All insects are colonized by microorganisms on the insect exoskeleton, in the gut and hemocoel, and within insect cells. The insect microbiota is generally different from microorganisms in the external environment, including ingested food. Specifically, certain microbial taxa are favored by the conditions and resources in the insect habitat, by their tolerance of insect immunity, and by specific mechanisms for their transmission. The resident microorganisms can promote insect fitness by contributing to nutrition, especially by providing essential amino acids, B vitamins, and, for fungal partners, sterols. Some microorganisms protect their insect hosts against pathogens, parasitoids, and other parasites by synthesizing specific toxins or modifying the insect immune system. Priorities for future research include elucidation of microbial contributions to detoxification, especially of plant allelochemicals in phytophagous insects, and resistance to pathogens; as well as their role in among-insect communication; and the potential value of manipulation of the microbiota to control insect pests.

1 Many insects derive nutritional advantage from persistent associations with microorganisms that variously synthesize essential nutrients or digest and detoxify ingested food. These persistent relationships are symbioses. 2 There is strong experimental evidence that symbiotic microorganisms provide plant sap-feeding insects with essential amino acids and contribute to the digestion of cellulose in some wood-feeding insects, including lower termites. Basic nutritional information is, however, lacking for many associations, including the relative roles of microbial and intrinsic sources of cellulose degradation in many insects and B-vitamin provisioning by microorganisms in blood-feeding insects. 3 Some nutritional interactions between insects and their symbiotic microorganisms vary among conspecifics and closely related species. This variation can, in principle, contribute to nutritional explanations for variation in the abundance and distribution of insects. For example, the plant utilization traits of phloem-feeding aphids and stinkbugs have been demonstrated to depend on the identity of microbial partners. Evidence that associations can evolve rapidly comes from the demonstration that the impact of the bacterium Wolbachia on natural populations of its insect host can change from deleterious to beneficial within two decades. 4 Developing genomic tools, especially massively parallel sequencing and metagenomic analyses, offer the opportunity to explore the metabolic capabilities of symbiotic microorganisms and their insect hosts, from which defined hypotheses of nutritional function can be constructed. Nutritional ecology provides the appropriate framework to test these hypotheses in the relevant ecological context.

Summary: The bacteria in the fruitfly Drosophila melanogaster of different life stages was quantified by 454 pyrosequencing of 16S rRNA gene amplicons. The sequence reads were dominated by 5 operational taxonomic units (OTUs) at ≤ 97% sequence identity that could be assigned to Acetobacter pomorum , A. tropicalis , Lactobacillus brevis , L. fructivorans and L. plantarum . The saturated rarefaction curves and species richness indices indicated that the sampling (85 000–159 000 reads per sample) was comprehensive. Parallel diagnostic PCR assays revealed only minor variation in the complement of the five bacterial species across individual insects and three D. melanogaster strains. Other gut‐associated bacteria included 6 OTUs with low %ID to previously reported sequences, raising the possibility that they represent novel taxa within the genera Acetobacter and Lactobacillus . A developmental change in the most abundant species, from L. fructivorans in young adults to A. pomorum in aged adults was identified; changes in gut oxygen tension or immune system function might account for this effect. Host immune responses and disturbance may also contribute to the low bacterial diversity in the Drosophila gut habitat.

The gut microorganisms in some animals are reported to include a core microbiota of consistently associated bacteria that is ecologically distinctive and may have coevolved with the host. The core microbiota is promoted by positive interactions among bacteria, favoring shared persistence; its retention over evolutionary timescales is evident as congruence between host phylogeny and bacterial community composition. This study applied multiple analyses to investigate variation in the composition of gut microbiota in drosophilid flies. First, the prevalence of five previously described gut bacteria (Acetobacter and Lactobacillus species) in individual flies of 21 strains (10 Drosophila species) were determined. Most bacteria were not present in all individuals of most strains, and bacterial species pairs co-occurred in individual flies less frequently than predicted by chance, contrary to expectations of a core microbiota. A complementary pyrosequencing analysis of 16S rRNA gene amplicons from the gut microbiota of 11 Drosophila species identified 209 bacterial operational taxonomic units (OTUs), with near-saturating sampling of sequences, but none of the OTUs was common to all host species. Furthermore, in both of two independent sets of Drosophila species, the gut bacterial community composition was not congruent with host phylogeny. The final analysis identified no common OTUs across three wild and four laboratory samples of D. melanogaster. Our results yielded no consistent evidence for a core microbiota in Drosophila. We conclude that the taxonomic composition of gut microbiota varies widely within and among Drosophila populations and species. This is reminiscent of the patterns of bacterial composition in guts of some other animals, including humans.

The advent of relatively inexpensive tools for characterizing microbial communities has led to an explosion of research exploring the diversity, ecology, and evolution of microbe-host systems. Some now question whether existing conceptual frameworks are adequate to explain microbe-host systems. One popular paradigm is the “holobiont-hologenome,” which argues that a host and its microbiome evolve as a single cooperative unit of selection (i.e., a superorganism). We argue that the hologenome is based on overly restrictive assumptions which render it an approach of little research utility. A host plus its microbiome is more effectively viewed as an ecological community of organisms that encompasses a broad range of interactions (parasitic to mutualistic), patterns of transmission (horizontal to vertical), and levels of fidelity among partners. The hologenome requires high partner fidelity if it is to evolve as a unit. However, even when this is achieved by particular host-microbe pairs, it is unlikely to hold for the entire host microbiome, and therefore the community is unlikely to evolve as a hologenome. Both mutualistic and antagonistic (fitness conflict) evolution can occur among constituent members of the community, not just adaptations at the “hologenome” level, and there is abundant empirical evidence for such divergence of selective interests among members of host-microbiome communities. We believe that the concepts and methods of ecology, genetics, and evolutionary biology will continue to provide a well-grounded intellectual framework for researching host-microbiome communities, without recourse to the limiting assumption that selection acts predominantly at the holobiont level.