Elevational Changes in Bacterial Microbiota Structure and Diversity in an Arthropod-Disease Vector

Abstract

Environmental conditions change rapidly along elevational gradients and have been found to affect community composition in macroscopic taxa, with lower diversity typically observed at higher elevations. In contrast, microbial community responses to elevation are still poorly understood. Specifically, the effects of elevation on vector-associated microbiota have not been studied to date, even though the within-vector microbial community is known to influence vector competence for a range of zoonotic pathogens. Here we characterize the structure and diversity of the bacterial microbiota in an important zoonotic disease vector, the sheep tick Ixodes ricinus, along replicated elevational gradient (630–1673 m) in the Swiss Alps. 16S rRNA sequencing of the whole within-tick bacterial microbiota of questing nymphs and adults revealed a decrease in Faith’s phylogenetic microbial alpha diversity with increasing elevation, while beta diversity analyses revealed a lower variation in microbial community composition at higher elevations. We also found a higher microbial diversity later in the season and significant differences in microbial diversity among tick life stages and sexes, with lowest microbial alpha diversity observed in adult females. No associations between tick genetic diversity and bacterial diversity were observed. Our study demonstrates systematic changes in tick bacterial microbiota diversity along elevational gradients. The observed patterns mirror diversity changes along elevational gradients typically observed in macroscopic taxa, and they highlight the key role of environmental factors in shaping within-host microbial communities in ectotherms.

The biogeography of host‐associated bacterial microbiomes: Revisiting classic biodiversity patterns

“…For microbiomes, in Anna's hummingbirds the relative abundance of certain bacterial lineages and the overall composition of faecal microbiomes vary with elevation, but microbiome diversity at the individual host level (e.g., the number of bacterial lineages) does not (Herder et al, 2021). A decrease in diversity with elevation was detected in bacterial communities associated with the sheep tick (Aivelo et al, 2021). Skin microbiome diversity also decreases with elevation in humans (Li et al, 2019), but increases with elevation in salamanders (Wolz et al, 2018) and shows no elevational trend in Puerto Rican frogs (Hughey et al, 2017).…”

“…Latitudinal diversity gradient Decrease in diversity with latitude Temperature, productivity, diversification and extinction rates, dispersal rates Traditional LDG (Dikongue & Segurel, 2017;Neu et al, 2021;Suzuki et al, 2020;Thompson et al, 2017) • Stronger LDG for external microbiomes • Stronger LDG across larger latitudinal range • LDG differs for aquatic and terrestrial environments Inverse LDG (Neu et al, 2021;Thompson et al, 2017) No LDG (Corby-Harris et al, 2007;Morelan et al, 2019) Elevational diversity gradient Decrease in diversity with elevation or diversity peak at intermediate elevations Temperature, precipitation, habitat area, competition, time since first colonization, dispersal rates Lower microbiome diversity at higher elevation (Aivelo et al, 2021;Li et al, 2019) • Stronger EDG for external microbiomes • Decrease in diversity with elevation • EDG driven by variation in host ecology and demography…”

Comparative Microbiome Analysis of Three Epidemiologically Important Tick Species in Latvia

“…Recent studies have increasingly shown that the tick microbiome varies by geographical origin, species, sex, life stages, environmental stress, tick immunity, host and blood meal [ 7 , 8 , 9 , 10 , 11 , 12 , 13 , 14 ]. In particular, the results showed that tick-associated bacterial communities are largely species-specific, and microbiota of nymphs and males appeared to be more diverse than those of adult females [ 7 , 9 , 10 , 12 ].…”

“…Recent studies have increasingly shown that the tick microbiome varies by geographical origin, species, sex, life stages, environmental stress, tick immunity, host and blood meal [ 7 , 8 , 9 , 10 , 11 , 12 , 13 , 14 ]. In particular, the results showed that tick-associated bacterial communities are largely species-specific, and microbiota of nymphs and males appeared to be more diverse than those of adult females [ 7 , 9 , 10 , 12 ]. The findings of several studies revealed that tick samples originating from geographically close locations had shown higher microbiome similarity [ 11 , 12 , 13 , 14 ].…”

“…The findings of several studies revealed that tick samples originating from geographically close locations had shown higher microbiome similarity [ 11 , 12 , 13 , 14 ]. In addition, the characterization of the bacterial microbiota in Ixodes ricinus ticks along a replicated elevational gradient revealed a lower variation in microbial community composition at higher elevations; also, a higher microbial diversity later in the season was reported [ 9 ].…”