Facultative Bacterial Endosymbionts Research Articles

Facultative endosymbionts modulate the aphid reproductive performance on wheat cultivars differing in contents of benzoxazinoids.

Facultative bacterial endosymbionts have the potential to influence the interactions between aphids, their natural enemies, and host plants. Among the facultative symbionts found in populations of the grain aphid Sitobion avenae in central Chile, the bacterium Regiella insecticola is the most prevalent. In this study, we aimed to investigate whether infected and cured aphid lineages exhibit differential responses to wheat cultivars containing varying levels of the benzoxazinoid DIMBOA (2,4-dihydroxy-7-methoxy-2H-1,4-benzoxazin-3(4H)-one), which is a xenobiotic compound produced by plants. Specifically, we examined the reproductive performance responses of the most frequently encountered genotypes of Sitobion avenae when reared on wheat seedlings expressing low, medium, and high concentrations of DIMBOA. Our findings reveal that the intrinsic rate of population increase (rm ) in cured lineages of Sitobion avenae genotypes exhibits a biphasic pattern, characterized by the lowest rm and an extended time to first reproduction on wheat seedlings with medium levels of DIMBOA. In contrast, the aphid genotypes harbouring Regiella insecticola display idiosyncratic responses, with the two most prevalent genotypes demonstrating improved performance on seedlings featuring an intermediate content of DIMBOA compared to their cured counterparts. This study represents the first investigation into the mediating impact of facultative endosymbionts on aphid performance in plants exhibiting varying DIMBOA contents. These findings present exciting prospects for identifying novel targets for aphid control by manipulating the presence of aphid symbionts. © 2023 Society of Chemical Industry.

The Susceptibility of Bemisia tabaci Mediterranean (MED) Species to Attack by a Parasitoid Wasp Changes between Two Whitefly Strains with Different Facultative Endosymbiotic Bacteria.

In this study, two strains of the mitochondrial lineage Q1 of Bemisia tabaci MED species, characterized by a different complement of facultative bacterial endosymbionts, were tested for their susceptibility to be attacked by the parasitoid wasp Eretmocerus mundus, a widespread natural enemy of B. tabaci. Notably, the BtHC strain infected with Hamiltonella and Cardinium was more resistant to parasitization than the BtHR strain infected with Hamiltonella and Rickettsia. The resistant phenotype consisted of fewer nymphs successfully parasitized (containing the parasitoid mature larva or pupa) and in a lower percentage of adult wasps emerging from parasitized nymphs. Interestingly, the resistance traits were not evident when E. mundus parasitism was compared between BtHC and BtHR using parasitoids originating from a colony maintained on BtHC. However, when we moved the parasitoid colony on BtHR and tested E. mundus after it was reared on BtHR for four and seven generations, we saw then that BtHC was less susceptible to parasitization than BtHR. On the other hand, we did not detect any difference in the parasitization of the BtHR strain between the three generations of E. mundus tested. Our findings showed that host strain is a factor affecting the ability of E. mundus to parasitize B. tabaci and lay the basis for further studies aimed at disentangling the role of the facultative endosymbiont Cardinium and of the genetic background in the resistance of B. tabaci MED to parasitoid attack. Furthermore, they highlight that counteradaptations to the variation of B. tabaci defence mechanisms may be rapidly selected in E. mundus to maximize the parasitoid fitness.

Diversity of endosymbiotic bacteria in the pea aphid (Acyrthosiphon pisum) on alfalfa in Chile

Facultative bacterial endosymbionts are prevalent in aphid pest species and key organisms for the rapid adaptation to changing environment conditions under agricultural management. Facultative endosymbiont interactions allow beneficial phenotypes of insect hosts, providing resistance against natural enemies, fungal infections as well as enhanced resistance to thermal conditions, among others. These interactions have been highlighted as important modulators in the evolution of aphid defenses, being a key aspect for the invasive potential of aphids as pests. In this study, we have examined the bacterial community diversity associated to the pea aphid Acyrthosiphon pisum on alfalfa (Medicago sativa L.) crops in Central Chile by determining the presence and abundance of the seven most common facultative endosymbionts reported for aphid species, including: Hamiltonella defensa, Regiella insecticola, Serratia symbiotica, Spiroplasma sp., Rickettsia sp., Rickettsiella viridis and Fukatsuia symbiotica (or pea aphid X-type symbiont’ PAXS), using a PCR-based approach across species-specific primers, in 16 alfalfa fields during the Chilean spring in the Maule Region. We reported six of the seven endosymbiont species studied, observing a high frequency of infected aphids being the endosymbiont H. defensa, the most predominant among the aphid populations in the different alfalfa fields studied. As H. defensa has been extensively studied in its defensive role to parasitoids, we discuss implications for biological control of this aphid pests. We also discuss the absence of a relevant defensive endosymbiont such as F. symbiotica in the Chilean pea aphid populations and potential implications for the success of the pea aphid biological control program.

Plant-mediated rifampicin treatment of Bemisia tabaci disrupts but does not eliminate endosymbionts

Whiteflies are among the most important global insect pests in agriculture; their sustainable control has proven challenging and new methods are needed. Bacterial symbionts of whiteflies are poorly understood potential target of novel whitefly control methods. Whiteflies harbour an obligatory bacterium, Candidatus Portiera aleyrodidarum, and a diverse set of facultative bacterial endosymbionts. Function of facultative microbial community is poorly understood largely due to the difficulty in their selective elimination without removal of the primary endosymbiont. Since the discovery of secondary endosymbionts, antibiotic rifampicin has emerged as the most used tool for their manipulation. Its effectiveness is however much less clear, with contrasting reports on its effects on the endosymbiont community. The present study builds upon most recent method of rifampicin application in whiteflies and evaluates its ability to eliminate obligatory Portiera and two facultative endosymbionts (Rickettsia and Arsenophnus). Our results show that rifampicin reduces but does not eliminate any of the three endosymbionts. Additionally, rifampicin causes direct negative effect on whiteflies, likely by disrupting mitochondria. Taken together, results signify the end of a rifampicin era in whitefly endosymbiont studies. Finally, we propose refinement of current quantification and data analysis methods which yields additional insights in cellular metabolic scaling.

Paratransgenic manipulation of a tsetse microRNA alters the physiological homeostasis of the fly's midgut environment.

Tsetse flies are vectors of parasitic African trypanosomes, the etiological agents of human and animal African trypanosomoses. Current disease control methods include fly-repelling pesticides, fly trapping, and chemotherapeutic treatment of infected people and animals. Inhibiting tsetse's ability to transmit trypanosomes by strengthening the fly's natural barriers can serve as an alternative approach to reduce disease. The peritrophic matrix (PM) is a chitinous and proteinaceous barrier that lines the insect midgut and serves as a protective barrier that inhibits infection with pathogens. African trypanosomes must cross tsetse's PM in order to establish an infection in the fly, and PM structural integrity negatively correlates with trypanosome infection outcomes. Bloodstream form trypanosomes shed variant surface glycoproteins (VSG) into tsetse's gut lumen early during the infection establishment, and free VSG molecules are internalized by the fly's PM-producing cardia. This process results in a reduction in the expression of a tsetse microRNA (miR275) and a sequential molecular cascade that compromises PM integrity. miRNAs are small non-coding RNAs that are critical in regulating many physiological processes. In the present study, we investigated the role(s) of tsetse miR275 by developing a paratransgenic expression system that employs tsetse's facultative bacterial endosymbiont, Sodalis glossinidius, to express tandem antagomir-275 repeats (or miR275 sponges). This system induces a constitutive, 40% reduction in miR275 transcript abundance in the fly's midgut and results in obstructed blood digestion (gut weights increased by 52%), a significant increase (p-value < 0.0001) in fly survival following infection with an entomopathogenic bacteria, and a 78% increase in trypanosome infection prevalence. RNA sequencing of cardia and midgut tissues from paratransgenic tsetse confirmed that miR275 regulates processes related to the expression of PM-associated proteins and digestive enzymes as well as genes that encode abundant secretory proteins. Our study demonstrates that paratransgenesis can be employed to study microRNA regulated pathways in arthropods that house symbiotic bacteria.

Facultative endosymbionts of aphid populations from coastal dunes of the North Sea

Aphids establish symbiotic associations with a diverse assemblage of mutualistic bacteria. Some of them are not required for the host’s survival but still have a crucial impact on the biology and ecology of their host. Facultative symbionts may modify important host-life-history traits and affect the interactions of aphids with other members of the community. So far several species of aphid have been reported to occur in coastal dunes. Given the extreme environmental conditions of this type of habitat and the wide distribution along the European coast of some aphid species, these aphids would be expected to show variation in their facultative endosymbionts. However, there is currently no information available for these species. To address this question, we collected specimens from different populations of aphids (i.e. Schizaphis rufula, Laingia psammae and Rhopalosiphum padi) associated with the dune grass Ammophila arenaria in several locations of the North and the Irish Sea. By means of specific diagnostic PCR’s we checked for the presence of facultative bacterial endosymbionts in these populations. Results of this explorative assessment showed variation in the endosymbiont community according to species and location. All populations sampled along the North Sea coast were associated with the facultative endosymbiont Serratia symbiotica. Hamiltonella defensa was only detected in some specimens coming from the population in Het Zwin, Belgium. Regiella insecticola and the γ-protobacteria X-type were only found associated with the population of Schizaphis rufula in De Panne, Belgium. Although further experiments are necessary to characterize the nature of these symbiotic relationships, our correlation analyses showed a significant co-occurrence of S. symbiotica with H. defensa and R. insecticola with X-type protobacteria suggesting reciprocal regulatory functions. No significant correlation was detected between the number of mummies (i.e. carcasses of aphids parasitized by wasps) and the occurrence of bacterial symbionts. The potential role of these symbionts in coastal dune ecosystems is discussed.

Large-scale and significant expression from pseudogenes in Sodalis glossinidius - a facultative bacterial endosymbiont.

The majority of bacterial genomes have high coding efficiencies, but there are some genomes of intracellular bacteria that have low gene density. The genome of the endosymbiont Sodalis glossinidius contains almost 50 % pseudogenes containing mutations that putatively silence them at the genomic level. We have applied multiple ‘omic’ strategies, combining Illumina and Pacific Biosciences Single-Molecule Real-Time DNA sequencing and annotation, stranded RNA sequencing and proteome analysis to better understand the transcriptional and translational landscape of Sodalis pseudogenes, and potential mechanisms for their control. Between 53 and 74 % of the Sodalis transcriptome remains active in cell-free culture. The mean sense transcription from coding domain sequences (CDSs) is four times greater than that from pseudogenes. Comparative genomic analysis of six Illumina-sequenced Sodalis isolates from different host Glossina species shows pseudogenes make up ~40 % of the 2729 genes in the core genome, suggesting that they are stable and/or that Sodalis is a recent introduction across the genus Glossina as a facultative symbiont. These data shed further light on the importance of transcriptional and translational control in deciphering host–microbe interactions. The combination of genomics, transcriptomics and proteomics gives a multidimensional perspective for studying prokaryotic genomes with a view to elucidating evolutionary adaptation to novel environmental niches.

The price of protection: a defensive endosymbiont impairs nymph growth in the bird cherry-oat aphid, Rhopalosiphum padi.

Bacterial endosymbionts have enabled aphids to adapt to a range of stressors, but their effects in many aphid species remain to be established. The bird cherry‐oat aphid, Rhopalosiphum padi (Linnaeus), is an important pest of cereals worldwide and has been reported to form symbiotic associations with Serratia symbiotica and Sitobion miscanthi L‐type symbiont endobacteria, although the resulting aphid phenotype has not been described. This study presents the first report of R. padi infection with the facultative bacterial endosymbiont Hamiltonella defensa. Individuals of R. padi were sampled from populations in Eastern Scotland, UK, and shown to represent seven R. padi genotypes based on the size of polymorphic microsatellite markers; two of these genotypes harbored H. defensa. In parasitism assays, survival of H. defensa‐infected nymphs following attack by the parasitoid wasp Aphidius colemani (Viereck) was 5 fold higher than for uninfected nymphs. Aphid genotype was a major determinant of aphid performance on two Hordeum species, a modern cultivar of barley H. vulgare and a wild relative H. spontaneum, although aphids infected with H. defensa showed 16% lower nymph mass gain on the partially resistant wild relative compared with uninfected individuals. These findings suggest that deploying resistance traits in barley will favor the fittest R. padi genotypes, but symbiont‐infected individuals will be favored when parasitoids are abundant, although these aphids will not achieve optimal performance on a poor quality host plant.

Facultative bacterial endosymbionts shape parasitoid food webs in natural host populations: A correlative analysis

Facultative bacterial endosymbionts can protect their aphid hosts from natural enemies such as hymenopteran parasitoids. As such, they have the capability to modulate interactions between aphids, parasitoids and hyperparasitoids. However, the magnitude of these effects in natural aphid populations and their associated parasitoid communities is currently unknown. Moreover, environmental factors such as plant fertilization and landscape complexity are known to affect aphid–parasitoid interactions but it remains unclear how such environmental factors affect the interplay between aphids, parasitoids and endosymbionts.Here, we tested whether facultative endosymbionts confer protection to parasitoids in natural populations of the English grain aphid, Sitobion avenae, and if this is affected by plant fertilization and landscape complexity. Furthermore, we examined whether the effects of facultative endosymbionts can cascade up to the hyperparasitoid level and increase primary‐hyperparasitoid food web specialization.Living aphids and mummies were collected in fertilized and unfertilized plots within 13 wheat fields in Central Germany. We assessed the occurrence of primary parasitoid, hyperparasitoid and endosymbiont species in aphids and mummies using a newly established molecular approach.Facultative endosymbiont infection rates were high across fields (~80%), independent of whether aphids were parasitized or unparasitized. Aphid mummies exhibited a significantly lower share of facultative endosymbiont infection (~38%). These findings suggest that facultative endosymbionts do not affect parasitoid oviposition behaviour, but decrease parasitoid survival in the host. Facultative endosymbiont infection rates were lower in mummies collected from fertilized compared to unfertilized plants, indicating that plant fertilization boosts the facultative endosymbiont protective effect. Furthermore, we found strong evidence for species‐specific and negative cascading effects of facultative endosymbionts on primary and hyperparasitoids, respectively. Facultative endosymbionts impacted parasitoid assemblages and increased the specialization of primary‐hyperparasitoid food webs: these effects were independent from and much stronger than other environmental factors.The current findings strongly suggest that facultative endosymbionts act as a driving force in aphid–parasitoid–hyperparasitoid networks: they shape insect community composition at different trophic levels and modulate, directly and indirectly, the interactions between aphids, parasitoids and their environment.

Incidence of Facultative Bacterial Endosymbionts in Spider Mites Associated with Local Environments and Host Plants.

Spider mites are frequently associated with multiple endosymbionts whose infection patterns often exhibit spatial and temporal variation. However, the association between endosymbiont prevalence and environmental factors remains unclear. Here, we surveyed endosymbionts in natural populations of the spider mite, Tetranychus truncatus, in China, screening 935 spider mites from 21 localities and 12 host plant species. Three facultative endosymbiont lineages, Wolbachia, Cardinium, and Spiroplasma, were detected at different infection frequencies (52.5%, 26.3%, and 8.6%, respectively). Multiple endosymbiont infections were observed in most local populations, and the incidence of individuals with the Wolbachia-Spiroplasma coinfection was higher than expected from the frequency of each infection within a population. Endosymbiont infection frequencies exhibited associations with environmental factors: Wolbachia infection rates increased at localities with higher annual mean temperatures, while Cardinium and Spiroplasma infection rates increased at localities from higher altitudes. Wolbachia was more common in mites from Lycopersicon esculentum and Glycine max compared to those from Zea mays This study highlights that host-endosymbiont interactions may be associated with environmental factors, including climate and other geographically linked factors, as well as the host's food plant.IMPORTANCE The aim of this study was to examine the incidence of endosymbiont distribution and the infection patterns in spider mites. The main findings are that multiple endosymbiont infections were more common than expected and that endosymbiont infection frequencies were associated with environmental factors. This work highlights that host-endosymbiont interactions need to be studied within an environmental and geographic context.

Plantmediated horizontal transmission of Wolbachia between whiteflies

Maternal transmission is the main transmission pathway of facultative bacterial endosymbionts, but phylogenetically distant insect hosts harbor closely related endosymbionts, suggesting that horizontal transmission occurs in nature. Here we report the first case of plant-mediated horizontal transmission of Wolbachia between infected and uninfected Bemisia tabaci AsiaII7 whiteflies. After infected whiteflies fed on cotton leaves, Wolbachia was visualized, both in the phloem vessels and in some novel ‘reservoir’ spherules along the phloem by fluorescence in situ hybridization using Wolbachia-specific 16S rRNA probes and transmission electron microscopy. Wolbachia persisted in the plant leaves for at least 50 days. When the Wolbachia-free whiteflies fed on the infected plant leaves, the majority of them became infected with the symbiont and vertically transmitted it to their progeny. Multilocus sequence typing and sequencing of the wsp (Wolbachia surface protein) gene confirmed that the sequence type of Wolbachia in the donor whiteflies, cotton phloem and the recipient whiteflies are all identical (sequence type 388). These results were replicated using cowpea and cucumber plants, suggesting that horizontal transmission is also possible through other plant species. Our findings may help explain why Wolbachia bacteria are so abundant in arthropods, and suggest that in some species, Wolbachia may be maintained in populations by horizontal transmission.

The Role of Lipid Competition for Endosymbiont-Mediated Protection against Parasitoid Wasps in Drosophila.

ABSTRACTInsects commonly harbor facultative bacterial endosymbionts, such as Wolbachia and Spiroplasma species, that are vertically transmitted from mothers to their offspring. These endosymbiontic bacteria increase their propagation by manipulating host reproduction or by protecting their hosts against natural enemies. While an increasing number of studies have reported endosymbiont-mediated protection, little is known about the mechanisms underlying this protection. Here, we analyze the mechanisms underlying protection from parasitoid wasps in Drosophila melanogaster mediated by its facultative endosymbiont Spiroplasma poulsonii. Our results indicate that S. poulsonii exerts protection against two distantly related wasp species, Leptopilina boulardi and Asobara tabida. S. poulsonii-mediated protection against parasitoid wasps takes place at the pupal stage and is not associated with an increased cellular immune response. In this work, we provide three important observations that support the notion that S. poulsonii bacteria and wasp larvae compete for host lipids and that this competition underlies symbiont-mediated protection. First, lipid quantification shows that both S. poulsonii and parasitoid wasps deplete D. melanogaster hemolymph lipids. Second, the depletion of hemolymphatic lipids using the Lpp RNA interference (Lpp RNAi) construct reduces wasp success in larvae that are not infected with S. poulsonii and blocks S. poulsonii growth. Third, we show that the growth of S. poulsonii bacteria is not affected by the presence of the wasps, indicating that when S. poulsonii is present, larval wasps will develop in a lipid-depleted environment. We propose that competition for host lipids may be relevant to endosymbiont-mediated protection in other systems and could explain the broad spectrum of protection provided.

Diversity, frequency, and geographic distribution of facultative bacterial endosymbionts in introduced aphid pests.

Facultative bacterial endosymbionts in insects have been under intense study during the last years. Endosymbionts can modify the insect's phenotype, conferring adaptive advantages under environmental stress. This seems particularly relevant for a group of worldwide agricultural aphid pests, because endosymbionts modify key fitness-related traits, including host plant use, protection against natural enemies and heat tolerance. Aimed to understand the role of facultative endosymbionts on the success of introduced aphid pests, the distribution and abundance of 5 facultative endosymbionts (Hamiltonella defensa, Regiella insecticola, Serratia symbiotica, Rickettsia and Spiroplasma) were studied and compared in 4 cereal aphids (Sitobion avenae, Diuraphis noxia, Metopolophium dirhodum and Schizaphis graminium) and in the pea aphid Acyrthosiphon pisum complex from 2 agroclimatic zones in Chile. Overall, infections with facultative endosymbionts exhibited a highly variable and characteristic pattern depending on the aphid species/host race and geographic zone, which could explain the success of aphid pest populations after their introduction. While S. symbiotica and H. defensa were the most frequent endosymbionts carried by the A. pisum pea-race and A. pisum alfalfa-race aphids, respectively, the most frequent facultative endosymbiont carried by all cereal aphids was R. insecticola. Interestingly, a highly variable composition of endosymbionts carried by S. avenae was also observed between agroclimatic zones, suggesting that endosymbionts are responding differentially to abiotic variables (temperature and precipitations). In addition, our findings constitute the first report of bacterial endosymbionts in cereal aphid species not screened before, and also the first report of aphid endosymbionts in Chile.

A facultative endosymbiont in aphids can provide diverse ecological benefits.

Ecologically important traits of insects are often affected by facultative bacterial endosymbionts. This is best studied in the pea aphid Acyrthosiphon pisum, which is frequently infected by one or more of eight facultative symbiont species. Many of these symbiont species have been shown to provide one ecological benefit, but we have little understanding of the range of effects that a single strain can have. Here, we describe the phenotypes conferred by three strains of the recently discovered bacterium known as X‐type (Enterobacteriaceae), each in their original aphid genotype which also carries a Spiroplasma symbiont. All comparisons are made between aphids that are coinfected with Spiroplasma and X‐type and aphids of the same genotype that harbour only Spiroplasma. We show that in all cases, infection with X‐type protects aphids from the lethal fungal pathogen Pandora neoaphidis, and in two cases, resistance to the parasitoid Aphidius ervi also increases. X‐type can additionally affect aphid stress responses – the presence of X‐type increased reproduction after the aphids were heat‐stressed. Two of the three strains of X‐type are able to provide all of these benefits. Under benign conditions, the aphids tended to suffer from reduced fecundity when harbouring X‐type, a mechanism that might maintain intermediate frequencies in field populations. These findings highlight that a single strain of a facultative endosymbiont has the potential to provide diverse benefits to its aphid host.

The intracellular bacterium Wolbachia uses parasitoid wasps as phoretic vectors for efficient horizontal transmission.

Facultative bacterial endosymbionts are associated with many arthropods and are primarily transmitted vertically from mother to offspring. However, phylogenetic affiliations suggest that horizontal transmission must also occur. Such horizontal transfer can have important biological and agricultural consequences when endosymbionts increase host fitness. So far horizontal transmission is considered rare and has been difficult to document. Here, we use fluorescence in situ hybridization (FISH) and multi locus sequence typing (MLST) to reveal a potentially common pathway of horizontal transmission of endosymbionts via parasitoids of insects. We illustrate that the mouthparts and ovipositors of an aphelinid parasitoid become contaminated with Wolbachia when this wasp feeds on or probes Wolbachia-infected Bemisia tabaci AsiaII7, and non-lethal probing of uninfected B. tabaci AsiaII7 nymphs by parasitoids carrying Wolbachia resulted in newly and stably infected B. tabaci matrilines. After they were exposed to infected whitefly, the parasitoids were able to transmit Wolbachia efficiently for the following 48 h. Whitefly infected with Wolbachia by parasitoids had increased survival and reduced development times. Overall, our study provides evidence for the horizontal transmission of Wolbachia between insect hosts by parasitic wasps, and the enhanced survival and reproductive abilities of insect hosts may adversely affect biological control programs.

The genome of Cardinium cBtQ1 provides insights into genome reduction, symbiont motility, and its settlement in Bemisia tabaci.

Many insects harbor inherited bacterial endosymbionts. Although some of them are not strictly essential and are considered facultative, they can be a key to host survival under specific environmental conditions, such as parasitoid attacks, climate changes, or insecticide pressures. The whitefly Bemisia tabaci is at the top of the list of organisms inflicting agricultural damage and outbreaks, and changes in its distribution may be associated to global warming. In this work, we have sequenced and analyzed the genome of Cardinium cBtQ1, a facultative bacterial endosymbiont of B. tabaci and propose that it belongs to a new taxonomic family, which also includes Candidatus Amoebophilus asiaticus and Cardinium cEper1, endosymbionts of amoeba and wasps, respectively. Reconstruction of their last common ancestors’ gene contents revealed an initial massive gene loss from the free-living ancestor. This was followed in Cardinium by smaller losses, associated with settlement in arthropods. Some of these losses, affecting cofactor and amino acid biosynthetic encoding genes, took place in Cardinium cBtQ1 after its divergence from the Cardinium cEper1 lineage and were related to its settlement in the whitefly and its endosymbionts. Furthermore, the Cardinium cBtQ1 genome displays a large proportion of transposable elements, which have recently inactivated genes and produced chromosomal rearrangements. The genome also contains a chromosomal duplication and a multicopy plasmid, which harbors several genes putatively associated with gliding motility, as well as two other genes encoding proteins with potential insecticidal activity. As gene amplification is very rare in endosymbionts, an important function of these genes cannot be ruled out.

EXPERIMENTAL EVOLUTION OF PARASITOID INFECTIVITY ON SYMBIONT-PROTECTED HOSTS LEADS TO THE EMERGENCE OF GENOTYPE SPECIFICITY

Host-parasitoid interactions may lead to strong reciprocal selection for traits involved in host defense and parasitoid counterdefense. In aphids, individuals harboring the facultative bacterial endosymbiont, Hamiltonella defensa, exhibit enhanced resistance to parasitoid wasps. We used an experimental evolution approach to investigate the ability of the parasitoid wasp, Lysiphlebus fabarum, to adapt to the presence of H. defensa in its aphid host Aphis fabae. Sexual populations of the parasitoid were exposed for 11 generations to a single clone of A. fabae, either free of H. defensa or harboring artificial infections with three different isolates of H. defensa. Parasitoids adapted rapidly to the presence of H. defensa in their hosts, but this adaptation was in part specific to the symbiont isolate they were evolving against and did not result in an improved infectivity on all symbiont-protected hosts. Comparisons of life-history traits among the evolved lines of parasitoids did not reveal any evidence for costs of adaptation to H. defensa in terms of correlated responses that could constrain such adaptation. These results show that parasitoids readily evolve counter-adaptations to heritable defensive symbionts of their hosts, but that different symbiont strains impose different evolutionary challenges. The symbionts thus mediate the host-parasite interaction by inducing line-by-line genetic specificity.

Bacterial endosymbionts in field-collected samples of Trialeurodes sp. nr. abutiloneus (Hemiptera: Aleyrodidae)

Facultative bacterial endosymbionts are common, influential associates of arthropods, yet their movement among host species has not been well documented. Plant-mediated transmission of Rickettsia has been shown for the whitefly Bemisia tabaci. Bemisia tabaci in USA cotton fields harbors the secondary symbionts Rickettsia and Hamiltonella, and co-occurs with Trialeurodes sp. nr. abutiloneus whiteflies. To determine whether symbionts may be shared, the microbial diversity of these whiteflies on cotton across the USA was analyzed. Trialeurodes sp. nr. abutiloneus bore Portiera, Pseudomonas, Serratia, Arsenophonus and Wolbachia. No Rickettsia or Hamiltonella were detected. These results provide no evidence for horizontal transmission of symbionts between these whitefly genera.

Cover Caption

Aphids may harbor a wide variety of facultative bacterial endosymbionts. These symbionts are transmitted maternally with high fidelity and they show horizontal transmission as well, albeit at rates too low to enable infectious spread. Such symbionts need to provide a net fitness benefit to their hosts to persist and spread. Several symbionts have achieved this by evolving the ability to protect their hosts against parasitoids. Reviewing empirical work and some models, I explore the evolutionary ecology of symbiont-conferred resistance to parasitoids in order to understand how defensive symbiont frequencies are maintained at the intermediate levels observed in aphid populations. I further show that defensive symbionts alter the reciprocal selection between aphids and parasitoids by augmenting the heritable variation for resistance, by increasing the genetic specificity of the host-parasitoid interaction, and by inducing environment-dependent trade-offs. These effects are conducive to very dynamic, symbiont-mediated coevolution that is driven by frequency-dependent selection. Finally I argue that defensive symbionts represent a problem for biological control of pest aphids, and I propose to mitigate this problem by exploiting the parasitoids' demonstrated ability to rapidly evolve counteradaptations to symbiont-conferred resistance.

Worldwide Populations of the Aphid Aphis craccivora Are Infected with Diverse Facultative Bacterial Symbionts

Facultative bacterial endosymbionts can play an important role in the evolutionary trajectory of their hosts. Aphids (Hemiptera: Aphididae) are infected with a wide variety of facultative endosymbionts that can confer ecologically relevant traits, which in turn may drive microevolutionary processes in a dynamic selective environment. However, relatively little is known about how symbiont diversity is structured in most aphid species. Here, we investigate facultative symbiont species richness and prevalence among world-wide populations of the cowpea aphid, Aphis craccivora Koch. We surveyed 44 populations of A. craccivora, and detected 11 strains of facultative symbiotic bacteria, representing six genera. There were two significant associations between facultative symbiont and aphid food plant: the symbiont Arsenophonus was found at high prevalence in A. craccivora populations collected from Robinia sp. (locust), whereas the symbiont Hamiltonella was almost exclusively found in A. craccivora populations from Medicago sativa (alfalfa). Aphids collected from these two food plants also had divergent mitochondrial haplotypes, potentially indicating the formation of specialized aphid lineages associated with food plant (host-associated differentiation). The role of facultative symbionts in this process remains to be determined. Overall, observed facultative symbiont prevalence in A. craccivora was lower than that of some other well-studied aphids (e.g., Aphis fabae and Acyrthosiphon pisum), possibly as a consequence of A. craccivora's almost purely parthenogenetic life history. Finally, most (70 %) of the surveyed populations were polymorphic for facultative symbiont infection, indicating that even when symbiont prevalence is relatively low, symbiont-associated phenotypic variation may allow population-level evolutionary responses to local selection.