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.