Fear of natural enemies in non-human animals is a concept dating back to the time of Darwin. Now recognized as a non-consumptive effect, the ecological and evolutionary impact of fear has been studied in a number of predator-prey systems within the last few decades. However, comparatively little consideration has been given to the non-consumptive effects that parasites have on their hosts, which have evolved behaviors to avoid parasites, impacting habitat selection, mate choice, and foraging activity. These avoidance behaviors create a “landscape of disgust,” wherein hosts navigate to avoid parasites, akin to the “landscape of fear” in prey. Evolutionarily speaking, however, predators and parasites are but two examples of natural enemies. Pathogens, parasites, predators, and parasitoids, among others, each exert their own fitness cost on the victims they attack. Since animals likely evolve in the presence of multiple natural enemies, they must adopt a range of avoidance behaviors to navigate through the resulting “landscape of peril.” Therefore, in line with recent efforts to combine the landscapes of fear and disgust, we offer a theoretical framework to better understand the impacts of natural enemies on the evolution of trait-mediated avoidance behaviors in animals. More precisely, we look at how victims may evolve to allocate energy optimally among distinct avoidance behaviors under the selective pressures imposed by different types of natural enemy. This framework is then put into the more realistic context of a food web, which highlights the impact of trophic interactions and trophic level on the evolution of avoidance behaviors.

中文翻译：

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恐惧和厌恶的综合景观：无数自然敌人中回避行为的演变

对非人类动物天敌的恐惧是一个可以追溯到达尔文时代的概念。现在被认为是一种非消耗性效应，在过去的几十年里，已经在许多捕食者-猎物系统中研究了恐惧对生态和进化的影响。然而，相对较少考虑寄生虫对其宿主的非消耗性影响，宿主进化出避免寄生虫的行为，影响栖息地选择、配偶选择和觅食活动。这些回避行为创造了一种“厌恶景观”，宿主通过导航来避开寄生虫，类似于猎物的“恐惧景观”。然而，从进化上讲，捕食者和寄生虫只是天敌的两个例子。病原体、寄生虫、捕食者和拟寄生物等，每个人都对他们攻击的受害者施加自己的健康成本。由于动物可能会在存在多个天敌的情况下进化，因此它们必须采取一系列回避行为来应对由此产生的“危险境地”。因此，根据最近将恐惧和厌恶的景观结合起来的努力，我们提供了一个理论框架，以更好地了解天敌对动物性状介导的回避行为进化的影响。更准确地说，我们研究了在不同类型的天敌施加的选择压力下，受害者如何进化以在不同的回避行为之间优化分配能量。然后将该框架置于更现实的食物网环境中，突出了营养相互作用和营养水平对回避行为演变的影响。