Combining species distribution models and population genomics underlines the determinants of range limitation in an emerging parasite

Abstract

Understanding the drivers of species distribution is necessary in order to properly predict the future geographical ranges of colonizing species. Yet this task is challenging for species involved in intimate interactions, such as parasites, since their distribution is likely shaped by a complex interplay between environmental-related and host-related factors. Here we developed an original approach combining species distribution models (SDMs) and population genomics to test whether the local environmental conditions or the host genomic background most likely limits the colonization of an emerging freshwater fish ectoparasite, Tracheliastes polycolpus. We hypothesized that the absence of T. polycolpus in some areas may be due to an unsuitable environment in these areas (the ‘environmental suitability hypothesis') and/or to the presence of resistant hosts in these areas (the ‘genomic background hypothesis'). Using a SDM set at the French spatial extent, we first found that the environmental conditions of an uninfected area were as suitable for the parasite as those of infected areas. Then, using single nucleotide polymorphisms (SNPs) data at the host genome scale, we demonstrated that there was a strong association between the spatial occurrence of parasites and the host genomic background. In particular, the area in which the parasite was absent sustained a unique host population from a genomic standpoint, and ninety SNPs were significantly associated to the infection status (parasitized versus unparasitized) of individual hosts. We concluded that the spatial distribution of T. polycolpus (and its colonization potential) was more likely limited by intrinsic host characteristics associated to parasite resistance, rather than to the local environmental conditions. This study illustrates the usefulness of combining modeling and genomic approaches to reveal the determinants of species distribution and to improve predictions about their future ranges.