Learning can be detrimental for a parasitic wasp.

Valeria Bertoldi,Gabriele Rondoni,Eric Conti,Ezio Peri,Jacques Brodeur,Nicolas Desneux

doi:10.1371/journal.pone.0238336

Valeria Bertoldi, Gabriele Rondoni + Show 4 more

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https://doi.org/10.1371/journal.pone.0238336

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Abstract

Animals have evolved the capacity to learn, and the conventional view is that learning allows individuals to improve foraging decisions. The parasitoid Telenomus podisi has been shown to parasitize eggs of the exotic stink bug Halyomorpha halys at the same rate as eggs of its coevolved host, Podisus maculiventris, but the parasitoid cannot complete its development in the exotic species. We hypothesized that T. podisi learns to exploit cues from this non-coevolved species, thereby increasing unsuccessful parasitism rates. We conducted bioassays to compare the responses of naïve vs. experienced parasitoids on chemical footprints left by one of the two host species. Both naïve and experienced females showed a higher response to footprints of P. maculiventris than of H. halys. Furthermore, parasitoids that gained an experience on H. halys significantly increased their residence time within the arena and the frequency of re-encounter with the area contaminated by chemical cues. Hence, our study describes detrimental learning where a parasitoid learns to associate chemical cues from an unsuitable host, potentially re-enforcing a reproductive cul-de-sac (evolutionary trap). Maladaptive learning in the T. podisi—H. halys association could have consequences for population dynamics of sympatric native and exotic host species.

Highlights

Animal decision-making, which is involved in processes such as resource and habitat selection, mate choice and progeny allocation, relies on innate behaviour, stochastic processes, physiological feedbacks and learning
Total residence time of T. podisi varied depending on the insect species footprint (Gaussian GLM: F(1, 159) = 53.78, P < 0.0001, the previous experience (F(1, 158) = 16.83, P < 0.0001) and the interaction of these two factors (F(1, 157) = 4.28, P = 0.04)
Following a rewarded experience on H. halys, the number of re-encounters with this species was similar to the number of re-encounters of naïve females tested on P. maculiventris (Fig 1B)

Summary

Introduction

Animal decision-making, which is involved in processes such as resource and habitat selection, mate choice and progeny allocation, relies on innate behaviour (instinct), stochastic processes, physiological feedbacks (e.g., hormonal signalling) and learning (reviewed in [1]). In order to cope with spatial and temporal variability in resources, parasitic wasps have evolved the capacity to associate host-related chemical cues to host availability and suitability [2,3,4,5,6]. They further consolidate and improve this capacity through learning processes [7,8,9,10], resulting in increased reproductive success [3, 11,12,13].

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