Predicting evolution in experimental range expansions of an aquatic model system

Abstract

Predicting range expansion dynamics is an important goal of both fundamental and applied research in conservation and global change biology. However, this is challenging if ecological and evolutionary processes occur on the same time scale. Using the freshwater ciliate Paramecium caudatum, we combined experimental evolution and mathematical modeling to assess the predictability of evolutionary change during range expansions. In the experiment, we followed ecological dynamics and trait evolution in independently replicated microcosm populations in range core and front treatments, where episodes of natural dispersal alternated with periods of population growth. These eco-evolutionary conditions were recreated in a predictive mathematical model, parametrized with dispersal and growth data of the 20 founder strains in the experiment. We found that short-term evolution was driven by selection for increased dispersal in the front treatment and general selection for higher growth rates in all treatments. There was a good quantitative match between predicted and observed trait changes. Phenotypic divergence was further mirrored by genetic divergence between range core and front treatments. In each treatment, we found the repeated fixation of the same cytochrome c oxidase I (COI) marker genotype, carried by strains that also were the most likely winners in our model. Long-term evolution in the experimental range front lines resulted in the emergence of a dispersal syndrome, namely a competition—colonization trade-off. Altogether, both model and experiment highlight the potential importance of dispersal evolution as a driver of range expansions. Thus, evolution at range fronts may follow predictable trajectories, at least for simple scenarios, and predicting these dynamics may be possible from knowledge of few key parameters.

Range expansion is both slower and more variable with rapid evolution across a spatial gradient in temperature

“…Recent studies have highlighted that rapid evolution can complicate our ability to predict the ecoevolutionary dynamics of range expansions (Miller et al 2020;Shaw et al 2023;Williams et al 2019;Zilio et al 2023). Here, we used replicate range-expanding populations to empirically test whether the presence of selection from an abiotic gradient across landscapes could modify the among-replicate variability, and hence predictability, of range expansion speed.…”

Experimental evolution of dispersal: Unifying theory, experiments and natural systems

“…We see three main ways to improve integration between conceptual theory, modelling and evolution experiments. First, modelling and experimental evolution can be strengthened by mutually informing each study design—tailored experiments can validate analytical or statistical models, aid in model selection or evaluate predictability (Zilio et al, 2023; Figure 1, arrow 3 and 4). For example, theory has shown that high levels of genetic polymorphism in dispersal traits and/or high mutation rates can accelerate range expansion and alter trade‐offs between reproductive output and movement/dispersal capacity (Elliott & Cornell, 2012; Morris et al, 2019).…”