Intraspecific variation in immune gene expression and heritable symbiont density.

Holly L. Nichols,Benjamin J. Parker,Omid Saleh Ziabari,Elliott B. Goldstein,Francis Michael Jiggins

doi:10.1371/journal.ppat.1009552

Holly L. Nichols, Benjamin J. Parker + Show 3 more

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https://doi.org/10.1371/journal.ppat.1009552

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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 endosymbiont Regiella 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 the Trifolium biotype are strongly associated with Regiella. Using RNAseq, we compare patterns of gene expression in response to Regiella in aphid genotypes from multiple biotypes, and we show that Trifolium aphids experience no downregulation of immune gene expression while hosting Regiella and 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, Regiella symbionts 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 of Regiella have 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.

Highlights

Most insects harbor heritable microbes that have important effects on host fitness [1,2,3]
We show that immune mechanisms play a role in intraspecific variation in the density of a heritable bacterial symbiont
We established lines that have the same aphid host genotype (LSR1, collected from Medicago sativa [44]) with two different strains of Regiella: one from each of the two main phylogenetic clades of Regiella found in natural populations of pea aphids [43]

Summary

Introduction

Most insects harbor heritable microbes that have important effects on host fitness [1,2,3]. A key aspect of these symbioses is variation. Host taxonomy has been shown to play a role in structuring heritable microbial communities [4,5,6]. In addition to microbiome composition, hosts vary in other aspects of symbioses like the density of microbial infections [9,10]. Two closely-related species of Nasonia wasps vary in the density at which they harbor Wolbachia bacteria, and this variation is due to a single gene that somehow suppresses maternal transmission of bacteria [11]. Except for a few examples, little is known about the mechanisms that underlie variation in heritable symbioses or the evolutionary genetics of these interactions [12]

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