Thermal niche evolution of functional traits in a tropical marine phototroph

Abstract

Land-based plants and ocean-dwelling microbial phototrophs known as phytoplankton, are together responsible for almost all global primary production. Habitat warming associated with anthropogenic climate change has detrimentally impacted marine primary production, with the effects observed on regional and global scales. In contrast to slower-growing higher plants, there is considerable potential for phytoplankton to evolve rapidly with changing environmental conditions. The energetic constraints associated with adaptation in phytoplankton are not yet understood, but are central to forecasting how global biogeochemical cycles respond to contemporary ocean change. Here, we demonstrate a number of potential trade-offs associated with high-temperature adaptation in a tropical microbial eukaryote, Amphidinium massartii (dinoflagellate). Most notably, the population became high-temperature specialized (higher fitness within a narrower thermal envelope and higher thermal optimum), and had a greater nutrient requirement for carbon, nitrogen and phosphorus. Evidently, the energetic constraints associated with living at elevated temperature alter competiveness along other environmental gradients. While high-temperature adaptation led to an irreversible change in biochemical composition (i.e., an increase in fatty acid saturation), the mechanisms underpinning thermal evolution in phytoplankton remain unclear, and will be crucial to understanding whether the trade-offs observed here are species-specific or are representative of the evolutionary constraints in all phytoplankton.

Nitrogen limitation inhibits marine diatom adaptation to high temperatures

“…Natural genetic diversity of phytoplankton populations can alleviate the effect of N limitation if better adapted genotypes to both stressors (warming and nutrient limitation) are present in the population. However, the results of the present work and others (Baker et al ) suggest that trade‐offs between adaptation to high temperatures and resource limitation may be general, constraining the response to selection in phytoplankton. Declines in species richness may lead to decreased productivity (Cermeño et al ).…”

“…Recent laboratory experiments document fast thermal adaptation: within several hundred generations, the optimum temperature for growth and niche width increased in phytoplankton grown above their thermal optimum (Listmann et al 2016;O'Donnell et al 2018). However, little is known about how other stressors affect thermal adaptation (Boyd & Hutchins 2012;Boyd et al 2015;Baker et al 2018).…”

“…We know of no published studies that look at the interactive effects of high temperature and nutrient limitation on phytoplankton adaptation. Thermal adaptation can increase the nutrient requirements of phytoplankton (Baker et al ), suggesting that lower nutrient levels could affect the potential for phytoplankton to adapt to high temperatures. If nutrient limitation impedes thermal adaptation, phytoplankton biomass and diversity may decline more severely than predicted for nutrient‐replete conditions.…”

Gene regulation underpinning increased thermal tolerance in a laboratory‐evolved coral photosymbiont

“…Specifically, experimental evolution is the study of evolutionary processes occurring in experimental populations in response to the conditions imposed upon them (Kawecki et al., 2012). A small number of temperature selection experiments have been carried out in various species of microalgae (Baker et al., 2018; Flores‐Moya, Costas, & López‐Rodas, 2008; Flores‐Moya et al., 2012; Hinners, Kremp, & Hense, 2017; Jin, Gao, & Beardall, 2013; Listmann, LeRoch, Schlüter, Thomas, & Reusch, 2016; O’Donnell, Hamman, Johnson, Klausmeier, & Litchman, 2017; Padfield, Yvon‐Durocher, Buckling, Jennings, & Yvon‐Durocher, 2016; Schaum, Buckling, Smirnoff, Studholme, & Yvon‐Durocher, 2018; Schaum & Collins, 2014; Schlüter et al., 2014), and three studies to date have shown rapid adaptation in Symbiodiniaceae to elevated temperatures using experimental evolution (Chakravarti et al., 2017; Chakravarti & van Oppen, 2018; Huertas, Rouco, Lopez‐Rodas, & Costas, 2011). First, two unknown species of the Symbiodiniaceae were able to grow at 30°C with similar rates to the wild‐type populations at ambient temperature after only ~70 generations of laboratory selection (Huertas et al., 2011).…”

Genotypic similarity among algal symbionts corresponds to associations with closely related coral hosts

“…Genetic variation present within algal species has remained largely unstudied as a source that may fuel such adaptation (Buerger et al 2020;Parkinson, Banaszak, Altman, LaJeunesse, & Baums 2015a). The potential for genetic variation within algal species to fuel adaptation to changing conditions can be assessed in the laboratory via experimental evolution experiments where algal strains are selected over several generations under heat stress conditions (Baker et al 2018;Buerger et al 2020;Chakravarti & van Oppen 2018). In one instance, Symbiodiniaceae strains adapted to heat stress selection in vitro but once introduced into the coral partner, gains were not always retained highlighting the complexity of adaptation in the context of mutualistic partners (Buerger et al 2020).…”