The analysis of immunological profiles in wild animals: a case study on immunodynamics in the field vole, Microtus agrestis

Abstract

A revolutionary advance in ecological immunology is that postgenomic technologies now allow molecular mediators defined in laboratory models to be measured at the mRNA level in field studies of many naturally occurring species. Here, we demonstrate the application of such an approach to generate meaningful immunological profiles for wild mammals. We sampled a natural field vole population across the year (n = 307) and developed a battery of cellular assays in which functionally different pro- and anti-inflammatory signalling responses (transcription factors and cytokines) were activated and quantified by Q-PCR. Temporal trends were the strongest feature in the expression data, although some life history stages (mating vs. nonmating males and pregnant females) were also associated with significant variation. There was a striking set of significant negative associations between inflammatory mediators and condition indices reflecting packed erythrocyte volume and relative liver size, spleen size and splenocyte count. Grouped (principal component) measures of inflammatory and anti-inflammatory expression were high in winter, with minima in the breeding season that occurred earlier for grouped anti-inflammatory responses than for grouped inflammatory responses. Some individual immunological mediators also showed patterns unrelated to the breeding season or annual periodic cues. For example, interferon regulatory factor 5 (IRF5) expression declined throughout the study period, indicating a systematic trend in antimicrobial defences. Pinpointing the causes and consequences of such variation may help identify underlying environmental drivers of individual fitness and demographic fluctuation.

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

“…However, the opposite pattern or an absence of relation were detected for Mx2 and Tnf-a gene. Similarly, Jackson et al (2011) showed that wild field voles with a poorer body condition were characterized by a higher levels of proinflammatory cytokine expression. They suggested that other undetermined environmental drivers, pathogens or immunopathological conditions might account for this unexpected result.…”

An ecosystem approach to understanding and managing within-host parasite community dynamics

“…Chronic, sublethal infections may provide the best examples of such ecosystem engineering because they can have long-lasting effects on the environment, creating conditions for significant ecological and evolutionary responses from other coinfecting parasites and the host [13,80]. Using contemporary immunological tools it may be possible to assess how the environment is altered by infection, and which immune factors or other within-host habitat components are affected [81][82][83], thereby allowing predictions about the role of parasite ecosystem engineers on host condition.…”

Host–parasite biology in the real world: the field voles of Kielder

“…The dataset used for the immunological work, and also providing data for genetic studies (see later sections), was separate from these (Jackson et al 2011). It came from repeated trapping at two spatially separate sites from February 2008 to March 2009 and a further two from April 2009 to March 2010, and had both longitudinal and cross-sectional components.…”