Dobzhansky-Muller and Wolbachia-Induced Incompatibilities in a Diploid Genetic System

Genetic incompatibilities are supposed to play an important role in speciation. A general (theoretical) problem is to explain the persistence of genetic diversity after secondary contact. Previous theoretical work has pointed out that Dobzhansky-Muller incompatibilities (DMI) are not stable in the face of migration unless local selection acts on the alleles involved in incompatibility. With local selection, genetic variability exists up to a critical migration rate but is lost when migration exceeds this threshold value. Here, we investigate the effect of intracellular bacteria Wolbachia on the stability of hybrid zones formed after the Dobzhansky Muller model. Wolbachia are known to cause a cytoplasmic incompatibility (CI) within and between species. Incorporating intracellular bacteria Wolbachia can lead to a significant increase of critical migration rates and maintenance of divergence, primarily because Wolbachia-induced incompatibility acts to reduce frequencies of F1 hybrids. Wolbachia infect up to two-thirds of all insect species and it is therefore likely that CI co-occurs with DMI in nature. The results indicate that both isolating mechanisms strengthen each other and under some circumstances act synergistically. Thus they can drive speciation processes more forcefully than either when acting alone.     

Maintenance of adaptive differentiation by Wolbachia induced bidirectional cytoplasmic incompatibility: the importance of sib-mating and genetic systems

Background  

Bacteria of the genus Wolbachia are reproductive parasites widespread among arthropods. The most common effect arising from the presence of Wolbachia in a population is Cytoplasmic Incompatibility (CI), whereby postmating reproductive isolation occurs in crosses between an infected male and an uninfected female, or when a male is infected with a different strain of Wolbachia to that of the female (bidirectional CI). Previous theoretical models have demonstrated that bidirectional CI can contribute to the genetic divergence of populations in haploid and diploid organisms. However, haplodiploid organisms were not considered in these models even though they include Nasonia parasitoid wasps – the best example of the implication of Wolbachia in ongoing speciation. Moreover, previous work did not investigate inbreeding mating systems, which are frequently observed in arthropod species.     

The effect of Wolbachia versus genetic incompatibilities on reinforcement and speciation

Wolbachia is a widespread group of intracellular bacteria commonly found in arthropods. In many insect species, Wolbachia induce a cytoplasmic mating incompatibility (CI). If different Wolbachia infections occur in the same host species, bidirectional CI is often induced. Bidirectional CI acts as a postzygotic isolation mechanism if parapatric host populations are infected with different Wolbachia strains. Therefore, it has been suggested that Wolbachia could promote speciation in their hosts. In this article we investigate theoretically whether Wolbachia-induced bidirectional CI selects for premating isolation and therefore reinforces genetic divergence between parapatric host populations. To achieve this we combined models for Wolbachia dynamics with a well-studied reinforcement model. This new model allows us to compare the effect of bidirectional CI on the evolution of female mating preferences with a situation in which postzygotic isolation is caused by nuclear genetic incompatibilities (NI). We distinguish between nuclear incompatibilities caused by two loci with epistatic interactions, and a single locus with incompatibility among heterozygotes in the diploid phase. Our main findings are: (1) bidirectional CI and single locus NI select for premating isolation with a higher speed and for a wider parameter range than epistatic NI; (2) under certain parameter values, runaway sexual selection leads to the increase of an introduced female preference allele and fixation of its preferred male trait allele in both populations, whereas under others it leads to divergence in the two populations in preference and trait alleles; and (3) bidirectional CI and single locus NI can stably persist up to migration rates that are two times higher than seen for epistatic NI. The latter finding is important because the speed with which mutants at the preference locus spread increases exponentially with the migration rate. In summary, our results show that bidirectional CI selects for rapid premating isolation and so generally support the view that Wolbachia can promote speciation in their hosts.     

Effects of host interaction with Wolbachia on cytoplasmic incompatibility in the two‐spotted spider mite Tetranychus urticae

The endosymbiotic bacterium Wolbachia pipientis infects a wide range of arthropods and induces a variety of reproductive anomalies, including cytoplasmic incompatibility (CI). Three populations of the two‐spotted spider mite, Tetranychus urticae, were investigated in the present study. Based on gene sequencing, they had different host genetic backgrounds but were infected with the same Wolbachia strain. We also examined the CI level relative to host background, male age, Wolbachia density, and Ankyrin (ANK) gene expression in T. urticae. The results of the present study suggest that: (1) CI differences between populations appear to be a result of host genetic background; (2) male age is not a factor determining intensity of CI; (3) Wolbachia density in males may serve as threshold factor necessary for the CI to occur in T. urticae, after which other factors become important in determining the strength of CI; and (4) hosts may modulate CI intensity through modulation of ANK gene expression in males. Our results describe a new type of interaction between Wolbachia and its hosts, and the effect of the interactions on CI. Further investigations on the functions of Wolbachia ankyrin gene products and their host targets, particularly with respect to host reproductive manipulation, are also imperative.     

Population genetics of Wolbachia‐infected,parthenogenetic and uninfected,sexual populations of Tetrastichus coeruleus (Hymenoptera: Eulophidae)

Wolbachia are endosymbiotic bacteria known to manipulate the reproduction of their hosts. These manipulations are expected to have consequences on the population genetics of the host, such as heterozygosity levels, genetic diversity and gene flow. The parasitoid wasp Tetrastichus coeruleus has populations that are infected with parthenogenesis‐inducing Wolbachia and populations that are not infected. We studied the population genetics of T. coeruleus between and within Wolbachia‐infected and uninfected populations, using nuclear microsatellites and mitochondrial DNA. We expected reduced genetic diversity in both DNA types in infected populations. However, migration and gene flow could introduce new DNA variants into populations. We therefore paid special attention to individuals with unexpected (genetic) characteristics. Based on nuclear and mitochondrial DNA, two genetic clusters were evident: a thelytokous cluster containing all Wolbachia‐infected, parthenogenetic populations and an arrhenotokous cluster containing all uninfected, sexual populations. Nuclear and mitochondrial DNA did not exhibit concordant patterns of variation, although there was reduced genetic diversity in infected populations for both DNA types. Within the thelytokous cluster, there was nuclear DNA variation, but no mitochondrial DNA variation. This nuclear DNA variation may be explained by occasional sex between infected females and males, by horizontal transmission of Wolbachia, and/or by novel mutations. Several females from thelytokous populations were uninfected and/or heterozygous for microsatellite loci. These unexpected characteristics may be explained by migration, by inefficient transmission of Wolbachia, by horizontal transmission of Wolbachia, and/or by novel mutations. However, migration has not prevented the build‐up of considerable genetic differentiation between thelytokous and arrhenotokous populations.     

Wolbachia-induced unidirectional cytoplasmic incompatibility and speciation: mainland-island model

Bacteria of the genus Wolbachia are among the most common endosymbionts in the world. In many insect species these bacteria induce a sperm-egg incompatibility between the gametes of infected males and uninfected females, commonly called unidirectional cytoplasmic incompatibility (CI). It is generally believed that unidirectional CI cannot promote speciation in hosts because infection differences between populations will be unstable and subsequent gene flow will eliminate genetic differences between diverging populations. In the present study we investigate this question theoretically in a mainland-island model with migration from mainland to island. Our analysis shows that (a) the infection polymorphism is stable below a critical migration rate, (b) an (initially) uninfected "island" can better maintain divergence at a selected locus (e.g. can adapt locally) in the presence of CI, and (c) unidirectional CI selects for premating isolation in (initially) uninfected island populations if they receive migration from a Wolbachia-infected mainland. Interestingly, premating isolation is most likely to evolve if levels of incompatibility are intermediate and if either the infection causes fecundity reductions or Wolbachia transmission is incomplete. This is because under these circumstances an infection pattern with an infected mainland and a mostly uninfected island can persist in the face of comparably high migration. We present analytical results for all three findings: (a) a lower estimation of the critical migration rate in the presence of local adaptation, (b) an analytical approximation for the gene flow reduction caused by unidirectional CI, and (c) a heuristic formula describing the invasion success of mutants at a mate preference locus. These findings generally suggest that Wolbachia-induced unidirectional CI can be a factor in divergence and speciation of hosts.     

Bidirectional cytoplasmic incompatibility and the stable coexistence of two Wolbachia strains in parapatric host populations

Wolbachiaare intracellular bacteria which are very widely distributed among arthropods. In many insect species Wolbachiaare known to induce cytoplasmic mating incompatibility (CI). It has been suggested that Wolbachiacould promote speciation in their hosts if parapatric host populations are infected with two different Wolbachiastrains causing bidirectional mating incompatibilities. A necessary condition for this speciation scenario to work is that the two Wolbachiastrains can stably coexist. The following study investigates this problem analysing a mathematical model with two host populations and migration between them. We show that the stability of bidirectional CI can be fully described in terms of a critical migration rate which is defined as the highest migration below which a stable coexistence of two Wolbachiastrains is possible. For some special cases we could derive analytical solutions for the critical migration rate; for the general case estimations of the critical migration rate are given. Our main finding is that bidirectional CI can stably persist in the face of high migration and can be as high as over 15% per generation for CI levels observed in nature. These results have implications for the potential of Wolbachiato promote genetic divergence and speciation in their hosts.     

Phylogeography of the parasitic fly Batrachomyia in the Wet Tropics of north-east Australia, and susceptibility of host frog lineages in a mosaic contact zone

Parasites could differentially impact intraspecific host lineages due to genetic, phenotypic, ecological, or behavioural differences between the lineages, or the development of reproductive isolation between them. Batrachomyia (Diptera: Chloropidae) are flies that exclusively parasitize Australian frogs, and in the Wet Tropics rainforest of north‐east Australia larvae are largely restricted to the green‐eyed tree frog Litoria genimaculata (Anura: Hylidae). This frog species consists of two highly divergent genetic lineages that overlap in two nearby, but independent, contact zones. At one contact zone there has been extensive phenotypic divergence and speciation between the lineages whereas, at the other contact relatively lower levels of phenotypic divergence and reproductive isolation suggest that speciation has not occurred. In the present study we tested: (1) whether the deep phylogeographic divergence between northern and southern host populations is mirrored by congruent genetic structuring in the parasite populations and (2) whether the host lineages are differentially impacted by parasitism. We found that the two divergent frog lineages are parasitized by a single lineage of Batrachomyia, which exhibits strikingly little phylogeographic structuring. We found a significant difference in Batrachomyia prevalence between the host lineages at mixed lineage sites in both contact zones, with the magnitude and direction of this effect being consistent in both. The pattern did not differ between the two contacts even though recent phenotypic divergence and speciation has occurred between the lineages at one contact but not the other. Taken together, this suggests a fundamental difference in susceptibility between the genetically divergent host lineages. Using weight relative to body length as a measure of body condition, we found no differential impact of parasitism on the body condition of each host lineage, and no evidence that parasitism impacts the body condition of the host in general. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 92 , 593–603.     

Loss of cytoplasmic incompatibility and minimal fecundity effects explain relatively low Wolbachia frequencies in Drosophila mauritiana

Maternally transmitted Wolbachia bacteria infect about half of all insect species. Many Wolbachia cause cytoplasmic incompatibility (CI) and reduced egg hatch when uninfected females mate with infected males. Although CI produces a frequency‐dependent fitness advantage that leads to high equilibrium Wolbachia frequencies, it does not aid Wolbachia spread from low frequencies. Indeed, the fitness advantages that produce initial Wolbachia spread and maintain non‐CI Wolbachia remain elusive. wMau Wolbachia infecting Drosophila mauritiana do not cause CI, despite being very similar to CI‐causing wNo from Drosophila simulans (0.068% sequence divergence over 682,494 bp), suggesting recent CI loss. Using draft wMau genomes, we identify a deletion in a CI‐associated gene, consistent with theory predicting that selection within host lineages does not act to increase or maintain CI. In the laboratory, wMau shows near‐perfect maternal transmission; but we find no significant effect on host fecundity, in contrast to published data. Intermediate wMau frequencies on the island of Mauritius are consistent with a balance between unidentified small, positive fitness effects and imperfect maternal transmission. Our phylogenomic analyses suggest that group‐B Wolbachia, including wMau and wPip, diverged from group‐A Wolbachia, such as wMel and wRi, 6–46 million years ago, more recently than previously estimated.     

The transmission and effects of Wolbachia bacteria in parasitoids

Wolbachia bacteria are obligatory intracellular parasites of arthropods and have been detected in about 70 species of parasitic wasps and three parasitoid flies. Wolbachia are transmitted cytoplasmically (maternally) and modify host reproduction in different ways to enhance their own transmission: parthenogenesis induction (PI), cytoplasmic incompatibility (CI), or feminization (F) of genetic males. Only PI and CI are known in parasitoids. PI-Wolbachia cause thelytoky in otherwise arrhenotokous parasitoids by generating diploid (rather than haploid) unfertilized wasp eggs. CI-Wolbachia cause incompatibility of crosses between infected males and uninfected females because the paternally derived chromosomes fail to decondense and are destroyed after syngamy. More complex situations arise when hosts harbor multiple infections, which can lead to bidirectional incompatibility and may be involved in parasitoid speciation. The relative fitness of infected and uninfected hosts is important to the population dynamics of Wolbachia, and more data are needed. Evolutionary conflict should be common between host genes, Wolbachia genes, and other "selfish" genetic elements. Wolbachia-specific PCR primers are now available for several genes with different rates of evolution. These primers will permit rapid screening in future studies of spatial and temporal patterns of single and multiple infection. Molecular phylogenies show that CI- and PI-Wolbachia do not form discrete clades. In combination with experimental transfection data, this result suggests that host reproductive alterations depend on the interaction between attributes of both Wolbachia and host. Moreover, Wolbachia isolates from closely related hosts do not usually cluster together, and phylogenies suggest that Wolbachia may have radiated after their arthropod hosts. Both results support considerable horizontal transmission of Wolbachia between host species over evolutionary time. Natural horizontal transmisson between parasitoids and their hosts, or with entomoparasitic nematodes or ectoparasitic mites, remains a tantalizing but equivocal possibility. Received: November 27, 1998 / Accepted: January 15, 1999     

The impacts of cytoplasmic incompatibility factor (cifA and cifB) genetic variation on phenotypes

Wolbachia are maternally transmitted, intracellular bacteria that can often selfishly spread through arthropod populations via cytoplasmic incompatibility (CI). CI manifests as embryonic death when males expressing prophage WO genes cifA and cifB mate with uninfected females or females harboring an incompatible Wolbachia strain. Females with a compatible cifA-expressing strain rescue CI. Thus, cif-mediated CI confers a relative fitness advantage to females transmitting Wolbachia. However, whether cif sequence variation underpins incompatibilities between Wolbachia strains and variation in CI penetrance remains unknown. Here, we engineer Drosophila melanogaster to transgenically express cognate and non-cognate cif homologs and assess their CI and rescue capability. Cognate expression revealed that cifA;B native to D. melanogaster causes strong CI, and cognate cifA;B homologs from two other Drosophila-associated Wolbachia cause weak transgenic CI, including the first demonstration of phylogenetic type 2 cifA;B CI. Intriguingly, non-cognate expression of cifA and cifB alleles from different strains revealed that cifA homologs generally contribute to strong transgenic CI and interchangeable rescue despite their evolutionary divergence, and cifB genetic divergence contributes to weak or no transgenic CI. Finally, we find that a type 1 cifA can rescue CI caused by a genetically divergent type 2 cifA;B in a manner consistent with unidirectional incompatibility. By genetically dissecting individual CI functions for type 1 and 2 cifA and cifB, this work illuminates new relationships between cif genotype and CI phenotype. We discuss the relevance of these findings to CI’s genetic basis, phenotypic variation patterns, and mechanism.     

Independent cytoplasmic incompatibility induced by Cardinium and Wolbachia maintains endosymbiont coinfections in haplodiploid thrips populations

Cardinium and Wolbachia are common maternally inherited reproductive parasites that can coinfect arthropods, yet interactions between both bacterial endosymbionts are rarely studied. For the first time, we report their independent expression of complete cytoplasmic incompatibility (CI) in a coinfected host, and CI in a species of the haplodiploid insect order Thysanoptera. In Pezothrips kellyanus, Cardinium‐induced CI resulted in a combination of male development (MD) and embryonic female mortality (FM) of fertilized eggs. In contrast, Wolbachia‐induced CI resulted in FM together with postembryonic mortality not previously reported as a CI outcome. Both endosymbionts appeared to not influence fecundity but virgins produced more offspring than mated females. In coinfected individuals, Wolbachia density was higher than Cardinium. Wolbachia removal did not impact Cardinium density, suggesting a lack of competition within hosts. Maternal transmission was complete for Wolbachia and high for Cardinium. Our data support theoretical predictions and empirical detection of high endosymbiont prevalence in field populations of the native range of this pest thrips. However, previous findings of more frequent loss of Wolbachia than Cardinium, particularly in field populations of the host's invasive range, suggest that genetic diversity or varying environmental factors between field populations also play a role in shaping host‐endosymbiont dynamics.     

Wolbachia Divergence and the Evolution of Cytoplasmic Incompatibility in Culex pipiens

Many insect species harbor Wolbachia bacteria that induce cytoplasmic incompatibility (CI), i.e. embryonic lethality in crosses between infected males and uninfected females, or between males and females carrying incompatible Wolbachia strains. The molecular mechanism of CI remains unknown, but the available data are best interpreted under a modification–rescue model, where a mod function disables the reproductive success of infected males’ sperm, unless the eggs are infected and express a compatible resc function. Here we examine the evolution of CI in the mosquito Culex pipiens, harbouring a large number of closely related Wolbachia strains structured in five distinct phylogenetic groups. Specifically, we used a worldwide sample of mosquito lines to assess the hypothesis that genetic divergence should correlate with the divergence of CI properties on a low evolutionary scale. We observed a significant association of Wolbachia genetic divergence with CI patterns. Most Wolbachia strains from the same group were compatible whereas those from different groups were often incompatible. Consistently, we found a strong association between Wolbachia groups and their mod-resc properties. Finally, lines from the same geographical area were rarely incompatible, confirming the conjecture that the spatial distribution of Wolbachia compatibility types should be constrained by selection. This study indicates a clear correlation between Wolbachia genotypes and CI properties, paving the way toward the identification of the molecular basis of CI through comparative genomics.     

Bidirectional Cytoplasmic Incompatibility Induced by Cross-Order Transfection of Wolbachia: Implications for Control of the Host Population

Wolbachia are widespread endosymbionts in arthropods and some nematodes. This genus of bacteria is known to manipulate host reproduction by inducing cytoplasmic incompatibility (CI). This important phenotype is implicated in the control of host populations since Wolbachia can suppress host populations through the induction of CI in a way similar to the sterile insect technique. Here, we identified a candidate CI-inducing Wolbachia strain from the parasitic wasp Scleroderma guani (wSguBJ) by sequencing and phylogenetic analysis. This Wolbachia strain was then isolated, purified, and artificially transfected into the new whitefly host Bemisia tabaci through nymphal microinjection. Infection frequency monitoring by molecular detection showed that 60–80 % of the offspring from transfected whitefly populations was infected with wSguBJ six generations after the transfer. Laboratory rearing experiments indicated that the artificial transfection caused no significant difference in the numbers of offspring between the transfected and naturally infected populations and had no significant detrimental effects on the development of transfected males, although the development of transfected females was delayed. Reciprocal crossings revealed that bidirectional CI was induced between the transfected and naturally infected whiteflies. These data indicated that the cross-order transfer of the heterologous Wolbachia strain by nymphal microinjection was successful. Mass release of the transfected males that could stably carry the heterologous Wolbachia without significant compromise of fecundity/development may provide an alternative approach to control of host populations.     

What generates the diversity of Wolbachia—arthropod interactions?

Wolbachia are strictly endocellular, vertically transmitted bacteria associated with insects and crustaceans. This group of parasites modify their hosts' reproduction so as to increase their own fitness. This paper reviews the variability of these parasitic alterations and their consequences for host biology and populations. Wolbachia induce cytoplasmic incompatibility (a characteristic apparently specific to Wolbachia) in several insects and one isopod crustacean; parthenogenesis (thelytoky) in haplo-diploid insects; feminization in various isopods. The consequences of these phenomena on speciation, population dynamics and genetic polymorphism are discussed. The variability of the mechanisms of host sex determination is one important factor responsible for the diversity of Wolbachia-host interactions. However, parasite characteristics, such as the capacity to disturb host mitosis, and the ability to be horizontally transferred between hosts, also appear to play a role in this diversity.     

Intraspecific Colour Variation among Lizards in Distinct Island Environments Enhances Local Camouflage

Within-species colour variation is widespread among animals. Understanding how this arises can elucidate evolutionary mechanisms, such as those underlying reproductive isolation and speciation. Here, we investigated whether five island populations of Aegean wall lizards (Podarcis erhardii) have more effective camouflage against their own (local) island substrates than against other (non-local) island substrates to avian predators, and whether this was linked to island differences in substrate appearance. We also investigated whether degree of local substrate matching varied among island populations and between sexes. In most populations, both sexes were better matched against local backgrounds than against non-local backgrounds, particularly in terms of luminance (perceived lightness), which usually occurred when local and non-local backgrounds were different in appearance. This was found even between island populations that historically had a land connection and in populations that have been isolated relatively recently, suggesting that isolation in these distinct island environments has been sufficient to cause enhanced local background matching, sometimes on a rapid evolutionary time-scale. However, heightened local matching was poorer in populations inhabiting more variable and unstable environments with a prolonged history of volcanic activity. Overall, these results show that lizard coloration is tuned to provide camouflage in local environments, either due to genetic adaptation or changes during development. Yet, the occurrence and extent of selection for local matching may depend on specific conditions associated with local ecology and biogeographic history. These results emphasize how anti-predator adaptations to different environments can drive divergence within a species, which may contribute to reproductive isolation among populations and lead to ecological speciation.     

The effect of Wolbachia on genetic divergence between populations: models with two-way migration

Wolbachia are intracellular bacteria that cause various reproduction alterations in their hosts, including cytoplasmic incompatibility (CI), an incompatibility between sperm and egg that typically results in embryonic death. We investigate theoretically the effects of Wolbachia-induced bidirectional CI on levels of divergence between two populations, where there is migration in both directions and differential selection at a single locus. The main findings are as follows: Wolbachia differences in the two populations are maintained up to a threshold migration rate, above which the system collapses to a single Wolbachia type; differential selection at a nuclear locus increases the threshold migration rate below which Wolbachia polymorphisms are maintained; Wolbachia differences between the populations enhance their genetic divergence at the selected locus by reducing the "effective migration rate," and even moderate levels of CI can cause large population differences in allele frequencies; and asymmetric CI can induce strong asymmetries in effective migration rate and dramatically alter the pattern of genetic divergence compared with the No Wolbachia situation. We derive an analytical approximation for the effective migration rate, which matches the simulation results for most parameter values. These results generally support the view that CI Wolbachia can contribute to genetic divergence between populations.     

Drosophila Adaptation to Viral Infection through Defensive Symbiont Evolution

Microbial symbionts can modulate host interactions with biotic and abiotic factors. Such interactions may affect the evolutionary trajectories of both host and symbiont. Wolbachia protects Drosophila melanogaster against several viral infections and the strength of the protection varies between variants of this endosymbiont. Since Wolbachia is maternally transmitted, its fitness depends on the fitness of its host. Therefore, Wolbachia populations may be under selection when Drosophila is subjected to viral infection. Here we show that in D. melanogaster populations selected for increased survival upon infection with Drosophila C virus there is a strong selection coefficient for specific Wolbachia variants, leading to their fixation. Flies carrying these selected Wolbachia variants have higher survival and fertility upon viral infection when compared to flies with the other variants. These findings demonstrate how the interaction of a host with pathogens shapes the genetic composition of symbiont populations. Furthermore, host adaptation can result from the evolution of its symbionts, with host and symbiont functioning as a single evolutionary unit.     

When can ecological speciation be detected with neutral loci?

It is not yet clear under what conditions empirical studies can reliably detect progress toward ecological speciation through the analysis of allelic variation at neutral loci. We use a simulation approach to investigate the range of parameter space under which such detection is, and is not, likely. We specifically test for the conditions under which divergent natural selection can cause a ‘generalized barrier to gene flow’ that is present across the genome. Our individual‐based numerical simulations focus on how population divergence at neutral loci varies in relation to recombination rate with a selected locus, divergent selection on that locus, migration rate and population size. We specifically test whether genetic differences at neutral markers are greater between populations in different environments than between populations in similar environments. We find that this expected signature of ecological speciation can be detected under part of the parameter space, most consistently when divergent selection is strong and migration is intermediate. By contrast, the expected signature of ecological speciation is not reliably detected when divergent selection is weak or migration is low or high. These findings provide insights into the strengths and weaknesses of using neutral markers to infer ecological speciation in natural systems.     

The mushroom habitat as an ecological arena for global exchange of Wolbachia

Wolbachia infect a variety of arthropod and nematode hosts, but in arthropods, host phylogenetic relationships are usually poor predictors of strain similarity. This suggests that new infections are often established by horizontal transmission. To gain insight into the factors affecting the probability of horizontal transmission among host species, we ask how host phylogeny, geographical distribution and ecology affect patterns of Wolbachia strain similarity. We used multilocus sequence typing (MLST) to characterize Wolbachia strain similarity among dipteran hosts associated with fleshy mushrooms. Wolbachia Supergroup A was more common than Supergroup B in Diptera, and also more common in mycophagous than non‐mycophagous Diptera. Within Supergroup A, host family within Diptera had no effect on strain similarity, and there was no tendency for Wolbachia strains from sympatric host species to be more similar to one another than to strains from hosts in different biogeographical realms. Supergroup A strains differed between mycophagous and non‐mycophagous Diptera more than expected by chance, suggesting that ecological associations can facilitate horizontal transmission of Wolbachia within mycophagous fly communities. For Supergroup B, there were no significant associations between strain similarity and host phylogeny, biogeography, or ecology. We identified only two cases in which closely related hosts carried closely related Wolbachia strains, evidence that Wolbachia‐host co‐speciation or early introgression can occur but may not be a major contributor to overall strain diversity. Our results suggest that horizontal transmission of Wolbachia can be influenced by host ecology, thus leading to partial restriction of Wolbachia strains or strain groups to particular guilds of insects.