Borrelia afzelii alters reproductive success in a rodent host

Abstract

The impact of a pathogen on the fitness and behaviour of its natural host depends upon the host-parasite relationship in a given set of environmental conditions. Here, we experimentally investigated the effects of Borrelia afzelii, one of the aetiological agents of Lyme disease in humans, on the fitness of its natural rodent host, the bank vole (Myodes glareolus), in semi-natural conditions with two contrasting host population densities. Our results show that B. afzelii can modify the reproductive success and spacing behaviour of its rodent host, whereas host survival was not affected. Infection impaired the breeding probability of large bank voles. Reproduction was hastened in infected females without alteration of the offspring size at birth. At low density, infected males produced fewer offspring, fertilized fewer females and had lower mobility than uninfected individuals. Meanwhile, the infection did not affect the proportion of offspring produced or the proportion of mating partner in female bank voles. Our study is the first to show that B. afzelii infection alters the reproductive success of the natural host. The effects observed could reflect the sickness behaviour due to the infection or they could be a consequence of a manipulation of the host behaviour by the bacteria.

Keywords: Borrelia afzelii; Myodes glareolus; fitness; host–pathogen interaction; natural host; zoonosis.

Figure 1.

The estimated probability of reproduction for a bank vole (±95% CI) depends on their B. afzelii infection treatment (uninfected individuals in solid black, N = 68, infected individuals in dashed grey, N = 68) and their body size (measured as the body mass before injection). In small bank voles, there is no effect of B. afzelii infection on breeding probability. In large bank voles, by contrast, uninfected individuals have higher breeding probability than infected individuals. The observed values are shown with open circles.

Figure 2.

The estimated reproductive success of male bank voles depends on the interaction between B. afzelii infection (uninfected individuals in black, N = 34, infected individuals in grey, N = 34) and population density. (a) Predicted proportion of females successfully fertilized by a male bank vole (±95% CI) as a function of infection and density. (b) Predicted proportion of offspring sired by a male bank vole (±95% CI) as a function of infection and density (electronic supplementary material, table S2). The observed values are shown with open circles.

Figure 3.

The estimated home range (in m²) of male bank voles in the enclosures (±95% CI) depends on the interaction between B. afzelii infection (uninfected individuals in black, N = 13, infected individuals in grey, N = 14) and population density. At low population density, uninfected males have much larger home ranges than B. afzelii-infected males. At high population density, infection with B. afzelii does not affect the home range of male bank voles (electronic supplementary material, table S2). The observed values are shown with open circles.

Figure 4.

Estimated parturition delay in female bank voles (±95% CI) depends on B. afzelii infection (uninfected individuals in black, N = 23; infected individuals in grey, N = 22) and population density (table 1 and electronic supplementary material S4). The observed values are shown with open circles.