical Entomology 46, 664–670.CrossRefGoogle ScholarPubMed
Picard, C. J. and Wells, J. D. (2010). The population genetic structure of North American Lucilia sericata (Diptera: Calliphoridae), and the utility of genetic assignment methods for reconstruction of postmortem corpse relocation. Forensic Science International 195, 63–67.CrossRefGoogle ScholarPubMed
Plaisance, L., Rousset, V., Morand, S., Littlewood, D. T. J. (2008). Colonization of Pacific islands by parasites of low dispersal ability: phylogeography of two monogenean species parasitizing butterflyfishes in the South Pacific Ocean. Journal of Biogeography 35, 76–87.CrossRefGoogle Scholar
Polley, L. and Thompson, R. C. A. (2009). Parasite zoonoses and climate change: molecular tools for tracking shifting boundaries. Trends in Parasitology 25, 285–291.CrossRefGoogle ScholarPubMed
Poulin, R. (2011). Uneven distribution of cryptic diversity among higher taxa of parasitic worms. Biology Letters 7, 241–244.CrossRefGoogle ScholarPubMed
Poulin, R., Krasnov, B. R. and Mouillot, D. (2011). Host specificity in phylogenetic and geographic space. Trends in Parasitology 27, 355–361.CrossRefGoogle ScholarPubMed
Riddle, B. R., Dawson, M. N., Hadly, E. A., Hafner, D. J., Hickerson, M. J., Mantooth, S. J. and Yoder, A. D. (2008). The role of molecular genetics in sculpting the future of integrative biogeography. Progress in Physical Geography 32, 173–202.CrossRefGoogle Scholar
Robinson, A. S., Vreysen, M. J. B., Hendrichs, J. and Feldmann, U. (2009). Enabling technologies to improve area-wide integrated pest management programmes for the control of screwworms. Medical and Veterinary Entomology 23, 1–7.CrossRefGoogle ScholarPubMed
Roca, A. L., Georgiadis, N., Pecon-Slattery, J. and O'Brien, S. J. (2001). Genetic evidence for two species of elephant in Africa. Science 293, 1473–1477.CrossRefGoogle ScholarPubMed
Rose, H. and Wall, R. (2011). Modelling the impact of climate change on spatial patterns of disease risk: Sheep blowfly strike by Lucilia sericata in Great Britain. International Journal for Parasitology 41, 739–746.CrossRefGoogle ScholarPubMed
Rosenthal, B. M. (2009). How has agriculture influenced the geography and genetics of animal parasites? Trends in Parasitology 25, 67–70.CrossRefGoogle ScholarPubMed
Rubinoff, D., Cameron, S. and Will, K. (2006). A genomic perspective on the shortcomings of mitochondrial DNA for barcoding identification. Journal of Heredity 97, 581–594.CrossRefGoogle ScholarPubMed
Schnyder, M., Maurelli, M. P., Morgoglione, M. E., Kohler, L., Deplazes, P., Torgerson, P., Cringoli, G. and Rinaldi, L. (2011). Comparison of faecal techniques including FLOTAC for copromicroscopic detection of first stage larvae of Angiostrongylus vasorum. Parasitology Research 109, 63–69.CrossRefGoogle ScholarPubMed
Scoble, J. and Lowe, A. J. (2010). A case for incorporating phylogeography and landscape genetics into species distribution modelling approaches to improve climate adaptation and conservation planning. Diversity and Distributions 16, 343–353.CrossRefGoogle Scholar
Schucan, A., Schnyder, M., Tanner, I., Barutzki, D., Traversa, D. and Deplazes, P. (2012). Detection of specific antibodies in dogs infected with Angiostrongylus vasorum. Veterinary Parasitology 185, 216–224.CrossRefGoogle ScholarPubMed
Smith, M. A., Wood, M. D., Janzen, D. H., Hallwachs, W. and Hebert, P. D. N. (2007). DNA barcodes affirm that 16 species of apparently generalist tropical parasitoid flies (Diptera: Tachinidae) are not all generalists. Proceedings of the National Academy of Sciences, USA 104, 4967–4872.CrossRefGoogle Scholar
Smith, M. A., Woodley, N. E., Janzen, D. H., Hallwachs, W. and Hebert, P. D. N. (2006). DNA barcodes reveal cryptic host-specificity within the presumed polyphagous members of a genus of parasitoid flies (Diptera: Tachinidae). Proceedings of the National Academy of Sciences, USA 103, 3657–3662.CrossRefGoogle ScholarPubMed
Solano, P., Ravel, S. and Meeûs, T. de (2010). How can tsetse population genetics contribute to African trypanosomiasis control? Trends in Parasitology 26, 255–263.CrossRefGoogle ScholarPubMed
Stefka, J., Hoeck, P. E. A., Keller, L. F. and Smith, V. S. (2011). A hitchhiker's guide to the Galapagos: co-phylogeography of Galapagos mockingbirds and their parasites. BMC Evolutionary Biology 11, 284.CrossRefGoogle Scholar
Stefka, J., Hypsa, V. and Scholz, T. (2009). Interplay of host specificity and biogeography in the population structure of a cosmopolitan endoparasite: microsatellite study of Ligula intestinalis (Cestoda). Molecular Ecology 18, 1187–1206.CrossRefGoogle ScholarPubMed
Stevens, J. and Wall, R. (1996). Species, sub-species and hybrid populations of the blowflies Lucilia cuprina and Lucilia sericata (Diptera: Calliphoridae). Proceedings of the Royal Society of London Series B: Biological Sciences 263, 1335–1341.Google ScholarPubMed
Stevens, J. and Wall, R. (1997). The evolution of ectoparasitism in the genus Lucilia (Diptera: Calliphoridae). International Journal for Parasitology 27, 51–59.CrossRefGoogle ScholarPubMed
Stevens, J. R. and Wallman, J. F. (2006). The evolution of myiasis in humans and other animals in the Old and New Worlds (part I): phylogenetic analyses. Trends in Parasitology 22, 129–136.CrossRefGoogle ScholarPubMed
Stevens, J. R., Wall, R. and Wells, J. D. (2002). Paraphyly in Hawaiian hybrid blowfy populations and the evolutionary history of anthropophilic species. Insect Molecular Biology 11, 141–148.CrossRefGoogle ScholarPubMed
Stevens, J. R., Wallman, J. F., Otranto, D., Wall, R. and Pape, T. (2006). The evolution of myiasis in humans and other animals in the Old and New Worlds (part II): biological and life-history studies. Trends in Parasitology 22, 181–188.CrossRefGoogle ScholarPubMed
Taylor, D. B., Hammack, L. and Roehrdanz, R. L. (1991). Reproductive compatibility and mitochondrial DNA restriction site analysis of New World screwworm, Cochliomyia hominivorax, from North Africa and Central America. Medical and Veterinary Entomology 5, 145–152.CrossRefGoogle ScholarPubMed
Taylor, D. B., Szalanski, A. L. and Peterson, R. D. (1996). Mitochondrial DNA variation in screwworm. Medical and Veterinary Entomology 10, 161–169.CrossRefGoogle ScholarPubMed
Tellam, R. L. and Bowles, V. M. (1997). Control of blowfly strike in sheep: Current strategies and future prospects. International Journal for Parasitology 27, 261–273.CrossRefGoogle ScholarPubMed
Thompson, R. C. A., Lymbery, A. J. and Smith, A. (2010). Parasites, emerging disease and wildlife conservation. International Journal for Parasitology 40, 1163–1170.CrossRefGoogle ScholarPubMed
Thomson, R. C., Wang, I. J. and Johnson, J. R. (2010). Genome-enabled development of DNA markers for ecology, evolution and conservation. Molecular Ecology 19, 2184–2195.CrossRefGoogle ScholarPubMed
Toon, A. and Hughes, J. (2008). Are lice good proxies for host history? A comparative analysis of the Australian magpie, Gymnorhina tibicen, and two species of feather louse. Heredity 101, 127–135.CrossRefGoogle ScholarPubMed
Torres, T. T. and Azeredo-Espin, A. M. L. (2009). Population genetics of New World screwworm from the Caribbean: insights from microsatellite data. Medical and Veterinary Entomology 23, 23–31.CrossRefGoogle ScholarPubMed
Tourle, R., Downie, D. A. and Villet, M. H. (2009). Flies in the ointment: a morphological and molecular comparison of Lucilia cuprina and Lucilia sericata (Diptera: Calliphoridae) in South Africa. Medical and Veterinary Entomology 23, 6–14.CrossRefGoogle ScholarPubMed
Traversa, D. and Guglielmini, C. (2008). Feline aelurostrongylosis and canine angiostrongylosis: a challenging diagnosis for two emerging verminous pneumonia infections. Veterinary Parasitology 157, 163–174.CrossRefGoogle ScholarPubMed
Voigt, C. C. and Kelm, D. H. (2006). Host preferences of the common vampire bat (Desmodus rotundus; Chiroptera) assessed by stable isotopes. Journal of Mammalogy 87, 1–6.CrossRefGoogle Scholar
Vreysen, M. J. B., Gerado-Abaya, J. and Cayol, J. P. (2007). Lessons from area-wide integrated pest management (AW-IPM) programmes with an SIT component: an FAO/IAEA perspective. Area-wide Control of Insect Pests: from Research to Field Implementation (ed. by Vreysen, M. J. B., Robinson, A. S. and Hendrichs, J.), pp. 723–744. Springer, Dordrecht.CrossRefGoogle Scholar
Wall, R. and Ellse, L. S. (2011). Climate change and livestock parasites: integrated management of sheep blowfly strike in a warmer environment. Global Change Biology 17, 1770–1777.CrossRefGoogle Scholar
Wall, R., Rose, H., Ellse, L. and Morgan, E. (2011). Livestock ectoparasites: Integrated management in a changing climate. Veterinary Parasitology 180, 82–89.CrossRefGoogle Scholar
Waltari, E., Hoberg, E. P., Lessa, E. P. and Cook, J. A. (2007). Eastward Ho: phylogeographic perspectives on colonization of hosts and parasites across the Beringean nexus. Journal of Biogeography 34, 561–574.CrossRefGoogle Scholar
Wang, X., Tedford, R. H., Van Valkenberg, B. and Wayne, R. K. (2004). Ancestry: Evolutionary history, molecular systematic, and evolutionary ecology of Canidae. In The Biology and Conservation of Wild Canids (ed. MacDonald, D. W. and Sillero-Zubiri, C.), pp. 39–54. Oxford University Press, Oxford, UK.CrossRefGoogle Scholar
Wells, J. D. and Stevens, J. R. (2008). Application of DNA-Based Methods in Forensic Entomology. Annual Review of Entomology 53, 103–120.CrossRefGoogle ScholarPubMed
Westram, A. M., Baumgartner, C., Keller, I. and Jokela, J. (2011). Are cryptic host species also cryptic to parasites? Host specificity and geographical distribution of acanthocephalan parasites infecting freshwater Gammarus. Infection Genetics and Evolution 11, 1083–1090.CrossRefGoogle ScholarPubMed
Whiteman, N. K., Kimball, R. T. and Parker, P. G. (2007). Co-phylogeography and comparative population genetics of the threatened Galapagos hawk and three ectoparasite species: ecology shapes population histories within parasite communities. Molecular Ecology 16, 4759–4773.CrossRefGoogle ScholarPubMed
Wilkinson, G. S. (1985). The social organization of the common vampire bat. 11. Mating systems, genetic structure and relatedness. Behavioural Ecology and Sociobiology 17, 111–121.CrossRefGoogle Scholar
Witt, J. D. S., Threloff, D. L. and Hebert, P. D. N. (2006). DNA barcoding reveals extraordinary cryptic diversity in an amphipod genus: implications for desert spring conservation. Molecular Ecology 15, 3073–3082.CrossRefGoogle Scholar
Yamakawa, Y., McGarry, J. W., Denk, D., Dukes-McEwan, J., MacDonald, N., Mas, A., McConnell, F., Tatton, B., Valentine, E. G., Wayne, J., Williams, J. M. and Hetzel, U. (2009). Emerging canine angiostrongylosis in northern England: five fatal cases. Veterinary Record 164, 149–152.CrossRefGoogle ScholarPubMed
Zachos, F. E. (2009). Gene trees and species trees: mutual influences and interdependencies of population genetics and systematics. Journal of Zoological Systematics and Evolutionary Research 47, 209–218.CrossRefGoogle Scholar