Genetic Diversity of the Cestode Echinococcus multilocularis in Red Foxes at a Continental Scale in Europe

Abstract

BackgroundAlveolar echinococcosis (AE) is a severe helminth disease affecting humans, which is caused by the fox tapeworm Echinococcus multilocularis. AE represents a serious public health issue in larger regions of China, Siberia, and other regions in Asia. In Europe, a significant increase in prevalence since the 1990s is not only affecting the historically documented endemic area north of the Alps but more recently also neighbouring regions previously not known to be endemic. The genetic diversity of the parasite population and respective distribution in Europe have now been investigated in view of generating a fine-tuned map of parasite variants occurring in Europe. This approach may serve as a model to study the parasite at a worldwide level.Methodology/Principal FindingsThe genetic diversity of E. multilocularis was assessed based upon the tandemly repeated microsatellite marker EmsB in association with matching fox host geographical positions. Our study demonstrated a higher genetic diversity in the endemic areas north of the Alps when compared to other areas.Conclusions/SignificanceThe study of the spatial distribution of E. multilocularis in Europe, based on 32 genetic clusters, suggests that Europe can be considered as a unique global focus of E. multilocularis, which can be schematically drawn as a central core located in Switzerland and Jura Swabe flanked by neighbouring regions where the parasite exhibits a lower genetic diversity. The transmission of the parasite into peripheral regions is governed by a “mainland–island” system. Moreover, the presence of similar genetic profiles in both zones indicated a founder event.

Historical Aspects of Echinococcosis

“…Knapp et al (2009a) studied the genetic diversity of E. multilocularis in Europe using the microsatelite marker EmsB in association with matching the fox hosts geographical positions. A central core of the European focus was identified in Switzerland and the Swabian Jura (Germany) flanked by neighbouring regions where E. multilocularis exhibits a lower genetic diversity than that in the centre.…”

Dynamics of Echinococcus multilocularis infection in red fox populations with high and low prevalence of this parasite in Poland (2007–2014)

“…Moreover, mathematical calculation based on two examinations of red foxes between 1996 and 2003 in the Netherlands showed that the parasite prevalence is increasing in number and is spreading northward at the speed of 2.7 km per year (29). Furthermore, the expansive character of E. multilocularis infection was confirmed and described based on the analysis of the genetic diversity of this species in France (16,30) and the whole Europe (15). In Europe, the increasing trend of E. multilocularis infection in red foxes is observed.…”

Phylogenetic Pattern, Evolutionary Processes and Species Delimitation in the Genus Echinococcus

“…Genetically different E. multilocularis worms were found in in 38% of 13 foxes in Hokkaido, Japan (Nakao et al, 2003), 52% of 25 foxes in France (Knapp et al, 2008) and 35% of 125 foxes throughout Europe (Knapp et al, 2009), while genetically different E. granulosus worms were found in 50% of dogs in Argentina (Haag et al, 2011). These data suggest that it is not unusual for definitive hosts to be infected with genetically different worms of the same species.…”

“…There have been far fewer studies on other species, but Knapp et al (2009) found microsatellite allelic diversity in E. multilocularis in Europe to be greatest in historically endemic areas centred on Switzerland and lower in northern and eastern regions where the parasite has only been recently recorded. Nakao et al (2010b) found low levels of mtDNA diversity in E. multilocularis in the Tibetan Plateau and suggested that the species was introduced to this region by a recent range extension of the red fox (Vulpes vulpes), although this hypothesis requires confirmation because there does not seem to be independent evidence of such a range extension (Kutschera et al, 2013).…”

“…The North American, Asian and European clades are hypothesized to have then undergone cycles of isolation in glacial refugia and dispersal from these refugia during inter-glacial periods (Nakao et al 2013b). In Europe, for example, Nakao et al (2009) proposed an introduction of E. multilocularis in the late Pleistocene, with contraction and subsequent spread from glacial refugia, such as the Iberian, Italian and Balkan peninsulas, presumably initially to the genetically diverse Alpine arch region of Switzerland, southern Germany, eastern France and Austria (Knapp et al, 2009(Knapp et al, , 2015.…”