How bottlenecks shape adaptive potential: from theory and microbiology to conservation biology

Abstract

Wild populations frequently undergo demographic changes that can destabilize their persistence and, thus, the equilibrium of ecosystems. For instance, habitat loss due to human activities leads to a drastic population size reduction, a process called a bottleneck. By reducing genetic diversity, a bottleneck may prevent a population from adapting to subsequent environmental changes. In the context of climate change, it is crucial to accurately predict how populations evolve after a bottleneck and how it affects their persistence. Mathematical models have provided valuable insights into the impact of bottlenecks on adaptive potential of populations. However, their application to wild populations requires further improvement. Empirical testing of these theoretical predictions is mainly conducted using microbial populations. Thus, it remains unclear what the implications of the results are at the macroscopic scale, although this information is crucial for conservation biology. Here, we aim to determine the extent to which the knowledge acquired through evolutionary theory and experimental microbiology can be applied to wild populations. To achieve this, we address the following questions: (i) What do theory and microbiology experiments tell us about the influence of bottlenecks on the ability of populations to adapt to future environmental changes? (ii) Can these theoretical predictions be applied to wild populations? and (iii) What is missing to better predict the evolution of wild populations after a bottleneck? We analyze how the four main evolutionary processes (mutation, genetic drift, natural selection, and gene flow) influence the outcome of a bottlenecked population. By linking theory, microbial experiments, and empirical studies on natural populations, we identify research directions that could help improve the management of bottlenecked populations and plead for increased communication between these fields.