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. 2024 Aug 19;14(8):e70163.
doi: 10.1002/ece3.70163. eCollection 2024 Aug.

Interrelation of the spatial and genetic structure of tick-borne encephalitis virus, its reservoir host (Myodes glareolus), and its vector (Ixodes ricinus) in a natural focus area

Lea Kauer  1 , Gerhard Dobler  2 , Hannah M Schmuck  3 , Lidia Chitimia-Dobler  2 , Martin Pfeffer  3 , Ralph Kühn  1   4
Affiliations

Interrelation of the spatial and genetic structure of tick-borne encephalitis virus, its reservoir host (Myodes glareolus), and its vector (Ixodes ricinus) in a natural focus area

Lea Kauer et al. Ecol Evol. .

Abstract

Tick-borne encephalitis (TBE) virus is considered the medically most important arthropod-borne virus in Europe. Although TBE is endemic throughout central Europe, ticks and rodents determine its maintenance in small, difficult-to-assess, natural foci. We investigated the interrelation between the population genetics of the main TBE virus (TBEV) vector tick (Ixodes ricinus), the most important reservoir host (Myodes glareolus, syn. Clethrionomys glareolus), and TBEV. Rodents and ticks were sampled on 15 sites within an exploratory study area, which has been screened regularly for TBEV occurrence in ticks for more than 10 years. On all 15 sites, ticks and bank voles were sampled, screened for TBEV presence via serology and RT-PCR, and genetically examined. Moreover, TBEV isolates derived from these analyses were sequenced. In long-term TBEV foci bank vole populations show extraordinary genetic constitutions, leading to a particular population structure, whereas ticks revealed a panmictic genetic structure overall sampling sites. Landscape genetics and habitat connectivity modeling (analysis of isolation by resistance) showed no landscape-related barriers explaining the genetic structure of the bank vole populations. The results suggest that bank voles do not simply serve as TBEV reservoirs, but their genetic composition appears to have a significant influence on establishing and maintaining long-term natural TBEV foci, whereas the genetic structure of TBEV's main vector I. ricinus does not play an important role in the sustainability of long-term TBEV foci. A thorough investigation of how and to which extent TBEV and M. glareolus genetics are associated is needed to further unravel the underlying mechanisms.

Keywords: bank voles; habitat corridors; host–parasite ecology; landscape genetics; tick‐borne disease; zoonosis.

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Conflict of interest statement

The authors declare that there are no conflicts of interest.

Figures

FIGURE 1
FIGURE 1
Result of DAPC analysis of 266 bank vole samples from 15 populations color‐coded by RedGreenBlue transformation.
FIGURE 2
FIGURE 2
Genetic differentiation and composition of bank vole populations. (a) Synthesis map combining geographical and genetic data of the bank vole populations after PCoA analysis based on the genetic cluster data, visualized by RedGreenBlue transformation (b) Bank vole individuals cluster affiliation based on PCoA analysis visualized by RedGreenBlue transformation.
FIGURE 3
FIGURE 3
Result of DAPC analysis of 428 Ixodes ricinus samples from 15 populations color‐coded by RedGreenBlue transformation.
FIGURE 4
FIGURE 4
Genetic differentiation and composition of Ixodes ricinus populations. (a) Synthesis map combining geographical with genetic data of the I. ricinus populations after PCoA analysis based on the genetic cluster data, visualized by RedGreenBlue transformation (b) I. ricinus individuals cluster affiliation based on PCoA analysis visualized by RedGreenBlue transformation.
FIGURE 5
FIGURE 5
Genetic differentiation of TBE virus isolates. (a) Synthesis map combining geographical with genetic data of the TBEV isolates after PCoA analysis visualized by RedGreenBlue transformation (b) UPGMA Tree of TBEV virus isolates based on PCoA analysis, nodes are color‐coded according to the RedGreenBlue transformed PCoA axis. This phylogeny is based on 46 silent point mutations.
FIGURE 6
FIGURE 6
Habitat suitability and corridor analysis for bank voles. (a) Habitat suitability surface of the sampling area (b) Modeled least‐cost paths and corridors for bank voles connecting the sampling sites.
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