Introduction
Predicting ecological dynamics and species’ range shifts has become a major goal for conservation and management strategies in times of global climate and environmental change (1). Indeed, whether the outcomes of range expansions or biological invasions can be predicted at all remains highly debated in ecology even in simple settings, due to the intrinsic stochasticity of these phenomena (2, 3). Moreover, evolutionary processes occur at the same time scale as ecological dynamics during range expansions (4, 5), potentially exacerbating the uncertainty of outcomes (6).
Theory shows that range expansions can involve the concurrent evolution of dispersal and other traits (4, 7) and lead to the emergence of dispersal syndromes (8, 9). Individuals with greater dispersal propensity are the first to reach the range front, and they will reproduce with conspecifics that have the same fast spreader characteristics (10, 11). Consequently, high dispersal ability and correlated life-history traits evolve in the range front populations due to spatial selection and spatially assortative mating (12, 13). Since expansion speeds are mainly influenced by dispersal and reproduction (14, 15), the two traits can be rapidly selected and evolve simultaneously. However, if dispersal is costly (16) there may be trade-offs with other traits. Higher reproduction at the range front may come at the expense of lower competitive ability (17), recalling the competition-colonisation trade-off in classic species coexistence models (18).
Fast evolution in range front populations can produce eco-evolutionary feedbacks and thereby speed up the expansion process (6, 13, 19–21). In the emblematic example of the cane toad (Rhinella marina ) expansion in Australia, increased dispersal at the range front coincided with evolutionary change in behavioural, morphological and demographic traits, promoting the speed of the toad expansion (4, 22). Growing empirical evidence from other natural populations and biological systems (23, 24) suggest that dispersal evolution at range fronts is a common phenomenon. Recently, experimental evolution and microcosm landscapes have been used to test fundamental predictions and mimic range expansions in the laboratory. Experiments with ciliates (25), arthropods (26–29) or plants (5) well showed the rapid evolution of dispersal and other dispersal-related traits during the experimental range expansions. However, whether we can accurately predict these eco-evolutionary dynamics from prior information on the genetic or phenotypic characteristics of the expanding populations remains an open question (30).
Coupling microcosm experiments with mathematical modelling and genetic analyses provides a possible way forward to assess the predictability of range expansions (31). In micro/mesocosm landscapes, we can study the repeatability of range expansions through independent replicates under controlled conditions. Using specifically tailored and parametrised mathematical models, we can then formalise putative processes of range expansion dynamics and confront predicted with observed outcomes. Genetic analysis can further characterise the degree of similarity among experimental replicates and link phenotypic trait change to genetic change.
Here, moving a step forward from previous ecological models (2, 3), we employed such a combined approach to assess the predictability of evolutionary outcomes of range expansions in an aquatic model organism, the freshwater protozoan Paramecium caudatum . Following previous studies (25, 32), we used interconnected 2-patch systems to establish a range front treatment (6 lines), where recurrent episodes of dispersal alternated with intermittent periods of population growth (Fig. 1A). In the contrasting range core treatment only the non-dispersing individuals were maintained (6 lines), and in a third control treatment the dispersing individuals were mixed and propagated with the non-dispersing (3 lines). We recreated these experimental treatments in a predictive mathematical model, parameterised for dispersal and growth characteristics of the 20 Paramecium strains that were used to assemble the founder populations (total of 15 lines) in the evolutionary experiment. Thus, starting from standing genetic variation, we compared predicted and observed short-term trait evolution in front and core populations, and assessed the repeatability of evolutionary outcomes at the genotypic level after 30 dispersal/growth cycles. Long-term evolution was tracked over the course of three years (160 cycles). Our main finding is that short-term evolutionary outcomes were highly predictable and essentially depend on two parameters (genetic variation in dispersal and growth). Data-model matching was decoupled in the long run, possibly due to de novo evolution and the emergence of a dispersal syndrome at range fronts.