Andrew J. Irwin

The evolutionary inheritance of elemental stoichiometry in marine phytoplankton

Phytoplankton is a nineteenth century ecological construct for a biologically diverse group of pelagic photoautotrophs that share common metabolic functions but not evolutionary histories. In contrast to terrestrial plants, a major schism occurred in the evolution of the eukaryotic phytoplankton that gave rise to two major plastid superfamilies. The green superfamily appropriated chlorophyll b, whereas the red superfamily uses chlorophyll c as an accessory photosynthetic pigment. Fossil evidence suggests that the green superfamily dominated Palaeozoic oceans. However, after the end-Permian extinction, members of the red superfamily rose to ecological prominence. The processes responsible for this shift are obscure. Here we present an analysis of major nutrients and trace elements in 15 species of marine phytoplankton from the two superfamilies. Our results indicate that there are systematic phylogenetic differences in the two plastid types where macronutrient (carbon:nitrogen:phosphorus) stoichiometries primarily reflect ancestral pre-symbiotic host cell phenotypes, but trace element composition reflects differences in the acquired plastids. The compositional differences between the two plastid superfamilies suggest that changes in ocean redox state strongly influenced the evolution and selection of eukaryotic phytoplankton since the Proterozoic era.

OVERLAPPING GENERATIONS CAN PROMOTE ALTRUISTIC BEHAVIOR

Abstract. We use an inclusive fitness model to study the evolution of altruism in a patch‐structured population in which there is positive probability of breeder survival from one generation to the next. We find first that breeder survival promotes altruism and second that there is a marked difference between benefits of fecundity and benefits of survival. Under the first altruism is more strongly favored, and under the second altruism is less strongly favored than in a randomly mixing population.

Improved glycaemia correlates with liver fat reduction in obese, type 2 diabetes, patients given glucagon-like peptide-1 (GLP-1) receptor agonists.

Glucagon-like peptide-1 receptor agonists (GLP-1 RA) are effective for obese patients with type 2 diabetes mellitus (T2DM) because they concomitantly target obesity and dysglycaemia. Considering the high prevalence of non-alcoholic fatty liver disease (NAFLD) in patients with T2DM, we determined the impact of 6 months’ GLP-1 RA therapy on intrahepatic lipid (IHL) in obese, T2DM patients with hepatic steatosis, and evaluated the inter-relationship between changes in IHL with those in glycosylated haemoglobin (HbA1c), body weight, and volume of abdominal visceral and subcutaneous adipose tissue (VAT and SAT). We prospectively studied 25 (12 male) patients, age 50±10 years, BMI 38.4±5.6 kg/m2 (mean ± SD) with baseline IHL of 28.2% (16.5 to 43.1%) and HbA1c of 9.6% (7.9 to 10.7%) (median and interquartile range). Patients treated with metformin and sulphonylureas/DPP-IV inhibitors were given 6 months GLP-1 RA (exenatide, n = 19; liraglutide, n = 6). IHL was quantified by liver proton magnetic resonance spectroscopy (1H MRS) and VAT and SAT by whole body magnetic resonance imaging (MRI). Treatment was associated with mean weight loss of 5.0 kg (95% CI 3.5,6.5 kg), mean HbA1c reduction of 1·6% (17 mmol/mol) (0·8,2·4%) and a 42% relative reduction in IHL (−59.3, −16.5%). The relative reduction in IHL correlated with that in HbA1c (ρ = 0.49; p = 0.01) but was not significantly correlated with that in total body weight, VAT or SAT. The greatest IHL reduction occurred in individuals with highest pre-treatment levels. Mechanistic studies are needed to determine potential direct effects of GLP-1 RA on human liver lipid metabolism.

Polycystic Ovary Syndrome with Hyperandrogenism Is Characterized by an Increased Risk of Hepatic Steatosis Compared to Nonhyperandrogenic PCOS Phenotypes and Healthy Controls, Independent of Obesity and Insulin Resistance

CONTEXT Nonalcoholic fatty liver disease may be evident in women with polycystic ovary syndrome (PCOS), both conditions being associated with obesity and insulin resistance. However, few studies have accounted for the high prevalence of obesity in PCOS. OBJECTIVE The aim of this study was to determine whether PCOS is independently associated with hepatic steatosis, compared with healthy controls of similar age and body mass index (BMI), and whether steatosis is associated with hyperandrogenemia. DESIGN AND SETTING We conducted a cross-sectional, case-control study at two tertiary referral centers. PATIENTS Twenty-nine women with PCOS diagnosed by the Rotterdam criteria [aged 28 yr; 95% confidence interval (CI), 26-31; BMI, 33 kg/m2; 95% CI, 31-36] and 22 healthy controls (aged 29 yr; 95% CI, 28-31; BMI, 30 kg/m2; 95% CI, 28-33) were studied. METHODS Proton-magnetic resonance spectroscopy quantified hepatic and skeletal muscle fat; whole body magnetic resonance imaging quantified internal, visceral, and sc adipose tissue volumes. Differences were assessed between PCOS and controls using t tests, and between hyperandrogenic (HA) PCOS, PCOS with normal androgens (NA), and controls using analysis of covariance. RESULTS After statistical adjustment for BMI, HA-PCOS had significantly higher liver fat vs. NA-PCOS (3.7%; 95% CI, 0.6-13.1) and vs. controls (2.1%; 95% CI, 0.3-6.6). Similarly, after adjustment for homeostasis model assessment for insulin resistance, internal and visceral adipose tissue volumes, liver fat remained significantly greater in HA-PCOS compared to NA-PCOS and controls. CONCLUSION These data suggest that HA-PCOS is associated with hepatic steatosis, independent of obesity and insulin resistance.

Light Variability Illuminates Niche-Partitioning among Marine Picocyanobacteria

Prochlorococcus and Synechococcus picocyanobacteria are dominant contributors to marine primary production over large areas of the ocean. Phytoplankton cells are entrained in the water column and are thus often exposed to rapid changes in irradiance within the upper mixed layer of the ocean. An upward fluctuation in irradiance can result in photosystem II photoinactivation exceeding counteracting repair rates through protein turnover, thereby leading to net photoinhibition of primary productivity, and potentially cell death. Here we show that the effective cross-section for photosystem II photoinactivation is conserved across the picocyanobacteria, but that their photosystem II repair capacity and protein-specific photosystem II light capture are negatively correlated and vary widely across the strains. The differences in repair rate correspond to the light and nutrient conditions that characterize the site of origin of the Prochlorococcus and Synechococcus isolates, and determine the upward fluctuation in irradiance they can tolerate, indicating that photoinhibition due to transient high-light exposure influences their distribution in the ocean.

A universal driver of macroevolutionary change in the size of marine phytoplankton over the Cenozoic

The size structure of phytoplankton assemblages strongly influences energy transfer through the food web and carbon cycling in the ocean. We determined the macroevolutionary trajectory in the median size of dinoflagellate cysts to compare with the macroevolutionary size change in other plankton groups. We found the median size of the dinoflagellate cysts generally decreases through the Cenozoic. Diatoms exhibit an extremely similar pattern in their median size over time, even though species diversity of the two groups has opposing trends, indicating that the macroevolutionary size change is an active response to selection pressure rather than a passive response to changes in diversity. The changes in the median size of dinoflagellate cysts are highly correlated with both deep ocean temperatures and the thermal gradient between the surface and deep waters, indicating the magnitude and frequency of nutrient availability may have acted as a selective factor in the macroevolution of cell size in the plankton. Our results suggest that climate, because it affects stratification in the ocean, is a universal abiotic driver that has been responsible for macroevolutionary changes in the size structure of marine planktonic communities over the past 65 million years of Earths history.

Evolutionary inheritance of elemental stoichiometry in phytoplankton

The elemental composition of phytoplankton is a fusion of the evolutionary history of the host and plastid, resulting in differences in genetic constraints and selection pressures associated with environmental conditions. The evolutionary inheritance hypothesis predicts similarities in elemental composition within related taxonomic lineages of phytoplankton. To test this hypothesis, we measured the elemental composition (C, N, P, S, K, Mg, Ca, Sr, Fe, Mn, Zn, Cu, Co, Cd and Mo) of 14 phytoplankton species and combined these with published data from 15 more species from both marine and freshwater environments grown under nutrient-replete conditions. The largest differences in the elemental profiles of the species distinguish between the prokaryotic Cyanophyta and primary endosymbiotic events that resulted in the green and red plastid lineages. Smaller differences in trace element stoichiometry within the red and green plastid lineages are consistent with changes in trace elemental stoichiometry owing to the processes associated with secondary endosymbioses and inheritance by descent with modification.

Environmental control of diatom community size structure varies across aquatic ecosystems

Changes in the size structure of photoautotrophs influence food web structure and the biogeochemical cycling of carbon. Decreases in the median size of diatoms within communities, in concert with climate warming and water column stratification, have been observed over the Cenozoic in the ocean and over the last 50 years in Lake Tahoe. Decreases in the proportion of larger plankton are frequently observed in response to reduced concentrations of limiting nutrients in marine systems and large stratified lakes. By contrast, we show a decrease in the median size of planktonic diatoms in response to higher nutrient concentrations in a set of intermediate-sized alkaline lakes. Climate-induced increases in the frequency, duration and strength of water column stratification may select smaller planktonic species in the ocean and larger lakes owing to a reduction in nutrient availability and sinking rates, while light limitation, stimulated by nutrient eutrophication and high chlorophyll concentrations, may select smaller species within a community owing to their high light absorption efficiencies and lower sinking rates. The relative importance of different physiological and ecological rates and processes on the size structure of communities varies in different aquatic systems owing to varying combinations of abiotic and biotic constraints.

A multiyear estimate of the effective pollen donor pool for Albizia julibrissin

Studies of pollen movement in plant populations are often limited to a single reproductive event, despite concerns about the adequacy of single-year measures for perennial organisms. In this study, we estimate the effective number of pollen donors per tree from a multiyear study of Albizia julibrissin Durazz (mimosa, Fabaceae), an outcrossing, insect-pollinated tree. We determined 40 seedling genotypes for each of 15 seed trees during 4 successive years. A molecular analysis of variance of the pollen gametes fertilizing the sampled seeds was used to partition variation in pollen pools among seed trees, among years, and within single tree-year collections. Using these variance components, we demonstrate significant male gametic variability among years for individual trees. However, results indicate that yearly variation in the ‘global pollen pool’, averaged over all 15 seed trees for these 4 years, is effectively zero. We estimate the effective number of pollen donors for a single mimosa tree (Nep) to be 2.87. Single season analyses yield Nep∼2.05, which is 40% less than the value of Nep estimated from 4 years of data. We discuss optimal sampling for future studies designed to estimate Nep. Studies should include more trees, each sampled over at least a few years, with fewer seeds per tree per year than are needed for a traditional parentage study.

Light and nutrient availability affect the size-scaling of growth in phytoplankton.

Communities of marine phytoplankton consist of cells of many different sizes. The size-structure of these communities often varies predictably with environmental conditions in aquatic systems. It has been hypothesized that physiological differences in nutrient and light requirements and acquisition efficiencies contribute to commonly observed correlations between phytoplankton community size structure and resource availability. Using physiological models we assess how light and nutrient availability can alter the relative growth rates of phytoplankton species of different cell sizes. Our models predict a change in the size dependence of growth rate depending on the severity of limitation by light and nutrient availability. Under conditions of growth-saturated resource supply, phytoplankton growth rate (mol C cell(-1)time(-1)) scales with cell volume with a size-scaling exponent of 3/4; light limitation reduces the size-scaling exponent to approximately 2/3, and nutrient limitation decreases the exponent to 1/3 as a consequence of the size-scaling of resource acquisition. Exponents intermediate between 1/3 and 3/4 occur under intermediate availability of light and nutrients and depend on the size-scaling of pigment photoacclimation and the size range examined.