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Qin, M.; Jiang, L.; Qiao, G.; Chen, J. Phylosymbiotic Relationship between Insects and Symbionts. Encyclopedia. Available online: https://encyclopedia.pub/entry/52427 (accessed on 04 May 2024).
Qin M, Jiang L, Qiao G, Chen J. Phylosymbiotic Relationship between Insects and Symbionts. Encyclopedia. Available at: https://encyclopedia.pub/entry/52427. Accessed May 04, 2024.
Qin, Man, Liyun Jiang, Gexia Qiao, Jing Chen. "Phylosymbiotic Relationship between Insects and Symbionts" Encyclopedia, https://encyclopedia.pub/entry/52427 (accessed May 04, 2024).
Qin, M., Jiang, L., Qiao, G., & Chen, J. (2023, December 06). Phylosymbiotic Relationship between Insects and Symbionts. In Encyclopedia. https://encyclopedia.pub/entry/52427
Qin, Man, et al. "Phylosymbiotic Relationship between Insects and Symbionts." Encyclopedia. Web. 06 December, 2023.
Phylosymbiotic Relationship between Insects and Symbionts
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This entry is adapted from the peer-reviewed paper 10.3390/ijms242115836

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.

microbial community structure phylosymbiosis pattern stochastic effect codiversification ecological filtering

1. Introduction of Phylosymbiosis

Host–microbe symbioses play a crucial role in the ecological and evolutionary history of animals [1][2]. Recent advances in the field of host–microbe interactions have demonstrated the influence of host phylogeny and ecological factors on microbial community assembly [3][4][5]. Phylosymbiosis occurs when host-associated microbiota relationships are positively associated with host phylogenetic relatedness.
Phylosymbiosis is defined as “microbial community relationship parallels the host phylogeny”, in which “phylo” refers to host lineage and “symbiosis” refers to the coexistence of hosts and microbes (Figure 1) [6][7]. In other words, microbial community composition dissimilarities are positively associated with the accumulation of host genetic variation. Phylosymbiosis studies focus on the entire microbiota rather than individuals within the microbiota. The persistent and intimate association between microbes and their host is not the necessary assumption of this eco-evolutionary pattern [8].
Figure 1. Phylosymbiotic versus stochastic microbial community assemblages. Branches in the same color indicate the host and associated microbial community.
Pioneering studies on phylosymbiosis were performed on the parasitoid wasp genus Nasonia under rearing conditions [9], in which species-specific phylosymbiotic gut bacterial communities caused lethality in interspecific hybrids [7]. Afterward, Brooks et al. [10] revealed phylosymbiosis in other animals, including deer mice (Peromyscus), fruit flies (Drosophila), and mosquitoes (i.e., Anopheles, Aedes, and Culex). To date, interspecific phylosymbiotic structures of microbiota have been widely reported in insects, birds, fishes, and mammals [5][10][11][12][13][14][15][16][17][18]. However, phylosymbiosis remains poorly understood at the intraspecific level. Intraspecific phylosymbiosis has only been substantiated in the microbial communities from the American pika Ochotona princeps [19] and the aphid Mollitrichosiphum tenuicorpus [20]. The host taxa in insect phylosymbiosis studies to date cover orders, families, genera, and species, and the evolutionary history of hosts spans approximately 0.3–300 million years [6][21]. The strength of the phylosymbiotic signals between the host and microbiota varies across host taxa [8], and the phylosymbiotic relationships can be weakened with an increasing host evolutionary history [5][21].
Phylosymbiosis analyses typically employ 16S rRNA gene amplicon sequencing data as the input data of the microbial community. Multiple beta diversity distance metrics are usually required for the robustness of the results [8]. Furthermore, a reliable host phylogenetic tree is essential for the determination of phylosymbiosis patterns. The key to measuring phylosymbiosis is to assess the significant correlation between host phylogeny and microbiota beta diversity. Principal methods for quantifying phylosymbiosis are as follows: (1) topological congruency tests [10] utilizing the Robinson–Foulds metric [22] or matching cluster metric [23], or (2) a matrix correlation-based approach, e.g., the Mantel test [24] and Procrustean superimposition [25].

2. Phylosymbiosis in Insects

Insects constitute the most diverse group of animals and play crucial roles in terrestrial ecosystems [26]. Insects harbor a great variety of symbionts, which contribute significantly to the survival, growth, and fecundity of the host [2][27][28]. Additionally, symbionts could facilitate host adaptation to new ecological niches and potentially drive speciation in insects [1][29]. Insect microbial community structures have been found to be correlated with environmental habitat, diet, sex, life stage, and host insect identity and phylogeny [30][31][32]. Some studies highlighted the strongest impact of insect species on the associated microbial communities [30][33]. Currently, phylosymbiosis research in insects remains in its infancy, and phylosymbiosis has been confirmed in the orders Blattodea, Coleoptera, Diptera, Isoptera, Hemiptera, and Hymenoptera (Table 1).
Table 1. Summary of phylosymbiosis patterns in insects.

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

—

[34][35]

Diptera

Anopheles, Aedes, and Culex

8

100

Blood

Proteobacteria

—

[10][36]
 

Drosophila

6

63

Decaying fruit

Proteobacteria

—

[10]

Hemiptera

Greenideinae

53

83

Phloem sap

—

Buchnera aphidicola

[37][38]
 

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

[39][40]

Hymenoptera

Cephalotes

13

46

Pollen and honeydew

—

Cephaloticoccus

[41]
 

Ceratosolen

6

60

Fig

Wolbachia

—

[42][43]
 

Formica

14

30

Honeydew and nectar

Wolbachia, Lactobacillus,

Liliensternia, and Spiroplasma

  

[44][45]
 

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

—

[46][47]

3. Mechanisms Underlying Phylosymbiosis

In most animal systems, microbial transmission and host filtering are major factors influencing microbial community assembly [8][48]. The maintenance of microbes within insect populations usually relies on vertical and horizontal transmission. Strict vertical transmission can promote host–microbe codiversification and ensure the high fidelity of close host–microbe associations during a long evolutionary history. Horizontal transfer of microbes can occur between different individuals of the same or different host species. Horizontal transmissions within conspecifics improve the probability of convergence in microbiota, which may facilitate the appearance of phylosymbiosis [48][49]. However, horizontal transmissions between different host species may weaken the stability of long-lasting host–microbe associations and obscure the phylosymbiotic signatures of microbial communities. For example, significant phylogenetic correlations were not found within the bacterial communities of heteroecious aphids, in which frequent horizontal transmissions of secondary symbionts might have occurred [50][51]. Two typical patterns constitute another principal factor that shapes microbial communities, namely, microorganism filtration within the host. One is the species assortment assembly process, which emphasizes interspecific competition between microorganisms [52]. That is, microbial communities structured according to the species assortment model usually consist of microorganisms that occupy non-overlapping niches. The other is the habitat-filtering model, in which members of the microbiota with similar nutritional requirements tend to arise simultaneously [53][54]. In human gut microbiota with a phylosymbiotic signature, habitat filtering plays a more important role than species assortment [55].
Here, the researchers summarize the contributions of stochastic effects and deterministic forces (i.e., evolutionary and/or ecological factors) on governing the phylosymbiosis patterns in insects (Figure 2). Stochastic and deterministic effects are not mutually exclusive and can contribute to the phylosymbiotic microbiota in combination. For instance, phylosymbiosis in the ants of Cephalotes was attributed to a mix of environmental filtering and shared evolutionary history between ants and symbionts [41].
Figure 2. Mechanisms underlying phylosymbiosis. (A) Gain or loss of microbes arises from stochastic processes. (B) Evolutionary processes, such as codiversification, yield congruent phylogenetic trees of hosts and microbes. (C) Ecological filters select suitable environmental microbes to coexist with the hosts.

3.1. Stochastic Effects

Phylosymbiotic microbiota can be a consequence of stochastic effects, such as spatial limitations on microbial dispersal and random fluctuations in the abundance of microbes (Figure 2A) [56]. Dispersal is referred to as the movement and successful colonization of microbes across space [57]. Moeller et al. [58] revealed that the dispersal limitations of bacteria could promote the compositional divergence of gut microbial communities among mammalian species. In addition to spatial limitations, the composition of the microbial community can be disturbed by the rate and order of microbes that are added to the microbiota during dispersal processes [59]. The microbial dispersal associated with insects generally occurs in the extracellular transmission of microbes, including environmental acquisition, social behavior acquisition, coprophagy, smearing of the egg surface, and capsule or jelly-like secretion transmission [60].
Ecological drift leads to random variation in the relative abundance of species within the microbial community over time [61]. Microbes in low abundances are more susceptible to drift with subsequent extinction. Ecological drift can generate differences in microbial community composition when deterministic processes are weak [59]. In insects, microbiota profiling varies greatly across different groups, with extremes represented by some sap-feeding insects having few gut microbes but abundant intracellular symbionts and by detritivores and wood feeders harboring large and complex gut microbiota [62]. Currently, the effect of ecological drift as the sole factor structuring the microbiota has not been confirmed in any animal system. The phylosymbiotic microbial communities of insects are typically composed of diverse microbes, some of which are abundant and resident. Therefore, the phylosymbiosis pattern within insects is unlikely to be merely drift-driven. Ecological drift may play a part in the interactions with other community assembly processes in structuring insect microbiota.

3.2. Evolutionary Processes

Phylosymbiosis can arise from long-term and stable associations between microbes and hosts, such as coevolution and cospeciation. Here, the researchers use “coevolution” in the narrow sense, which emphasizes the reciprocity and simultaneity of evolutionary changes in interacting species [63]. Cospeciation can result from coevolution and occurs when hosts and microbes speciate simultaneously [64]. Demonstrating the coevolution of animals and symbionts under controlled conditions with laboratory models is difficult because it usually requires long periods of time. However, by utilizing phylogenetic and genomic analyses, we can deduce insect–symbiont coevolution [65][66]. Insects feeding on phloem sap, such as species of Hemiptera, possess symbionts that can provide nutrients to compensate for deficiencies in their food source [67][68]. Many hemipteran taxa and their bacterial endosymbionts rely on the biosynthetic and metabolic complementarity of essential nutrition to maintain intimate associations [29][69][70][71]. For instance, the primary endosymbiont Buchnera aphidicola has highly coadapted to and evolved with aphids for millions of years [72][73][74]. Likewise, such coevolutionary examples have been identified from extracellular gut symbionts that enable nutrient provisioning, e.g., Ishikawaella capsulate in plataspid stinkbugs [75] and Rosenkranzia clausaccus in acanthosomatid stinkbugs [76].
Codiversification represents another evolutionary process that underlies phylosymbiosis (Figure 2B). It occurs when hosts and microbes exhibit congruent phylogenetic trees but does not necessarily imply an occurrence of coevolution [77]. Codiversification can be a consequence of unidirectional selection; that is, microbes adapt to the evolutionary changes imposed by their hosts but not vice versa. In the social corbiculate bees, a strain-level phylogenetic association between the core gut bacteria Lactobacillus Firm-5 and the host bees was observed, which suggested host–microbe codiversification [78]. Other adaptation processes, such as host-shift speciation [79] and shared geographic isolation [80], can also contribute to matching phylogenies of microbes and host lineages.
Considering the low probability of the entirety of a microbial community being transmitted from mother to offspring with high fidelity, it seems unlikely that all microbiota members are involved in the aforementioned evolutionary processes driving phylosymbiosis. Early-arriving species can affect the ability of late-arriving species to establish themselves during community assembly, which is referred to as priority effects [81]. The importance of priority effects in shaping microbial community composition has been reviewed [82]. Moreover, multiple studies have revealed that highly connected keystone or hub microbes can determine the overall community structure via interspecific interactions [83][84][85]. The evolutionary processes underlying phylosymbiosis represented by coevolution rely on vertical transmissions to maintain the stable inheritance of “early-arriving species”. Heritable symbionts have proven to be universal in herbivorous insects [66][86]. For example, Buchnera is located in specialized bacteriocytes and maintained within aphid generations via direct maternal transmission [87]. In the green rice leafhopper Nephotettix cincticeps, the facultative symbiont Rickettsia is vertically transmitted to offspring paternally via an intrasperm passage as well as maternally via an ovarial passage [88]. Additionally, some extracellular gut symbionts can be maternally transmitted through host generations, such as the specific clade of γ-proteobacteria from acanthosomatid stinkbugs, which is maternally transmitted via egg smearing [89]. For social insects, e.g., Acromyrmex leaf-cutting ants [90] and the honey bee Apis mellifera [91], social acquisition of beneficial microbes is critical for specificity and partner fidelity in host–bacterial associations. These initial colonizing symbionts with vertical transmission may have served as keystones or hubs and are responsible for the host-species-specific microbial community composition, which provides the opportunity for phylosymbiosis to occur.

3.3. Ecological Filtering

Moran and Sloan [77] proposed that phylosymbiosis patterns could emerge from simple ecological filtering without any long-term coevolutionary mechanisms. In principle, some host traits can function as filters that exert a selective role on environmental microbes, and the microbes suitable according to these selective forces can coexist with the host (Figure 2C). It is possible that hosts maintain host-species-specific microbial communities via a strong selection of environmental microbes and then yield phylosymbiotic microbiota. Closely related hosts have similar physiological characteristics, immune systems, or microbial defense mechanisms [89][92][93][94], which may bring about the tendency to harbor similar microbial communities. 

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.

3.3.1. Immune System

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.

3.3.2. Diet

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].

3.3.3. Physiological Characteristics

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.

4. Future Directions for Research on Phylosymbiosis in Insects

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.

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Subjects: Entomology
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Man Qin
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Liyun Jiang
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Gexia Qiao
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Jing Chen
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Update Date: 15 Dec 2023
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