No abstract

Trait-based approaches to phytoplankton ecology have gained traction in recent decades as phenotypic traits are incorporated into ecological and biogeochemical models. Here, we use high-throughput phenotyping to explore both intra- and interspecific constraints on trait combinations that are expressed in the cosmopolitan marine diatom genus Thalassiosira. We demonstrate that within Thalassiosira, phenotypic diversity cannot be predicted from genotypic diversity, and moreover, plasticity can create highly divergent phenotypes that are incongruent with taxonomic grouping. Significantly, multivariate phenotypes can be represented in reduced dimensional space using principal component analysis with 77.7% of the variance captured by two orthogonal axes, here termed a ‘trait-scape’. Furthermore, this trait-scape can be recovered with a reduced set of traits. Plastic responses to the new environments expanded phenotypic trait values and the trait-scape, however, the overall pattern of response to the new environments was similar between strains and many trait correlations remained constant. These findings demonstrate that trait-scapes can be used to reveal common constraints on multi-trait plasticity in phytoplankton with divergent underlying phenotypes. Understanding how to integrate trait correlational constraints and trade-offs into theoretical frameworks like biogeochemical models will be critical to predict how microbial responses to environmental change will impact elemental cycling now and into the future.

Microbes form the base of food webs and drive biogeochemical cycling. Predicting the effects of microbial evolution on global elemental cycles remains a significant challenge due to the sheer number of interacting environmental and trait combinations. Here, we present an approach for integrating multivariate trait data into a predictive model of trait evolution. We investigated the outcome of thousands of possible adaptive walks parameterized using empirical evolution data from the alga Chlamydomonas exposed to high CO 2 . We found that the direction of historical bias (existing trait correlations) influenced both the rate of adaptation and the evolved phenotypes (trait combinations). Critically, we use fitness landscapes derived directly from empirical trait values to capture known evolutionary phenomena. This work demonstrates that ecological models need to represent both changes in traits and changes in the correlation between traits in order to accurately capture phytoplankton evolution and predict future shifts in elemental cycling.

Marine diatoms are important primary producers that can undergo multitrait changes in response to environmental or demographic perturbations. Here, we investigated how flexible multitrait correlations are over hundreds of generations, and how lineage diversity and phenotype diversity are related. We used a perturbation-evolution experiment with Thalassiosira diatoms in which they were 'knocked-off' their ancestral multitrait phenotype peak using repeated population bottlenecks, and were then allowed to grow unhindered as large populations. We found that most multitrait phenotypes were isolated but that in 10% of cases, phenotypes were connected by viable trajectories. Following the bottleneck perturbation, evolving in a +4 degrees Celsius environment favoured the discovery of novel multitrait phenotypes, while evolving in the ancestral environment most often resulted in the ancestral phenotype re-evolving. Finally, both trait values and trait correlations evolved in this experiment, with the most drastic changes in trait correlations being associated with lower growth rates. Our findings demonstrate that demographic events that result in decreases in fitness, such as population bottlenecks, have the potential to play an important role in the realised connectivity of phenotypes, as well as in shaping the relationship between lineage and phenotypic diversity in diatoms.

The high evolutionary potential of phytoplankton species allows them to rapidly adapt to global warming. Adaptations may occur in temperature-dependent traits, such as growth rate, cell size and life cycle processes. Using resurrection experiments with resting stages from living sediment archives, it is possible to investigate whether adaptation occurred. For this study, we revived resting cysts of the spring bloom dinoflagellate from recent and 100-year-old sediment layers from the Gulf of Finland, and compared temperature-dependent traits of recent and historic strains along a temperature gradient. We detected no changes in growth rates and cell sizes but a significant difference between recent and historic strains regarding resting cyst formation. The encystment rate of recent strains was significantly lower compared with historic strains which we interpret as an indication of adaptation to higher and more rapidly increasing spring temperatures. Low encystment rates may allow for bloom formation even if the threshold temperature inducing a loss of actively growing cells through resting cyst formation is exceeded. Our findings reveal that phenotypic responses of phytoplankton to changing temperature conditions may include hidden traits such as life cycle processes and their regulation mechanisms. This study emphasizes the potential of living sediment archives to investigate plankton responses and adaptation to global warming.