Plant and insect genetic variation mediate the impact of arbuscular mycorrhizal fungi on a natural plant–herbivore interaction

Pil U Rasmussen,Ayco J M Tack,Tarique Amin,Sari Timonen,Saskya Van Nouhuys,Alison E Bennett,Kristina Karlsson Green

doi:10.1111/een.12453

Abstract

1. While both arbuscular mycorrhizal (AM) fungi and plant and insect genotype are well known to influence plant and herbivore growth and performance, information is lacking on how these factors jointly influence the relationship between plants and their natural herbivores.2. The aim of the present study was to investigate how a natural community of arbuscular mycorrhizal fungi affects the growth of the perennial herb Plantago lanceolata L. (Plantaginaceae), as well as its interaction with the Glanville fritillary butterfly [Melitaea cinxia L. (Nymphalidae)]. For this, a multifactorial experiment was conducted using plant lines originating from multiple plant populations in the Åland Islands, Finland, grown either with or without mycorrhizal fungi. For a subset of plant lines, the impact of mycorrhizal inoculation, plant line, and larval family on the performance of M. cinxia larvae were tested.3. Arbuscular mycorrhizal inoculation did not have a consistently positive or negative impact on plant growth or herbivore performance. Instead, plant genetic variation mediated the impact of arbuscular mycorrhizal fungi on plant growth, and both plant genetic variation and herbivore genetic variation mediated the response of the herbivore. For both the plant and insect, the impact of the arbuscular mycorrhizal community ranged from mutualistic to antagonistic. Overall, the present findings illustrate that genetic variation in response to mycorrhizal fungi may play a key role in the ecology and evolution of plant–insect interactions.

Highlights

Studies of belowground–aboveground interactions have shown that soil biota can play an important role in plant growth and plant defence against natural enemies (Bezemer & van Dam, 2005; Tack et al, 2015; Biere & Goverse, 2016)
We focused on plant line per se, as (i) we were only looking at a subset of plant lines from two populations and (ii) the results on plant performance showed that the main variation in plant performance was within plant populations
50 days after inoculation there was a strong effect of arbuscular mycorrhizal (AM) fungal treatment on leaf length, the number of leaves, and leaf area, but both the strength and direction of the effect differed between plant lines (Fig. 2a,b, Table 1)

Summary

Introduction

Studies of belowground–aboveground interactions have shown that soil biota can play an important role in plant growth and plant defence against natural enemies (Bezemer & van Dam, 2005; Tack et al, 2015; Biere & Goverse, 2016). We lack insights into how genetic variation in the aboveground community influences the nature of interactions among the aboveground and belowground communities. Such interactions between the soil biota and genetic variation within the aboveground community may influence the ecology and evolution of aboveground species interactions (Tack et al, 2015; Mursinoff & Tack, 2017). To explore this within a multitrophic context, we may first assess how soil biota and plant genetic. Differences have been found in how herbivores respond to AM fungi depending on their feeding guild (e.g. sucker, chewer) leading to either positive (Gange & West, 1994; Goverde et al, 2000; Koricheva et al, 2009) or negative (Gange & West, 1994; Koricheva et al, 2009) effects of AM fungi on herbivore performance

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