Experimental evolution of environmental tolerance, acclimation, and physiological plasticity in a randomly fluctuating environment

Abstract

Environmental tolerance curves, representing absolute fitness against the environment, are an empirical assessment of the fundamental niche, and emerge from the phenotypic plasticity of underlying phenotypic traits. Dynamic plastic responses of these traits can lead to acclimation effects, whereby recent past environments impact current fitness. Theory predicts that higher levels of phenotypic plasticity should evolve in environments that fluctuate more predictably, but there have been few experimental tests of these predictions. Specifically, we still lack experimental evidence for the evolution of acclimation effects in response to environmental predictability. Here, we exposed 25 genetically diverse populations of the halotolerant microalgae Dunaliella salina to different constant salinities, or to randomly fluctuating salinities, for over 200 generations. The fluctuating treatments differed in their autocorrelation, which determines the similarity of subsequent values, and thus environmental predictability. We then measured acclimated tolerance surfaces, mapping population growth rate against past (acclimation) and current (assay) environments. We found that experimental mean and variance in salinity caused the evolution of niche position (optimal salinity) and breadth, with respect to not only current but also past (acclimation) salinity. We also detected weak but significant evidence for evolutionary changes in response to environmental predictability, with higher predictability leading notably to lower optimal salinities and stronger acclimation effect of past environment on current fitness. We further showed that these responses are related to the evolution of plasticity for intracellular glycerol, the major osmoregulatory mechanism in this species. However, the direction of plasticity evolution did not match simple theoretical predictions. Our results underline the need for a more explicit consideration of the dynamics of environmental tolerance and its underlying plastic traits to reach a better understanding of ecology and evolution in fluctuating environments.

Phenotypic plasticity evolves at multiple biological levels in response to environmental predictability in a long-term experiment with a halotolerant microalga

“…Such consistent evolution of plasticity across levels may indicate that many unmeasured integrated traits exhibit similar evolutionary responses to environmental predictability as those we have measured here (cell morphology), such that their transcriptomic (and, to some extent, epigenetic) basis is less subject to redundancies. Interestingly, in a study focusing on other lines from this same experiment [ 56 ], we found that plasticity of intracellular glycerol concentration—a major mechanism for osmoregulation in this species [ 57 , 58 ]—also evolved in response to environmental predictability, but in the opposite direction (higher plasticity in populations from unpredictable environments). However, this was mostly explained by the higher glycerol levels maintained by populations from unpredictable treatments (relative to those from predictable treatments) at intermediate and high salinities (but not at low salinity), which can be interpreted as a benefit of maintaining hyperoptimal phenotypes when fitness functions are highly asymmetrical [ 59 ], as shown in this species with respect to salinity transitions [ 24 , 56 ].…”

Predicting the evolution of adaptation and plasticity from temporal environmental change

“…Environmental change is complex, and our ability to predict evolutionary responses to it is still poor (Rescan et al, 2022). In particular, there is growing recognition of the need to better account for the complexity of temporal environmental change in biological predictions (Bates et al, 2018;Dillon et al, 2016;Helmuth et al, 2014;Vinton et al, 2022).…”

“…It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for this this version posted February 13, 2023. ; https://doi.org/10.1101/2023.02.12.528221 doi: bioRxiv preprint seasonality relative to generation time in longer-lived species (reviewed by Williams et al, 2017). However, plasticity did not always respond to predictability as expected when it was induced and selected simultaneously, arguing that theory tailored for developmentally plastic traits may not hold for those adjusted continually through life (see also Rescan et al, 2022). Since fewer models have explored the dynamics of labile traits (Beaman et al, 2016;Lande, 2014; see also review section above), this points to a need to better understand the role of predictability in their evolution (Rescan et al, 2022).…”

“…seasonality relative to generation time in longer-lived species (reviewed by Williams et al, 2017). However, plasticity did not always respond to predictability as expected when it was induced and selected simultaneously, arguing that theory tailored for developmentally plastic traits may not hold for those adjusted continually through life (see also Rescan et al, 2022). Since fewer models have explored the dynamics of labile traits (Beaman et al, 2016;Lande, 2014; see also review section above), this points to a need to better understand the role of predictability in their evolution (Rescan et al, 2022).…”

“…Populations in highly-stochastic environments may thus be prone to genetic drift, risking loss of genetic diversity and fitness (Lande & Shannon, 1996;Tufto, 2015). In general, however, we still lack a thorough understanding of how different components of environmental change combine to shape adaptation and plasticity, and their rates of evolution, across populations and landscapes (Catullo et al, 2019;Rescan et al, 2022;Shaw & Etterson, 2012;Vinton et al, 2022;Visser, 2008). This understanding is crucial to predicting adaptive capacity and persistence under the fast-paced and complex nature of climate change.…”