Sinéad Collins

John Raven pioneered the field of algae ecophysiology, advancing our understanding of cellular resource economics, carbon acquisition, and energy allocation. His work laid the foundation for investigating integrative physiology, linking growth-survival trade-offs across diverse environments. The sea ice habitat provides an excellent framework to continue the research John championed. With steep temperature-salinity gradients, algae survival requires a shift in physiology that we are only beginning to understand. We developed two small scale, reproducible icecosms to investigate physiological changes associated with incorporation into sea ice and survival potential post-melt. Fragilariopsis cylindrus and Nitzschia frigida , known for their association with the ice environment, and Porosira glacialis , known for its association with the ice edge, were used to mechanistically link physical properties with algal physiology and post-melt survival. We observe incorporation into the ice of F. cylindrus and N. frigida alongside vertical photophysiological profiles of F. cylindrus revealing inhospitable conditions in the top compared to the bottom layers of ice. N. frigida and P. glacialis remain viable within the ice and retain the capacity to seed populations following melt. Our results establish icecosms as experimental framework to investigate ecophysiological responses of sea ice algae and provide a foundation toward ecological and evolutionary questions.

Phytoplankton are the major primary producers in the Southern Ocean, are important to global nutrient cycles, and are at the base of marine food webs. Polar ecosystems are unique in their extended periods of darkness in the winter, and prolonged darkness has the potential to exert selection that affects diatom population composition if there is differential survival in the dark, the variation in population growth rates in subsequent light periods, or both. We tested whether prolonged darkness has the potential to exert within-species selection on a model polar diatom species by exposing five strains of the polar diatom Porosira glacialis to prolonged darkness at two different temperatures in the laboratory. We measured population survival in the dark, growth rate upon re-illumination, and between-strain variability in these traits. We found a pronounced decline in survival and growth rate with time spent in the dark, as well as important intraspecific variation in the tested strains. Declines in survival and growth were exacerbated at a higher temperature. Our results show that the darkness of polar night can exert intraspecific selection in a common Southern Ocean diatom.

Summary: Phytoplankton are the major primary producers in the Southern Ocean, participate in the global carbon cycle, nutrient cycles, and are at the base of the food-web. These polar ecosystems are unique in their extended periods of darkness in the winter. Prolonged darkness has the potential to exert selection that affects the composition of diatom communities if there is differential survival of diatoms in the dark, variation in population growth rates in subsequent light periods, or both. We tested whether prolonged darkness has the potential to exert within-species selection on a model polar diatom species by exposing 5 strains of the polar diatom Porosira glacialis to prolonged darkness at two different temperatures in the laboratory. We measured population survival in the dark, growth rate upon re-illumination, and between strain variability in these traits. We found a pronounced decline in survival and growth rate with time spent in the dark, as well as important intraspecific variation in these. Higher temperature exacerbated declines in growth and survival. Our results show that the darkness of polar night can exert selection within diatom species, with implications for phytoplankton community composition and subsequent impacts on Southern Ocean biogeochemical cycles.

Phytoplankton are photosynthetic marine microbes that affect food webs, nutrient cycles and climate regulation. Their roles are determined by correlated phytoplankton functional traits including cell size, chlorophyll content and cellular composition. Here, we explore patterns of evolution in interrelated trait values and correlations. Because both chance events and natural selection contribute to phytoplankton trait evolution, we used population bottlenecks to diversify six genotypes of Thalassiosirid diatoms. We then evolved them as large populations in two environments. Interspecific variation and within-species evolution were visualized for nine traits and their correlations using reduced axes (a trait-scape). Our main findings are that shifts in trait values resulted in movement of evolving populations within the trait-scape in both environments, but were more frequent when large populations evolved in a novel environment. Which trait relationships evolved was population-specific, but greater departures from ancestral trait correlations were associated with lower population growth rates. There was no single master trait that could be used to understand multi-trait evolution. Instead, repeatable multi-trait evolution occurred along a major axis of variation defined by several diatom traits and trait relationships. Because trait-scapes capture changes in trait relationships and values together, they offer an insightful way to study multi-trait variation.

Marine microbes like diatoms make up the base of marine food webs and drive global nutrient cycles. Despite their key roles in ecology, biogeochemistry, and biotechnology, we have limited empirical data on how forces other than adaptation may drive diatom diversification, especially in the absence of environmental change. One key feature of diatom populations is frequent extreme reductions in population size, which can occur both in situ and ex situ as part of bloom-and-bust growth dynamics. This can drive divergence between closely related lineages, even in the absence of environmental differences. Here, we combine experimental evolution and transcriptome landscapes (t-scapes) to reveal repeated evolutionary divergence within several species of diatoms in a constant environment. We show that most of the transcriptional divergence can be captured on a reduced set of axes, and that repeatable evolution can occur along a single major axis of variation defined by core ortholog expression comprising common metabolic pathways. Previous work has associated specific transcriptional changes in gene networks with environmental factors. Here, we find that these same gene networks diverge in the absence of environmental change, suggesting these pathways may be central in generating phenotypic diversity as a result of both selective and random evolutionary forces. If this is the case, these genes and the functions they encode may represent universal axes of variation. Such axes that capture suites of interacting transcriptional changes during diversification improve our understanding of both global patterns in local adaptation and microdiversity, as well as evolutionary forces shaping algal cultivation.

Unicellular photosynthetic marine microbes, or phytoplankton, make up the base of marine food webs and drive global nutrient cycles. Despite their key roles in ecology and biogeochemistry, we have a limited understanding of how the basic features of their demographics along with dynamic environments affect trait evolution. A key feature of diatom ecology is frequent extreme reductions in population size, both as part of their bloom-and-bust growth dynamics, and as a result of living within ocean currents. Here, we use experimental evolution to understand which metabolic pathways and functions readily diversify in diatom populations following population bottleneck events. We subjected replicate populations of six genetically distinct diatom strains to population bottlenecks and then subsequently allowed them to evolve as large populations in the absence of environmental change. Phylogenies and global expression of orthologs were generally strain-specific, indicating that vertical (inherited) evolutionary constraints largely determine the occupation of specific locations in the transcriptional landscape (i.e. tran-scape). Following bottlenecks and subsequent evolution as large populations, transcriptional networks of most populations returned to those of the ancestral population. However, at least one replicate population per lineage migrated in the tran-scape, demonstrating that evolutionary changes in gene expression patterns and transcriptional relationships can be driven by population bottlenecks even in the absence of environmental change. Importantly, the orthologs dominating transcriptional diversification resided in common, central metabolic pathways. These data advance our understanding of constraints and patterns of transcriptional relationships underlying trait evolution in microbes that drive global food webs and elemental cycles.

Despite the potential of standing genetic variation to rescue communities and shape future adaptation to climate change, high levels of uncertainty are associated with intraspecific trait variation in marine phytoplankton. Recent model intercomparisons have pointed to an urgent need to reduce uncertainty in the projected responses of marine ecosystems to climate change, including Southern Ocean (SO) surface waters, which are among the most rapidly warming habitats on Earth. Because SO phytoplankton growth responses to warming sea surface temperature (SST) are poorly constrained, we developed a high‐throughput growth assay to simultaneously examine inter‐ and intra‐specific thermal trait variation in a group of 43 taxonomically diverse and biogeochemically important SO phytoplankton called diatoms. We found significant differential growth performance among species across thermal traits, including optimum and maximum tolerated growth temperatures. Within species, coefficients of variation ranged from 3% to 48% among strains for those same key thermal traits. Using SO SST projections for 2100, we predicted biogeographic ranges that differed by up to 97% between the least and most tolerant strains for each species, illustrating the role that strain‐specific differences in temperature response can play in shaping predictions of future phytoplankton biogeography. Our findings revealed the presence and scale of thermal trait variation in SO phytoplankton and suggest these communities may already harbour the thermal trait diversity required to withstand projected 21st‐century SST change in the SO even under severe climate forcing scenarios.

Marine microbial communities are extremely complex and diverse. The number of locally coexisting species often vastly exceeds the number of identifiable niches, and taxonomic composition often appears decoupled from local environmental conditions. This is contrary to the view that environmental conditions should select for a few locally well‐adapted species. Here we use an individual‐based eco‐evolutionary model to show that virtually unlimited taxonomic diversity can be supported in highly evolving assemblages, even in the absence of niche separation. With a steady stream of heritable changes to phenotype, competitive exclusion may be weakened, allowing sustained coexistence of nearly neutral phenotypes with highly divergent lineages. This behaviour is robust even to abrupt environmental perturbations that might be expected to cause strong selection pressure and an associated loss of diversity. We, therefore, suggest that rapid evolution and individual‐level variability are key drivers of species coexistence and maintenance of microbial biodiversity.