Host defences against cuckoo parasitism in a changing world

查尔斯·达尔文把自然界比作一个“纠缠的银行”，在这个银行里，生物的进化不仅是为了应对物理环境的变化，也是为了应对与其他生物——竞争对手、捕食者和寄生虫——不断变化的相互作用。最近杜鹃数量的减少提供了一个机会，可以通过实地实验来测试它们的宿主如何适应幼虫寄生威胁的降低。杜鹃是自然界最臭名昭著的骗子之一：它在其他物种的巢中产卵（每个寄主巢一个），当小杜鹃孵化出来时，它会把寄主的蛋和幼鸟赶出去。主人注定要养一只小布谷鸟，而不是自己的一窝。这种相互作用引发了一场“进化军备竞赛”：宿主进化出了防御杜鹃的能力（攻击成年杜鹃并射出杜鹃蛋），而杜鹃也进化出了战胜这些防御的技巧（快速产卵以避免宿主发现，产卵的大小和颜色都模仿宿主的蛋）。我们最近的工作表明，芦苇莺的宿主对寄生风险的反应是不同的。我们的第一个问题是：苇莺如何评估被寄生的风险？当寄生率高时，芦莺很容易接近成年杜鹃，如果它们看到鸟巢里有杜鹃（真实的杜鹃或实验放置的模型杜鹃），它们更有可能拒绝卵。因此，防御受到当地布谷鸟活动的个人信息的影响。然而，在低寄生率下，芦莺更不愿意接近杜鹃，而巢中的杜鹃不太可能引发卵子排斥。这表明防御也受到其他线索的影响。我们的实验表明，芦苇莺通过窃听邻居（社会信息）来扩大他们对当地杜鹃活动的信息来源。如果他们目睹邻居围攻布谷鸟，他们更有可能接近并围攻布谷鸟回到自己的巢穴。然而，我们不知道寄生风险的社会信息是否会刺激卵子排斥，无论是它本身还是通过对个人信息的启动反应。我们将测试芦苇莺对卵的排斥反应（对模型杜鹃卵的反应）如何受到它们对寄生风险评估的影响（因呈现成年杜鹃模型而异）。通过对照实验，我们将改变本地寄生风险的个人信息（在焦点对自己的巢中有一只杜鹃）和社会信息（在邻居的领地上有一只杜鹃加芦苇莺的鸣叫广播）。我们的第二个问题是：在未被寄生的宿主种群中，防御措施的动员速度有多快？最近杜鹃的数量下降（自20世纪80年代以来，英国的杜鹃数量下降了65%）导致了许多小的、孤立的、未被寄生的芦苇莺种群，这些种群缺乏防御措施（围攻成年杜鹃和排斥卵）。在12个这样的彩环鸟种群中，我们将展示成年杜鹃或对照的模型，无害的入侵者，并将杜鹃蛋模型添加到巢穴中，以测试当地杜鹃活动的个人和社会信息如何重新点燃围攻和排斥蛋的防御。然后我们将监测这些种群，以测试防御如何传播到新定居的种群。我们的第三个问题是：naïve宿主物种最初是如何获得防御能力的？我们将利用对杜鹃没有防御能力的寄主Prunella modularis，通过实验来测试成年杜鹃作为新敌人的个人和社会信息是否会诱导对成年杜鹃的防御并刺激对杜鹃卵的反应。我们希望这项研究将提供新的见解，了解生物如何在不断变化的世界中获取来自敌人的威胁信息，如何快速获得防御，以及行为变化（在本例中是对新敌人的识别）如何通过将生物暴露于新的选择压力中为进化变化奠定基础。

Charles Darwin likened the natural world to an "entangled bank" in which organisms evolve not only in response to changes in their physical environment but also to ever changing interactions with other organisms - competitors, predators and parasites. The recent decline in cuckoos provides an opportunity to test, by field experiments, how their hosts have adapted to the reduced threat of brood parasitism. The cuckoo is one of Nature's most notorious cheats: it lays its eggs in the nests of other species (one per host nest) and when the young cuckoo hatches it evicts the host's eggs and young. The hosts are then doomed to raise a young cuckoo instead of a brood of their own. This interaction has provoked an "evolutionary arms race": hosts have evolved defences against cuckoos (attacking adult cuckoos and ejecting cuckoo eggs), while cuckoos have evolved tricks to beat these defences (rapid laying to avoid host detection, and eggs that mimic host eggs in size and colour). Our recent work has shown that reed warbler hosts vary their defences in response to parasitism risk.Our first question is: How do reed warblers assess parasitism risk? When parasitism rates are high, reed warblers readily approach adult cuckoos and they are more likely to reject an egg if they see a cuckoo at their nest (a real one or a model cuckoo placed by experiment). Therefore defences are influenced by personal information of local cuckoo activity. However, at low rates of parasitism, reed warblers are more reluctant to approach cuckoos and a cuckoo at the nest is less likely to trigger egg rejection. This suggests that defences are also influenced by other cues. Our experiments have revealed that reed warblers widen their source of information about local cuckoo activity by eavesdropping on neighbours (social information). If they have witnessed neighbours mobbing a cuckoo, they are more likely to approach and mob a cuckoo back at their own nest. However, we do not know whether social information of parasitism risk stimulates egg rejection, either on its own or by priming responses to personal information.We will test how egg rejection by reed warblers (responses to model cuckoo eggs) is influenced by their assessment of parasitism risk (varied by presenting models of adult cuckoos). With controlled experiments, we will vary both personal information of local parasitism risk (a cuckoo at the focal pair's own nest) and social information (a cuckoo plus broadcast of reed warbler mobbing calls on a neighbour's territory). Our second question is: How rapidly are defences mobilised in unparasitised host populations? The recent decline in cuckoos (65% decline in the UK since the 1980's) has resulted in many small, isolated, unparasitised reed warbler populations, where defences (mobbing adult cuckoos and egg rejection) are absent. At twelve such populations of colour-ringed birds, we will present models of adult cuckoos or control, harmless intruders, and add model cuckoo eggs to nests, to test how mobbing and egg rejection defences might be reignited by personal and social information of local cuckoo activity. We will then monitor these populations to test how defences spread to newly-settling pairs.Our third question is: How might a naïve host species first acquire defences? Using the dunnock, Prunella modularis, a host that has no defences against cuckoos, we will test by experiment whether personal and social information of the adult cuckoo as a novel enemy can induce defences against adult cuckoos and stimulate responses to cuckoo eggs.We hope that this study will provide novel insights into how organisms acquire information about threats from enemies in a changing world, how rapidly defences are acquired, and how behavioural change (in this case recognition of a new enemy) might set the stage for evolutionary change by exposing organisms to new selection pressures.