Impact of intraspecific variation in insect microbiomes on host phenotype and evolution

Abstract

Microbes can be an important source of phenotypic plasticity in insects. Insect physiology, behaviour, and ecology are influenced by individual variation in the microbial communities held within the insect gut, reproductive organs, bacteriome, and other tissues. It is becoming increasingly clear how important the insect microbiome is for insect fitness, expansion into novel ecological niches, and novel environments. These investigations have garnered heightened interest recently, yet a comprehensive understanding of how intraspecific variation in the assembly and function of these insect-associated microbial communities can shape the plasticity of insects is still lacking. Most research focuses on the core microbiome associated with a species of interest and ignores intraspecific variation. We argue that microbiome variation among insects can be an important driver of evolution, and we provide examples showing how such variation can influence fitness and health of insects, insect invasions, their persistence in new environments, and their responses to global environmental changes. A and B are two stages of an individual or a population of the same species. The drivers lead to a shift in the insect associated microbial community, which has consequences for the host. The complex interplay of those consequences affects insect adaptation and evolution and influences insect population resilience or invasion.

A and B are two stages of an individual or a population of the same species. The drivers lead to a shift in the insect associated microbial community, which has consequences for the host. The complex interplay of those consequences affects insect adaptation and evolution and influences insect population resilience or invasion.

Fig. 1. Warming reduces microbial community diversity and survival, feeding, and cold tolerance responses in termites.

Experimental warming in Eastern subterranean termites (Reticulitermes flavipes) resulted in a reduction in gut prokaryotic diversity, especially when exposed to elevated temperature treatment (35 °C) (p < 0.05). The community composition also exhibited significant differences with Bacteroidetes symbionts increasing markedly under warming. Stress tolerance of termites also declined with a reduction in feeding, survival and cold tolerance responses observed [149]. While feeding activity and dispersal of termites is expected to rise under warming [150], gut dysbiosis due to warming may alter their survival and persistence.

Fig. 2. Vertically transmitted Klebsiella oxytoca influences Oriental fruit fly mate selection.

The Oriental fruit fly (Bactrocera dorsalis) harbours a diversity of gut symbionts, of which vertically transmitted Enterobacteriaceae bacteria Klebsiella oxytoca are reported to enhance mate selection [151]. In the absence of this symbiont, significant reduction in mate attraction (via olfaction, p < 0.0001) and mating outcome (via sperm deposition, p < 0.0001) for gnotobiotic virgin females has been reported [152]. Subsequently reinfected with this symbiont, virgin female flies regain both mate attraction and sperm accumulation responses from male flies [152]. By increasing the likelihood of successful mating, K. oxytoca along with other symbionts can facilitate the invasion success of the Oriental fruit fly.