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

Abstract

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.

Arbuscular mycorrhizal fungi influence host infection during epidemics in a wild plant pathosystem

“…Building upon such studies, we also show evidence of changes in host-parasite interactions due to association with a microbial mutualist. Protective symbionts are known from the plant and animal literature, and are thought to play an important role in determining host fitness (Brownlie & Johnson, 2009; May & Nelson, 2014; King et al ., 2016; Sochard et al ., 2020). Studies from agricultural plant species have shown that association with mycorrhizal fungi can reduce the negative effects of pathogens (Norman et al ., 1996; Pozo et al ., 2002; Li et al ., 2010; Song et al ., 2015; Berdeni et al ., 2018), and theoretical studies speculate as to how mycorrhizal benefits might counteract reductions in host fitness due to pathogens and affect diversity in natural communities (Bachelot et al ., 2015).…”

“…Protective symbionts – species that provide defensive benefits to their hosts – help determine the outcome of species interactions and, thus, shape ecological and evolutionary dynamics between hosts and parasites (Brownlie & Johnson, 2009; May & Nelson, 2014; King et al ., 2016; Sochard et al ., 2020). Despite their importance, ecological studies examining the role of protective symbionts in influencing host-parasite interactions in natural populations and communities are rare (Oliver et al ., 2014; Hafer-Hahmann & Vorburger, 2021).…”

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

“…A total of eight lines deriving from the three genetically distinct clones were used in this study to compare potential intra- and intergenotype differences ( Table 1 ). These lines were chosen following experiments showing evidence for differences in defensive behaviours against parasitoids between clones carrying or not carrying H. defensa [ 13 ]. Injections with H. defensa originating from different genotypes into a common aphid host genotype were done to disentangle potential host and endosymbiont effects on EBF responses.…”

“…Secondly, at least 15 different biotypes, specialised to different host plants, have been well-characterised in A. pisum , and for each biotype, different genotypes are available [ 7 , 8 , 9 ]. Thirdly, the pea aphid shows a diversity in endosymbiotic bacteria, which can be eliminated or transfected in different genetic backgrounds, and the influence of such bacteria on behavioural traits has been previously reported [ 10 , 11 , 12 , 13 , 14 ]. Finally, like other aphid species, the pea aphid reproduces parthenogenetically during most of its annual life cycle, and thus, clonal individuals can be obtained for experiments, which facilitates the dissection of genetic and environmental components of phenotypic variation.…”

“…As H. defensa was shown to confer protection against natural enemies [ 5 ], this endosymbiont might modify responses to the alarm pheromone. Indeed, it was shown that defensive behaviours (aggressivity and escape) in an aphid colony attacked by a natural enemy (whether a parasitoid or a predator) were less important when they are infected by H. defensa [ 10 , 11 , 13 ]. This observation leads to the question of whether the reduction of aggressivity and escape in infected aphids might originate from a higher antennal detection threshold of the alarm pheromone and a decrease of the behavioural avoidance response.…”