Specific Gene Expression Responses to Parasite Genotypes Reveal Redundancy of Innate Immunity in Vertebrates

Abstract

Vertebrate innate immunity is the first line of defense against an invading pathogen and has long been assumed to be largely unspecific with respect to parasite/pathogen species. However, recent phenotypic evidence suggests that immunogenetic variation, i.e. allelic variability in genes associated with the immune system, results in host-parasite genotype-by-genotype interactions and thus specific innate immune responses. Immunogenetic variation is common in all vertebrate taxa and this reflects an effective immunological function in complex environments. However, the underlying variability in host gene expression patterns as response of innate immunity to within-species genetic diversity of macroparasites in vertebrates is unknown. We hypothesized that intra-specific variation among parasite genotypes must be reflected in host gene expression patterns. Here we used high-throughput RNA-sequencing to examine the effect of parasite genotypes on gene expression patterns of a vertebrate host, the three-spined stickleback (Gasterosteus aculeatus). By infecting naïve fish with distinct trematode genotypes of the species Diplostomum pseudospathaceum we show that gene activity of innate immunity in three-spined sticklebacks depended on the identity of an infecting macroparasite genotype. In addition to a suite of genes indicative for a general response against the trematode we also find parasite-strain specific gene expression, in particular in the complement system genes, despite similar infection rates of single clone treatments. The observed discrepancy between infection rates and gene expression indicates the presence of alternative pathways which execute similar functions. This suggests that the innate immune system can induce redundant responses specific to parasite genotypes.

Transcriptome profiling of immune tissues reveals habitat‐specific gene expression between lake and river sticklebacks

“…Of 1060 DE genes between control and challenged fish in the head kidney (Haase et al . ), six overlapped with the DE genes from our study (all in the spleen). Of 1415 DE genes in the gill (Haase et al .…”

“…Of 1415 DE genes in the gill (Haase et al . ), 25 overlapped with our set of DE genes (12 in the head kidney and 14 in the spleen, including 1 in both tissues, Table ).…”

“…In another recent parasite infection study, laboratory‐bred lake sticklebacks (from the G1_L population) were challenged with the trematode D. pseudospathaceum (Haase et al . ), and DE was assessed in the head kidney and in the gill. Of 1060 DE genes between control and challenged fish in the head kidney (Haase et al .…”

“… For the DE genes Haase et al . identified in gill, only the overlapped DE genes we identified in both head kidney and spleen are shown. …”

“…; Haase et al . ). Our study describes gene expression differences in an ecological framework, highlighting habitat‐specific expression of genes that might be involved in adaptation.…”