PhD THESIS

Population genetic aspects of a newly established parasite-host system between the nematode invader Anguillicola crassus, and the North Atlantic freshwater eels, Anguilla sp.


Keywords: Ecological parasitology - Invasion biology - Population genetics - Phylogeography - Molecular ecology - Biogeography - Admixture clines - Simulation

THESIS DOWNLOAD

Chapter 3:

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

For animal parasites, it has been suggested that host movement is one of the most decisive forces shaping population structure. Animal host migration facilitates gene flow over large distances (Blouin et al. 1995; McCoy et al. 2003; Criscione & Blouin 2004), and likely causes the breakdown of parasite population structure (Nadler et al. 1995). Relying on newly derived microsatellite loci (Wielgoss et al. 2007), and standard mitochondrial markers, I studied the population structure and phylogeography of an exotic nematode, Anguillicoloides crassus (Wielgoss et al. 2008), which recently invaded the European freshwater eel, Anguilla anguilla out of Asia (Lefebvre, Wielgoss et al. 2012). I provided evidence that Europe was invaded only once from Taiwan, and that subsequently, genetic diversity was lost due to random drift by successive spread of the parasite from North to South. However, dispersal is punctuated in the same North-to-South direction most likely by an existing zoogeographic barrier to invertebrate species. The finding of reduced genetic diversity in invasive nematodes compared to native Asian populations is congruent with the patterns found in many other invasive species (Dlugosch & Parker 2008).The clarification of the nematode’s invasion history and distribution patterns also served as baseline to understand other recent geographic colonizations. First, I demonstrated that previously introduced North American samples share nuclear and mitochondrial signatures with Japanese specimens, which indicates a separate source population from the European invasion (Wielgoss et al. 2008). In contrast, the spread of the parasite to the remote Island of Reunion situated in the Indian Ocean appears to be tightly linked with the European invasion (Sasal et al. 2008), which was based on the circumstantial findings of shared unique mitochondrial haplotypes and the presence of nonindigenous eels on this Island.

Figure: Individual-based cluster representation based on Bayesian inference of population structure (adapted from: Wielgoss et al. 2008)

Chapter 5:

Genetic signatures in an invasive parasite of Anguilla anguilla correlate with differential stock management

Beside the potentially negative influences of the nematode, its widespread occurrence in Europe can also offer useful potential. Relying on the identified population structure in Europe, we have a genetic baseline to test the utility of parasites as biological tags, which has a long tradition in fish stock identification (MacKenzie 2002). I demonstrated that microsatellite markers are sensitive to different immigration rates by contrasting two differently managed eel stocks (Wielgoss et al. 2010; see review provided in Gorton et al. 2012). Stocks disrupted by recent stocking (River Rhine) display significant deviations from Hardy-Weinberg Equilibrium, compared to a system with natural glass eel recruitment (River Frémur). This signal is consistent over all four genetic markers used, and is due to the presence of first generation migrants from all around Europe. Therefore, this method can assist to discern anthropogenically driven stocking from naturally occurring eel recruitment. Taken together, my work highlighted that the invasive spread of the eel parasite can facilitate the application of molecular markers to decipher recent movement of the economically important eel hosts, and thus indicate both anthropogenic stocking activities or natural migrations as host genetic markers are much less informative.
Figure: Schematic representation of the level of gene flow between American (orange coloration; left hand side) and European eels (blue coloration; right hand side). Arrows depict directionality of the migration parameter m from either eel species scaled by the mutation rate (m = M/μ, with M being the migration rate per generation per gene copy, and µ being the mutation rate). Thickness of arrows indicates strength of gene flow (adapted from Wielgoss et al. 2014).

Chapter 6:

Introgressive hybridization and latitudinal admixture clines in North Atlantic eels

Hybridization, the interbreeding of diagnosably divergent species, is a major focus in evolutionary studies. Eels, both from North America and Europe migrate through the Atlantic to mate in a vast, overlapping area in the Sargasso Sea. Due to the lack of direct observation, it is unknown how these species remain reproductively isolated. The detection of inter-species hybrids in Iceland suggests on-going gene flow, but few studies to date have addressed the influence of introgression on genetic differentiation in North Atlantic eels. I could show that while mitochondrial lineages remain completely distinct on both sides of the Atlantic, limited hybridization is detectable with nuclear DNA markers (Wielgoss et al. 2014). The nuclear hybridization signal peaks in the northern areas and decreases towards the southern range limits on both continents according to Bayesian assignment analyses. By simulating increasing proportions of both F1 hybrids and admixed individuals from the southern to the northern-most locations, we were able to generate highly significant isolation-by-distance patterns in both cases, reminiscent of previously published data for the European eel. Finally, fitting an isolation-with-migration model to our data supports the hypothesis of recent asymmetric introgression and refutes the alternative hypothesis of ancient polymorphism. Fluctuating degrees of introgressive hybridization between Atlantic eel species are sufficient to explain temporally varying correlations of geographic and genetic distances reported for populations of the European eel.