The microbiota of a wild butterfly species over three decades of climate change

Thermal stress can disturb microbial communities associated with host species. As microbes can support essential functions related to host metabolism, physiology, nutrition and immunity, changes in microbial communities can have severe fitness consequences for the host. Although the effects of thermal conditions on host-associated microbiomes have been demonstrated in controlled laboratory settings, how climate change might affect the structure and functionality of microbial communities in wild populations remain poorly understood. Here, we took advantage of the well-characterized long-term field survey of the Glanville fritillary butterfly ( Melitaea cinxia ) metapopulation on the Åland islands, in the Baltic Sea, to fill this gap. We investigated whether bacterial communities associated with larvae show signs of gradual temporal change in response to slow environmental warming across a 28-year period, or whether these communities responded through abrupt change following a sudden drought event that triggered bottlenecks in their butterfly host population. Using a combination of 16S rRNA metabarcoding and metagenomic sequencing, we first showed that M. cinxia harbours a set of stable resident bacteria, including Pseudomonas , Telluria , and Enterobacteriaceae bacteria. But we also characterized a gradual shift in the M. cinxia associated bacterial community over three decades of increasing temperatures and decreasing precipitations. This shift was not unidirectional for all bacterial taxa, as the dominant Telluria and Pseudomonas showed opposing responses to environmental trends. Additionally, the 2018 extreme drought, which triggered acute host population bottlenecks, was associated with a severe disruption of M. cinxia microbiota, and the loss of key Enterobacteriaceae taxa. However, the M. cinxia bacterial community seemed to be able to recover towards pre-drought structure in subsequent years, suggesting a degree of resilience to acute climatic perturbations in this microbial system.