Milligan William R, Hayward Laura K, Sella Guy
Department of Biological Sciences, Columbia University, New York, NY, USA.
Institute of Science and Technology Austria, Klosterneuburg, Austria.
bioRxiv. 2025 May 17:2025.05.15.654234. doi: 10.1101/2025.05.15.654234.
The question of when adaptation involves genetic changes of large effect versus a polygenic response traces back to early debates around Darwin's "Origin of Species" and remains unanswered today. While there are compelling reasons to expect polygenic adaptation to be common, direct evidence for it is still lacking. In turn, there are hundreds of examples of large effect adaptations across species, but it is unclear whether they are a common occurrence in any given species. Synthesizing the different lines of evidence is further complicated by differences in study designs, limitations and biases. Here, we reframe this long-standing question in terms of the trait under selection and ask how the genetic basis of adaptation is expected to depend on key properties of the genetic variation in the trait (i.e., the trait genetics) and on the changes in selection pressures that act on it (i.e., the "trait ecology"). To study this question, we consider a quantitative trait subject to stabilizing selection and model the response to selection when a population at mutation-selection-drift balance experiences a sudden shift in the optimal value. Using this model, we delimit how the contributions of large effect and polygenic changes to adaptation depend on the genetics and ecology of the trait, as well as other salient factors. This theory allows us to formulate testable predictions about when different modes of adaptation are expected and to outline a framework within which to interpret disparate sources of evidence about the genetic basis of adaptation.
适应是涉及大效应基因变化还是多基因反应这一问题可追溯到达尔文《物种起源》早期的争论,至今仍未得到解答。虽然有令人信服的理由预期多基因适应很常见,但仍缺乏直接证据。反过来,跨物种有数百个大效应适应的例子,但尚不清楚它们在任何特定物种中是否常见。研究设计、局限性和偏差的差异使综合不同证据线索的工作更加复杂。在这里,我们根据受选择的性状重新构建这个长期存在的问题,并询问适应的遗传基础如何预期取决于性状遗传变异的关键属性(即性状遗传学)以及作用于其上的选择压力的变化(即“性状生态学”)。为了研究这个问题,我们考虑一个受稳定选择的数量性状,并对处于突变 - 选择 - 漂变平衡的种群在最优值突然变化时对选择的反应进行建模。使用这个模型,我们界定了大效应和多基因变化对适应的贡献如何取决于性状的遗传学和生态学以及其他显著因素。这个理论使我们能够对何时预期不同的适应模式做出可检验的预测,并勾勒出一个框架,在其中解释关于适应遗传基础的不同证据来源。