The evolutionary spread of a trait that benefits individuals of one species in their interactions with a second species may be constrained by “ecological costs” if the trait also has detrimental effects on interactions with a third species in the environment. In particular, the identification of ecological costs may help explain why natural plant populations often display less-than-maximal resistance against natural enemies—even when the plant populations possess substantial genetic variation that could serve as raw material for evolving greater resistance. One such resistance trait that confers an obvious fitness advantage, yet is maintained in populations at intermediate levels, is the strategy of resistance-by-ducking displayed by certain species of goldenrods ( Solidago ). In a ducking individual, the stem temporarily nods near the apex during a time in spring that coincides with the oviposition season of several herbivores. I investigated whether the fitness benefits of ducking in terms of deterring apex-galling insects may be offset by ecological costs posed by a common sap-sucking specialist—the red goldenrod aphid, Uroleucon nigrotuberculatum . In a controlled outdoor experiment, ducking was associated with significantly lower antixenosis (i.e., reduced preference), antibiosis (reduced performance), and indirect resistance against aphids. Specifically, aphids colonized ducking plants at a higher rate than erect-stemmed plants; populations of aphids on bagged ducking plants increased more quickly than on bagged erect-stemmed plants; and aphid populations on erect-stemmed plants were wiped out more quickly by natural enemies than on ducking plants when bags were removed. To the extent that aphid damage reduces goldenrod’s fitness, these ecological costs may be responsible for limiting the ducking trait to intermediate levels in goldenrod populations. Because most plant species are attacked by multiple types of herbivores, ecological costs of resistance mechanisms are likely to be more widespread than is generally appreciated, though their subtlety may make them challenging to identify.

中文翻译：

---

以抗毒、抗生和间接抗蚜为货币的黄花闪避策略的生态成本

如果性状对与环境中的第三种物种的相互作用也有不利影响，那么在与第二个物种的相互作用中使一个物种的个体受益的特征的进化传播可能会受到“生态成本”的限制。特别是，生态成本的确定可能有助于解释为什么天然植物种群通常对天敌表现出低于最大的抗性——即使植物种群具有大量的遗传变异，可以作为进化出更大抗性的原材料。一种赋予明显的适应性优势，但在中等水平的种群中仍保持的抗性特征是某些种类的一枝黄花（Solidago）表现出的抗性策略。在一个躲避的个体中，在春季恰逢几种食草动物的产卵季节，茎在顶端附近暂时点头。我调查了躲避在阻止先端害虫方面的健康益处是否会被常见的吸汁专家——红花蚜虫 Uroleucon nigrotuberculatum 造成的生态成本抵消。在一项受控的户外实验中，躲避与显着降低的抗毒作用（即降低偏好）、抗生作用（降低性能）和对蚜虫的间接抗性有关。具体而言，蚜虫以比直立茎植物更高的速度定植鸭子植物。袋装鸭子植物上的蚜虫数量比袋装直茎植物上的蚜虫数量增加得更快；去除袋子后，直立茎植物上的蚜虫种群被天敌消灭的速度比躲避植物上的蚜虫种群更快。就蚜虫损害降低一枝花的适应性而言，这些生态成本可能是将一枝花种群的回避性状限制在中间水平的原因。由于大多数植物物种受到多种食草动物的攻击，抗性机制的生态成本可能比人们普遍认为的更为普遍，尽管它们的微妙性可能使它们难以识别。