Abstract

In natural environments, plants have to deal with a wide range of different herbivores whose communities vary in time and space. It is believed that the chemical diversity within plant species has mainly arisen from selection pressures exerted by herbivores. So far, the effects of chemical diversity on plant resistance have mostly been assessed for arthropod herbivores. However, also gastropods, such as slugs, can cause extensive damage to plants. Here we investigate to what extent individual Solanum dulcamara plants differ in their resistance to slug herbivory and whether this variation can be explained by differences in secondary metabolites. We performed a series of preference assays using the grey field slug (Deroceras reticulatum) and S. dulcamara accessions from eight geographically distinct populations from the Netherlands. Significant and consistent variation in slug preference was found for individual accessions within and among populations. Metabolomic analyses showed that variation in steroidal glycoalkaloids (GAs) correlated with slug preference; accessions with high GA levels were consistently less damaged by slugs. One, strongly preferred, accession with particularly low GA levels contained high levels of structurally related steroidal compounds. These were conjugated with uronic acid instead of the glycoside moieties common for Solanum GAs. Our results illustrate how intraspecific variation in steroidal glycoside profiles affects resistance to slug feeding. This suggests that also slugs should be considered as important drivers in the co-evolution between plants and herbivores.

Highlights

  • Plants interact with a large diversity of organisms such as herbivores and pathogens

  • We utilized the naturally available genetic variation within and among populations of S. dulcamara to address the following specific questions: (1) Is there intraspecific variation in gastropod resistance in S. dulcamara? (2) What are the underlying chemical mechanisms explaining variation in gastropod resistance in S. dulcamara? We addressed these questions in a series of bioassays using the grey field slug (GFS, Deroceras reticulatum Müller) as a gastropod model species

  • Differences in the relative leaf disc consumption between the most and least preferred accessions within populations ranged from 8% in Texel Dry (TD07: 13%; TD11: 5%) to 62% in Zandvoort Dry (ZD11: 63%; ZD04: 1%)

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Summary

Introduction

Plants interact with a large diversity of organisms such as herbivores and pathogens (van Dam 2009). It has been postulated that the large chemical diversity observed in plants today has resulted from the multitude of interactions with herbivores. Each herbivore species may require a specific defence strategy. Generalist herbivores are usually deterred by high levels of secondary metabolites, whereas specialist herbivores have evolved mechanisms to overcome plant defences and may even be attracted by specific secondary metabolites (Ali and Agrawal 2012). Herbivore communities are not constant in time and space. The dominant herbivore species which is exerting the strongest selection pressure on local defence traits may differ among plant populations (Agrawal 2007; Johnson 2011).

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