Abstract
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.
Highlights
Given the rapid anthropogenic environmental changes experienced by organisms around the world, there is an increasing need for an ability to understand and predict the evolutionary dynamics of wild populations [1, 2]
Despite good empirical examples of the adaptive evolution of traits with a simple genetic architecture [3,4,5], the picture is very different for quantitative traits, which in most cases are a function of many genes of small effect [6]
In line with other morphological traits [12, 13], variation in body mass has a significant additive genetic component (VA = 4.34 g2, 95% CI [2.40; 7.36]), which corresponds to a heritability (h2) of 0.21
Summary
Given the rapid anthropogenic environmental changes experienced by organisms around the world, there is an increasing need for an ability to understand and predict the evolutionary dynamics of wild populations [1, 2]. There is an abundant literature showing that both directional selection [10, 11] and heritable genetic variation [12, 13] are common, these pre requisites of Darwinian evolution rarely allow us to explain evolutionary trends retrospectively, let alone to make predictions for the future [9, 14]. Both natural and sexual selection almost universally favour larger and heavier individuals [15]. While species do tend to grow larger over geological time-scales [16,17,18,19], this rate of evolution is orders of magnitude slower than predicted from the strength of selection and heritability observed in contemporary populations [9, 20, 21]
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