Landscape features and helminth co-infection shape bank vole immunoheterogeneity, with consequences for Puumala virus epidemiology

Abstract

Heterogeneity in environmental conditions helps to maintain genetic and phenotypic diversity in ecosystems. As such, it may explain why the capacity of animals to mount immune responses is highly variable. The quality of habitat patches, in terms of resources, parasitism, predation and habitat fragmentation may, for example, trigger trade-offs ultimately affecting the investment of individuals in various immunological pathways. We described spatial immunoheterogeneity in bank vole populations with respect to landscape features and co-infection. We focused on the consequences of this heterogeneity for the risk of Puumala hantavirus (PUUV) infection. We assessed the expression of the Tnf-a and Mx2 genes and demonstrated a negative correlation between PUUV load and the expression of these immune genes in bank voles. Habitat heterogeneity was partly associated with differences in the expression of these genes. Levels of Mx2 were lower in large forests than in fragmented forests, possibly due to differences in parasite communities. We previously highlighted the positive association between infection with Heligmosomum mixtum and infection with PUUV. We found that Tnf-a was more strongly expressed in voles infected with PUUV than in uninfected voles or in voles co-infected with the nematode H. mixtum and PUUV. H. mixtum may limit the capacity of the vole to develop proinflammatory responses. This effect may increase the risk of PUUV infection and replication in host cells. Overall, our results suggest that close interactions between landscape features, co-infection and immune gene expression may shape PUUV epidemiology.

Among‐lake reciprocal transplants induce convergent expression of immune genes in threespine stickleback

“…; Guivier et al . ). Extensive convergence in immune gene expression, shown here, highlights the magnitude and importance of environmental effects on host immunity in nature, which are relatively stronger than the fixed between‐population differences, for most genes examined here.…”

“…; Guivier et al . ), contributing to positive selection on host genes (Duffy & Sivars‐Becker ), genetic polymorphisms (Yasukochi & Satta ), local adaptation (Eizaguirre et al . ), population divergence (Scharsack et al .…”

Preliminary insights into the genetics of bank vole tolerance to Puumala hantavirus in Sweden

“…We evaluated variability at eight single nucleotide polymorphisms that have been previously identified in M. glareolus from Fennoscandia (see for details Supporting Information Table ; Guivier et al, ; Dubois, Galan, et al, ). Note that we focused on a single SNP within Tnf promoter as it had previously been shown to be involved in PUUV/ M. glareolus interaction (Guivier et al, ). We used KASP genotyping services from LGC company (Genotyping by Allele‐Specific Amplification; Cuppen, ) to genotype all sampled voles at these SNPs.…”

“…Additional studies of bank vole populations aimed at characterizing spatial differences in SNP allele frequencies or gene expression levels in candidate genes presumably repressing PUUV replication. These studies reported that tumor necrosis factor (Tnf) promoter polymorphisms and variations in Mx2 gene expression correlated with PUUV distribution in bank vole populations and NE epidemiology (Dubois, Galan, et al, 2017;Guivier et al., 2010;Guivier, Galan, Henttonen, Cosson, & Charbonnel, 2014).…”

Immunology in wild nonmodel rodents: an ecological context for studies of health and disease

“…This information content is attested to by the increasing use of transcriptomic approaches in modern biology. More specifically, early indications in wild rodents suggest that gene expression measurements, especially if interpreted with the complexity of post‐transcriptional dynamics in mind, do contain much useful information.…”