Ecological rigidity and the hardness of selection in the wild

Hutchinson’s ecological theater and evolutionary play is a classical view of evolutionary ecology—ecology provides a template in which evolution occurs. An opposing view is that ecological and evolutionary changes are like two actors on a stage, intertwined by density- and frequency-dependence. These opposing views correspond to hard and soft selection respectively. While often presented as diametrically opposed, both types of selection can occur simultaneously, yet we largely lack knowledge of the relative importance of hard versus soft selection in the wild. I use a dataset of 3000 individual gall makers from 15 wild local populations over 5 years to investigate the hardness of selection. I show that enemy attack consistently favors some gall sizes over others (hard selection) but that these biases can be fine-tuned by density- and frequency-dependence (soft selection). As a result, selection is hard and soft in roughly equal measures, but the importance of each type varies as species interactions shift. I conclude that eco-evolutionary dynamics should occur when a mix of hard and soft selection acts on a population. This work contributes to the rapprochement of disparate views of evolutionary ecology—ecology is neither a rigid theater nor a flexible actor, but instead embodies components of both.

哈钦森的生态剧场与进化戏剧（Hutchinson’s ecological theater and evolutionary play）是进化生态学的经典视角——生态学为进化过程提供了发生的框架。与之对立的观点则认为，生态与进化变化如同舞台上的两位演员，通过密度依赖（density-dependence）与频率依赖（frequency-dependence）相互交织。这两种对立观点分别对应硬选择（hard selection）与软选择（soft selection）。尽管二者常被表述为截然对立，但两类选择可同时发生，然而目前学界对野外环境中硬选择与软选择的相对重要性仍知之甚少。本研究利用覆盖5年时间、取自15个野生本土种群的3000只造瘿生物（gall maker）个体数据集，对选择作用的硬度开展研究。研究结果显示，天敌侵袭始终对部分特定大小的虫瘿存在选择偏好（即硬选择），但这类选择偏向可通过密度依赖与频率依赖进行微调（即软选择）。因此，硬选择与软选择的作用强度大致相当，但二者的重要性会随物种间相互作用的动态变化而改变。本研究得出结论：当种群同时受到硬选择与软选择的共同作用时，便会触发生态进化动力学（eco-evolutionary dynamics）。本研究有助于协调进化生态学中两种截然不同的学术视角——生态学既非僵化的剧场，亦非灵活的演员，而是兼具二者的特征。