Small‐scale spatial variation in infection risk shapes the evolution of a Borrelia resistance gene in wild rodents

Abstract

Spatial variation in pathogen-mediated selection is predicted to influence the evolutionary trajectory of host populations and lead to spatial variation in their immunogenetic composition. However, to date few studies have been able to directly link small-scale spatial variation in infection risk to host immune gene evolution in natural, nonhuman populations. Here, we use a natural rodent-Borrelia system to test for associations between landscape-level spatial variation in Borrelia infection risk along replicated elevational gradients in the Swiss Alps and Toll-like receptor 2 (TLR2) evolution, a candidate gene for Borrelia resistance, across bank vole (Myodes glareolus) populations. We found that Borrelia infection risk (i.e., the product of Borrelia prevalence in questing ticks and the average tick load of voles at a sampling site) was spatially variable and significantly negatively associated with elevation. Across sampling sites, Borrelia prevalence in bank voles was significantly positively associated with Borrelia infection risk along the elevational clines. We observed a significant association between naturally occurring TLR2 polymorphisms in hosts and their Borrelia infection status. The TLR2 variant associated with a reduced likelihood of Borrelia infection was most common in rodent populations at lower elevations that face a high Borrelia infection risk, and its frequency changed in accordance with the change in Borrelia infection risk along the elevational clines. These results suggest that small-scale spatial variation in parasite-mediated selection affects the immunogenetic composition of natural host populations, providing a striking example that the microbial environment shapes the evolution of the host's immune system in the wild.

Peer Review #3 of "Bacterial microbiota composition of Ixodes ricinus ticks: the role of environmental variation, tick characteristics and microbial interactions (v0.1)"

“…The finding that B. garinii is less likely to occur at higher elevations is in line with previous observations (Jouda et al 2004b;Cornetti et al 2018) and may be explained by changes in PeerJ reviewing PDF | (2019:09:41295:1:1:NEW 3 Nov 2019)…”

“…For each sampling site, we compiled information on large-scale, site-level ecological variables by obtaining data on elevation, slope and aspect using DHM25, land use data from swissTLM3D (both from Federal Office of Topography swisstopo) and data on temperature and precipitation from Landscape Dynamics (Swiss Federal Research Institute for Water, Snow and Landscape Research WSL and Federal Office of Meteorology and Climatology MeteoSwiss, (Thornton et al 1997)). Data on I. ricinus abundance and the abundance of a key tick host, the bank vole (Myodes glareolus), as well as the ratio of bank vole to other rodents at our sampling sites were obtained from Cornetti et al (2018). Details on the different variables and a justification why they were included to characterise large-scale ecological conditions is provided in the Supplementary Material.…”

Human pathogen co-occurrence in Ixodes ricinus ticks: effects of landscape topography, climatic factors and microbiota interactions

“…For each sampling site, we compiled information on elevation, slope and aspect using DHM25 and land use data from swissTLM3D (both from Federal Office of Topography swisstopo) and information on temperature and precipitation provided by Landscape Dynamics (Swiss Federal Research Institute for Water, Snow and Landscape Research WSL and Federal Office of Meteorology and Climatology MeteoSwiss, [48]). Information on I. ricinus abundance and the abundance of a key tick host, the bank vole ( Myodes glareolus ), as well as the ratio of bank vole to other rodents at our sampling sites were obtained from [43]. Details on and justification for variables is provided in the Supplementary Material.…”

“…Spatial variation in pathogen occurrence and prevalence is often pronounced [41]. For some pathogens, such as B. afzelii , previous studies have identified a range of ecological factors such as elevation and its associated abiotic factors [42, 43] or vegetation type and its associated effects on host communities [44], which contribute to this spatial variation. For other pathogens, however, the ecological drivers of distribution and prevalence remain poorly understood and little is known about the role of other microbes in influencing pathogen occurrence in I. ricinus ticks.…”

Parasite‐mediated selection in a natural metapopulation of Daphnia magna

“…Host-parasite systems are ideal for investigating local adaptation at the metapopulation level because parasites exert strong selection on their hosts (Barber & Dingemanse, 2010;Cornetti, Hilfiker, Lemoine, & Tschirren, 2018;Haldane, 1949), which can in turn lead to local adaptation (Karvonen & Seehausen, 2012;Spichtig & Kawecki, 2004). In addition, variation in parasite presence or abundance can be quantified and is ubiquitous in natural populations, even at small geographic scales (Goren & Ben-Ami, 2013;Laine, 2006;Roy & St-Louis, 2017).…”