Quality-quantity tradeoffs drive functional trait evolution in a model microalgal “climate change winner”

Abstract

Phytoplankton are the unicellular photosynthetic microbes that form the base of aquatic ecosystems, and their responses to global change will impact everything from food web dynamics to global nutrient cycles. Some taxa respond to environmental change by increasing population growth rates in the short-term, and, based on this, are projected to increase in frequency over decades. To gain insight into how functional traits in these projected "climate change winners" change over different timescales, we evolved populations of microalgae in ameliorated environments for several hundred generations. While populations initially responded to environmental amelioration by increasing photosynthesis and population growth rates as expected, this response was not sustained. Instead, most populations evolved to allocate a smaller proportion of carbon to growth while increasing their ability to tolerate and metabolise reactive oxygen species (ROS). This diversion of fixed carbon from growth to catabolism underlies a quality-quantity tradeoff in daughter cell production which drives the evolution of population growth rates and of functional traits that underlie the ecological and biogeochemical roles of phytoplankton. There is intraspecific variation in the trait combinations that evolve, but all are consistent with mitigating ROS production and accumulation in ameliorated environments over hundreds of generations. This offers both an evolutionary and a metabolic framework for understanding how functional traits can change in primary producers projected to be "climate change winners", and suggests that short-term population booms and associated trait shifts have the potential to be dampened or reversed if environmental amelioration persists.

Presence of a resident species aids invader evolution

“…ROS are a natural by-product of cellular 245 metabolism, but can damage the cell at high quantities [53]. Therefore, higher tolerance 246 toward or lower quantities of ROS may infer a fitness benefit [54]. Taking into account 247 growth rates across all temperature treatments, the invader became more of a generalist, with 248 better performance across multiple environments.…”

“…We tested how capable samples were of detoxifying harmful reactive oxygen species (ROS) 507 and also estimated the intra-cellular ROS levels in order to gain an estimate on whether 508 samples under unfavourable conditions experience more stress, and are therefore producing 509 more/ being less able to detoxify ROS. We used the protocols established by [54,62]. 510 Samples from 'unfavourable environments' had higher intra-cellular ROS content, were less 511 well able to detoxify harmful ROS (Supporting Figures 2,3, 11).…”

“…Our results suggest that under warming and increased climate variability, invasions through 254 small, warm-adapted taxa with intrinsically elevated metabolic and growth rates may become 255 more frequent ('tropicalisations', see [57,58]), with nigh-unpredictable consequences on 256 aquatic ecosystems as a whole. As changes in fitness, cell size and metabolic activity are 257 often linked [59,60], it stands to reason that one possible mechanisms for higher invader 258 fitness in our invader samples lies in their ability to rapidly down-regulate cell size [61][62][63], 259 which in turn might be what is giving rise to their ability to better handle reactive oxygen 260 species [54,62] ( Figure 4B and Supporting Figure 10 -the smallest cells had highest fitness 261 and were better able to detoxify ROS). The dynamics and mechanisms of increasing fitness 262 under constant directional selection are well understood [64,65], and experimental evolution 263 lends itself well to linking environmental cause to evolutionary effect, but it is limited in 264 accurately deciphering the mechanisms that underlie trait evolution.…”

The role of changes in environmental quality in multitrait plastic responses to environmental and social change in the model microalga Chlamydomonas reinhardtii

“…The strains CC‐125, CC‐1691, CC‐2931 of Chlamydomonas reinhardtii were used in these experiments. We used single‐strain populations that were previously evolved in ambient CO 2 and high CO 2 (2,000 µatm) for 90 growth cycles in TAP media under similar measured temperature and light conditions that we use here for our control HL conditions (Lindberg & Collins, 2020). For each strain, we used 3 independently evolved high CO 2 populations, and 3 independently evolved ambient CO 2 populations, for a total of 18 independently evolved populations in this study.…”

“…We refer to populations evolved at high CO 2 as “high‐evolved” and populations evolved at ambient CO 2 as “ambient‐evolved”. All populations were grown in sterile microwell plates in 2 ml of modified Tris‐Acetate‐Phosphate (TAP) media (Harris, 2009) at a standard temperature of 25°C (Lindberg & Collins, 2020). The acetate was not added in this experiment so that CO 2 was the only source of added carbon for the growing populations (TP media).…”