Insect-associated bacterial communities across an anthropogenic landscape.

Abstract

Anthropogenic activities induce drastic changes in land use that are at least partly responsible for the ongoing global patterns of macro-biodiversity erosion. These habitat changes also impact the fitness of the resilient species, through direct effects on diet and/or indirect environmental effects. Although microbial communities associated with species can crucially influence a diverse set of their host's biological functions, studies on how microbial communities associated with wild species respond to habitat degradation remain scarce. We use metacommunities of two sympatric herbivorous insect species specialized in feeding on Plantago lanceolata that occurs across a network of natural meadows, pastures, and roadsides, as a model system to test the hypothesis that habitat degradation can also impact their associated microbial communities. The Glanville fritillary butterfly, Melitaea cinxia, and the weevil Mecinus pascuorum were sampled from local meadow habitats affected by various levels of disturbance (e.g., roads, agricultural fields, and buildings). The two species carry very distinct microbiota, either highly diverse and transient for the butterfly or dominated by a few resident bacterial symbionts for the weevil. Spatial characteristics of the focal habitat patch, namely the area of the meadow or the location of the meadow, explained the largest proportion of the variation in microbial community composition in both species, but these effects were significant only in the weevil. In contrast to our prediction, despite a minor increase in bacterial diversity along the gradient of habitat degradation, the overall composition of the microbiota was unchanged across habitats in both host species. Overall, local environmental characteristics other than habitat degradation explain the microbial associations in the two herbivorous insects of this system.

Importance: This research dives into the impact of habitat degradation on bacterial communities associated with wild herbivorous insect species, utilizing the ecologically relevant and well-characterized fragmented landscape of the Åland Islands, Finland. This study is crucial as habitat degradation driven by anthropogenic activities (i.e., land use change and habitat fragment size) poses a growing threat to global biodiversity. Indeed, as microbial partners play a pivotal role in the ecology and adaptation of their host species to their environment, there is a pressing need to comprehend how the host-associated microbial diversity responds to their host environmental changes to evaluate their contribution to the escalating patterns of biodiversity erosion globally. However, despite extensive research on the impact of habitat degradation on macro-species, the effects on microbial communities remain an understudied aspect of species ecology.