The importance of spatial and temporal environmental variation in shaping ecosystem dynamics is well appreciated, yet the ecological consequences of dynamic spatial variability, that is, the temporal patterning of spatial variation, remain unresolved. Here, we experimentally generate temporally fluctuating thermal environments that have either a negative, positive, or neutral relationship between the mean spatial environmental temperature and the degree of thermal spatial heterogeneity. We test the hypothesis that the timing of spatial variation relative to diel temperature cycles can meaningfully alter movement patterns and population dynamics, using the motile green algae Chlamydomonas reinhardtii. Our results indicate that C. reinhardtii individuals growing in environments with positive relationships between spatial variability and mean temperature show reduced population growth rates, more directed movement as indicated by a reduced turning angle, and decreased negative thermotaxis over time, relative to those growing in environments with a negative relationship between spatial variability and mean temperature. We additionally document substantial regional variation in the dynamics of natural spatial variability by collecting summer water temperature measurements from five ponds in the Mount Saint Helens watershed, WA, USA. Our results collectively suggest that the dynamics of spatial variation are an underappreciated but salient feature within the broader interwoven fabric of spatiotemporal variation.

A prerequisite for the survival and reproduction of organisms is to successfully navigate thermal environmental conditions that unfold over time and space. While effective movement behaviour has been highlighted as a key mechanism by which organisms and populations may persist amidst the backdrop of directional environmental warming, it remains unclear how behavioural plasticity may mediate such effects, particularly across time‐scales that span multiple generations. Here, we examine the capacity for transgenerational plasticity to alter the movement behaviour of the motile green algae Chlamydomonas reinhardtii in response to changes in thermal conditions. We first acclimated C. reinhardtii populations to thermal environments near (25°C), below (12.5°C) or above (37.5°C) the temperature range that maximizes population growth rate. Subsequently, we assayed the micro‐spatial scale movement behaviour of these populations in thermally homogeneous environments across a period of 2 weeks in each respective environment, with the goal of evaluating the influence of thermal history on movement behaviour in a novel thermal environment. Our results indicate that thermal history can mediate the movement patterns of C. reinhardtii individuals for up to 10 generations and that the trajectory by which phenotypes converge on their acclimated values can be highly nonlinear. Subsequently, we demonstrated—using a dispersal assay in spatially variable environments—that thermal acclimation history can additionally alter movement patterns at ecologically relevant scales. Collectively these findings indicate the possibility for transgenerational plasticity to modify behaviour across extended time‐scales and converge on acclimated states via nonlinear trajectories. Understanding the efficacy of behaviour for navigating novel thermal environments, such as environments anticipated amidst environmental warming, may thus require considering past as well as present environmental conditions. Read the free Plain Language Summary for this article on the Journal blog.