Rapid thermal adaptation in a marine diatom reveals constraints and trade-offs.

Rapid evolution in response to environmental change will likely be a driving force determining the distribution of species across the biosphere in coming decades. This is especially true of microorganisms, many of which may evolve in step with warming, including phytoplankton, the diverse photosynthetic microbes forming the foundation of most aquatic food webs. Here we tested the capacity of a globally important, model marine diatom Thalassiosira pseudonana, for rapid evolution in response to temperature. Selection at 16 and 31°C for 350 generations led to significant divergence in several temperature response traits, demonstrating local adaptation and the existence of trade-offs associated with adaptation to different temperatures. In contrast, competitive ability for nitrogen (commonly limiting in marine systems), measured after 450 generations of temperature selection, did not diverge in a systematic way between temperatures. This study shows how rapid thermal adaptation affects key temperature and nutrient traits and, thus, a population's long-term physiological, ecological, and biogeographic response to climate change.

Understanding temporal variability across trophic levels and spatial scales in freshwater ecosystems.

A tenet of ecology is that temporal variability in ecological structure and processes tends to decrease with increasing spatial scales (from locales to regions) and levels of biological organization (from populations to communities). However, patterns in temporal variability across trophic levels and the mechanisms that produce them remain poorly understood. Here we analyzed the abundance time series of spatially structured communities (i.e., metacommunities) spanning basal resources to top predators from 355 freshwater sites across three continents. Specifically, we used a hierarchical partitioning method to disentangle the propagation of temporal variability in abundance across spatial scales and trophic levels. We then used structural equation modeling to determine if the strength and direction of relationships between temporal variability, synchrony, biodiversity, and environmental and spatial settings depended on trophic level and spatial scale. We found that temporal variability in abundance decreased from producers to tertiary consumers but did so mainly at the local scale. Species population synchrony within sites increased with trophic level, whereas synchrony among communities decreased. At the local scale, temporal variability in precipitation and species diversity were associated with population variability (linear partial coefficient, ß = 0.23) and population synchrony (ß = -0.39) similarly across trophic levels, respectively. At the regional scale, community synchrony was not related to climatic or spatial predictors, but the strength of relationships between metacommunity variability and community synchrony decreased systematically from top predators (ß = 0.73) to secondary consumers (ß = 0.54), to primary consumers (ß = 0.30) to producers (ß = 0). Our results suggest that mobile predators may often stabilize metacommunities by buffering variability that originates at the base of food webs. This finding illustrates that the trophic structure of metacommunities, which integrates variation in organismal body size and its correlates, should be considered when investigating ecological stability in natural systems. More broadly, our work advances the notion that temporal stability is an emergent property of ecosystems that may be threatened in complex ways by biodiversity loss and habitat fragmentation.

Characterization of transplanted green fluorescent protein+ bone marrow cells into adipose tissue.

Following transplantation of green fluorescent protein (GFP)-labeled bone marrow (BM) into irradiated, wild-type Sprague-Dawley rats, propagated GFP(+) cells migrate to adipose tissue compartments. To determine the relationship between GFP(+) BM-derived cells and tissue-resident GFP(-) cells on the stem cell population of adipose tissue, we conducted detailed immunohistochemical analysis of chimeric whole fat compartments and subsequently isolated and characterized adipose-derived stem cells (ASCs) from GFP(+) BM chimeras. In immunohistochemistry, a large fraction of GFP(+) cells in adipose tissue were strongly positive for CD45 and smooth muscle actin and were evenly scattered around the adipocytes and blood vessels, whereas all CD45(+) cells within the blood vessels were GFP(+). A small fraction of GFP(+) cells with the mesenchymal marker CD90 also existed in the perivascular area. Flow cytometric and immunocytochemical analyses showed that cultured ASCs were CD45(-)/CD90(+)/CD29(+). There was a significant difference in both the cell number and phenotype of the GFP(+) ASCs in two different adipose compartments, the omental (abdominal) and the inguinal (subcutaneous) fat pads; a significantly higher number of GFP(-)/CD90(+) cells were isolated from the subcutaneous depot as compared with the abdominal depot. The in vitro adipogenic differentiation of the ASCs was achieved; however, all cells that had differentiated were GFP(-). Based on phenotypical analysis, GFP(+) cells in adipose tissue in this rat model appear to be of both hematopoietic and mesenchymal origin; however, infrequent isolation of GFP(+) ASCs and their lack of adipogenic differentiation suggest that the contribution of BM to ASC generation might be minor.

Experimental evolution of phytoplankton fatty acid thermal reaction norms.

Temperature effects on the fatty acid (FA) profiles of phytoplankton, major primary producers in the ocean, have been widely studied due to their importance as industrial feedstocks and to their indispensable role as global producers of long-chain, polyunsaturated FA (PUFA), including omega-3 (ω3) FA required by organisms at higher trophic levels. The latter is of global ecological concern for marine food webs, as some evidence suggests an ongoing decline in global marine-derived ω3 FA due to both a global decline in phytoplankton abundance and to a physiological reduction in ω3 production by phytoplankton as temperatures rise. Here, we examined both short-term (physiological) and long-term (evolutionary) responses of FA profiles to temperature by comparing FA thermal reaction norms of the marine diatom Thalassiosira pseudonana after ~500 generations (ca. 2.5 years) of experimental evolution at low (16°C) and high (31°C) temperatures. We showed that thermal reaction norms for some key FA classes evolved rapidly in response to temperature selection, often in ways contrary to our predictions based on prior research. Notably, 31°C-selected populations showed higher PUFA percentages (including ω3 FA) than 16°C-selected populations at the highest assay temperature (31°C, above T. pseudonana's optimum temperature for population growth), suggesting that high-temperature selection led to an evolved ability to sustain high PUFA production at high temperatures. Rapid evolution may therefore mitigate some of the decline in global phytoplankton-derived ω3 FA production predicted by recent studies. Beyond its implications for marine food webs, knowledge of the effects of temperature on fatty acid profiles is of fundamental importance to our understanding of the mechanistic causes and consequences of thermal adaptation.

The roles of standing genetic variation and evolutionary history in determining the evolvability of anti-predator strategies.

Standing genetic variation and the historical environment in which that variation arises (evolutionary history) are both potentially significant determinants of a population's capacity for evolutionary response to a changing environment. Using the open-ended digital evolution software Avida, we evaluated the relative importance of these two factors in influencing evolutionary trajectories in the face of sudden environmental change. We examined how historical exposure to predation pressures, different levels of genetic variation, and combinations of the two, affected the evolvability of anti-predator strategies and competitive abilities in the presence or absence of threats from new, invasive predator populations. We show that while standing genetic variation plays some role in determining evolutionary responses, evolutionary history has the greater influence on a population's capacity to evolve anti-predator traits, i.e. traits effective against novel predators. This adaptability likely reflects the relative ease of repurposing existing, relevant genes and traits, and the broader potential value of the generation and maintenance of adaptively flexible traits in evolving populations.