Evolution during population spread affects plant performance in stressful environments

Abstract

Reliable predictions of population spread rates are essential to forecast biological invasions. Recent studies have shown that populations spreading through favourable habitat can rapidly evolve higher dispersal and reproductive rates at the expansion front, which accelerates spread velocity. However, spreading populations are likely to eventually encounter stressful conditions in the expanded range. How evolution during spread in favourable environments affects subsequent population growth in harsher environments is currently unknown. We examined evolutionary change in performance under drought, interspecific competition, and heat stress for populations of Arabidopsis thaliana that experienced six generations of spread through replicated experimental landscapes of favourable habitat. To quantify how population performance under stress differed between leading edge and founding populations, we combined individual tests of genotype performance under stress with knowledge of the genotype frequency changes that occurred over the replicate invasions. After spreading through favourable environments, the average silique production of individuals exposed to drought or interspecific competition was lower in leading edge than founding populations. This change was driven by the evolution of lower intrinsic silique production, which was correlated with increased seed size, a trait that evolved as populations spread. The ability of plants to tolerate drought or interspecific competition, however, did not change markedly during spread. Heat tolerance did increase in leading edge populations, and this trait was associated with the evolution of taller plants during spread through favourable habitat. Synthesis. We conclude that evolution during spread in favourable environments may affect the ability of populations to grow under stressful conditions as experienced in the expanded range, through changes in either intrinsic fecundity or stress tolerance. Thus, evolution during spread may constrain or extend the eventual range limit of nonnative species invasions.

Consequences of intraspecific variation in seed dispersal for plant demography, communities, evolution and global change

“…However, these evolutionary changes may affect how populations subsequently respond to stressful environments such as those expected during range shifts under climate change. In experimental invasions of A. thaliana , an evolutionary increase in seed size over six generations of spread was associated with a subsequent reduction in population performance under drought stress (Lustenhouwer et al 2019). Thus, intraspecific variation in dispersal and seed traits and their evolution will influence the ability of plants to respond to anthropogenic and global climate change.…”

Trait differentiation between native and introduced populations of the invasive plant Sonchus oleraceus L. (Asteraceae)

“…Several recent studies have shown that alien plants can undergo rapid evolution through trait adaptation to novel selection pressures (e.g. Molina-Montenegro et al 2018;van Boheemen et al 2019a;Lustenhouwer et al 2019;Brandenburger et al 2019a, b). Rapid trait adaptation may be driven by several processes; for example, the Evolution of Increased Competitive Ability (EICA) hypothesis posits that there is an evolutionary shift from costly defensive abilities to competitive performance in introduced populations, due to the absence of co-introduced specialist enemies (Blossey and Notzold 1995).…”

“…Other traits relating to plant phenology (Turner et al 2014) and resource acquisition efficiency (e.g. specific leaf area, leaf and stem dry matter content, carbon to nitrogen ratio of seeds and leaves, Wright et al 2004;Grassein et al 2010)) have also been shown to rapidly change following introduction as a result of competition for novel resources (Gioria and Osborne 2014;Lustenhouwer et al 2019). Many recent studies have shown that climate niche envelopes occupied by invasive plants in their introduced ranges can differ substantially to native ranges and exposure to novel climatic regimes may select for divergent traits of alien plant populations (Early and Sax 2014;Moran and Alexander 2014;van Boheemen et al 2019a).…”

The distinct phenotypic signatures of dispersal and stress in an arthropod model: from physiology to life history

“…This means relationships between stress resistance and dispersal can be equally driven by fitness expectations after immigration in novel environments (Renault et al, 2018). In some cases, traits or contexts favoring dispersal do actually favor stress tolerance (Lustenhouwer et al, 2019). As the probability of arriving in, or crossing, marginal/suboptimal habitat should increase in heterogeneous environments, stress-resistant individuals may eventually profit most from dispersal, giving rise to positive correlations between these traits in such contexts.…”