Population structure of the parasitic nematode Anguillicola crassus, an invader of declining North Atlantic eel stocks

Abstract

Probably half of all animal species exhibit a parasitic lifestyle and numerous parasites have recently expanded their distribution and host ranges due to anthropogenic activities. Here, we report on the population genetic structure of the invasive nematode Anguillicola crassus, a parasite in freshwater eels, which recently spread from Asia to Europe and North America. Samples were collected from the newly colonized naïve host species Anguilla anguilla (Europe) and Anguilla rostrata (North America), and from indigenous Anguilla japonica in Taiwan and Japan. Using seven microsatellite loci and one mitochondrial marker, we show that the parasite's population structure in Europe mirrors the zoogeographic Boreal Lusitanian break along the English Channel. Both the north-to-south decline of nuclear allelic diversity and the loss of private alleles in the same direction are consistent with a significant isolation-by-distance pattern based on ρST values. In combination with the specific topology of the distance tree among nematode populations, our data suggest that Europe was invaded only once from Taiwan, and that subsequently, genetic diversity was lost due to random drift. On the contrary, the North American sample shares distinct nuclear and mitochondrial signatures with Japanese specimens. We propose that the genetic structure in Europe was shaped by long-range anthropogenic eel host transfers in the north and a single dispersal event into the southwest. The genetically distinct Brittany sample at the edge of the Boreal Lusitanian boundary is indicative of natural dispersal of fish hosts since recruitment occurs naturally there and invertebrate host dissemination is interrupted due to oceanic currents.