Department of Natural Resource Sciences, McGill University, 21,111 Lakeshore Road, Ste-Anne-de-Bellevue, QC, H9X 3V9, Canada.
BMC Evol Biol. 2010 Jan 20;10:19. doi: 10.1186/1471-2148-10-19.
Altruistic 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.
We 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.
Cornicle 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.
利他性的防御行为对进化构成了挑战，因为这些行为对行为者自身具有较高的代价，却能使接受者受益。当防御行为指向亲缘个体时，它可以通过间接适应度利益进行进化。防御行为的利他性往往难以确定，因为行为者自身可能获得直接适应度利益，或者这种行为可能是由于其他个体的自私胁迫导致的，尤其是在社会性动物中。非社会性的孤雌生殖蚜虫形成了同系繁殖的蚜虫群体，这是检验防御行为是否具有利他性的理想模型。当蚜虫受到天敌（如寄生蜂）攻击时，它们会释放肛刺分泌物。这些分泌物包含一种警报信息素，可向邻居（同系繁殖个体）发出危险警报，从而为行为者提供间接适应度利益。然而，接触肛刺分泌物也会阻碍攻击者，从而为行为者提供直接适应度利益。
我们通过评估将肛刺分泌物涂抹到攻击者身上的直接和间接适应度后果，以及通过操纵可从行为中受益的同系繁殖个体数量，来检验肛刺分泌物是否具有利他性这一假说。我们观察了在大小不同的谷物蚜虫 Sitobion avenae 斑块（2、6 和 12 只蚜虫）中单独觅食的寄生蜂 Aphidius rhopalosiphi。涂抹了寄生虫的蚜虫并没有因寄生率降低或寄生虫处理时间增加而受益。然而，涂抹过寄生虫的蚜虫用于梳理的时间比例增加，觅食的时间比例减少，这导致在宿主斑块中宿主遭遇和产卵率降低。此外，个体的涂抹率随着群体中同系繁殖个体数量的增加而增加。
蚜虫的肛刺分泌物对寄生蜂具有利他性，因为它们没有为释放分泌物的个体提供直接适应度利益，仅通过邻近的同系繁殖个体提供间接适应度利益。此外，肛刺分泌物的使用与其利他性一致，因为这种行为的发生与间接适应度利益的大小、可受益的同系繁殖个体数量呈正相关。本研究为非社会性动物中存在的亲缘导向的利他性防御行为提供了证据。
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