The Timescale of Phenotypic Plasticity and Its Impact on Competition in Fluctuating Environments

Abstract

Although phenotypic plasticity can be advantageous in fluctuating environments, it may come too late if the environment changes fast. Complementary chromatic adaptation is a colorful form of phenotypic plasticity, where cyanobacteria tune their pigmentation to the prevailing light spectrum. Here, we study the timescale of chromatic adaptation and its impact on competition among phytoplankton species exposed to fluctuating light colors. We parameterized a resource competition model using monoculture experiments with green and red picocyanobacteria and the cyanobacterium Pseudanabaena, which can change its color within ∼7 days by chromatic adaptation. The model predictions were tested in competition experiments, where the incident light color switched between red and green at different frequencies (slow, intermediate, and fast). Pseudanabaena (the flexible phenotype) competitively excluded the green and red picocyanobacteria in all competition experiments. Strikingly, the rate of competitive exclusion was much faster when the flexible phenotype had sufficient time to fully adjust its pigmentation. Thus, the flexible phenotype benefited from its phenotypic plasticity if fluctuations in light color were relatively slow, corresponding to slow mixing processes or infrequent storms in their natural habitat. This shows that the timescale of phenotypic plasticity plays a key role during species interactions in fluctuating environments.Keywords: adaptive dynamics, cyanobacteria, phycocyanin, phycoerythrin, resource competition theory, Synechococcus.Fluctuations in environmental conditions pose serious challenges to organisms. Many organisms respond to environmental changes by physiological and morphological adaptations. This flexible strategy, known as phenotypic plasticity, may improve their fitness in the new environments (Agrawal 2001). For example, plants increase their leaf area during periods of reduced light (Sultan and Bazzaz 1993), cladocerans develop armored helmets in the presence of predators (Woltereck 1909;Laforsch and Tollrian 2004), and some green algae aggregate into colonies to reduce their edibility for grazers (Hessen and Van Donk 1993;Lampert et al. 1994).Intuitively, phenotypic plasticity seems a suitable strategy to cope with environmental fluctuations. However, adaptation takes time. If adaptation is too slow, organisms will not be able to keep up with changes in their environment, resulting in a permanent mismatch between the physiology of the organisms and their environmental conditions. Indeed, theory shows that adaptation can even be disadvantageous when it has a strong time delay (Padilla and Adolph 1996;Gabriel 2005). Yet, although many studies have investigated phenotypic plasticity in fluctuating environments (e.g., Chesson et al. 2004;Egas et al. 2004;Abrams 2006aAbrams , 2006bGélinas et al. 2007; Van der Stap et al. 2007), the timescale of phenotypic adaptation has received surprisingly little attention (Miner et al. 2005).The colorful process of complementary chromatic ad-E170 ...

Phycoerythrin-specific bilin lyase–isomerase controls blue-green chromatic acclimation in marineSynechococcus

“…Such an advantage appears to be conferred by CA3, which is beneficial in environments where the red-to green-light ratio varies over time periods longer than the CA3 acclimation time (28). Given the remarkable ubiquity and abundance of marine Synechococcus in the world's oceans, CA4 must be a globally significant light color acclimation process.…”

Assessing triclosan-induced ecological and trans-generational effects in natural phytoplankton communities: a trait-based field method

“…Assessing the importance of physiological, ecological and evolutionary responses Phytoplankton are able to survive in adverse habitats as a result of physiological acclimation, which is supported by generally plastic phenotypes (Stomp et al 2008;Huertas et al 2010). Here we identified a series of response traits (Table 2) whose average levels per population at the end of the experiment were significantly linked to TCS exposure.…”

Trait plasticity in species interactions: a driving force of community dynamics

“…2e). A prime example is the occurrence of complementary chromatic adaptation in cyanobacteria which changes the pigment composition and hence light absorption spectra of species (Stomp et al 2008). The light conditions for coexistence between cyanobacteria with fixed red or green phenotypes are less stringent than for coexistence between the phenotypically plastic species and either of the fixed phenotypes (Stomp et al 2008).…”