As a consequence of environmental change, it is expected that shifts in temperature and precipitation patterns will infl uence parasite communities and their hosts with unpredictable impact. Parasites play a vital role in ecosystems but there is only limited quantitative data which describe the eff ects of environmental parameters under natural conditions. We investigated the infl uence of rainfall, relative humidity and temperature on the prevalence, abundance and infection intensity of nematodes in southern Africa by studying the gastro-intestinal helminth community of the striped mouse Rhabdomys pumilio. Along a precipitation gradient from the Cape of South Africa to northern Namibia we trapped 470 mice over a geographical distance of about 1400 km. Faecal egg counts of 439 sampled individuals and dissections of 161 gastro-intestinal tracts revealed 15 diff erent helminth species. Th e most abundant nematode species harboured in 62.6% of all infected mice were the oxyurid Syphacia obvelata followed jointly by two species (Heligmonina spira and Neoheligmonella capensis) of the subfamily Nippostrongylinae (43.7%). We found a signifi cant positive correlation between mean annual precipitation (rainfall and relative humidity) and nematode infestation rates of animals and a negative correlation with temperature. In addition, we found associations between precipitation and diff erent qualitative measurements of parasite burden (mean nematode species richness, mean number of nematode worms and infection intensity per individual host). Th e similarity in nematode species composition decreased with distance between all study sites. Our study indicates for the fi rst time an association between climatic variables and parasite prevalence and abundance along a continuous natural climatic gradient in a small mammal. Th ese results might be incorporated in the development of models which can predict possible threats for the balance of ecosystems and shifts in infestation patterns due to global changes.
Major histocompatibility complex (MHC) variability is believed to be maintained by pathogen-driven selection, mediated either through heterozygous advantage or frequency-dependent selection. However, empirical support for these hypotheses under natural conditions is rare. In this study, we investigated the genetic constitution of the functionally important MHC class II gene (DRB exon 2) and the parasite load in a population of the striped mouse (Rhabdomys pumilio) in the Southern Kalahari. Fifty-eight individuals were genetically examined and the endoparasite load was quantified by counting fecal helminth eggs by using a modified McMaster technique. Thirty-four animals (58.6%) were infected. We identified 20 different MHC alleles with high levels of sequence divergence between alleles. Particularly, the antigen-binding sites revealed a significant higher rate of nonsynonymous substitutions (d(N)) than synonymous substitutions (d(S)), giving strong evidence of balancing selection. Heterozygosity did influence the infection status (being infected or not) and the individual fecal egg count (FEC) value with significantly higher values observed in homozygous individuals. Furthermore, a positive relationship was found between specific alleles and parasite load. The allele Rhpu-DRB*1 significantly occurred more frequently in infected individuals and in individuals with high FEC values (high parasite load). Individuals with the allele Rhpu-DRB*1 had a 1.5-fold higher chance of being infected than individuals without this allele (odds ratio test, P < 0.05). Contrarily, the allele Rhpu-DRB*8 significantly occurred more frequent in individuals with low FEC values. Our results support the hypotheses that MHC polymorphism in R. pumilio is maintained through pathogen-driven selection acting by both heterozygosity advantage and frequency-dependent selection.
Differences in host susceptibility to different parasite types are largely based on the degree of matching between immune genes and parasite antigens. Specifically the variable genes of the major histocompatibility complex (MHC) play a major role in the defence of parasites. However, underlying genetic mechanisms in wild populations are still not well understood because there is a lack of studies which deal with multiple parasite infections and their competition within. To gain insights into these complex associations, we implemented the full record of gastrointestinal nematodes from 439 genotyped individuals of the striped mouse, Rhabdomys pumilio. We used two different multivariate approaches to test for associations between MHC class II DRB genotype and multiple nematodes with regard to the main pathogen-driven selection hypotheses maintaining MHC diversity and parasite species-specific co-evolutionary effects. The former includes investigations of a ‘heterozygote advantage’, or its specific form a ‘divergent-allele advantage’ caused by highly dissimilar alleles as well as possible effects of specific MHC-alleles selected by a ‘rare allele advantage’ ( = negative ‘frequency-dependent selection’). A combination of generalized linear mixed models (GLMMs) and co-inertia (COIA) analyses made it possible to consider multiple parasite species despite the risk of type I errors on the population and on the individual level. We could not find any evidence for a ‘heterozygote’ advantage but support for ‘divergent-allele’ advantage and infection intensity. In addition, both approaches demonstrated high concordance of positive as well as negative associations between specific MHC alleles and certain parasite species. Furthermore, certain MHC alleles were associated with more than one parasite species, suggesting a many-to-many gene-parasite co-evolution. The most frequent allele Rhpu-DRB*38 revealed a pleiotropic effect, involving three nematode species. Our study demonstrates the co-existence of specialist and generalist MHC alleles in terms of parasite detection which may be an important feature in the maintenance of MHC polymorphism.
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