Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts

Wolbachia are the most abundant bacterial endosymbionts among arthropods. Although maternally inherited, they do not conform to the widespread view that vertical transmission inevitably selects for beneficial symbionts. Instead, Wolbachia are notorious for their reproductive parasitism which, although lowering host fitness, ensures their spread. However, even for reproductive parasites it can pay to enhance host fitness. Indeed, there is a recent upsurge of reports on Wolbachia‐associated fitness benefits. Therefore, the question arises how such instances of mutualism are related to the phenotypes of reproductive parasitism. Here, we review the evidence of Wolbachia mutualisms in arthropods, including both facultative and obligate relationships, and critically assess their biological relevance. Although many studies report anti‐pathogenic effects of Wolbachia, few actually prove these effects to be relevant to field conditions. We further show that Wolbachia frequently have beneficial and detrimental effects at the same time, and that reproductive manipulations and obligate mutualisms may share common mechanisms. These findings undermine the idea of a clear‐cut distinction between Wolbachia mutualism and parasitism. In general, both facultative and obligate mutualisms can have a strong, and sometimes unforeseen, impact on the ecology and evolution of Wolbachia and their arthropod hosts. Acknowledging this mutualistic potential might be the key to a better understanding of some unresolved issues in the study of Wolbachia–host interactions.     

Costs and benefits of Wolbachia infection in immature Aedes albopictus depend upon sex and competition level

Bacterial endosymbionts induce various effects on hosts and can dramatically impact host fitness and development. An example is provided by obligate, maternally-inherited Wolbachia, which infect a broad range of invertebrates. Wolbachia are capable of altering host reproduction, thereby promoting infection spread. Wolbachia also pose direct physiological costs and benefits to hosts, complicating their categorization as parasites or mutualists. This study examines for an effect of Wolbachia infection in intra-specific larval competition by Aedes albopictus mosquitoes, with the goal of examining for an impact of Wolbachia infection in mixed populations. Similar to prior work examining for an influence of Wolbachia infection on the fitness of A. albopictus in adults, the results presented here support the hypothesized impact of Wolbachia across all life stages, including immatures. The differential competitiveness of infected larvae detected in our experiments indicates that Wolbachia infected A. albopictus females are less competitive relative to uninfected females when competing under highly competitive conditions. In contrast, under low competitive pressures, infected females experience higher survivorship. Thus, Wolbachia infection shifts from parasitism to mutualism as a function of developmental conditions. Results are discussed in relation to the invasion and persistence of Wolbachia in A. albopictus populations.The results are important to the evolution of stable Wolbachia symbioses, including Wolbachia invasion of an uninfected population. The resulting infection dynamics that occur in an infected population are discussed.     

Transitions in symbiosis: evidence for environmental acquisition and social transmission within a clade of heritable symbionts

A dynamic continuum exists from free-living environmental microbes to strict host-associated symbionts that are vertically inherited. However, knowledge of the forces that drive transitions in symbiotic lifestyle and transmission mode is lacking. Arsenophonus is a diverse clade of bacterial symbionts, comprising reproductive parasites to coevolving obligate mutualists, in which the predominant mode of transmission is vertical. We describe a symbiosis between a member of the genus Arsenophonus and the Western honey bee. The symbiont shares common genomic and predicted metabolic properties with the male-killing symbiont Arsenophonus nasoniae, however we present multiple lines of evidence that the bee Arsenophonus deviates from a heritable model of transmission. Field sampling uncovered spatial and seasonal dynamics in symbiont prevalence, and rapid infection loss events were observed in field colonies and laboratory individuals. Fluorescent in situ hybridisation showed Arsenophonus localised in the gut, and detection was rare in screens of early honey bee life stages. We directly show horizontal transmission of Arsenophonus between bees under varying social conditions. We conclude that honey bees acquire Arsenophonus through a combination of environmental exposure and social contacts. These findings uncover a key link in the Arsenophonus clades trajectory from free-living ancestral life to obligate mutualism, and provide a foundation for studying transitions in symbiotic lifestyle.Subject terms: Microbial ecology, Molecular evolution, Bacterial evolution, Bacterial genetics, Phylogenetics     

Supergroup C Wolbachia,mutualist symbionts of filarial nematodes,have a distinct genome structure

Wolbachia pipientis is possibly the most widespread endosymbiont of arthropods and nematodes. While all Wolbachia strains have historically been defined as a single species, 16 monophyletic clusters of diversity (called supergroups) have been described. Different supergroups have distinct host ranges and symbiotic relationships, ranging from mutualism to reproductive manipulation. In filarial nematodes, which include parasites responsible for major diseases of humans (such as Onchocerca volvulus, agent of river blindness) and companion animals (Dirofilaria immitis, the dog heartworm), Wolbachia has an obligate mutualist role and is the target of new treatment regimens. Here, we compare the genomes of eight Wolbachia strains, spanning the diversity of the major supergroups (A–F), analysing synteny, transposable element content, GC skew and gene loss or gain. We detected genomic features that differ between Wolbachia supergroups, most notably in the C and D clades from filarial nematodes. In particular, strains from supergroup C (symbionts of O. volvulus and D. immitis) present a pattern of GC skew, conserved synteny and lack of transposable elements, unique in the Wolbachia genus. These features could be the consequence of a distinct symbiotic relationship between C Wolbachia strains and their hosts, highlighting underappreciated differences between the mutualistic supergroups found within filarial nematodes.     

Comparative Genomics of Insect-Symbiotic Bacteria: Influence of Host Environment on Microbial Genome Composition

Commensal symbionts, thought to be intermediary amid obligate mutualists and facultative parasites, offer insight into forces driving the evolutionary transition into mutualism. Using macroarrays developed for a close relative, Escherichia coli, we utilized a heterologous array hybridization approach to infer the genomic compositions of a clade of bacteria that have recently established symbiotic associations: Sodalis glossinidius with the tsetse fly (Diptera, Glossina spp.) and Sitophilus oryzae primary endosymbiont (SOPE) with the rice weevil (Coleoptera, Sitophilus oryzae). Functional biologies within their hosts currently reflect different forms of symbiotic associations. Their hosts, members of distant insect taxa, occupy distinct ecological niches and have evolved to survive on restricted diets of blood for tsetse and cereal for the rice weevil. Comparison of genome contents between the two microbes indicates statistically significant differences in the retention of genes involved in carbon compound catabolism, energy metabolism, fatty acid metabolism, and transport. The greatest reductions have occurred in carbon catabolism, membrane proteins, and cell structure-related genes for Sodalis and in genes involved in cellular processes (i.e., adaptations towards cellular conditions) for SOPE. Modifications in metabolic pathways, in the form of functional losses complementing particularities in host physiology and ecology, may have occurred upon initial entry from a free-living to a symbiotic state. It is possible that these adaptations, streamlining genomes, act to make a free-living state no longer feasible for the harnessed microbe.     

Wolbachia distribution in selected beetle taxa characterized by PCR screens and MLST data

Wolbachia (Alphaproteobacteria) is an inherited endosymbiont of arthropods and filarial nematodes and was reported to be widespread across insect taxa. While Wolbachia's effects on host biology are not understood from most of these hosts, known Wolbachia‐induced phenotypes cover a spectrum from obligate beneficial mutualism to reproductive manipulations and pathogenicity. Interestingly, data on Wolbachia within the most species‐rich order of arthropods, the Coleoptera (beetles), are scarce. Therefore, we screened 128 species from seven beetle families (Buprestidae, Hydraenidae, Dytiscidae, Hydrophilidae, Gyrinidae, Haliplidae, and Noteridae) for the presence of Wolbachia. Our data show that, contrary to previous estimations, Wolbachia frequencies in beetles (31% overall) are comparable to the ones in other insects. In addition, we used Wolbachia MLST data and host phylogeny to explore the evolutionary history of Wolbachia strains from Hydraenidae, an aquatic lineage of beetles. Our data suggest that Wolbachia from Hydraenidae might be largely host genus specific and that Wolbachia strain phylogeny is not independent to that of its hosts. As this contrasts with most terrestrial Wolbachia–arthropod systems, one potential conclusion is that aquatic lifestyle of hosts may result in Wolbachia distribution patterns distinct from those of terrestrial hosts. Our data thus provide both insights into Wolbachia distribution among beetles in general and a first glimpse of Wolbachia distribution patterns among aquatic host lineages.     

The ecological and medical aspects of the symbiosis between Escherichia coli and man

In this work different variants of the symbiosis of E. coli with a human body are analyzed, and the symbiotic relationships between them are shown to follow the type mutualism, commensalism, parasitism and habitation. The authors emphasize that the multiplicity of variants of bacteria-host relationships is based on the phenotypic polymorphism of E. coli clones (clone lines). Taking into account their ecological (symbiotic) features and biomedical importance, all E. coli clones are divided into 4 groups (clusters): mutualists as nonpathogenic organisms; commensals as potential pathogens (causing extraintestinal E. coli infections); parasites as real pathogens (causing acute intestinal infections); "occasional" symbionts of man. The proposition on the cluster structure of E. coli as a species is formulated.     

Arsenophonus and Sodalis Symbionts in Louse Flies: an Analogy to the Wigglesworthia and Sodalis System in Tsetse Flies

Symbiosis between insects and bacteria result in a variety of arrangements, genomic modifications, and metabolic interconnections. Here, we present genomic, phylogenetic, and morphological characteristics of a symbiotic system associated with Melophagus ovinus, a member of the blood-feeding family Hippoboscidae. The system comprises four unrelated bacteria representing different stages in symbiosis evolution, from typical obligate mutualists inhabiting bacteriomes to freely associated commensals and parasites. Interestingly, the whole system provides a remarkable analogy to the association between Glossina and its symbiotic bacteria. In both, the symbiotic systems are composed of an obligate symbiont and two facultative intracellular associates, Sodalis and Wolbachia. In addition, extracellular Bartonella resides in the gut of Melophagus. However, the phylogenetic origins of the two obligate mutualist symbionts differ. In Glossina, the mutualistic Wigglesworthia appears to be a relatively isolated symbiotic lineage, whereas in Melophagus, the obligate symbiont originated within the widely distributed Arsenophonus cluster. Although phylogenetically distant, the two obligate symbionts display several remarkably similar traits (e.g., transmission via the host''s “milk glands” or similar pattern of genome reduction). To obtain better insight into the biology and possible role of the M. ovinus obligate symbiont, “Candidatus Arsenophonus melophagi,” we performed several comparisons of its gene content based on assignments of the Cluster of Orthologous Genes (COG). Using this criterion, we show that within a set of 44 primary and secondary symbionts, “Ca. Arsenophonus melophagi” is most similar to Wigglesworthia. On the other hand, these two bacteria also display interesting differences, such as absence of flagellar genes in Arsenophonus and their presence in Wigglesworthia. This finding implies that a flagellum is not essential for bacterial transmission via milk glands.     

Mode of development and interspecific avian brood parasitism

Avian interspecific brood parasites differ considerably in theircommitment to parasitism; 87 species are obligate brood parasites,whereas 35 species are known to be facultative brood parasites.This variation is strongly related to mode of development. Obligateparasitism is found almost exclusively in altricial species,whereas facultative interspecific parasitism is predominantin precocial birds. We propose that the association betweenmode of development and form of parasitism reflects a fundamentaldifference between altricial and precocial birds in the relativebenefits of emancipation from parental care after laying. Weargue that altricial brood parasites obtain such a large increasein realized fecundity by avoiding the costs of parental carethat obligate parasitism is favored over facultative parasitism.In contrast, precocial brood parasites gain relatively littlein terms of increased fecundity via obligate parasitism, andmuch of this increase could potentially be gained by facultativeparasitism. Thus, obligate interspecific brood parasitism willnot be favored in precocial birds. Three factors influence thisdifference between altricial and precocial species: (1) altricialbirds have relatively more energy and nutrients with which tolay additional eggs, (2) altricial birds can produce more eggsfor the same amount of energy and nutrients, and (3) altricialbirds realize a greater relative gain in fecundity for eachadditional egg laid. We suggest further that facultative interspecificparasitism in birds may originate simply through a carry overof intraspecific parasitism; 29 of 33 facultative interspecificparasites also parasitize conspecifics. Facultative parasitismof other species would provide a greater range of potentialhost nests and could be maintained as an evolutionarily stableend point by the same mechanisms that maintain intraspecificbrood parasitism. [Behav Ecol 1991;2:309–318]     

Wolbachia在我国广赤眼蜂种群内的感染

Wolbachia是广泛分布于节肢动物生殖组织内的一类细胞内共生菌,它属于原细菌的α亚类,能够通过调控寄主的生殖活动而促进其在寄主种群中的扩散。通过对wsp 基因的克隆及PCR-RFLP分析确定了Wolbachia在我国广赤眼蜂种群内的存在,并发现有2种Wolbachia 菌系的感染,命名为wEvaA和wEvaB。经过克隆分离得到了这2种Wolbachia的wsp基因序列,在GenBank的登录号为AY390279和 AY390280 ,并由基于wsp基因的聚类树中发现,这两种Wolbachia菌系均属于A组。     

Influence of oxidative homeostasis on bacterial density and cost of infection in Drosophila–Wolbachia symbioses

The evolution of symbioses along the continuum between parasitism and mutualism can be influenced by the oxidative homeostasis, that is the balance between reactive oxygen species (ROS) and antioxidant molecules. Indeed, ROS can contribute to the host immune defence to regulate symbiont populations, but are also toxic. This interplay between ROS and symbiosis is notably exemplified by recent results in arthropod–Wolbachia interactions. Wolbachia are symbiotic bacteria involved in a wide range of interactions with their arthropods hosts, from facultative, parasitic associations to obligatory, mutualistic ones. In this study, we used Drosophila–Wolbachia associations to determine whether the oxidative homeostasis plays a role in explaining the differences between phenotypically distinct arthropod–Wolbachia symbioses. We used Drosophila lines with different Wolbachia infections and measured the effects of pro‐oxidant (paraquat) and antioxidant (glutathione) treatments on the Wolbachia density and the host survival. We show that experimental manipulations of the oxidative homeostasis can reduce the cost of the infection through its effect on Wolbachia density. We discuss the implication of this result from an evolutionary perspective and argue that the oxidative homeostasis could underlie the evolution of tolerance and dependence on Wolbachia.     

The role of parasites in generating evolutionary novelty

In this review, David Bermudes and Keith Joiner discuss the interrelationship between parasitism and mutualism and examine the parallel mechanisms used by parasites and mutualists to access and persist within the intracellular environment. By drawing analogies with mutualistic associations, they suggest mechanisms by which some parasites may ultimately benefit their hosts. They further speculate that some hosts may even become dependent upon their parasites.     

HOW TO PREVENT CHEATING: A DIGESTIVE SPECIALIZATION TIES MUTUALISTIC PLANT-ANTS TO THEIR ANT-PLANT PARTNERS

Mutualisms often involve reciprocal adaptations of both partners. Acacia ant-plants defended by symbiotic Pseudomyrmex ant mutualists secrete sucrose-free extrafloral nectar, which is unattractive to generalists. We aimed to investigate whether this extrafloral nectar can also exclude exploiters, that is nondefending ant species. Mutualist workers discriminated against sucrose whereas exploiters and generalists with no affinity toward Acacia myrmecophytes preferred sucrose, because mutualist workers lacked the sucrose-cleaving enzyme invertase, which is present in workers of the other two groups. Sucrose uptake induced invertase activity in workers of parasites and generalists, but not mutualists, and in larvae of all species: the mutualists loose invertase during their ontogeny. This reduced metabolic capacity ties the mutualists to their plant hosts, but it does not completely prevent the mutualism from exploitation. We therefore investigated whether the exploiters studied here are cheaters (i.e., have evolved from former mutualists) or parasites (exploiters with no mutualistic ancestor). A molecular phylogeny demonstrates that the exploiter species did not evolve from former mutualists, and no evidence for cheaters was found. We conclude that being specialized to their partner can prevent mutualists from becoming cheaters, whereas other mechanisms are required to stabilize a mutualism against the exploitation by parasites.     

Global stability of obligate mutualism in community modules with facultative mutualists

Mutualism is a fundamental building block of ecological communities and an important driver of biotic evolution. Classic theory suggests that a pairwise two‐species obligate mutualism is fragile, with a large perturbation potentially driving both mutualist populations into extinction. In nature, however, there are many cases of pairwise obligate mutualism. Such pairwise obligate mutualisms are occasionally associated with additional interactions with facultative mutualists. Here, we use a mathematical model to show that when a two‐species obligate mutualism has a single additional link to a third facultative mutualist, the obligate mutualism can become permanently persistent. In the model, a facultative mutualist interacts with one of two inter‐dependent obligate mutualists, and the facultative mutualist enhances the persistence not only of its directly interacting obligate mutualist, but also that of the other obligate mutualist indirectly, enabling the permanent coexistence of the three mutualist species. The effect of the facultative mutualist is strong; it can allow a three‐species permanent coexistence even when two obligate mutualists by themselves are not sustainable (i.e. not locally stable). These results suggest that facultative mutualists can play a pivotal role for the persistence of obligate mutualisms, and contribute to a better understanding on the mechanisms maintaining more complex mutualistic networks of multiple species.     

Reversal of mutualism in a leafflower–leafflower moth association: the possible driving role of a third‐party partner

A major goal in the study of mutualism is to understand how co‐operation is maintained when mutualism may potentially turn into parasitism. Although certain mechanisms facilitate the persistence of mutualism, parasitic species have repeatedly evolved from mutualistic ancestors. However, documented examples of mutualism reversals are still rare. Leafflowers (Phyllantheae; Phyllanthaceae) include approximately 500 species that engage in obligate mutualism with leafflower moths (Epicephala; Gracillariidae), which actively pollinate flowers, and whose larvae feed on the resulting seeds. We found that the Taiwanese population of the Phyllanthus reticulatus species complex was associated with six sympatric Epicephala species, of which three were derived parasites that induced gall formation on flowers/buds and produced no seeds. Notably, two parasitic species have retained mutualistic pollination behaviour, suggesting that the parasitism was likely not selected for to reduce the cost of mutualism. We propose that the galling habit evolved as an adaptation to escape parasitism by a specialized braconid wasp. The tough gall produced by one species was almost free of braconid parasitism, and the swollen gall induced by the other species probably prevents attack as a result of the larger airspace inside the gall. Our findings suggest that the presence of a third‐party partner can greatly influence the evolutionary fate of mutualisms, regardless of whether the pairwise interaction continues to favour co‐operation.     

Comparative genomics of insect-symbiotic bacteria: influence of host environment on microbial genome composition

Commensal symbionts, thought to be intermediary amid obligate mutualists and facultative parasites, offer insight into forces driving the evolutionary transition into mutualism. Using macroarrays developed for a close relative, Escherichia coli, we utilized a heterologous array hybridization approach to infer the genomic compositions of a clade of bacteria that have recently established symbiotic associations: Sodalis glossinidius with the tsetse fly (Diptera, Glossina spp.) and Sitophilus oryzae primary endosymbiont (SOPE) with the rice weevil (Coleoptera, Sitophilus oryzae). Functional biologies within their hosts currently reflect different forms of symbiotic associations. Their hosts, members of distant insect taxa, occupy distinct ecological niches and have evolved to survive on restricted diets of blood for tsetse and cereal for the rice weevil. Comparison of genome contents between the two microbes indicates statistically significant differences in the retention of genes involved in carbon compound catabolism, energy metabolism, fatty acid metabolism, and transport. The greatest reductions have occurred in carbon catabolism, membrane proteins, and cell structure-related genes for Sodalis and in genes involved in cellular processes (i.e., adaptations towards cellular conditions) for SOPE. Modifications in metabolic pathways, in the form of functional losses complementing particularities in host physiology and ecology, may have occurred upon initial entry from a free-living to a symbiotic state. It is possible that these adaptations, streamlining genomes, act to make a free-living state no longer feasible for the harnessed microbe.     

Friend or foe? A behavioral and stable isotopic investigation of an ant–plant symbiosis

In ant–plant symbioses, the behavior of ant inhabitants affects the nature of the interaction, ranging from mutualism to parasitism. Mutualistic species confer a benefit to the plant, while parasites reap the benefits of the interaction without reciprocating, potentially resulting in a negative impact on the host plant. Using the ant–plant symbiosis between Cordia alliodora and its ant inhabitants as a model system, I examine the costs and benefits of habitation by the four most common ant inhabitants at La Selva Biological Station, Costa Rica. Costs are measured by counting coccoids associated with each ant species. Benefits include patrolling behavior, effectiveness at locating resources, and recruitment response. I also compare the diets of the four ant species using stable isotope analysis of nitrogen (N) and carbon (C). Ants varied in their rates of association with coccoids, performance of beneficial behaviors, and diet. These differences in cost, benefit, and diet among the ant species suggest differences in the nature of the symbiotic relationship between C. alliodora and its ants. Two of the ant species behave in a mutualistic manner, while the other two ant species appear to be parasites of the mutualism. I determined that the mutualistic ants feed at a higher trophic level than the parasitic ants. Behavioral and dietary evidence indicate the protective role of the mutualists, and suggest that the parasitic ants do not protect the plant by consuming herbivores.     

More than 400 million years of evolution and some plants still can't make it on their own: plant stress tolerance via fungal symbiosis

All plants in natural ecosystems are thought to be symbioticwith mycorrhizal and/or endophytic fungi. Collectively, thesefungi express different symbiotic lifestyles ranging from parasitismto mutualism. Analysis of Colletotrichum species indicates thatindividual isolates can express either parasitic or mutualisticlifestyles depending on the host genotype colonized. The endophytecolonization pattern and lifestyle expression indicate thatplants can be discerned as either disease, non-disease, or non-hosts.Fitness benefits conferred by fungi expressing mutualistic lifestylesinclude biotic and abiotic stress tolerance, growth enhancement,and increased reproductive success. Analysis of plant–endophyteassociations in high stress habitats revealed that at leastsome fungal endophytes confer habitat-specific stress toleranceto host plants. Without the habitat-adapted fungal endophytes,the plants are unable to survive in their native habitats. Moreover,the endophytes have a broad host range encompassing both monocotsand eudicots, and confer habitat-specific stress tolerance toboth plant groups. Key words: Colletotrichum, fungal endophytes, stress tolerance, symbiosis, symbiotic lifestyle Received 19 June 2007; Revised 25 November 2007 Accepted 30 November 2007     

Genetic characterization of <Emphasis Type="Italic">Wolbachia</Emphasis> from Great Salt Lake brine flies

Wolbachia are intracellular prokaryotic endosymbionts associated with a wide distribution of arthropod and nematode hosts. Their association ranges from parasitism to mutualism, and there is growing evidence that Wolbachia can have dramatic effects on host reproduction, physiology, and immunity. Although all Wolbachia are currently considered as single species, W. pipientis, phylogenetic studies reveal about a dozen monophyletic groups, each designated as a supergroup. This study uses 16S rRNA gene sequences to examine the genetic diversity of Wolbachia present in three species of Great Salt Lake brine flies, Cirrula hians, Ephydra gracilis, and Mosillus bidentatus. The brine fly Wolbachia sequences are highly similar, with an average nucleotide sequence divergence among the three species of 0.00174. The brine fly Wolbachia form a monophyletic group that is affiliated with a subset of supergroup B, indicating that this supergroup may be more diverse than previously thought. These findings expand the phylogenetic diversity of Wolbachia and extend their host range to taxa adapted to a hypersaline environment.