Limited effects of the maternal rearing environment on the behaviour and fitness of an insect herbivore and its natural enemy.

Jennifer M Slater,Lucy Gilbert,David Johnson,Alison J Karley,J Joe Hull

doi:10.1371/journal.pone.0209965

Jennifer M Slater, Lucy Gilbert + Show 3 more

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https://doi.org/10.1371/journal.pone.0209965

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Abstract

The maternal rearing environment can affect offspring fitness or phenotype indirectly via ‘maternal effects’ and can also influence a mother’s behaviour and fecundity directly. However, it remains uncertain how the effects of the maternal rearing environment cascade through multiple trophic levels, such as in plant-insect herbivore-natural enemy interactions. Pea aphids (Acyrthosiphon pisum) show differential fitness on host legume species, while generalist aphid parasitoids can show variable fitness on different host aphid species, suggesting that maternal effects could operate in a plant-aphid-parasitoid system. We tested whether the maternal rearing environment affected the behaviour and fitness of aphids by rearing aphids on two plant hosts that were either the same as or different from those experienced by the mothers. A similar approach was used to test the behaviour and fitness of parasitoid wasps in response to maternal rearing environment. Here, the host environment was manipulated at the plant or plant and aphid trophic levels for parasitoid wasps. We also quantified the quality of host plants for aphids and host aphids for parasitoid wasps. In choice tests, aphids and parasitoid wasps had no preference for the plant nor plant and aphid host environment on which they were reared. Aphid offspring experienced 50.8% higher intrinsic rates of population growth, 43.4% heavier offspring and lived 14.9% longer when feeding on bean plants compared to aphids feeding on pea plants, with little effect of the maternal rearing environment. Plant tissue nitrogen concentration varied by 21.3% in response to aphid mothers’ rearing environment, and these differences correlated with offspring fitness. Maternal effects in parasitoid wasps were only observed when both the plant and aphid host environment was changed: wasp offspring were heaviest by 10.9–73.5% when both they and their mothers developed in bean-reared pea aphids. Also, parasitoid wasp fecundity was highest by 38.4% when offspring were oviposited in the maternal rearing environment. These findings indicate that maternal effects have a relatively small contribution towards the outcome of plant-aphid-parasitoid interactions.

Highlights

The maternal rearing environment can have cascading effects on organisms and their offspring
The consequence of maternal effects is likely to be complex in host-parasitoid systems, because parasitoid wasp offspring fitness could be influenced by both the host environment and the environment experienced by the host
Three comparisons were undertaken: i) offspring pea aphid fitness was examined in response to two different maternal plant hosts and parasitoid wasp offspring fitness was examined in response to maternal experience of ii) pea aphids on two different plant hosts or iii) two different plant+aphid host combinations

Summary

Introduction

The maternal rearing environment can have cascading effects on organisms and their offspring. Maternal oviposition decisions could be affected by several factors including her age and previous experience, influencing the mother’s preference for certain environments to rear their offspring which may or may not result in them selecting a more suitable environment for their offspring’s development: this has been formalised into the preference-performance or ‘mother knows best’ hypothesis [4]. Current environmental conditions can affect directly the behaviour and fecundity of organisms, while offspring phenotype and fitness can be affected by their maternal environment via ‘maternal effects’ [5]. Resource availability, changing abiotic conditions, host defences and abundance of predators or parasites experienced by mothers can influence their offspring phenotype. The consequence of maternal effects is likely to be complex in host-parasitoid systems, because parasitoid wasp offspring fitness could be influenced by both the host environment (e.g. different species of aphid) and the environment experienced by the host (e.g. different plant species on which aphids have been feeding)

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