Macrogeographic population structure in a parasitic nematode with avian hosts

Much remains to be discovered about the population genetic structure of parasites, despite the importance of such knowledge to understanding the processes involved in the spread of drug resistance through populations. Here we present a study of population genetic diversity in Trichostrongylus tenuis, an avian parasitic nematode infecting both poultry and game birds, where anthelmintic use is common. We examined diversity of nicotinamide dehydrogenase subunit 4 (nad4) mtDNA sequences within and between seven locations: five in the UK (red grouse hosts), one in Iceland (domestic goose) and one in Norway (willow grouse). Within-UK comparisons showed high nucleotide diversity (π = 0.015, n = 23) but no structure between locations (ΦST = 0.022, P = 0.27), with over 97% of variation distributed within-hosts. The highest diversity was found in Iceland (π = 0.043, n = 4), and the lowest in Norway (π = 0.003, n = 4). Differentiation between countries was considerable (ΦCT = 0.44, P < 0.05), in spite of the potential mixing effects of gene flow via migrating wild hosts and the poultry trade. However, significant pairwise FST values were found only between Norway and the other locations. Phylogenetic analysis provided statistical support for a separate clade for Norwegian samples only, with unresolved diversity leading to a star-shaped relationship between Icelandic and UK haplotypes. These results suggest that Norwegian T. tenuis are isolated, but that there is some connectivity between UK and Icelandic populations. Although anthelmintic resistance has not yet been reported for T. tenuis, the population structure is such that emerging resistance has the potential to spread by gene flow over a large geographic scale.