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.

Heritability, selection, and the response to selection in the presence of phenotypic measurement error: Effects, cures, and the role of repeated measurements

“…As already noticed by Bonnet et al. (), the predicted evolutionary response derived from the Breeder's equation points in the opposite direction in the snow vole data than the estimate derived from the secondary theorem of selection (e.g., naive estimates vs. , with nonoverlapping credible intervals; Table ).…”

“…; Bonnet et al. ). Another quantity that is unaffected by independent transient effects, which we however did not further elaborate on here, is evolvability , defined as the squared coefficient of variation , where denotes the mean phenotypic value (Houle ).…”

“…Bonnet et al. () estimated heritability using an animal model with sex, age, Julian date (JD), squared Julian date, and the two‐ and three‐way interactions among sex, age, and Julian date as fixed effects. The inbreeding coefficient was included to avoid bias in the estimation of additive genetic variances (de Boer and Hoeschele ).…”

“…We illustrate these approaches with empirical quantitative trait analyses of body mass measurements taken in a population of snow voles in the Swiss alps (Bonnet et al. ).…”

Effects of extreme weather on two sympatric Australian passerine bird species

“…In addition, selection may act via reproduction in addition to viability, although it is worth noting that selection on body size via reproduction is typically positive (e.g. [54]). …”