Altruistic defence behaviours in aphids.

Gi-Mick Wu,Luc-Alain Giraldeau,Jacques Brodeur,Guy Boivin,Yannick Outreman

doi:10.1186/1471-2148-10-19

Abstract

BackgroundAltruistic anti-predatory behaviours pose an evolutionary problem because they are costly to the actor and beneficial to the recipients. Altruistic behaviours can evolve through indirect fitness benefits when directed toward kin. The altruistic nature of anti-predatory behaviours is often difficult to establish because the actor can obtain direct fitness benefits, or the behaviour could result from selfish coercion by others, especially in eusocial animals. Non-eusocial parthenogenetically reproducing aphids form colonies of clone-mates, which are ideal to test the altruistic nature of anti-predatory defence behaviours. Many aphids release cornicle secretions when attacked by natural enemies such as parasitoids. These secretions contain an alarm pheromone that alerts neighbours (clone-mates) of danger, thereby providing indirect fitness benefits to the actor. However, contact with cornicle secretions also hampers an attacker and could provide direct fitness to the actor.ResultsWe tested the hypothesis that cornicle secretions are altruistic by assessing direct and indirect fitness consequences of smearing cornicle secretions onto an attacker, and by manipulating the number of clone-mates that could benefit from the behaviour. We observed parasitoids, Aphidius rhopalosiphi, foraging singly in patches of the cereal aphid Sitobion avenae of varied patch size (2, 6, and 12 aphids). Aphids that smeared parasitoids did not benefit from a reduced probability of parasitism, or increase the parasitoids' handling time. Smeared parasitoids, however, spent proportionately more time grooming and less time foraging, which resulted in a decreased host-encounter and oviposition rate within the host patch. In addition, individual smearing rate increased with the number of clone-mates in the colony.ConclusionsCornicle secretions of aphids were altruistic against parasitoids, as they provided no direct fitness benefits to secretion-releasing individuals, only indirect fitness benefits through neighbouring clone-mates. Moreover, the use of cornicle secretions was consistent with their altruistic nature, because the occurrence of this behaviour increased with the size of indirect fitness benefits, the number of clone-mates that can benefit. This study provides evidence for a case of kin-directed altruistic defence outside eusocial animals.

Highlights

Altruistic anti-predatory behaviours pose an evolutionary problem because they are costly to the actor and beneficial to the recipients
We observed a total of 6019 encounters of which 1837 (31%) resulted in oviposition, and 132 (2%) included smearing of the parasitoid with cornicle secretions
Absence of direct fitness benefits For S. avenae, there is no direct fitness benefit from smearing the parasitoid A. rhopalosiphi, as our detailed analysis found no reduction in the probability of parasitism associated with smearing

Summary

Introduction

Altruistic anti-predatory behaviours pose an evolutionary problem because they are costly to the actor and beneficial to the recipients. The adaptive value of most anti-predatory behaviours is quite intuitive, as they lower the actor’s risk of mortality due to predation Behaviours such as alarm signalling in birds and mammals [1], predator inspection by fish [2,3] or aggressive defences by worker honeybees [4], pose an evolutionary challenge, because the cost of these behaviours is born by the actor, while other individuals (recipients) benefit from them. In the case of eusocial animals, anti-predatory behaviours are performed by non-reproductive castes such as worker or soldier ants [20] While these behaviours clearly benefit the reproductive queen(s) and not the actor, they may be the result of selfish control by the queen or by other individuals in the colonies [21,22]

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Discussion

Conclusion