An experimental test of the role of selection, drift and gene flow in shaping evolution in the wild

尽管处于进化生物学的核心，我们仍然对野生种群适应不断变化的环境的能力知之甚少。特别是，我们很难理解为什么行动中的进化看起来如此罕见，尽管遗传变异和自然选择--它的主要要求--似乎如此普遍。这种所谓的“停滞悖论”提出了一个问题，即我们是否需要（甚至）更好的理论和（甚至）更多的数据，或者野生环境中的进化实际上本质上是不可预测的。该项目旨在通过利用60多年来大山雀岛屿种群的基于个体的数据和一个独特的8年实验来回答这个基本问题，在这个实验中，我们对窝卵数进行了强人工选择，从而通过实验取代了这个种群的适应性最佳值。在这个实验结束近20年后，我们现在第一次能够调查当人工选择停止时发生了什么：自然选择是否导致离合器大小进化回到实验前的最佳状态？如果是的话，它进化的速度是否符合我们的预期？如果不是的话，这是不是因为当代另外两种主要的进化力量--基因流动和遗传漂变的后果？这些进化变化的非适应性驱动因素可能在限制适应方面发挥关键作用，特别是在小规模和孤立的种群中，从而阻碍了我们预测自然界进化变化的能力。但到目前为止，我们对它们如何与自然选择相互作用以塑造野外进化缺乏全面的了解。为了回答这些问题，我们建议利用这项独特实验提供的机会，对1000多只鸟类的基因组进行测序，并将这些数据与详细的个体生殖历史和多代家谱相结合，其中许多可以追溯到20世纪50年代长期监测计划的开始。结合这两种互补的资源将为我们提供一个实现两个不同但密切相关的目标的绝佳机会：首先，我们将测试行动中的进化对人工选择实验产生的自然选择的反应。这将为野外适应性进化提供一个实验测试。此外，通过使用和调整一套互补的最先进的分析方法，我们将能够为其他野生种群的进化动态的未来研究制定指导方针。在人工选择之后，平均窝卵数的变化受到（适应性）自然选择，以及（非适应性）随机遗传漂变，以及由大陆移民和岛内扩散介导的基因流动的影响。通过测试基本的进化模型，该项目有可能显著改变我们对自然种群适应潜力的理解，并将使我们更接近于回答进化生物学中一些存在已久的问题。在此过程中，我们将评估和完善现有的分析工具，并开发新的分析工具。我们将促进它们在其他种群中的应用，不仅因为它将提供对我们发现的一般性的洞察，而且因为它们将能够为野生种群的遗传管理提供信息，旨在保持遗传多样性和防止无意的选择和/或进化。最后，通过提供行动中进化的教科书例子及其驱动因素，该项目提供了一个向公众传达关键生物学概念的绝佳机会。

Despite being at the heart of evolutionary biology, we still have a remarkably poor understanding of the capacity of wild populations to adapt to changing environments. In particular, we struggle to understand why evolution-in-action appears to be so rare, despite genetic variation and natural selection - its main requirements - seemingly being so common. This so-called 'paradox of stasis' raises the question if we need (even) better theory and (even) more data, or if evolution in the wild is in fact inherently unpredictable. This project aims to answer this fundamental question by capitalising on over 60 years of individual-based data for an island population of great tits and a unique eight-year experiment in which we applied strong artificial selection on clutch size, thereby experimentally displacing this population from its adaptive optimum. Almost two decades after this experiment ended, we are now, for the first time, in the position to investigate what happened when artificial selection ceased: Did natural selection cause clutch size to evolve back to its pre-experimental optimum? If it did, is the speed at which it evolved back in line with our expectations? And if it is not, is this because of the consequences of the other two main contemporary evolutionary forces, gene flow and genetic drift? These non-adaptive drivers of evolutionary change may play a crucial role in constraining adaptation, especially in small and isolated populations, thereby hampering our ability to predict evolutionary change in nature. But as of yet, we lack a comprehensive understanding of how they interact with natural selection to shape evolution in the wild.To answer these questions, we propose to capitalise on the opportunities provided by this unique experiment by sequencing the genomes of over a thousand birds and combining these data with detailed individual reproductive histories and multi-generational family trees, many of which go back all the way to the start of the long-term monitoring program in the 1950's. Combining these two complementary resources will provide us with an exceptional opportunity to achieve two distinct but closely interrelated objectives.First, we will test for evolution-in-action in response to natural selection created by our artificial selection experiment. This will provide an experimental test for adaptive evolution in the wild. Furthermore, by using and adapting a complementary set of state-of-the-art analytical approaches, we will be able develop guidelines for future studies of the evolutionary dynamics of other wild populations.Second, we will ask if and how evolutionary (i.e., genetic) changes in mean clutch size during the aftermath of the artificial selection has been shaped by (adaptive) natural selection, as well as (non-adaptive) random genetic drift, and gene flow mediated by immigration from the mainland and dispersal within the island. By testing fundamental evolutionary models, this project has the potential to significantly alter our understanding of the adaptive potential of natural populations and will bring us closer to answering some of the longest-standing questions in evolutionary biology. In doing so, we will assess and refine existing, and develop new, analytical tools. We will promote their application to other populations, not only because it will provide an insight into the generality of our findings, but also because they will be able to inform the genetic management of wild populations aimed at maintaining genetic diversity and preventing inadvertent selection and/or evolution. Finally, by providing a textbook example of evolution-in-action, and its drivers, this project provides an exceptional opportunity to communicate key biological concepts to the general public.