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

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.

Fig 1. Predicted and observed rates of evolutionary change.

Rates of evolutionary change predicted by (from left to right) the breeder’s equation in its multivariate form (MBE), the multivariate breeder’s equation while constraining the genetic correlations to zero (MBE_{ρ = 0}), and the univariate breeder’s equation (UBE), followed by the phenotypic trend (PT), the trend in predicted breeding values (TPBV), and the genetic change estimated by the Price equation (GCPE). All bars represent posterior modes, with vertical lines indicating 95%CI. Raw data underlying this figure can be found in S1 Data.

Fig 2. Temporal variation in mass and estimated breeding values for mass.

(A): Year-specific mean mass corrected for age, sex, and date of measurement, with 95% CI. (B): Cohort-specific mean estimated breeding value for mass with their 95% CI, and the trend in breeding value with 95% CI. Note the different scaling of the y-axes in A and B. Raw data underlying this figure can be found in S1 Data.

Fig 3. Decomposition of selection by fitness component and source of variation.

Phenotypic, genetic, and environmental selection differential for total selection (lifetime reproductive success; LRS), fertility selection in males (ARS_♂) and females (ARS_♀), viability selection in juveniles (ϕ_Juv), as well as in adults (ϕ_A). All bars represent posterior modes, with vertical lines indicating 95% CI. Raw data underlying this figure can be found in S1 Data.

Fig 4. Snow-free season, timing of reproduction and selection for potential adult mass.

(A) Hypothetical scenario generating selection for lower body mass. In years with short summers (2008–2014), juveniles born late and having a large potential adult mass are still growing at the onset of winter and are therefore less likely to survive (blue vertical line). This results in selection for individuals with a low potential adult mass, despite mass covarying positively with survival on a within-individual level due to variation in age. (B) Births (black dots) only occur during the snow-free season (the depth of the snow cover is indicated by the thickness of the blue dots), (C) which in 2008–2014 has been shorter than in the preceding seven y. Therefore, (D) despite a positive phenotypic selection on body mass (blue), predicted adult mass was selectively neutral in 2006–2007 (brown) and was negatively selected in 2008–2014 (red). Raw data underlying this figure can be found in S1 Data.