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, 9 (1), 547

Population Structure and Dispersal Routes of an Invasive Parasite, Fascioloides Magna, in North America and Europe

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Population Structure and Dispersal Routes of an Invasive Parasite, Fascioloides Magna, in North America and Europe

Ludmila Juhásová et al. Parasit Vectors.

Abstract

Background: Fascioloides magna (Trematoda: Fasciolidae) is an important liver parasite of a wide range of free-living and domestic ruminants; it represents a remarkable species due to its large spatial distribution, invasive character, and potential to colonize new territories. The present study provides patterns of population genetic structure and admixture in F. magna across all enzootic regions in North America and natural foci in Europe, and infers migratory routes of the parasite on both continents.

Methods: In total, 432 individuals from five North American enzootic regions and three European foci were analysed by 11 microsatellite loci. Genetic data were evaluated by several statistical approaches: (i) the population genetic structure of F. magna was inferred using program STRUCTURE; (ii) the genetic interrelationships between populations were analysed by PRINCIPAL COORDINATES ANALYSIS; and (iii) historical dispersal routes in North America and recent invasion routes in Europe were explored using MIGRATE.

Results: The analysis of dispersal routes of the parasite in North America revealed west-east and south-north lineages that partially overlapped in the central part of the continent, where different host populations historically met. The exact origin of European populations of F. magna and their potential translocation routes were determined. Flukes from the first European focus, Italy, were related to F. magna from northern Pacific coast, while parasites from the Czech focus originated from south-eastern USA, particularly South Carolina. The Danube floodplain forests (third and still expanding focus) did not display relationship with any North American population; instead the Czech origin of the Danube population was indicated. A serial dilution of genetic diversity along the dispersion route across central and eastern Europe was observed. The results of microsatellite analyses were compared to previously acquired outputs from mitochondrial haplotype data and correlated with past human-directed translocations and natural migration of the final cervid hosts of F. magna.

Conclusions: The present study revealed a complex picture of the population genetic structure and interrelationships of North American and European populations, global distribution and migratory routes of F. magna and an origin of European foci.

Keywords: Fascioloides magna; Genetic interrelationships; Giant liver fluke; Microsatellites; Migratory routes; Parasite.

Figures

Fig. 1
Fig. 1
Bar plots from program STRUCTURE assigning all 432 Fascioloides magna individuals from North America (NA) and Europe (EU) into K = 2, 4 and 8 clusters and detailed structure of SAS region. Codes for NA enzootic regions, US states/Canadian province and EU natural foci are explained in Tables 1 and 2, respectively
Fig. 2
Fig. 2
Genetic population structure of Fascioloides magna from all North American (NA) and European (EU) populations (a), and interrelationships among NA populations (b-d) derived from PRINCIPAL COORDINATES ANALYSIS (PCoA). Circles, EU natural foci; squares, NA enzootic regions. a All NA and EU populations. b All NA populations. c Eastern NA clade inferred from mt data (Bazsalovicsová et al. [10]). d West-east NA lineage derived from MIGRATE analysis of microsatellites (present study). Codes for NA enzootic regions and EU natural foci are explained in Tables 1 and 2, respectively
Fig. 3
Fig. 3
Genetic population structure of Fascioloides magna from European (EU) populations (a) and interrelationships between EU and North American (NA) populations (b-d) based on the PRINCIPAL COORDINATES ANALYSIS (PCoA). Circles, EU natural foci; squares, NA enzootic regions. a Interrelationships between F. magna from Czech-Polish (CZ-PL) and Danube floodplain forests (DFF) foci. b Relatedness between flukes from Italy (IT) and western NA regions (RMT and NPC). c Comparison between F. magna from CZ-PL and particular states of SAS. d Differentiation of DFF from all NA enzootic regions. Codes for NA enzootic regions and EU natural foci are explained in Tables 1 and 2, respectively
Fig. 4
Fig. 4
Unrooted neighbour-joining (NJ) evolutionary tree based on pairwise DA distances among Fascioloides magna from Europe (EU) and North America (NA). a Tree representing F. magna from NA enzootic regions and EU natural foci. b Tree displaying F. magna from US states, Canadian provinces and EU countries coloured according to their respective region/locus. Dotted ovals, closest interrelationships between EU and NA populations. Codes for NA enzootic regions and EU natural foci are explained in Tables 1 and 2, respectively
Fig. 5
Fig. 5
Schematic reconstruction of transmission routes between North American (NA) and European (EU) populations of Fascioloides magna, and determination of the origin of EU populations derived from mtDNA haplotypes (Králová-Hromadová et al. [11]) and microsatellite analysis
Fig. 6
Fig. 6
Schematic presentation of the most possible scenarios of migration routes of F. magna on both continents using MIGRATE

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