Infection with Borrelia afzelii and manipulation of the egg surface microbiota have no effect on the fitness of immature Ixodes ricinus ticks

Abstract

Arthropod vectors carry vector-borne pathogens that cause infectious disease in vertebrate hosts, and arthropod-associated microbiota, which consists of non-pathogenic microorganisms. Vector-borne pathogens and the microbiota can both influence the fitness of their arthropod vectors, and hence the epidemiology of vector-borne diseases. The bacterium Borrelia afzelii, which causes Lyme borreliosis in Europe, is transmitted among vertebrate reservoir hosts by Ixodes ricinus ticks, which also harbour a diverse microbiota of non-pathogenic bacteria. The purpose of this controlled study was to test whether B. afzelii and the tick-associated microbiota influence the fitness of I. ricinus. Eggs obtained from field-collected adult female ticks were surface sterilized (with bleach and ethanol), which reduced the abundance of the bacterial microbiota in the hatched I. ricinus larvae by 28-fold compared to larvae that hatched from control eggs washed with water. The dysbiosed and control larvae were subsequently fed on B. afzelii-infected or uninfected control mice, and the engorged larvae were left to moult into nymphs under laboratory conditions. I. ricinus larvae that fed on B. afzelii-infected mice had a significantly faster larva-to-nymph moulting time compared to larvae that fed on uninfected control mice, but the effect was small (2.4% reduction) and unlikely to be biologically significant. We found no evidence that B. afzelii infection or reduction of the larval microbiota influenced the four other life history traits of the immature I. ricinus ticks, which included engorged larval weight, unfed nymphal weight, larva-to-nymph moulting success, and immature tick survival. A retrospective power analysis found that our sampling effort had sufficient power (> 80%) to detect small effects (differences of 5% to 10%) of our treatments. Under the environmental conditions of this study, we conclude that B. afzelii and the egg surface microbiota had no meaningful effects on tick fitness and hence on the R0 of Lyme borreliosis.

Beech tree masting explains the inter-annual variation in the fall and spring peaks of Ixodes ricinus ticks with different time lags

“…In our previous studies on inter-annual variation in the DON and DIN [ 15 , 39 ], we calculated annual means for the climate variables that were based on a 12-month calendar year. However, many steps in the tick life cycle happen over shorter time scales; for example, engorged larvae take ~ 6 to 8 weeks to moult into nymphs at room temperature [ 74 ]. Thus, tick life history traits may depend on climate variables that are operating over shorter temporal windows (e.g., seasons rather than years).…”

Female ticks (Ixodes scapularis) infected with Borrelia burgdorferi have increased overwintering survival, with implications for tick population growth

“…First, B. burgdorferi infection produces no measurable damage to ticks and is not pathogenic (Couret et al, 2022). In a related system, Borrelia afzelii infection had no effect on the survival of I. ricinis nymphs (Hurry et al, 2021). On the contrary, B. burgdorferi appear to benefit I. scapularis (Couret et al, 2022).…”

“…In a related system, Borrelia afzelii infection had no effect on the survival of I. ricinis nymphs (Hurry et al. , 2021). On the contrary, B. burgdorferi appear to benefit I. scapularis (Couret et al.…”

Female ticks (Ixodes scapularis) infected withBorrelia burgdorferihave increased overwintering survival, with implications for tick population growth

“…First, B. burgdorferi infection produces no measurable damage to ticks and is not pathogenic (Couret et al 2022). In a related system, Borrelia afzelii infection had no effect on the survival of I. ricinis nymphs (Hurry et al 2021). On the contrary, B. burgdorferi appears to benefit I. scapularis (Couret et al 2022).…”