scholarly journals A Link Between Communities of Protective Endosymbionts and Parasitoids of the Pea Aphid Revealed in Unmanipulated Agricultural Systems

2021 ◽  
Vol 9 ◽  
Author(s):  
Mélanie Leclair ◽  
Christelle Buchard ◽  
Frédérique Mahéo ◽  
Jean-Christophe Simon ◽  
Yannick Outreman
Keyword(s):  
Protective Effect ◽  
Acyrthosiphon Pisum ◽  
Pea Aphid ◽  
Parasitoid Wasps ◽  
Agricultural Systems ◽  
Natural Conditions ◽  
Symbiotic Associations ◽  
Cropping Season ◽  
Hamiltonella Defensa ◽  
Microbial Symbionts

In the last decade, the influence of microbial symbionts on ecological and physiological traits of their hosts has been increasingly recognized. However, most of these effects have been revealed under laboratory conditions, which oversimplifies the complexity of the factors involved in the dynamics of symbiotic associations in nature. The pea aphid, Acyrthosiphon pisum, forms a complex of plant-adapted biotypes, which strongly differ in the prevalence of their facultative endosymbionts. Some of the facultative endosymbionts of A. pisum have been shown to confer protection against natural enemies, among which Hamiltonella defensa is known to protect its host from parasitoid wasps. Here, we tested under natural conditions whether the endosymbiont communities of different A. pisum biotypes had a protective effect on their hosts and whether endosymbiotic associations and parasitoid communities associated with the pea aphid complex were linked. A space-time monitoring of symbiotic associations, parasitoid pressure and parasitoid communities was carried out in three A. pisum biotypes respectively specialized on Medicago sativa (alfalfa), Pisum sativum (pea), and Trifolium sp. (clover) throughout the whole cropping season. While symbiotic associations, and to a lesser extent, parasitoid communities were stable over time and structured mainly by the A. pisum biotypes, the parasitoid pressure strongly varied during the season and differed among the three biotypes. This suggests a limited influence of parasitoid pressure on the dynamics of facultative endosymbionts at a seasonal scale. However, we found a positive correlation between the α and β diversities of the endosymbiont and parasitoid communities, indicating interactions between these two guilds. Also, we revealed a negative correlation between the prevalence of H. defensa and Fukatsuia symbiotica in co-infection and the intensity of parasitoid pressure in the alfalfa biotype, confirming in field conditions the protective effect of this symbiotic combination.

scholarly journals Evidence for specificity in symbiont-conferred protection against parasitoids

2015 ◽  
Vol 282 (1811) ◽  
pp. 20150977 ◽  
Author(s):  
Ailsa H. C. McLean ◽  
H. Charles J. Godfray
Keyword(s):  
Genetic Diversity ◽  
Host Plants ◽  
Acyrthosiphon Pisum ◽  
Pea Aphid ◽  
Aphidius Ervi ◽  
Symbiotic Bacteria ◽  
Parasitoid Wasps ◽  
Bacterial Symbionts ◽  
Wasp Species ◽  
Hamiltonella Defensa

Many insects harbour facultative symbiotic bacteria, some of which have been shown to provide resistance against natural enemies. One of the best-known protective symbionts is Hamiltonella defensa , which in pea aphid ( Acyrthosiphon pisum ) confers resistance against attack by parasitoid wasps in the genus Aphidius (Braconidae). We asked (i) whether this symbiont also confers protection against a phylogenetically distant group of parasitoids (Aphelinidae) and (ii) whether there are consistent differences in the effects of bacteria found in pea aphid biotypes adapted to different host plants. We found that some H. defensa strains do provide protection against an aphelinid parasitoid Aphelinus abdominalis. Hamiltonella defensa from the Lotus biotype provided high resistance to A. abdominalis and moderate to low resistance to Aphidius ervi , while the reverse was seen from Medicago biotype isolates. Aphids from Ononis showed no evidence of symbiont-mediated protection against either wasp species and were relatively vulnerable to both. Our results may reflect the different selection pressures exerted by the parasitoid community on aphids feeding on different host plants, and could help explain the maintenance of genetic diversity in bacterial symbionts.

scholarly journals Aphid Heritable Symbiont Exploits Defensive Mutualism

2017 ◽  
Vol 83 (8) ◽  
Author(s):  
Matthew R. Doremus ◽  
Kerry M. Oliver
Keyword(s):  
Fungal Pathogens ◽  
Acyrthosiphon Pisum ◽  
Pea Aphid ◽  
Single Infection ◽  
Community Members ◽  
Content Type ◽  
Defensive Mutualism ◽  
Potential Alternative ◽  
Hamiltonella Defensa ◽  
Alternative Routes

ABSTRACT Insects and other animals commonly form symbioses with heritable bacteria, which can exert large influences on host biology and ecology. The pea aphid, Acyrthosiphon pisum, is a model for studying effects of infection with heritable facultative symbionts (HFS), and each of its seven common HFS species has been reported to provide resistance to biotic or abiotic stresses. However, one common HFS, called X-type, rarely occurs as a single infection in field populations and instead typically superinfects individual aphids with Hamiltonella defensa, another HFS that protects aphids against attack by parasitic wasps. Using experimental aphid lines comprised of all possible infection combinations in a uniform aphid genotype, we investigated whether the most common strain of X-type provides any of the established benefits associated with aphid HFS as a single infection or superinfection with H. defensa. We found that X-type does not confer protection to any tested threats, including parasitoid wasps, fungal pathogens, or thermal stress. Instead, component fitness assays identified large costs associated with X-type infection, costs which were ameliorated in superinfected aphids. Together these findings suggest that X-type exploits the aphid/H. defensa mutualism and is maintained primarily as a superinfection by “hitchhiking” via the mutualistic benefits provided by another HFS. Exploitative symbionts potentially restrict the functions and distributions of mutualistic symbioses with effects that extend to other community members. IMPORTANCE Maternally transmitted bacterial symbionts are widespread and can have major impacts on the biology of arthropods, including insects of medical and agricultural importance. Given that host fitness and symbiont fitness are tightly linked, inherited symbionts can spread within host populations by providing beneficial services. Many insects, however, are frequently infected with multiple heritable symbiont species, providing potential alternative routes of symbiont maintenance. Here we show that a common pea aphid symbiont called X-type likely employs an exploitative strategy of hitchhiking off the benefits of a protective symbiont, Hamiltonella. Infection with X-type provides none of the benefits conferred by other aphid symbionts and instead results in large fitness costs, costs lessened by superinfection with Hamiltonella. These findings are corroborated by natural infections in field populations, where X-type is mostly found superinfecting aphids with Hamiltonella. Exploitative symbionts may be common in hosts with communities of heritable symbionts and serve to hasten the breakdown of mutualisms.

scholarly journals Phage loss and the breakdown of a defensive symbiosis in aphids

2013 ◽  
Vol 280 (1751) ◽  
pp. 20122103 ◽  
Author(s):  
S. R. Weldon ◽  
M. R. Strand ◽  
K. M. Oliver
Keyword(s):  
Acyrthosiphon Pisum ◽  
Bacterial Symbiont ◽  
Parasitoid Wasps ◽  
Bacterial Symbionts ◽  
Delayed Onset ◽  
Lower Weight ◽  
Terrestrial Arthropods ◽  
Defensive Symbiosis ◽  
Hamiltonella Defensa ◽  
Secondary Endosymbiont

Terrestrial arthropods are often infected with heritable bacterial symbionts, which may themselves be infected by bacteriophages. However, what role, if any, bacteriophages play in the regulation and maintenance of insect–bacteria symbioses is largely unknown. Infection of the aphid Acyrthosiphon pisum by the bacterial symbiont Hamiltonella defensa confers protection against parasitoid wasps, but only when H. defensa is itself infected by the phage A. pisum secondary endosymbiont (APSE). Here, we use a controlled genetic background and correlation-based assays to show that loss of APSE is associated with up to sevenfold increases in the intra-aphid abundance of H. defensa . APSE loss is also associated with severe deleterious effects on aphid fitness: aphids infected with H. defensa lacking APSE have a significantly delayed onset of reproduction, lower weight at adulthood and half as many total offspring as aphids infected with phage-harbouring H. defensa , indicating that phage loss can rapidly lead to the breakdown of the defensive symbiosis. Our results overall indicate that bacteriophages play critical roles in both aphid defence and the maintenance of heritable symbiosis.

scholarly journals Costs and benefits of a superinfection of facultative symbionts in aphids

2006 ◽  
Vol 273 (1591) ◽  
pp. 1273-1280 ◽  
Author(s):  
Kerry M Oliver ◽  
Nancy A Moran ◽  
Martha S Hunter
Keyword(s):  
Acyrthosiphon Pisum ◽  
Quantitative Polymerase Chain Reaction ◽  
Critical Role ◽  
Natural Populations ◽  
Aphidius Ervi ◽  
Buchnera Aphidicola ◽  
Symbiotic Associations ◽  
Added Benefit ◽  
Hamiltonella Defensa ◽  
Micro Organisms

Symbiotic associations between animals and inherited micro-organisms are widespread in nature. In many cases, hosts may be superinfected with multiple inherited symbionts. Acyrthosiphon pisum (the pea aphid) may harbour more than one facultative symbiont (called secondary symbionts) in addition to the obligate primary symbiont, Buchnera aphidicola . Previously we demonstrated that, in a controlled genetic background, A. pisum infected with either Serratia symbiotica or Hamiltonella defensa (called R- and T-type in that study) were more resistant to attack by the parasitoid Aphidius ervi . Here, we examined the consequences of A. pisum superinfected with both resistance-conferring symbionts. We found that an A. pisum line co-infected with both S. symbiotica and H. defensa symbionts exhibits even greater resistance to parasitism by A. ervi than either of the singly infected lines. Despite this added benefit to resistance, superinfections of S. symbiotica and H. defensa symbionts appeared rare in our survey of Utah A. pisum symbionts, which is probably attributable to severe fecundity costs. Quantitative polymerase chain reaction estimates indicate that while the density of H. defensa is similar in singly and superinfected hosts, S. symbiotica densities increased dramatically in superinfected hosts. Over-proliferation of symbionts or antagonistic interactions between symbionts may be harmful to the aphid host. Our results indicate that in addition to host–symbiont interactions, interactions among the symbionts themselves probably play a critical role in determining the distributions of symbionts in natural populations.

scholarly journals Alarm Pheromone Responses Depend on Genotype, but Not on the Presence of Facultative Endosymbionts in the Pea Aphid Acyrthosiphon pisum

Insects ◽  
2021 ◽  
Vol 12 (1) ◽  
pp. 43
Author(s):  
Cesar Auguste Badji ◽  
Zoé Sol-Mochkovitch ◽  
Charlotte Fallais ◽  
Corentin Sochard ◽  
Jean-Christophe Simon ◽  
...  
Keyword(s):  
Alarm Pheromone ◽  
Acyrthosiphon Pisum ◽  
Bacterial Symbiont ◽  
Pea Aphid ◽  
Response Curves ◽  
Escape Behaviour ◽  
Locomotor Behaviour ◽  
Hamiltonella Defensa ◽  
Escape Responses ◽  
High Doses

Aphids use an alarm pheromone, E-β farnesene (EBF), to warn conspecifics of potential danger. The antennal sensitivity and behavioural escape responses to EBF can be influenced by different factors. In the pea aphid, Acyrthosiphon pisum, different biotypes are adapted to different legume species, and within each biotype, different genotypes exist, which can carry or not Hamiltonella defensa, a bacterial symbiont that can confer protection against natural enemies. We investigate here the influence of the aphid genotype and symbiotic status on the escape behaviour using a four-way olfactometer and antennal sensitivity for EBF using electroantennograms (EAGs). Whereas the investigated three genotypes from two biotypes showed significantly different escape and locomotor behaviours in the presence of certain EBF doses, the infection with H. defensa did not significantly modify the escape behaviour and only marginally influenced the locomotor behaviour at high doses of EBF. Dose-response curves of EAG amplitudes after stimulation with EBF differed significantly between aphid genotypes in correlation with behavioural differences, whereas antennal sensitivity to EBF did not change significantly as a function of the symbiotic status. The protective symbiont H. defensa does thus not modify the olfactory sensitivity to the alarm pheromone. How EBF sensitivity is modified between genotypes or biotypes remains to be investigated.

scholarly journals Trehalose and glucose levels regulate feeding behavior of the phloem-feeding insect, the pea aphid Acyrthosiphon pisum Harris

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Guang Wang ◽  
Jing-Jiang Zhou ◽  
Yan Li ◽  
Yuping Gou ◽  
Peter Quandahor ◽  
...  
Keyword(s):  
Feeding Behavior ◽  
Growth And Development ◽  
Acyrthosiphon Pisum ◽  
Pea Aphid ◽  
Feeding Time ◽  
Electrical Penetration Graph ◽  
Glucose Content ◽  
Glucose Levels ◽  
Phloem Feeding ◽  
Trehalose Content

AbstractTrehalose serves multifarious roles in growth and development of insects. In this study, we demonstrated that the high trehalose diet increased the glucose content, and high glucose diet increased the glucose content but decreased the trehalose content of Acyrthosiphon pisum. RNA interference (RNAi) of trehalose-6-phosphate synthase gene (ApTPS) decreased while RNAi of trehalase gene (ApTRE) increased the trehalose and glucose contents. In the electrical penetration graph experiment, RNAi of ApTPS increased the percentage of E2 waveform and decreased the percentage of F and G waveforms. The high trehalose and glucose diets increased the percentage of E2 waveform of A. pisum red biotype. The correlation between feeding behavior and sugar contents indicated that the percentage of E1 and E2 waveforms were increased but np, C, F and G waveforms were decreased in low trehalose and glucose contents. The percentage of np, E1 and E2 waveforms were reduced but C, F and G waveforms were elevated in high trehalose and glucose contents. The results suggest that the A. pisum with high trehalose and glucose contents spent less feeding time during non-probing phase and phloem feeding phase, but had an increased feeding time during probing phase, stylet work phase and xylem feeding phase.

scholarly journals Genetic identity and genotype × genotype interactions between symbionts outweigh species level effects in an insect microbiome

2021 ◽  
Author(s):  
Melanie R. Smee ◽  
Sally A. Raines ◽  
Julia Ferrari
Keyword(s):  
Species Interactions ◽  
Acyrthosiphon Pisum ◽  
Parasitoid Wasp ◽  
Extensive Study ◽  
Genetic Identity ◽  
Host Genotype ◽  
Species Identity ◽  
Microbial Symbionts ◽  
And Performance ◽  
Multiple Species

AbstractMicrobial symbionts often alter the phenotype of their host. Benefits and costs to hosts depend on many factors, including host genotype, symbiont species and genotype, and environmental conditions. Here, we present a study demonstrating genotype-by-genotype (G×G) interactions between multiple species of endosymbionts harboured by an insect, and the first to quantify the relative importance of G×G interactions compared with species interactions in such systems. In the most extensive study to date, we microinjected all possible combinations of five Hamiltonella defensa and five Fukatsuia symbiotica (X-type; PAXS) isolates into the pea aphid, Acyrthosiphon pisum. We applied several ecological challenges: a parasitoid wasp, a fungal pathogen, heat shock, and performance on different host plants. Surprisingly, genetic identity and genotype × genotype interactions explained far more of the phenotypic variation (on average 22% and 31% respectively) than species identity or species interactions (on average 12% and 0.4%, respectively). We determined the costs and benefits associated with co-infection, and how these compared to corresponding single infections. All phenotypes were highly reliant on individual isolates or interactions between isolates of the co-infecting partners. Our findings highlight the importance of exploring the eco-evolutionary consequences of these highly specific interactions in communities of co-inherited species.

CORNICLE LENGTH AS A CRITERION FOR SEPARATING FIELD-COLLECTED NYMPHAL INSTARS OF THE PEA APHID, ACYRTHOSIPHON PISUM (HOMOPTERA: APHIDIDAE)

1983 ◽  
Vol 115 (12) ◽  
pp. 1615-1619 ◽  
Author(s):  
William D. Hutchison ◽  
David B. Hogg
Keyword(s):  
Acyrthosiphon Pisum ◽  
Pea Aphid ◽  
Field Sample ◽  
Rearing Temperature ◽  
Multimodal Analysis

AbstractCornicle length measuremetns of Acyrthosiphon pisum (Harris) nymphs reared in the laboratory were instar-specific and unaffected by rearing temperature. A multimodal analysis of cornicle lengths of field-collected aphids clearly detected four distribution peaks (i.e., instars) in five different field populations, and there was generaaly little overlap between successive instar distributions. However, third and fourth instars in the spring field sample could not be separated accurately due to the shorter cornicle length of nymphs that developed from overwintered eggs. Cornicle length proved to be a useful criterion for separating virginoparous A. pisum instars in samples collected in southern Wisconsin.

scholarly journals The Phytopathogen Dickeya dadantii (Erwinia chrysanthemi 3937) Is a Pathogen of the Pea Aphid

2006 ◽  
Vol 72 (3) ◽  
pp. 1956-1965 ◽  
Author(s):  
Anne-Marie Grenier ◽  
Gabrielle Duport ◽  
Sylvie Pagès ◽  
Guy Condemine ◽  
Yvan Rahbé
Keyword(s):  
Acyrthosiphon Pisum ◽  
Ecological Impact ◽  
Sitophilus Oryzae ◽  
Pea Aphid ◽  
Erwinia Chrysanthemi ◽  
Future Research ◽  
Close Relative ◽  
Bacterial Cells ◽  
Dickeya Dadantii ◽  
Phytopathogenic Bacterium

ABSTRACT Dickeya dadantii (Erwinia chrysanthemi) is a phytopathogenic bacterium causing soft rot diseases on many crops. The sequencing of its genome identified four genes encoding homologues of the Cyt family of insecticidal toxins from Bacillus thuringiensis, which are not present in the close relative Pectobacterium carotovorum subsp. atrosepticum. The pathogenicity of D. dadantii was tested on the pea aphid Acyrthosiphon pisum, and the bacterium was shown to be highly virulent for this insect, either by septic injury or by oral infection. The lethal inoculum dose was calculated to be as low as 10 ingested bacterial cells. A D. dadantii mutant with the four cytotoxin genes deleted showed a reduced per os virulence for A. pisum, highlighting the potential role of at least one of these genes in pathogenicity. Since only one bacterial pathogen of aphids has been previously described (Erwinia aphidicola), other species from the same bacterial group were tested. The pathogenic trait for aphids was shown to be widespread, albeit variable, within the phytopathogens, with no link to phylogenetic positioning in the Enterobacteriaceae. Previously characterized gut symbionts from thrips (Erwinia/Pantoea group) were also highly pathogenic to the aphid, whereas the potent entomopathogen Photorhabdus luminescens was not. D. dadantii is not a generalist insect pathogen, since it has low pathogenicity for three other insect species (Drosophila melanogaster, Sitophilus oryzae, and Spodoptera littoralis). D. dadantii was one of the most virulent aphid pathogens in our screening, and it was active on most aphid instars, except for the first one, probably due to anatomical filtering. The observed difference in virulence toward apterous and winged aphids may have an ecological impact, and this deserves specific attention in future research.

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