With a little help from my friends: the roles of microbial symbionts in insect populations and communities

Abstract

To understand insect abundance, distribution and dynamics, we need to understand the relevant drivers of their populations and communities. While microbial symbionts are known to strongly affect many aspects of insect biology, we lack data on their effects on populations or community processes, or on insects' evolutionary responses at different timescales. How these effects change as the anthropogenic effects on ecosystems intensify is an area of intense research. Recent developments in sequencing and bioinformatics permit cost-effective microbial diversity surveys, tracking symbiont transmission, and identification of functions across insect populations and multi-species communities. In this review, we explore how different functional categories of symbionts can influence insect life-history traits, how these effects could affect insect populations and their interactions with other species, and how they may affect processes and patterns at the level of entire communities. We argue that insect-associated microbes should be considered important drivers of insect response and adaptation to environmental challenges and opportunities. We also outline the emerging approaches for surveying and characterizing insect-associated microbiota at population and community scales. This article is part of the theme issue 'Towards a toolkit for global insect biodiversity monitoring'.

Keywords: Wolbachia; adaptation; barcoding; facultative endosymbiont; microbiome; symbiosis.

Figure 1.

Insect–microbe symbioses are studied from different angles. A, The microbiome perspective concerns microbial communities’ composition and function across individuals, populations or species. B, The symbiont's perspective concerns specific microbial clades, focusing on their distribution, transmission, genomic evolution or functions. A distinct level of investigation concerns cellular and molecular mechanisms of host–symbiont interaction. C, The host perspective addresses questions about how symbionts affect insect life-history traits and functions. D, The population perspective concerns symbiont effects on insect populations—performance, functions, genetic diversity and evolutionary potential. E, The community perspective addresses questions about symbiotic host's interactions with other species in the community, and thus symbionts' indirect effects on community processes, composition and functions. Levels D and E are the focus of this review.

Figure 2.

Examples of insects that rely on symbionts to different extent and for different functions. (a) Planthoppers are among insects feeding on imbalanced diets that obligately depend on nutritional supplementation by specialized microbes that live within dedicated insect tissues and are transmitted transovarially across generations. (b) Many insects rely on complex, structured, reliably transmitted gut microbial communities that provide nutritional and defensive functions. In honeybees, such gut microbiota date back at least 100 Myr. (c) Ambrosia beetles are among the species that culture specialized fungi. Inoculated within tunnels that beetles construct in living trees, fungi are not only critical to overwhelming tree defenses but also serve as the beetles’ only food source. (d) Some insects depend on microbes acquired from the environment each generation. In Riptortus bean bugs, Caballeronia symbionts, acquired by nymphs from the soil, provide nutrients and can confer other benefits, including pesticide detoxification. (e) Controlling the microbial community in the environment can be essential for nutrition and safety. Burying beetle adults inoculate carcasses that their larvae develop in with their microbiota and provide them to larvae while spreading antimicrobial compounds that help control harmful bacteria. (f) Insects' reliance on protective symbionts can lead to specific adaptations and long-term co-diversification of partners. In beewolves, Streptomyces that protect cocoons from fungal pathogens are transmitted within dedicated antennal glands. (g). Symbionts often protect insects against a variety of environmental challenges. For example, several facultative endosymbionts protect pea aphids against a specialized fungal entomopathogen. (h) Insects commonly have their reproduction affected by symbionts—benefitting microbes, but not necessarily the hosts. For example, in a ladybird Adalia bipunctata, transovarially transmitting facultative endosymbionts kill male embryos, resulting in more resources for females. (i) Many insects do not seem to rely on specialized microbes. Ants in the genus Crematogaster are among those lacking observable amounts of microbiota within their digestive tract.

Figure 3.

Examples of symbiont effects on insect populations and communities. (a) Environmental pressures that aphid facultative endosymbionts can protect against, including the pressure of parasitoids, pathogens and heat, vary throughout a season, promoting certain symbiont associations. The shifting prevalence of alternative symbionts affects the competitive balance among clonal lineages that carry them, affecting population structure. (b) Rapid, continent-wide spread of nematode-defensive Spiroplasma symbiont in mushroom-feeding Drosophila neotestacea has resulted in the loss of host genetic diversity across populations. (c) Defensive symbionts can protect their hosts directly but also have a range of indirect effects on the same or other species. For example, they can negatively affect populations of parasitoids that also attack other species, thus indirectly protecting these species. (d) Facultative endosymbionts can transmit horizontally among species in a community and express the same effects in novel hosts. Hence, transmitting a parasitoid-protective symbiont to a new host species can make that species also resistant to parasitoids.

Figure 4.

Alternative approaches to the characterization of communities of insects and their associated microbes. (a) The primary DNA-based approaches to insect community characterization rely on reconstructing insect marker gene sequences, either from bulk multi-species samples (metabarcoding) or for large numbers of individual insects (barcoding). (b) The approaches to microbiome characterization in collections of wild insects vary considerably in plausible throughput and per-sample cost. The comparison of their strengths and limitations suggests how they can be applied and combined into a workflow that combines breadth and deep insights into selected symbioses.