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

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.

Multigenerational consequences of aphid size on offspring phenotype and reproduction

“…Previous studies investigating the relative importance of maternal effects and current environment in aphids indicated no role of maternal effects on mass or reproduction (McLean et al, 2009;Hu et al, 2016;Slater et al, 2019), or limited effects on mass (Hu et al, 2018), when offspring were reared in low-stress environments. However, each of these studies transferred aphid offspring to host plant species (or varieties) different than that of their mothers to test the consequences of host-switching, whereas we explored the effects of maternal resource stress (host plant quality or crowding) on offspring within the same host species.…”

“…To test the intergenerational effects of resource quality, we grew host plants at low or high levels of fertilizer, which has been shown to increase plant nitrogen (Awmack & Leather, 2002;Fagan et al, 2002;Slater et al, 2019), height, and biomass in Asclepias species (Hanson et al, 2017). Aphids tend to be limited by nitrogen, and the addition of nitrogen through fertilizer has been shown to benefit aphid fitness (Awmack & Leather, 2002;Fagan et al, 2002;Slater et al, 2019). In addition, NPK fertilization can reduce cardenolides, compounds produced by milkweed to deter herbivores (Agrawal et al, 2012).…”

Host plant diet affects growth and induces altered gene expression and microbiome composition in the wood white (Leptidea sinapis) butterfly

“…The impact of natal effects seems to be dependent on the studied insect taxonomic group. There was, for example, a limited effect of the maternal rearing environment on behaviour in pea aphids (Slater et al, 2019), but a significant association between natal origin and oviposition preference in water lily beetles (Verschut et al, 2017). It should be noted that we used wild-caught females for the preference test and we therefore have no control of potential natal effects -i.e., we do not know which host plants the females fed on as larvae.…”

Learning‐induced switching costs in a parasitoid can maintain diversity of host aphid phenotypes although biocontrol is destabilized under abiotic stress

“…Several studies have demonstrated the potential for parasitoids to experience a penalty—in the form of increased time for host location and handling—when switching between aphid hosts differing in quality (e.g. Slater, Gilbert, Johnson, & Karley, 2019) and illustrate that parasitoids can distinguish between parasitism‐resistant and ‐susceptible types due to symbiont‐conferred effects on aphid defensive behaviour or pheromone production susceptibility to parasitism (e.g. Dion, Polin, Simon, & Outreman, 2011; Oliver et al, 2012).…”