What can parasitoid wasps teach us about decision-making in insects?

Abstract

SummaryMillions of years of co-evolution have driven parasites to display very complex and exquisite strategies to manipulate the behaviour of their hosts. However, although parasite-induced behavioural manipulation is a widespread phenomenon, the underlying neuronal mechanisms are only now beginning to be deciphered. Here, we review recent advancements in the study of the mechanisms by which parasitoid wasps use chemical warfare to manipulate the behaviour of their insect hosts. We focus on a particular case study in which a parasitoid wasp (the jewel wasp Ampulex compressa) performs a delicate brain surgery on its prey (the American cockroach Periplaneta americana) to take away its motivation to initiate locomotion. Following a brief background account of parasitoid wasps that manipulate host behaviour, we survey specific aspects of the unique effects of the A. compressa venom on the regulation of spontaneous and evoked behaviour in the cockroach host.

Previous motor activity affects transition from uncertainty to decision-making in snails

“…These data show that snails do make a risky behavioural choice in vital circumstances. We use the terms decision-making and behavioural choice in a wider context as elsewhere (Esch et al, 2002;Friesen and Kristan, 2007;Libersat and Gal, 2013), with no speculation on any psychological processes.…”

Parasites: evolution’s neurobiologists

“…Biogenic amines such as dopamine, octopamine and serotonin are key neuromodulators that are commonly affected by parasitism (Adamo, 2012;Helluy, 2013;Libersat and Gal, 2013;Webster et al, 2013). Altering the functioning of these critical neural systems in non-parasitized animals causes predictable changes in behaviour [e.g.…”

“…The parasitic wasp Ampulex compressa uses multiple neuropharmacological agents to zombify its cockroach host (Libersat and Gal, 2013). The wasp venom, used by the wasp to change host behaviour, is a cocktail of substances (Libersat et al, 2009).…”

Investigating candidate neuromodulatory systems underlying parasitic manipulation: concepts, limitations and prospects

“…There are a few exceptions, however. Neurophysiological investigations on how parasitoid wasps make their host 'zombies' have revealed the astonishing potency of the venom cocktail in affecting decisionmaking processes and motivation level, rather than sensory-motor systems (Libersat et al, 2009;Libersat and Gal, 2013). In the classical model of parasitic manipulation, T. gondii-infected rodents, the innate aversion of rodents to the urine of cats -the definitive host -is specifically turned to attraction in T. gondiiinfected rodents, without a more general alteration in cognitive ability such as learned fear, neophobia and anxiety-like behaviour (Vyas et al, 2007).…”

“…Unravelling the role of a particular neuromodulator in an altered behaviour is no proof of the direct impact of a parasite on its regulation. However, such a direct modulatory effect of a parasite's secretion on a host's biogenic amine metabolism has been evidenced in the venom of a cockroach parasitoid (for reviews, see Libersat et al, 2009;Libersat and Gal, 2013) (Table1) and is strongly suspected from the expression of a specific T. gondii tyrosine hydroxylase gene modulating dopamine level in rat brain (Prandovszky et al, 2011).…”