Insects harbor diverse assemblages of bacterial and fungal symbionts, which play crucial roles in host life history. Insects and their various symbionts represent a good model for studying host–microbe interactions. Phylosymbiosis is used to describe an eco-evolutionary pattern, providing a new cross-system trend in the research of host-associated microbiota. The phylosymbiosis pattern is characterized by a significant positive correlation between the host phylogeny and microbial community dissimilarities.
Insects Examined |
No. of Species Sampled |
Evolutionary Time (Mya) |
Diet |
Core Microbe |
Obligate Symbiont |
References |
|
---|---|---|---|---|---|---|---|
Blattodea |
19 |
>300 |
Omnivory |
Bacteroidetes, Firmicutes, and Proteobacteria |
— |
[21] |
|
Coleoptera |
Dendroctonus frontalis species complex |
7 |
12 |
Phloem cell |
Ceratocystiopsis |
— |
|
Diptera |
Anopheles, Aedes, and Culex |
8 |
100 |
Blood |
Proteobacteria |
— |
|
Drosophila |
6 |
63 |
Decaying fruit |
Proteobacteria |
— |
[10] |
|
Hemiptera |
Greenideinae |
53 |
83 |
Phloem sap |
— |
Buchnera aphidicola |
|
Mollitrichosiphum |
8 |
18–19 |
Phloem sap |
— |
Buchnera aphidicola |
[33] |
|
Mollitrichosiphum tenuicorpus |
1 (26 colonies) |
11 |
Phloem sap |
— |
Buchnera aphidicola |
[20] |
|
Psylloidea |
102 |
350 |
Phloem sap |
— |
Carsonella ruddii |
||
Hymenoptera |
Cephalotes |
13 |
46 |
Pollen and honeydew |
— |
Cephaloticoccus |
[41] |
Ceratosolen |
6 |
60 |
Fig |
Wolbachia |
— |
||
Formica |
14 |
30 |
Honeydew and nectar |
Wolbachia, Lactobacillus, Liliensternia, and Spiroplasma |
|||
Nasonia |
4 |
<1 |
Fly puparium |
Proteobacteria, Firmicutes, and Actinobacteria |
— |
[10] |
|
Lepidoptera |
Heliconiini |
23 |
20–30 |
Pollen, nectar, and fruit |
Acinetobacter, Apibacter, Asaia, Commensalibacter, Enterobacter, Enterococcus, Lactococcus, Spiroplasma, and Pseudomonas |
— |
If the ecological factors that shape microbiota structures are highly phylogenetically conserved during host evolutionary history, we can observe a phylosymbiotic relationship between the host and microbiota [8]. Here, the researchers provide several potential ecological factors shaping the phylosymbiotic microbiota of insects.
Numerous studies have highlighted the importance of the host immune system in regulating microbial community composition [95][96][97][98]. Insects rely on physiological barriers and innate immune responses to defend themselves against pathogens [99][100]. The innate immune system of insects is composed of cellular immune responses by circulating hemocytes [101] and humoral immune responses. Although the hemocyte categories involved in cellular immune responses vary among different insect species, hemocyte functions primarily include phagocytosis, nodulation, and encapsulation [102][103][104]. Humoral defenses are modulated by the Toll, immune deficiency (IMD), Jun N-terminal kinase (JNK), Janus kinase/signal transducers and activators of transcription (JAK/STAT), and prophenoloxidase (PPO) pathways [100][105]. The expression of genes in these pathways subsequently results in antimicrobial peptide (AMP) production, reactive oxygen species (ROS) generation, and melanization. Insects depend on two pathways to regulate antimicrobial peptide generation, namely, the Toll pathway, which responds to fungi and most Gram-positive bacteria, and the IMD pathway, which is induced by Gram-negative bacteria [106].
The insect innate immune system not only defends against pathogens but also plays an important role in maintaining host–microbe symbiosis [107][108][109]. Serving as one of the model systems in Hemiptera, aphids lack several immune-related genes that are suspected to be essential in arthropod immunity [110]. Previous studies suggested that the reduced antimicrobial defense in aphid immunity is attributed to the maintenance of symbionts [111]. To be more specific, the extent of alteration in multiple aphid cellular immunity responses is related to the difference in facultative symbiont species [112]. Eusocial corbiculate bees, including honey bees, bumblebees, and stingless bees, harbor distinctive gut microbiota that are more similar among closely related bee species [78]. The exotic strain of the gut symbiont Gilliamella in honey bees induced higher prostaglandin (PG) production than the native strain, which increased the expression of genes in the IMD and Toll immune pathways [113]. These immune pathways then modulated the dual oxidase (Duox) production and ROS generation to inhibit the nonnative strain of Gilliamella.
There is increasing evidence that diet plays pivotal roles in shaping the microbiota structures of animals [16][32][114][115]. Diet has emerged as a key filter of mammalian gut microbiota [116][117]. The gut microbiota of nonflying mammals was strongly correlated with diet and host phylogeny [115]. Likewise, the microbial communities in bamboo-feeding insects were filtered by diet [31]. If diets themselves are phylogenetically nonindependent, they can serve as ecological filters and lead to phylosymbiotic microbiota. Moreover, complete dietary shifts over long evolutionary periods can disrupt the phylosymbiotic relationship between host and microbial communities [5].
Host plants are one of the major ecological factors shaping the bacterial communities of insect herbivores [31][32][118][119]. The gut microbial communities of caterpillars are dominated by transient and diet-associated bacteria [120], whereas major members of the adult-stage gut microbiota in butterflies are abundant and consistent [46]. The phylosymbiotic signature of microbiota within heliconiine butterflies may arise from the filtering of phylogenetically conserved diet preferences [46]. Within aphids, host–symbiont codiversification as well as filtering by host plants has been highlighted in structuring the phylosymbiotic microbiota of Greenideinae species [37].
Another candidate ecological filter underlying host species-specific microbiota is host physiological structure, such as gut [121] and proventriculus [122]. Biomolecules such as glycans and mucins secreted by the host intestinal wall shape different intestinal environments and are regulators of gut microbial community composition [123][124]. Other host-specific physical and chemical factors in the gut, including biochemical characteristics of the intestinal surface, pH, oxygen levels, and concentrations of metabolites, are also potential filtering factors of microbes. If these factors themselves are phylogenetically conserved over evolutionary history, the microbial communities might exhibit significant correlations with host phylogeny.
The selective filtering of microbes in the gut environment can explain major variations in the phylosymbiotic gut microbial communities in humans [55]. Compared with mammals, birds (e.g., cranes) have strong gastric acidity, which can serve as a microbial filter to limit host-associated differentiation in gut microbiota and subsequently result in weak phylosymbiotic signatures [14]. In insects, selective effects of the gut environment were experimentally confirmed in the cockroach gut microbiota [125]. Cockroaches preferentially select bacteria that are specifically adapted to their intestinal environment. The proventricular filtering mechanism in ants is responsible for the maintenance of ant–bacteria fidelity [122]. Although the importance of host physiological characteristics in filtering gut microbiota has been emphasized in certain insect groups, its role in shaping insect phylosymbiosis remains poorly understood.
While host–symbiont interactions have been documented across many insect groups, we still have a poor understanding of the prevalence of phylosymbiosis in insects. Phylosymbiotic investigations should be performed on a greater variety of insects to sufficiently disentangle the mechanisms underlying this pattern. In addition to bacterial and fungal communities, phylosymbiosis studies at the insect–virome level [126][127] will contribute to developing a comprehensive landscape of host–microbe symbioses. The application of metagenomic sequencing data in phylosymbiosis detection is recommended due to its finer-scale taxonomic and functional profiling. Integrated multi-omic analyses of the microbiome are advantageous in comprehending the mechanisms behind phylosymbiosis because they resolve linkages between host functions, microbial diversity, microbial functions, and environmental variables [128].
To date, most studies have focused on the impact of evolutionary processes on driving phylosymbiotic microbiota. Quantifying the contribution of ecological filtering factors in phylosymbiosis will greatly improve the understanding of the mechanisms behind these patterns. Host-specific biological characteristics and environmental factors should be identified and evaluated quantitatively in the future. It is more likely that a combination of multiple mechanisms rather than a single evolutionary or ecological process is involved in the development of phylosymbiosis; therefore, candidate mechanisms, including stochastic effects, evolutionary processes, and ecological filtering, need to be tested in a diversity of symbiosis systems in both evolutionary and ecological contexts.
This entry is adapted from the peer-reviewed paper 10.3390/ijms242115836