Bigger Is Fitter? Quantitative Genetic Decomposition of Selection Reveals an Adaptive Evolutionary Decline of Body Mass in a Wild Rodent Population

In natural populations, quantitative trait dynamics often do not appear to follow evolutionary predictions. Despite abundant examples of natural selection acting on heritable traits, conclusive evidence for contemporary adaptive evolution remains rare for wild vertebrate populations, and phenotypic stasis seems to be the norm. This so-called “stasis paradox” highlights our inability to predict evolutionary change, which is especially concerning within the context of rapid anthropogenic environmental change. While the causes underlying the stasis paradox are hotly debated, comprehensive attempts aiming at a resolution are lacking. Here, we apply a quantitative genetic framework to individual-based long-term data for a wild rodent population and show that despite a positive association between body mass and fitness, there has been a genetic change towards lower body mass. The latter represents an adaptive response to viability selection favouring juveniles growing up to become relatively small adults, i.e., with a low potential adult mass, which presumably complete their development earlier. This selection is particularly strong towards the end of the snow-free season, and it has intensified in recent years, coinciding which a change in snowfall patterns. Importantly, neither the negative evolutionary change, nor the selective pressures that drive it, are apparent on the phenotypic level, where they are masked by phenotypic plasticity and a non causal (i.e., non genetic) positive association between body mass and fitness, respectively. Estimating selection at the genetic level enabled us to uncover adaptive evolution in action and to identify the corresponding phenotypic selective pressure. We thereby demonstrate that natural populations can show a rapid and adaptive evolutionary response to a novel selective pressure, and that explicitly (quantitative) genetic models are able to provide us with an understanding of the causes and consequences of selection that is superior to purely phenotypic estimates of selection and evolutionary change.

在自然种群中，数量性状动力学往往并不遵循进化预测。尽管自然选择作用于遗传性状的实例比比皆是，但对于野生脊椎动物种群而言，当代适应性进化的确凿证据仍极为罕见，表型稳态似乎成为常态。所谓‘稳态悖论’凸显了我们预测进化变化的无力，这在快速的人为环境变化背景下尤为令人担忧。尽管对稳态悖论背后的原因存在激烈争论，但旨在解决问题的全面尝试却寥寥无几。在此，我们运用定量遗传学框架，分析了一野生啮齿动物种群个体层面的长期数据，并表明尽管存在体质量与适应度之间的正相关关系，但遗传变化却趋向于较低的体质量。后者代表了针对幼年个体存活度选择的适应性响应，即成为相对较小的成年个体，即具有较低潜在成年体质量的个体，这些个体可能更早完成发育。这种选择在无雪季节的末期尤为强烈，并且近年来有所加剧，与降雪模式的变化相吻合。重要的是，无论是负向进化变化，还是驱动它的选择性压力，在表型水平上均不显著，因为它们被表型可塑性和体质量与适应度之间非因果（即非遗传）的正相关关系所掩盖。在遗传水平上估计选择使我们能够揭示正在进行的适应性进化，并确定相应的表型选择性压力。因此，我们证明了自然种群能够对新的选择性压力表现出快速且适应性强的进化反应，并且明确（定量）的遗传模型能够为我们提供比纯表型估计的选择和进化变化更优越的理解。