Intraspecific variation in immune gene expression and heritable symbiont density

Abstract

Host genetic variation plays an important role in the structure and function of heritable microbial communities. Recent studies have shown that insects use immune mechanisms to regulate heritable symbionts. Here we test the hypothesis that variation in symbiont density among hosts is linked to intraspecific differences in the immune response to harboring symbionts. We show that pea aphids (Acyrthosiphon pisum) harboring the bacterial endosymbiontRegiella insecticola(but not all other species of symbionts) downregulate expression of key immune genes. We then functionally link immune expression with symbiont density using RNAi. The pea aphid species complex is comprised of multiple reproductively-isolated host plant-adapted populations. These ‘biotypes’ have distinct patterns of symbiont infections: for example, aphids from theTrifoliumbiotype are strongly associated withRegiella. Using RNAseq, we compare patterns of gene expression in response toRegiellain aphid genotypes from multiple biotypes, and we show thatTrifoliumaphids experience no downregulation of immune gene expression while hostingRegiellaand harbor symbionts at lower densities. Using F1 hybrids between two biotypes, we find that symbiont density and immune gene expression are both intermediate in hybrids. We propose that in this system,Regiellasymbionts are suppressing aphid immune mechanisms to increase their density, but that some hosts have adapted to prevent immune suppression in order to control symbiont numbers. This work therefore suggests that antagonistic coevolution can play a role in host-microbe interactions even when symbionts are transmitted vertically and provide a clear benefit to their hosts. The specific immune mechanisms that we find are downregulated in the presence ofRegiellahave been previously shown to combat pathogens in aphids, and thus this work also highlights the immune system’s complex dual role in interacting with both beneficial and harmful microbes.

Mechanisms and Evolution of Heritable Microbial Density in Insect Hosts

“…These data suggest that aphid innate immune mechanisms regulate symbiont density, complementing findings that aphid immune cells engulf Regiella ( 9 ). We have further found that “immune suppression” is especially strong in aphids harboring clade 2 Regiella , which reaches substantially higher densities in aphids and imposes stronger survival costs on hosts than other Regiella clades ( 1 , 8 ).…”

“…Higher density comes at a cost to aphid survival but provides no additional protection against fungi ( 1 ). In subsequent work, we have shown that aphids harboring Regiella decrease expression of innate immune system genes, including the key immune enzyme phenoloxidase, and we found that suppression of phenoloxidase via RNA interference (RNAi) leads to increased Regiella density ( 8 ). These data suggest that aphid innate immune mechanisms regulate symbiont density, complementing findings that aphid immune cells engulf Regiella ( 9 ).…”

“…As discussed above, the clover biotype has a close association with clade 2 Regiella ( 7 ). We used transcriptome sequencing (RNA-seq) to show that clover aphids do not experience any immune suppression when harboring clade 2 Regiella and harbor stable infections of these symbionts at lower densities than other biotypes ( 8 ). It is currently unclear if this strong association between clade 2 Regiella and clover aphids is a cause or consequence of these differences in immunity.…”

Frequent Drivers, Occasional Passengers: Signals of Symbiont-Driven Seasonal Adaptation and Hitchhiking in the Pea Aphid, Acyrthosiphon pisum

“…But, of course, facultative symbionts comprise just one source of heritable genetic variation in a pea aphid population. Given the extensive degree of variation encoded by the pea aphid genome, and its impacts on a range of ecologically relevant traits [ 119 , 120 , 121 ], it is clear that natural selection is acting on other heritable targets in the field, with a similar potential to drive rapid evolutionary change [ 122 , 123 ]. Such selection may, in turn, drive hitchhiking effects for facultative symbionts.…”

Physiological costs of facultative endosymbionts in aphids assessed from energy metabolism

“…Such phenotypic variations have been widely reported for different traits and are more likely the result of complex host genotype‐by‐symbiont genotype interactions (Parker et al, 2017; Vorburger & Gouskov, 2011). In various insect‐symbiont associations, fitness costs induced by endosymbionts have been positively correlated with the bacterial density (Cayetano et al, 2015; Nichols et al, 2021). In our study, nor fitness costs nor SMR were positively correlated with endosymbiont density.…”