Abstract
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.
Highlights
Antagonistic interactions such as host–parasite or prey–predator are major drivers of ecological and evolutionary processes and affect more globally biodiversity patterns and ecosystem functioning
Prevalent Symbiotic Associations and Parasitism Rates To search for a link between symbiont associations and parasitoid pressures, the parasitism rate due to a dominant parasitoid species or all parasitoid species was tested against the frequency of the symbiotic associations in each biotype using General Linear Mixed Models (LMM)
Since some microbial symbionts confer a protection against natural enemies to their hosts that can potentially alter food web interactions (Hafer and Vorburger, 2019; Mclean, 2019), our objectives were to test under natural conditions whether the parasitism rate of different A. pisum biotypes depended on their endosymbiont communities and whether symbiont communities and parasitoid communities associated with pea aphids were related
Summary
Antagonistic interactions such as host–parasite or prey–predator are major drivers of ecological and evolutionary processes and affect more globally biodiversity patterns and ecosystem functioning. Protective microbial symbionts have been wellstudied in insects with the best examples being the Spiroplasma bacterial endosymbiont which protects a mushroom-feeding fly Drosophila neotestacea from parasitic nematodes (Jaenike et al, 2010) or the Hamiltonella defensa bacterial endosymbiont which confers protection to aphids against hymenopteran parasitoids (Oliver et al, 2003) In both cases, the mechanisms of the symbiont-mediated protection involve the production of microbial toxins active against the parasite (Oliver and Perlman, 2020). This cost/benefit balance has been repeatedly invoked to explain intermediate frequencies of protective symbionts in natural populations of their hosts (Oliver et al, 2014) These bacterial symbionts being transmitted occasionally through horizontal transfer events, they may rapidly spread across both host populations and species, leading to rapid adaptations and invasion processes (Jaenike et al, 2010; Himler et al, 2011). These studies have been crucial in investigating the costs and benefits in hosting protective symbionts in presence or absence of parasitism, only few assessed the response of host–symbiont associations to varying pressure intensities of natural enemies and by extent, the link between symbiont communities and parasitoid communities in real and complex natural environments (Smith et al, 2015; Ye et al, 2018)
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