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      Fasciola hepatica demonstrates high levels of genetic diversity, a lack of population structure and high gene flow: possible implications for drug resistance

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          Highlights

          • Self-fertilisation does occur but is rare in field populations of Fasciola hepatica.

          • Some hosts harboured genotypically identical parasites (clones).

          • The presence of clones is consistent with clonal expansion and clumped transmission.

          • 84% of 1579 F. hepatica had unique genotypes, indicating high genetic diversity.

          • We found high gene flow, no population structure and low self-fertilisation rate.

          Abstract

          Fasciola hepatica, the liver fluke, is a trematode parasite of considerable economic importance to the livestock industry and is a re-emerging zoonosis that poses a risk to human health in F. hepatica-endemic areas worldwide. Drug resistance is a substantial threat to the current and future control of F. hepatica, yet little is known about how the biology of the parasite influences the development and spread of resistance. Given that F. hepatica can self-fertilise and therefore inbreed, there is the potential for greater population differentiation and an increased likelihood of recessive alleles, such as drug resistance genes, coming together. This could be compounded by clonal expansion within the snail intermediate host and aggregation of parasites of the same genotype on pasture. Alternatively, widespread movement of animals that typically occurs in the UK could promote high levels of gene flow and prevent population differentiation. We identified clonal parasites with identical multilocus genotypes in 61% of hosts. Despite this, 84% of 1579 adult parasites had unique multilocus genotypes, which supports high levels of genotypic diversity within F. hepatica populations. Our analyses indicate a selfing rate no greater than 2%, suggesting that this diversity is in part due to the propensity for F. hepatica to cross-fertilise. Finally, although we identified high genetic diversity within a given host, there was little evidence for differentiation between populations from different hosts, indicating a single panmictic population. This implies that, once those emerge, anthelmintic resistance genes have the potential to spread rapidly through liver fluke populations.

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          Most cited references71

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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            Rare Alleles as Indicators of Gene Flow

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              Epidemiology of fascioliasis in human endemic areas.

              S Mas-Coma (2005)
              Considered a secondary zoonotic disease until the mid-1990s, human fascioliasis is at present emerging or re-emerging in many countries, including increases of prevalence and intensity and geographical expansion. Research in recent years has justified the inclusion of fascioliasis in the list of important human parasitic diseases. At present, fascioliasis is a vector-borne disease presenting the widest known latitudinal, longitudinal and altitudinal distribution. Fasciola hepatica has succeeded in expanding from its European original geographical area to colonize five continents, despite theoretical restrictions related to its biology and in turn dependent upon environmental and human activities. Among the different epidemiological situations, human hypo- to hyperendemic areas, including epidemics, are noteworthy. A global analysis of the distribution of human cases shows that the expected correlation between animal and human fascioliasis only appears at a basic level. Areas presenting very high human prevalences and intensities, especially in children and females, have been recently described. In hypo- to hyperendemic areas of Central and South America, Europe, Africa and Asia, human fascioliasis presents a range of epidemiological characteristics related to a wide diversity of environments. Thus far well-known epidemiological patterns of fascioliasis may not always explain the transmission characteristics in any given area and control measures should consider the results of ecoepidemiological studies undertaken in the zones concerned.
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                Author and article information

                Contributors
                Journal
                Int J Parasitol
                Int. J. Parasitol
                International Journal for Parasitology
                Elsevier Science
                0020-7519
                1879-0135
                1 January 2017
                January 2017
                : 47
                : 1
                : 11-20
                Affiliations
                [a ]Veterinary Parasitology, Institute of Infection and Global Health, University of Liverpool, Liverpool L3 5RF, UK
                [b ]Centre for Genomic Research, Institute of Integrative Biology, University of Liverpool, Liverpool L69 7ZB, UK
                Author notes
                [* ]Corresponding author at: Veterinary Parasitology, Department of Infection Biology, Institute of Infection and Global Health, University of Liverpool, Liverpool L3 5RF, UK.Veterinary ParasitologyDepartment of Infection BiologyInstitute of Infection and Global HealthUniversity of LiverpoolLiverpoolL3 5RFUK nbeesley@ 123456liverpool.ac.uk
                Article
                S0020-7519(16)30256-9
                10.1016/j.ijpara.2016.09.007
                5264428
                27940066
                35edc585-f9b5-44aa-871d-86661358b148
                © 2016 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 15 July 2016
                : 1 September 2016
                : 7 September 2016
                Categories
                Article

                Parasitology
                fasciola hepatica,population genetics,anthelmintic resistance,diversity,self-fertilisation,gene flow,microsatellites

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