Abstract

Microbial symbionts often alter the phenotype of their host. Benefits and costs to hosts depend on many factors, including host genotype, symbiont species and genotype, and environmental conditions. Here, we present a study demonstrating genotype-by-genotype (G×G) interactions between multiple species of endosymbionts harboured by an insect, and the first to quantify the relative importance of G×G interactions compared with species interactions in such systems. In the most extensive study to date, we microinjected all possible combinations of five Hamiltonella defensa and five Fukatsuia symbiotica (X-type; PAXS) isolates into the pea aphid, Acyrthosiphon pisum. We applied several ecological challenges: a parasitoid wasp, a fungal pathogen, heat shock, and performance on different host plants. Surprisingly, genetic identity and genotype × genotype interactions explained far more of the phenotypic variation (on average 22% and 31% respectively) than species identity or species interactions (on average 12% and 0.4%, respectively). We determined the costs and benefits associated with co-infection, and how these compared to corresponding single infections. All phenotypes were highly reliant on individual isolates or interactions between isolates of the co-infecting partners. Our findings highlight the importance of exploring the eco-evolutionary consequences of these highly specific interactions in communities of co-inherited species.

Highlights

  • Interactions between eukaryotes and microbes are as ubiquitous as they are varied [1, 2]

  • We investigated whether infection status was important

  • The interaction between isolates did not impact on either the survival of co-infected aphids (LMM: χ216 = 18.80, p = 0.28), or on their subsequent fecundity (LMM: χ216 = 17.22, p = 0.37). This is the first study to demonstrate genotype-by-genotype (G×G) interactions between species of endosymbionts harboured by insects and the first to quantify the relative importance of G×G interactions relative to species interactions

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Summary

Introduction

Interactions between eukaryotes and microbes are as ubiquitous as they are varied [1, 2]. Many mutualistic microbes provide essential benefits to their host, often resulting in obligate symbiotic associations [3, 4]. There is a wide array of parasitic or pathogenic interactions between host and microbe [5,6,7], but intermediary situations are perhaps most common, whereby a “facultative” symbiont may provide conditional benefits to a host, but may incur a cost [8]. Research has uncovered many fascinating roles of microbes, yet often such research is conducted on a tractable one host—one microbe system

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