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.
Bibliographical noteFunding Information:
JMS was funded through The Scottish Food Security Alliance: Crops by the James Hutton Institute and the Universities of Aberdeen and Dundee. DJ received support from the N8 Agri-Food programme. LG and AJK were supported by the strategic research programme funded by the Scottish Government’s Rural and Environment Science and Analytical Services Division. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank Gill Banks for elemental analysis work, Jim Wilde for helping with plant maintenance, Carolyn Mitchell, Ruari Macleod, Tom Watson for practical support, Katharine Preedy and Daniel Leybourne for statistical advice and Tim Daniell, Lesley Lancaster, Julia Ferrari and five anonymous reviewers for helpful comments on the manuscript. JS was funded through The Scottish Food Security Alliance: Crops by the James Hutton Institute and the Universities of Aberdeen and Dundee. DJ received support from the N8 Agri-Food programme. LG and AK were supported by the strategic research programme funded by the Scottish Government’s Rural and Environment Science and Analytical Services Division. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
© 2019 Slater et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability StatementAll underlying data is available from the Dryad database (DOI: 10.5061/dryad.rf1b3).
FingerprintDive into the research topics of 'Limited effects of the maternal rearing environment on the behaviour and fitness of an insect herbivore and its natural enemy'. Together they form a unique fingerprint.
Data from: Limited effects of the maternal rearing environment on the behaviour and fitness of an insect herbivore and its natural enemy
Karley, A. J. (Creator), Gilbert, L. (Creator), Slater, J. (Creator) & Paton, G. (Data Manager), Dryad Digital Repository, 13 Jan 2019