Parasitoids induce production of the dispersal morph of the pea aphid, Acyrthosiphon pisum

Abstract

In animals, inducible morphological defences against natural enemies mostly involve structures that are protective or make the individual invulnerable to future attack. In the majority of such examples, predators are the selecting agent while examples involving parasites are much less common. Aphids produce a winged dispersal morph under adverse conditions, such as crowding or poor plant quality. It has recently been demonstrated that pea aphids, Acyrthosiphon pisum, also produce winged offspring when exposed to predatory ladybirds, the first example of an enemy‐induced morphological change facilitating dispersal. We examined the response of A. pisum to another important natural enemy, the parasitoid Aphidius ervi, in two sets of experiments. In the first set of experiments, two aphid clones both produced the highest proportion of winged offspring when exposed as colonies on plants to parasitoid females. In all cases, aphids exposed to male parasitoids produced a higher mean proportion of winged offspring than controls, but not significantly so. Aphid disturbance by parasitoids was greatest in female treatments, much less in male treatments and least in controls, tending to match the pattern of winged offspring production. In a second set of experiments, directly parasitised aphids produced no greater proportion of winged offspring than unparasitised controls, thus being parasitised itself is not used by aphids for induction of the winged morph. The induction of wing development by parasitoids shows that host defences against parasites may also include an increased rate of dispersal away from infected habitats. While previous work has shown that parasitism suppresses wing development in parasitised individuals, our experiments are the first to demonstrate a more indirect influence of parasites on insect polyphenism. Because predators and parasites differ fundamentally in a variety of attributes, our finding suggests that the wing production in response to natural enemies is of general occurrence in A. pisum and, perhaps, in other aphids.

Evolution of transgenerational immunity in invertebrates

“…that there is low cross-immunity), mothers are expected to invest more in the immune protection of the philopatric, non-dispersing morph, than on the dispersing one. This prediction could be tested in insects producing both apterous and winged (alate) forms, such as aphids [51][52][53], ants [54,55], and termites [56], or in species that exhibit a sex-biased dispersal, such as gypsy moths [57] and midges [57]. In each of these cases, the philopatric morph or sex is expected to accrue greater benefits from a higher maternal investment in immunity than the dispersing one.…”

Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics

“…Experimental work with the pea aphid, Acyrthosiphon pisum, found that alate (winged morph) production could be induced by the presence of a predator such as a ladybird (Sloggett & Weisser, 2002). For most species, this effect has not been considered, although predator-induced prey dispersal is likely to have some interesting consequences for the stability of spatial predator-prey systems.…”

Wing dimorphism in aphids

“…In contrast, the mere presence of particular natural enemies may elicit an increase in winged morph production in the pea aphid, Acyrthosiphon pisum (Dixon and Agarwala, 1999;Weisser et al, 1999;Sloggett and Weisser, 2002;Kunert and Weisser, 2003) (parasitization may also directly affect wing development, see below). The induction of winged morphs seems to result from increased tactile stimulation triggered by either predator avoidance behavior or from the release of aphid alarm pheromone .…”