Phytoplankton Assemblage Characteristics in Recurrently Fluctuating Environments

Annual variations in biogeochemical and physical processes can lead to nutrient variability and seasonal patterns in phytoplankton productivity and assemblage structure. In many coastal systems river inflow and water exchange with the ocean varies seasonally, and alternating periods can arise where the nutrient most limiting to phytoplankton growth switches. Transitions between these alternating periods can be sudden or gradual and this depends on human activities, such as reservoir construction and interbasin water transfers. How such activities might influence phytoplankton assemblages is largely unknown. Here, we employed a multispecies, multi-nutrient model to explore how nutrient loading switching mode might affect characteristics of phytoplankton assemblages. The model is based on the Monod-relationship, predicting an instantaneous growth rate from ambient inorganic nutrient concentrations whereas the limiting nutrient at any given time was determined by Liebig’s Law of the Minimum. Our simulated phytoplankton assemblages self-organized from species rich pools over a 15-year period, and only the surviving species were considered as assemblage members. Using the model, we explored the interactive effects of complementarity level in trait trade-offs within phytoplankton assemblages and the amount of noise in the resource supply concentrations. We found that the effect of shift from a sudden resource supply transition to a gradual one, as observed in systems impacted by watershed development, was dependent on the level of complementarity. In the extremes, phytoplankton species richness and relative overyielding increased when complementarity was lowest, and phytoplankton biomass increased greatly when complementarity was highest. For low-complementarity simulations, the persistence of poorer-performing phytoplankton species of intermediate R*s led to higher richness and relative overyielding. For high-complementarity simulations, the formation of phytoplankton species clusters and niche compression enabled higher biomass accumulation. Our findings suggest that an understanding of factors influencing the emergence of life history traits important to complementarity is necessary to predict the impact of watershed development on phytoplankton productivity and assemblage structure.     

Fluctuating Environments and Phytoplankton Community Structure: A Stochastic Model

Spatial heterogeneity in organism and resource distributions can generate temporal heterogeneity in resource access for simple organisms like phytoplankton. The role of temporal heterogeneity as a structuring force for simple communities is investigated via models of phytoplankton with contrasting life histories competing for a single fluctuating resource. A stochastic model in which environmental and demographic stochasticity are treated separately is compared with a model with deterministic resource variation to assess the importance of stochasticity. When compared with the deterministic model, the stochastic model allows for coexistence over a wider range of parameter values (or life-history types). The model suggests that demographic stochasticity alone is far more important in increasing the possibility of coexistence than environmental stochasticity alone. However, the combined effects of both types of stochasticity produce the largest likelihood of coexistence. Finally, the influence of relative nutrient levels and nutrient pulse frequency on these results is addressed. We relate our findings to variable environment theory with evidence for both relative nonlinearity and the storage effect acting in this model. We show for the first time that temporal dynamics generated by demographic stochasticity may operate like the storage effect at particular spatial scales.     

Optimal Recombination Rate in Fluctuating Environments

The optimal recombination rate which maximizes the long-term geometric average of the population fitness is studied for a two-locus haploid model, assuming that the fitnesses of genotypes AB, Ab, aB and ab are 1 + s(t), 1 - s(t), 1 - s(t), and 1 + s(t), respectively, where s(t) follows various stationary stochastic processes with the average zero. With positive recombination, the polymorphism is stably maintained at both loci. After an initial transient phase, the dynamics are reduced to one dimension, and are analyzed for weak selection limit, strong selection limit, and selection with two state Markovian jump. Results are: (1) If the environmental fluctuation has a predominant periodic component, ropt is approximately inversely proportional to the period irrespective of selection intensity. (2) If the fluctuation is a superposition of many periodic components, the one with the longest period is the most effective in determining ropt because the genetic dynamics cannot track very quick fluctuations (low pass filter effect). (3) If the power spectrum density is decreasing with the frequency, as in pink, or 1/f noises, ropt is small when selection is weak, and increases with the selection intensity. Numerical calculation of the genetic dynamics of a recombination modifier supports all these predictions for the evolutionarily stable recombination rate.     

Nematode Reproduction in Environments of Fluctuating Aeration

Reproduction of Aphelenchus avenae, reared on Rhizoctonia solani growing on steamed wheat seeds and Caenorhabditis sp., reared on a mixed bacterial culture grown on oatmeal, was significantly reduced at 5% oxygen and inhibited at 4% oxygen and below. Aeration ranging from atmospheric air (21%) to 10% oxygen had no effect on reproduction. Close interval (5 days or less) fluctuations, between high and low oxygen concentrations, inhibited population buildup of Hemicycliophora arenaria on tomato in soil, and of A. avenae and Caenorhabditis sp. in vitro. In soil tests with H. arenaria exposed to 12 hr of nitrogen every three days (in air) inhibited the rate of buildup compared to controls maintained in continuous air. With the in vitro studies, as little as 4 hr nitrogen every 3 days (stored in air) significantly influenced the population numbers.     

Uncoupled Analysis of Stochastic Reaction Networks in Fluctuating Environments

The dynamics of stochastic reaction networks within cells are inevitably modulated by factors considered extrinsic to the network such as, for instance, the fluctuations in ribosome copy numbers for a gene regulatory network. While several recent studies demonstrate the importance of accounting for such extrinsic components, the resulting models are typically hard to analyze. In this work we develop a general mathematical framework that allows to uncouple the network from its dynamic environment by incorporating only the environment''s effect onto the network into a new model. More technically, we show how such fluctuating extrinsic components (e.g., chemical species) can be marginalized in order to obtain this decoupled model. We derive its corresponding process- and master equations and show how stochastic simulations can be performed. Using several case studies, we demonstrate the significance of the approach.     

Establishment Probability in Fluctuating Environments: A Branching Process Model

We study the establishment probability of invaders in stochastically fluctuating environments and the related issue of extinction probability of small populations in such environments, by means of an inhomogeneous branching process model. In the model it is assumed that individuals reproduce asexually during discrete reproduction periods. Within each period, individuals have (independent) Poisson distributed numbers of offspring. The expected numbers of offspring per individual are independently identically distributed over the periods. It is shown that the establishment probability of an invader varies over the reproduction periods according to a stable distribution. We give a method for simulating the establishment probabilities and approximations for the expected establishment probability. Furthermore, we show that, due to the stochasticity of the establishment success over different periods, the expected success of sequential invasions is larger then that of simultaneous invasions and we study the effects of environmental fluctuations on the extinction probability of small populations and metapopulations. The results can easily be generalized to other offspring distributions than the Poisson.     

Evolution under Fluctuating Environments Explains Observed Robustness in Metabolic Networks

A high level of robustness against gene deletion is observed in many organisms. However, it is still not clear which biochemical features underline this robustness and how these are acquired during evolution. One hypothesis, specific to metabolic networks, is that robustness emerges as a byproduct of selection for biomass production in different environments. To test this hypothesis we performed evolutionary simulations of metabolic networks under stable and fluctuating environments. We find that networks evolved under the latter scenario can better tolerate single gene deletion in specific environments. Such robustness is underlined by an increased number of independent fluxes and multifunctional enzymes in the evolved networks. Observed robustness in networks evolved under fluctuating environments was “apparent,” in the sense that it decreased significantly as we tested effects of gene deletions under all environments experienced during evolution. Furthermore, when we continued evolution of these networks under a stable environment, we found that any robustness they had acquired was completely lost. These findings provide evidence that evolution under fluctuating environments can account for the observed robustness in metabolic networks. Further, they suggest that organisms living under stable environments should display lower robustness in their metabolic networks, and that robustness should decrease upon switching to more stable environments.     

Memory and Fitness Optimization of Bacteria under Fluctuating Environments

Bacteria prudently regulate their metabolic phenotypes by sensing the availability of specific nutrients, expressing the required genes for their metabolism, and repressing them after specific metabolites are depleted. It is unclear, however, how genetic networks maintain and transmit phenotypic states between generations under rapidly fluctuating environments. By subjecting bacteria to fluctuating carbon sources (glucose and lactose) using microfluidics, we discover two types of non-genetic memory in Escherichia coli and analyze their benefits. First, phenotypic memory conferred by transmission of stable intracellular lac proteins dramatically reduces lag phases under cyclical fluctuations with intermediate timescales (1–10 generations). Second, response memory, a hysteretic behavior in which gene expression persists after removal of its external inducer, enhances adaptation when environments fluctuate over short timescales (<1 generation). Using a mathematical model we analyze the benefits of memory across environmental fluctuation timescales. We show that memory mechanisms provide an important class of survival strategies in biology that improve long-term fitness under fluctuating environments. These results can be used to understand how organisms adapt to fluctuating levels of nutrients, antibiotics, and other environmental stresses.     

Difference Inadaptive Dispersal Ability Can Promote Species Coexistence in Fluctuating Environments

Theories and empirical evidence suggest that random dispersal of organisms promotes species coexistence in spatially structured environments. However, directed dispersal, where movement is adjusted with fitness-related cues, is less explored in studies of dispersal-mediated coexistence. Here, we present a metacommunity model of two consumers exhibiting directed dispersal and competing for a single resource. Our results indicated that directed dispersal promotes coexistence through two distinct mechanisms, depending on the adaptiveness of dispersal. Maladaptive directed dispersal may promote coexistence similar to random dispersal. More importantly, directed dispersal is adaptive when dispersers track patches of increased resources in fluctuating environments. Coexistence is promoted under increased adaptive dispersal ability of the inferior competitor relative to the superior competitor. This newly described dispersal-mediated coexistence mechanism is likely favored by natural selection under the trade-off between competitive and adaptive dispersal abilities.     

Seasonal Periodicity in Lacustrine Phytoplankton and the Theory of Ecological Succession

An attempt has been made to examine the extent to which seasonal periodicity of lacustrine phytoplankton corresponds to the general concepts of the theory of ecological succession. The study was carried out on an eutrophic lake (Aydat, France). As REYNOLDS (1980, 1984) suggests, the seasonal periodicity of phytoplankton is an autogenic succession which may be perturbed by allogenic physical processes that change the initial direction of the succession. Thus, in this lake, only spring succession of phytoplankton can be considered as a true succession, consistent with the theory of ecological succession in that it was a directional and predictable phenomenon leading to an increasing complexity of community.     

The Evolution of Canalization and Evolvability in Stable and Fluctuating Environments

Using a multilinear model of epistasis we explore the evolution of canalization (reduced mutational effects) and evolvability (levels of additive genetic variance) under different forms of stabilizing and fluctuating selection. We show that the total selection acting on an allele can be divided into a component deriving from adaptation of the trait mean, a component of canalizing selection favoring alleles that epistatically reduce the effects of other allele substitutions, and a component of conservative selection disfavoring rare alleles. While canalizing selection operates in both stable and fluctuating environments, it may not typically maximize canalization, because it gets less efficient with increasing canalization, and reaches a balance with drift, mutation and indirect selection. Fluctuating selection leads to less canalized equilibria than stabilizing selection of comparable strength, because canalization then becomes influenced by erratic correlated responses to shifting trait adaptation. We conclude that epistatic systems under bounded fluctuating selection will become less canalized than under stabilizing selection and may support moderately increased evolvability if the amplitude of fluctuations is large, but canalization is still stronger and evolvability lower than expected under neutral evolution or under patterns of selection that shift the trait in directions of positive (reinforcing) epistasis.     

Fluctuating Environments Maintain Genetic Diversity through Neutral Fitness Effects and Balancing Selection

Genetic variation is the raw material upon which selection acts. The majority of environmental conditions change over time and therefore may result in variable selective effects. How temporally fluctuating environments impact the distribution of fitness effects and in turn population diversity is an unresolved question in evolutionary biology. Here, we employed continuous culturing using chemostats to establish environments that switch periodically between different nutrient limitations and compared the dynamics of selection to static conditions. We used the pooled Saccharomyces cerevisiae haploid gene deletion collection as a synthetic model for populations comprising thousands of unique genotypes. Using barcode sequencing, we find that static environments are uniquely characterized by a small number of high-fitness genotypes that rapidly dominate the population leading to dramatic decreases in genetic diversity. By contrast, fluctuating environments are enriched in genotypes with neutral fitness effects and an absence of extreme fitness genotypes contributing to the maintenance of genetic diversity. We also identified a unique class of genotypes whose frequencies oscillate sinusoidally with a period matching the environmental fluctuation. Oscillatory behavior corresponds to large differences in short-term fitness that are not observed across long timescales pointing to the importance of balancing selection in maintaining genetic diversity in fluctuating environments. Our results are consistent with a high degree of environmental specificity in the distribution of fitness effects and the combined effects of reduced and balancing selection in maintaining genetic diversity in the presence of variable selection.     

Effects of Fluctuating Temperature on Germination and Emergence of Seeds in Different Moisture Environments

Seeds of calabrese and carrot were sown in soil at differentmoisture contents or were germinated in polyethylene glycolsolution of equivalent water potential. The seeds were alsosubjected to temperature environments which were either constant,altering at 12 h intervals, or changing smoothly and continuouslyin a daily cycle. The environments had similar mean temperatures,similar accumulated numbers of day-degrees, and the changing-temperatureenvironments had similar upper and lower temperature limits.In soil, at low and moderate moisture stress, seedlings of bothcrops emerged faster in the changing-temperature environmentsthan at constant temperature; at high moisture stress, emergenceoccurred only in the changing temperature environments. In osmoticsolutions, germination (radicle emergence) of calabrese seedswas faster in changing-temperature environments, but germinationof carrot seeds was unaffected by the temperature treatments.The results indicate that interaction between moisture stressand temperature environment is important and that results ofexperiments run at both constant moisture stress and constanttemperature together may not relate directly to the field situation.     

Developmental Stability of DROSOPHILA MELANOGASTER under Artificial and Natural Selection in Constant and Fluctuating Environments

Populations of Drosophila melanogaster in constant 25° and fluctuating 20/29° environments showed increases in developmental stability, indicated by decreases in bilateral asymmetry of sterno-pleural chaeta number. In both environments, rates of decrease in asymmetry were greater under natural selection (control lines) than under artificial stabilizing selection. Overall mean asymmetry was greater in the fluctuating environment.—There was no evidence that decreased asymmetry was due to heterozygosity, and the decline in asymmetry was not explained by the decline in chaeta number in the lines under only natural selection. However, the decline was consistent with changes in total phenotypic variance and environmental variance.—The divergence between lines after 39 generations of selection was seen in differences in asymmetry and also in the genotype-environment interaction expressed in cross-culturing experiments.     

Sporadic Disturbances in Fluctuating Coral Reef Environments: El Nino and Coral Reef Development in the Eastern Pacific

The disastrous effects of the intense 1982–83 El Niño-SouthernOscillation (ENSO) bring new insight into the long-term developmentof eastern Pacific coral reefs. The 1988–83 ENSO sea surfacewarming event caused extensive reef coral bleaching (loss ofsymbiotic zooxanthellae), resulting in up to 70–95% coralmortality on reefs in Costa Rica, Panama, Colombia and Ecuador.In the Galapagos Islands (Ecuador), most coral reefs experienced>95% coral mortality. Also, several coral species experiencedextreme reductions in population size, and local and regionalextinctions. The El Niño event spawned secondary disturbances,such as increased predation and bioerosion, that continue toimpact reef-building corals. The death of Pocillopora colonieswith their crustacean guards eliminated coral barriers now allowingthe corallivore Acanthaster planci access to formerly protectedcoral prey. Sea urchins and other organisms eroded disturbedcorals at rates that exceed carbonate production, potentiallyresulting in the elimination of existing reef buildups. In otherreefbuilding regions following extensive, catastrophic coralmortality, rapid recovery often occurs through the growth ofsurviving corals, recruitment of new corals from nearby sourcepopulations, and survival of consolidated reef surfaces. Inthe eastern Pacific, however, the return of upwelling conditionsand the survival of coral predators and bioeroders hamper coralreef recovery by reducing recruitment success and eroding coralreef substrates. Thus, coral reef growth that occurs betweendisturbance events is not conserved. Repeated El Niñodisturbances, which have occurred throughout the recent geologichistory of the eastern Pacific, prevent coral communities fromincreasing in diversity and limit the development and persistenceof significant reef features. The poor development of easternPacific coral reefs throughout Holocene and perhaps much ofPleistocene time may result from recurrent thermal disturbancesof the intensity of the 1982–83 El Niño event.     

Herbivores and the Spatial Distributions of the Phytoplankton. II. Estimating Grazing in Planktonic Environments

Large errors are made when laboratory measurements of the ingestion rate of herbivorous zoo-plankton are used to estimate grazing in planktonic environments. The errors arise because the spatial heterogeneity in natural plankton distributions is greater than the heterogeneity present in laboratory experiments. Two probability models are developed for extrapolating laboratory measurements of ingestion to planktonic environments. Both models require sample statistics of the plankton distributions, and these are estimated from sampling studies of the small scale distribution of marine plankton. One model predicts laboratory measurements overestimate the ration obtained by an individual copepod by 30 %. A second model predicts errors exceeding ±50 % are possible when laboratory measurements are used to estimate the grazing by a population of cope-pods.