Stress-induced changes in abundance differ among obligate and facultative endosymbionts of the soybean aphid.

Laramy S Enders,Nicholas J Miller

doi:10.1002/ece3.1908

Abstract

Bacterial endosymbionts can drive evolutionary novelty by conferring adaptive benefits under adverse environmental conditions. Among aphid species there is growing evidence that symbionts influence tolerance to various forms of stress. However, the extent to which stress inflicted on the aphid host has cascading effects on symbiont community dynamics remains poorly understood. Here we simultaneously quantified the effect of host-plant induced and xenobiotic stress on soybean aphid (Aphis glycines) fitness and relative abundance of its three bacterial symbionts. Exposure to soybean defensive stress (Rag1 gene) and a neurotoxic insecticide (thiamethoxam) substantially reduced aphid composite fitness (survival×reproduction) by 74±10% and 92±2%, respectively, which in turn induced distinctive changes in the endosymbiont microbiota. When challenged by host-plant defenses a 1.4-fold reduction in abundance of the obligate symbiont Buchnera was observed across four aphid clonal lines. Among facultative symbionts of Rag1-stressed aphids, Wolbachia abundance increased twofold and Arsenophonus decreased 1.5-fold. A similar pattern was observed under xenobiotic stress, with Buchnera and Arsenophonus titers decreasing (1.3-fold) and Wolbachia increasing (1.5-fold). Furthermore, variation in aphid virulence to Rag1 was positively correlated with changes in Arsenophonus titers, but not Wolbachia or Buchnera. A single Arsenophonus multi-locus genotype was found among aphid clonal lines, indicating strain diversity is not primarily responsible for correlated host-symbiont stress levels. Overall, our results demonstrate the nature of aphid symbioses can significantly affect the outcome of interactions under stress and suggests general changes in the microbiome can occur across multiple stress types.

Highlights

There is a growing appreciation of the complex evolutionary networks, involving a spectrum of mutualistic, conditionally beneficial and parasitic interactions between insects and microbes (Frago et al 2012; Sugio et al 2014)
We addressed the following questions: (1) Do obligate and facultative symbionts respond differently to stress imposed on the aphid host? (2) Do different stress types produce unique changes in the microbiome? and (3) Are the effects of stress correlated in aphids and their bacterial symbionts? We employed a multi-level approach that measured the effect of plant defensive stress inflicted through expression of the soybean Rag1 (Resistance to Aphis glycines) gene and exposure to a neurotoxic insecticide on aphid fitness and endosymbiont relative abundance
Aphid mortality was low on control plants across all aphid clonal lines after 48 h (6 Æ 1%), but mortality ranged from 31 Æ 4% to 67 Æ 3% on Rag1

Summary

Introduction

There is a growing appreciation of the complex evolutionary networks, involving a spectrum of mutualistic, conditionally beneficial and parasitic interactions between insects and microbes (Frago et al 2012; Sugio et al 2014). Bacterial symbionts can manipulate host reproduction (Duron et al 2008), promote adaptive divergence (Janson et al 2008; Hansen and Moran 2014) and mediate host response to various forms of environmental stress (Oliver et al 2010). Investigating insect-microbial interactions under environmental stress can begin to illuminate the role symbionts play in adaptive processes. Unraveling the molecular basis of mutualistic and defensive symbioses has received considerable attention (Dunbar et al 2007; Oliver et al 2009; Hansen and Moran 2014), eco-evolutionary aspects are relatively unexplored (Kwiatkowski and Vorburger 2012; Russell et al 2013; Oliver et al 2014).

Results

Discussion

Conclusion