Data from: The consequences of lifetime and evolutionary exposure to toxic prey: changes in avoidance behavior through ontogeny

Responses to novel threats (e.g. invasive species) can involve genetic changes or plastic shifts in phenotype. There is controversy over the relative importance of these processes for species survival of such perturbations, but we are realizing they are not mutually exclusive. Native eastern fence lizards (Sceloporus undulatus) have adapted to top-down predation pressure imposed by the invasive red imported fire ant (Solenopsis invicta) via changes in adult (but not juvenile) lizard antipredator behavior. Here we examine the largely ignored, but potentially equally important, bottom-up effect of fire ants as toxic prey for lizards. We test how fire ant consumption (or avoidance) is affected by lifetime (via plasticity) and evolutionary (via natural selection) exposure to fire ants by comparing field-caught and lab-reared lizards, respectively, from fire ant invaded and uninvaded populations. More naive juveniles from invaded populations ate fire ants than did adults, reflecting a natural ontogenetic dietary shift away from ants. Lab-reared lizards from the invaded site were less likely to eat fire ants than were those from the uninvaded site, suggesting a potential evolutionary shift in feeding behavior. Lifetime and evolutionary exposure interacted across ontogeny, however, and field-caught lizards from the invaded site exhibited opposite ontogenetic trends; adults were more likely to eat fire ants than were juveniles. Our results suggest that plastic and evolutionary processes may both play important roles in permitting species survival of novel threats. We further reveal how complex interactions can shape adaptive responses to multi-modal impacts imposed by invaders: in our system fire ants impose stronger bottom-up selection than top-down selection, with each selection regime changing differently across lizard ontogeny.

针对新型威胁（如入侵物种）的应对策略可涉及遗传改变或表型可塑性（phenotypic plasticity）变化。目前学界对于这两类过程在物种应对此类扰动的存活中相对重要性仍存在争议，但现已明确二者并非互斥。本土东部栅栏蜥（Sceloporus undulatus）已通过成体（而非幼体）的反捕食行为改变，适应了入侵性红火蚁（Solenopsis invicta）施加的自上而下捕食（top-down predation）压力。本研究聚焦此前被大幅忽视，但潜在重要性相当的另一维度：红火蚁作为蜥蜴有毒猎物的自下而上效应（bottom-up effect）。我们分别以红火蚁入侵种群与未入侵种群的野外捕获蜥蜴和实验室繁育蜥蜴为研究对象，以此检验蜥蜴对红火蚁的取食（或回避）行为，如何受终生暴露（对应表型可塑性）与演化暴露（对应自然选择（natural selection））的影响。相较于成体，来自入侵种群的未经验幼体取食红火蚁的比例更高，这反映出蜥蜴随个体发育自然发生的、转向远离蚁类的食性转变。来自入侵区域的实验室繁育蜥蜴，其取食红火蚁的概率低于来自未入侵区域的个体，这提示取食行为可能发生了潜在的演化改变。然而，终生暴露与演化暴露在个体发育过程中存在交互作用；来自入侵区域的野外捕获蜥蜴则呈现出相反的个体发育趋势：其成体取食红火蚁的概率高于幼体。本研究结果表明，可塑性过程与演化过程均可能在物种应对新型威胁的存活中发挥重要作用。我们还进一步揭示了复杂的交互作用如何塑造物种对入侵者施加的多模态影响的适应性响应：在本研究体系中，红火蚁施加的自下而上选择（bottom-up selection）压力强于自上而下选择（top-down selection）压力，且两种选择模式随蜥蜴个体发育呈现出不同的变化趋势。