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

Abstract

Research on the interactions between the field voles (Microtus agrestis) of Kielder Forest and their natural parasites dates back to the 1930s. These early studies were primarily concerned with understanding how parasites shape the characteristic cyclic population dynamics of their hosts. However, since the early 2000s, research on the Kielder field voles has expanded considerably and the system has now been utilized for the study of host-parasite biology across many levels, including genetics, evolutionary ecology, immunology and epidemiology. The Kielder field voles therefore represent one of the most intensely and broadly studied natural host-parasite systems, bridging theoretical and empirical approaches to better understand the biology of infectious disease in the real world. This article synthesizes the body of work published on this system and summarizes some important insights and general messages provided by the integrated and multidisciplinary study of host-parasite interactions in the natural environment.

Fig. 1.

The field vole, Microtus agrestis.

Fig. 2.

Map of longitudinal (white, labelled) and cross-sectional (all) sites within Kielder Forest and surrounding area.

Fig. 3.

Predicted probability of seroconverting for male field voles from Kielder. Variation by month, body condition score (4 = black lines; 8 = grey lines) and red blood cells (RBCs) (past density fixed at 50). In the simulation, anaemic (dashed lines) represents individuals with 3 million RBCs mL⁻¹, and normocytic (solid lines) represents voles with 8 million RBCs mL⁻¹. Modified from Beldomenico et al. (2009b).

Fig. 4.

The web of interactions and magnitude of effects between microparasite species in the Kielder field voles. Positive associations (odds ratio [OR]>1) are in red, negative associations (OR<1) in blue, with intensity of line reflecting the magnitude of an effect. 95% confidence intervals of OR shown in parentheses. Infection history associated with effect also noted: N = negative, P = positive. NP therefore signifies no infection at t_-1 and infection at t₀. Thus, for example, individuals with chronic B. microti infections are ∼2 times more likely to be infected with A. phagocytophilum (OR = 2·34) while those with new B. microti infection are ∼5 times more likely to be infected (OR = 5·43). From Telfer et al. (2010).

Fig. 5.

Causes and consequences of immunogenetic variation in Kielder voles. Polymorphism within cytokine genes – interacting with non-genetic factors – has a discernible effect on the transcription of immune genes and thus on host immune phenotype. Phenotypic variation in immune responses leads to variation among individuals in resistance to a taxonomically diverse range of endemic pathogens, the selective pressures of which drive the maintenance of cytokine genetic diversity. From Turner and Paterson (2013).