Harbouring the secondary endosymbiont Regiella insecticola increases predation risk and reproduction in the cereal aphid Sitobion avenae

Ramírez-Cáceres, Guillermo E.; Moya-Hernández, Mario G.; Quilodrán, Manuel; Nespolo, Roberto F.; Ceballos, Ricardo; Villagra, Cristian A.; Ramı́rez, Claudio C.

doi:10.1007/s10340-019-01090-z

Cited by 16 publications

(12 citation statements)

References 45 publications

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“…Nevertheless, a detrimental effect of R. insecticola on the fitness of S. avenae clones, is not consistent with our field data, where higher levels of infection with R. insecticola were observed in the different aphid clones studied. These results are consistent with a previous experimental observation for a S. avenae clone; where naturally Regiella-infected aphids presented a higher population growth on wheat than on barley, while harboring R. insecticola negatively affect the growth of aphids on barley when compared with naturally uninfected aphids [ 33 ]. Notably, this experiment was carried out using a single aphid clone collected in Chile [G2 in 22], which correspond to the same multilocus genotype of the aphid clone G1 observed predominantly during the period of crop colonization in this present study.…”

Section: Discussionsupporting

confidence: 92%

“…Similarly, in other aphid species like the pea aphid, R. insecticola does not confer resistance against parasitoids [ 2 , 69 ] and only one strain of this endosymbiont has been shown to protection against the parasitoid A. colemani in the aphid Myzus persicae [ 70 ]; thus, representing a limited evidence for a defensive role against parasitoids for R. insecticola . Even more Regiella-infected S. avenae could increase the risk of parasitism [ 57 ] and even predation [ 33 ]. A recent behavioral study found that R. insecticola -harbored aphids were more predated by the coccinellid predator Hippodamia variegata than uninfected aphids of the grain aphid S. avenae [ 33 ].…”

Section: Discussionmentioning

confidence: 99%

“…Even more Regiella-infected S. avenae could increase the risk of parasitism [ 57 ] and even predation [ 33 ]. A recent behavioral study found that R. insecticola -harbored aphids were more predated by the coccinellid predator Hippodamia variegata than uninfected aphids of the grain aphid S. avenae [ 33 ]. H. variegata is the most abundant species (~50% of all coccinellid individuals) among the coccinellid group attacking S. avenae in the field [ 67 ].…”

Section: Discussionmentioning

confidence: 99%

“…While other field studies have shown a potential protective effect of endosymbionts in S. avenae against an assemblage of parasitoids [ 26 ]. As well as, increasing evidence for host-plant use mediated effects of endosymbionts have been reported for S. avenae , which show a significant variation among host clones on different host plants [ 31 , 32 , 33 ]. Here, we have addressed the seasonal dynamics of endosymbiont infections among different host clones of the grain aphid ( S. avenae ) on two cereal crops (wheat and oat) and whether their presence affects the total hymenopteran parasitism of aphid hosts at the field level.…”

Section: Introductionmentioning

confidence: 99%

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Effect of the Genotypic Variation of an Aphid Host on the Endosymbiont Associations in Natural Host Populations

Zepeda-Paulo

Lavandero

2021

Insects

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Understanding the role of facultative endosymbionts on the host’s ecology has been the main aim of the research in symbiont–host systems. However, current research on host–endosymbiont dynamics has failed to examine the genetic background of the hosts and its effect on host–endosymbiont associations in real populations. We have addressed the seasonal dynamic of facultative endosymbiont infections among different host clones of the grain aphid Sitobion avenae, on two cereal crops (wheat and oat) and whether their presence affects the total hymenopteran parasitism of aphid hosts at the field level. We present evidence of rapid seasonal shifts in the endosymbiont frequency, suggesting a positive selection of endosymbionts at the host-level (aphids) through an agricultural growing season, by two mechanisms; (1) an increase of aphid infections with endosymbionts over time, and (2) the seasonal replacement of host clones within natural populations by increasing the prevalence of aphid clones closely associated to endosymbionts. Our results highlight how genotypic variation of hosts can affect the endosymbiont prevalence in the field, being an important factor for understanding the magnitude and direction of the adaptive and/or maladaptive responses of hosts to the environment.

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Section: Discussionsupporting

confidence: 92%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Effect of the Genotypic Variation of an Aphid Host on the Endosymbiont Associations in Natural Host Populations

Zepeda-Paulo

Lavandero

2021

Insects

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“…Although this may sound counter-intuitive, reduction of defensive behaviors could be beneficial to the aphid by avoiding costly and redundant protection against parasitoids ( Dion et al 2011 ). However, the generality of this phenomenon across the different types of protective symbioses is little known ( Dion et al 2011 ; Ramírez-Cáceres et al 2019 ).…”

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confidence: 99%

Influence of “protective” symbionts throughout the different steps of an aphid–parasitoid interaction

et al. 2020

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Microbial associates are widespread in insects, some conferring a protection to their hosts against natural enemies like parasitoids. These protective symbionts may affect the infection success of the parasitoid by modifying behavioral defenses of their hosts, the development success of the parasitoid by conferring a resistance against it or by altering life-history traits of the emerging parasitoids. Here, we assessed the effects of different protective bacterial symbionts on the entire sequence of the host-parasitoid interaction (i.e. from parasitoid attack to offspring emergence) between the pea aphid, Acyrthosiphon pisum, and its main parasitoid, Aphidius ervi and their impacts on the life-history traits of the emerging parasitoids. To test whether symbiont-mediated phenotypes were general or specific to particular aphid-symbiont associations, we considered several aphid lineages, each harboring a different strain of either Hamiltonella defensa or Regiella insecticola, two protective symbionts commonly found in aphids. We found that symbiont species and strains had a weak effect on the ability of aphids to defend themselves against the parasitic wasps during the attack and a strong effect on aphid resistance against parasitoid development. While parasitism resistance was mainly determined by symbionts, their effects on host defensive behaviors varied largely from one aphid-symbiont association to another. Also, the symbiotic status of the aphid individuals had no impact on the attack rate of the parasitic wasps, the parasitoid emergence rate from parasitized aphids nor the life-history traits of the emerging parasitoids. Overall, no correlations between symbiont effects on the different stages of the host-parasitoid interaction was observed, suggesting no trade-offs or positive associations between symbiont-mediated phenotypes. Our study highlights the need to consider various sequences of the host-parasitoid interaction to better assess the outcomes of protective symbioses and understand the ecological and evolutionary dynamics of insect-symbiont associations.

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An Aphid Pest Superclone Benefits From a Facultative Bacterial Endosymbiont in a Host‐Dependent Manner, Leading to Reproductive and Proteomic Changes

Mahieu,

González‐González,

Rubio‐Meléndez

et al. 2024

Arch Insect Biochem Physiol

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The English grain aphid, Sitobion avenae, is a significant agricultural pest affecting wheat, barley, and oats. In Chile, the most prevalent and persistent clone (superclone) of S. avenae harbors the facultative endosymbiont bacterium Regiella insecticola. To determine the role of this bacterium in the reproductive success of this superclone, the presence of R. insecticola was manipulated to assess its impact on (1) the reproductive performance of this clone on two host plant species (wheat and barley), (2) the production of winged morphs, (3) changes in the insects' proteomic profiles, and (4) the root/shoot ratio of plant. It was found that the reproductive performance of this S. avenae superclone varied across host plants, depending on the presence of the facultative bacterial endosymbiont. Aphids infected with R. insecticola showed higher reproductive success on wheat, while the opposite effect was observed on barley. Aphid biomass was greater when infected with R. insecticola, particularly on barley. Additionally, aphids harboring R. insecticola exhibited a higher proportion of winged individuals on both host plants. Protein regulation in aphids on wheat was lower compared to those on barley. A higher root/shoot biomass ratio was observed in wheat plants compared to barley when infested by R. insecticola‐infected aphid. Thus, R. insecticola significantly influences the reproductive performance and proteomic profile of a S. avenae superclone, with these effects shaped by the host plant. This suggests that the interaction between the host plant and the facultative endosymbiont contributes to the ecological success of this superclone.

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Harbouring the secondary endosymbiont Regiella insecticola increases predation risk and reproduction in the cereal aphid Sitobion avenae

Cited by 16 publications

References 45 publications

Effect of the Genotypic Variation of an Aphid Host on the Endosymbiont Associations in Natural Host Populations

Effect of the Genotypic Variation of an Aphid Host on the Endosymbiont Associations in Natural Host Populations

Influence of “protective” symbionts throughout the different steps of an aphid–parasitoid interaction

An Aphid Pest Superclone Benefits From a Facultative Bacterial Endosymbiont in a Host‐Dependent Manner, Leading to Reproductive and Proteomic Changes

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