Abstract

The ability to learn is ubiquitous in animals but highly variable within and between species, populations and individuals. Diet-related circumstances, such as diet quantity and quality can influence both long-term constitutive (genetic; by selection) and short-term operational (non-genetic; by the immediate circumstances) learning performance. Here, we scrutinized the causes of loss of learning ability, following multi-generational feeding on pollen, in a line of the predatory mite Amblyseius swirskii, which was previously well able to learn prey during early life, enhancing foraging later in life. We investigated whether, and, if so, how quickly, a transgenerational diet switch to live prey restores the early learning ability of foraging predatory mites. The first experiment shows that the early learning ability was restored after switching the diet of the pollen-fed predator line to live spider mites for two generations before conducting the behavioral assay. The second experiment reveals that offspring regained their learning ability if the diet of their mothers was switched from pollen to spider mites for 3 or 10 days before offspring production. Both experiments in concert suggest transgenerational, pollen-induced operational loss of learning ability in the predatory mite A. swirskii. Maternally-transmitted nutrient deficiency and/or maternally-induced epigenetic changes are the most plausible explanations for the pollen diet-induced loss of learning ability. Our study represents a key example for maternal diet-induced variation in learning ability.

Highlights

  • Learning is a ubiquitous phenomenon in animals, both vertebrates and invertebrates (Alloway 1972; Papaj and Lewis 1993; Smid and Vet 2006), and observed in plantinhabiting predatory mites of the family Phytoseiidae (Schausberger 2007; Rahmani et al 2009; Schausberger et al 2010; Walzer and Schausberger 2011; Strodl and Schausberger 2012)

  • Upon receipt in October 2013, the population was split into two lines: one line was reared on ‘Nutrimite’ (Biobest, Westerlo, Belgium), a diet exclusively consisting of cattail pollen T. angustifolia, and the other was reared on a diet of two-spotted spider mites Tetranychus urticae Koch (Tetranychidae)

  • Thrips-experienced predators from the SM–SM and PO–SM lines were faster in attacking thrips than thrips–naıve predators, which was not the case for predators from the PO–PO line

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Summary

Introduction

Learning is a ubiquitous phenomenon in animals, both vertebrates and invertebrates (Alloway 1972; Papaj and Lewis 1993; Smid and Vet 2006), and observed in plantinhabiting predatory mites of the family Phytoseiidae (Schausberger 2007; Rahmani et al 2009; Schausberger et al 2010; Walzer and Schausberger 2011; Strodl and Schausberger 2012). Cases in point for constitutive and operational diet-related variability in learning expression come from the fruit fly Drosophila melanogaster. Mery and Kawecki (2003, 2004) compared two lines of flies originating from the same base population, a high-learning and a low-learning line, in various contexts. Xia et al (1997) observed a diet-induced shift in learning expression in D. melanogaster. After transferring young flies of the two lines to the other medium, and rearing the progeny on the new medium, loss of learning ability was observed in flies originating from the standard medium within three generations. Flies formerly reared on the Peking medium regained their learning ability and memory formation within five generations after transferring them to the standard medium. The work by Xia et al (1997) clearly demonstrated a causal relationship between multi-generational malnutrition and learning ability of fruit flies

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