Mosquito-mediated niche construction of pitcher plant-associated bacterial communities

Microbes are fundamental to ecosystem function in both host-associated and environmental systems, though these interactions are often studied in isolation. Trophic processes carried out by hosts may influence their potential symbiont pool in systems where symbionts are acquired from the environment. Here, we use the eco-evolutionary framework of niche construction to consider the relationship between host trophic activities and microbial symbiosis. Niche construction describes the process by which organisms change their environment to the benefit or detriment of their fitness. We propose that active manipulation of environmental microbiota by hosts may be an underexplored example of this concept. We use the obligate tripartite symbiosis between the pitcher plant mosquito, Wyeomyia smithii, the northern carnivorous pitcher plant, Sarracenia purpurea, and their associated microbiota to test this hypothesis by exploring how microbial communities are adaptively altered by trophic activities of W. smithii mosquitoes across their life cycle. We report three independent lines of evidence to support adaptive niche construction in this system, leveraging data from amplicon sequencing and microbiota manipulation experiments using axenic (germ-free) and gnotobiotic (recolonized) individuals. First, we characterized bacterial taxa deposited by single adult females during egg-laying and associated with increased larval fitness. Next, we documented changes to composition of pitcher-derived bacterial communities passaged through high larval densities that were associated with increased larval fitness. Lastly, we exposed germ-free W. smithii larvae to titrations of parentally- and environmentally-derived microbiota and observed concomitant shifts in bacterial community composition and larval fitness. Overall, our results provide a novel example of host-mediated niche construction to favor environmental microbial communities that positively impact host fitness over time.