Host-parasite interactions in non-native invasive species are dependent on the levels of standing genetic variation at the immune locus

Abstract

Background: Parasites may mediate the success of biological invasions through their effect on host fitness and thus, on host population growth and stability. However, a release from the pressure of parasites is strongly related to the genetic differentiation of the host. In invasive host populations, the number of available genetic variants, allowing them to 'fight' the infection, are likely to be influenced by founder events and genetic drift. The level standing genetic variation of invasive populations may be crucial in successfully adapting to new environments and resisting diseases. We studied invasive populations of raccoon that experienced a random reduction in genetic diversity during the establishment and evaluated the relationship between host immune genetic diversity and intestinal parasites infection.

Results: We distinguished two different genetic clusters that are characterized by different sets of functionally relevant MHC-DRB alleles. Both clusters were characterized by considerably different allele-parasite associations and different levels of parasite infection. The specific resistance MHC-DRB alleles explained the lower prevalence of Digenea parasites. An increased infection intensity was related to the presence of two MHC-DRB alleles. One of these alleles significantly decreased in frequency over time, causing a decrease of Digenea abundance in raccoons in consecutive years.

Conclusions: Our findings suggest that intestinal parasites can exert selective pressure on an invasive host with lowered levels of immune genetic diversity and contribute to promoting local adaptation over time. The random genetic drift that created the two different genetic clusters in the invasive raccoon range imposed completely different MHC-parasite associations, strongly associated with the infection status of populations. Our findings underline the role of standing genetic variation in shaping host-parasite relationships and provide empirical support that functional genetic variation may be, at least partly, responsible for differences in the success of invasive populations.

Keywords: Cestoda; Digenea; Genetic drift; Immune genetic diversity; Intestinal parasites; Invasive populations; MHC-DRB; Raccoon; Standing genetic variation.

Fig. 1

Scatterplot of the genetic differentiation across individuals resulting from discriminant analysis of principal components (DAPC) for the genetic structure of raccoon individuals MHC DRB locus. Individuals are presented as separate dots with colours denoting sampling locations and inclusion of 95% inertia ellipses. Abbreviations correspond to the sampling locations presented on Fig. 2. The inset shows the discriminant analysis (DA) eigenvalues

Fig. 2

Geographical locations of invasive raccoon populations. MHC-DRB allele frequencies found in two genetic clusters shown by the pie charts. The dots represent the locations of sampled populations

Fig. 3

The association between prevalence or infection intensity of Digenea and Cestoda and presence/absence of particular alleles or host age estimated from the general and generalized linear mixed models. Only significant effects for MHC-DRB alleles are shown

Fig. 4

The overtime changes in the frequency of the Prlo-DRB*04 allele (A) Prlo-DRB*19 allele (B) and the abundance of Digenea parasites (C) in raccoons from Warta Mouth National Park (PL1 and PL2 see Fig. 2). The effects of raccoon sex and age are not shown