Complex population dynamics in microbial systems

The study of spatial and temporal population dynamics has a long history in ecology, going back to the beginning of the 1900´s. Both intrinsic and extrinsic mechanisms are involved in determining the temporal and spatial occurrences of populations and species. Different dynamic patterns result from the strength and the interplay of the two mechanisms. The fact that in-trinsic driven population dynamics are woven together with extrinsic, often stochastic dynamics makes analyses of intrinsic mechanisms difficult and led to a controversial discussion about the relevance in nature. However, there is a gap between results from mathematical modelling showing the occurrence and meaning of intrinsically driven dynamics, and empirical proves. Recently, laboratory experiments under clearly defined and controlled conditions were shown to be a suitable tool to study intrinsic, deterministic population dynam-ics. Deterministic chaos is one type of dynamic behaviour exhibited by a change in one or more intrinsic parameters beside extinction, damped oscil-lations, and stable limit cycle. Most discussed is the relevance of chaotic be-haviour in population dynamics, due to the fact that empirical evidence is lim-ited to a simple one-species system. Furthermore, chaotic fluctuations are thought to lead to extinction of a population, because chaotic dynamics can obtain very small population sizes, even more vulnerable when mixed together with stochastic events. The question, if chaos occurs in the real world and under which circumstances chaos may be found in nature, is still open. Clearly defined laboratory experiments were established to analyse intrinsically driven dynamics in a multi-species system. Different dynamic behaviours were found in chemostat experiments with a two-prey-one-predator system of a bacterivorous ciliate as the predator and two bacteria strains as the prey organisms. The different population dynamics - extinction, damped oscillations, stable limit cycles and chaos - were triggered by a change in the dilution rate of the chemostat system and verified by calculations of the corresponding Lyapunov exponents. Therewith, chaos was shown in an experimental three-species system for the first time. The different dynamics in the microbial food web revealed a surprisingly short transition (4-7 days) to a different dynamic behaviour when the dilution rate as the control parameter was changed. All dynamics persisted in experiments when different local populations with different dynamics (chemostats with different dilution rates) were coupled. Experiments showed that the dynamic behaviours of the coupled populations were only triggered by the demographic parameter � in this case the dilution rate - and reacted independent of the constant inflow of organisms from populations with different dynamics. Here, we were able to shed more light on the question about the relevance of chaos in the real world. In conclusion spatio-temporal chaos might be more common in nature than generally assumed. Microbial communities with fast reproduction rates might be favoured candidates to show chaos and other complex dynamics in nature. Intrinsically driven dynamics might be persistent when perturbated by a constant fluctuating inflow of organisms and might lead to the establishment of chaos in habitats with constant flows (e.g. aquatic organisms in rivers and oceanic currents, and water drainage to groundwater). The fast transition to a different dynamic behaviour after a change in a control parameter shows how distinct intrinsic driven processes might be. A reason why chaotic dynamics in nature are not observed might be due too the large sampling intervals in most field studies

Co-evolution as an important component explaining microbial predator-prey interaction

Predator-prey relationships belong to the most important and well-studied ecological interactions in nature. Understanding the underlying mechanisms is important to predict community dynamics and to estimate coexistence probability. Historically, evolution has been considered to be too slow to affect such ecological interactions. However, evolution can occur within ecological time scales, potentially affecting predator-prey communities. In an antagonistic pair-wise relationship the prey might evolve to minimize the effect caused by the predator (e.g. mortality), while the predator might evolve to maximize the effect (e.g. food intake). Evolution of one of the species or even co-evolution of both species in predator-prey relationships is often difficult to estimate from population dynamics without measuring of trait changes in predator and/or prey population. Particularly in microbial systems, where microorganisms evolve quickly, determining whether co-evolution occurs in predator-prey systems is challenging. We simulate observational data using quantitative trait evolution models and show that the interaction between bacteria and ciliates can be best explained as a co-evolutionary process, where both the prey and predator evolve. Evolution by prey alone explains the data less well, whereas the models with predator evolution alone or no evolution are both failing. We conclude that that ecology and evolution both interact in shaping community dynamics in microcosms. Ignoring the contribution of evolution might lead to incorrect conclusions.Peer reviewe

Effect of mutation supply on population dynamics and trait evolution in an experimental microbial community

Mutation supply can influence evolutionary and thereby ecological dynamics in important ways which have received little attention. Mutation supply influences features of population genetics, such as the pool of adaptive mutations, evolutionary pathways and importance of processes, such as clonal interference. The resultant trait evolutionary dynamics, in turn, can alter population size and species interactions. However, controlled experiments testing for the importance of mutation supply on rapid adaptation and thereby population and community dynamics have primarily been restricted to the first of these aspects. To close this knowledge gap, we performed a serial passage experiment with wild-type Pseudomonas fluorescens and a mutant with reduced mutation rate. Bacteria were grown at two resource levels in combination with the presence of a ciliate predator. A higher mutation supply enabled faster adaptation to the low-resource environment and anti-predatory defence. This was associated with higher population size at the ecological level and better access to high-recurrence mutational targets at the genomic level with higher mutation supply. In contrast, mutation rate did not affect growth under high-resource level. Our results demonstrate that intrinsic mutation rate influences population dynamics and trait evolution particularly when population size is constrained by extrinsic conditions.Peer reviewe

Dynamical trade-offs arise from antagonistic coevolution and decrease intraspecific diversity

Trade-offs play an important role in evolution. Without trade-offs, evolution would maximize fitness of all traits leading to a "master of all traits". The shape of trade-offs has been shown to determine evolutionary trajectories and is often assumed to be static and independent of the actual evolutionary process. Here we propose that coevolution leads to a dynamical trade-off. We test this hypothesis in a microbial predator-prey system and show that the bacterial growth-defense trade-off changes from concave to convex, i.e., defense is effective and cheap initially, but gets costly when predators coevolve. We further explore the impact of such dynamical trade-offs by a novel mathematical model incorporating de novo mutations for both species. Predator and prey populations diversify rapidly leading to higher prey diversity when the trade-off is concave (cheap). Coevolution results in more convex (costly) trade-offs and lower prey diversity compared to the scenario where only the prey evolves.Peer reviewe

Repeatable ecological dynamics govern the response of experimental communities to antibiotic pulse perturbation

By exposing an experimental 34-species bacterial community to different levels of pulse antibiotic disturbance with or without immigration, the authors identify a highly repeatable community response, the magnitude of which increases with increasing antibiotic levels. In an era of pervasive anthropogenic ecological disturbances, there is a pressing need to understand the factors that constitute community response and resilience. A detailed understanding of disturbance response needs to go beyond associations and incorporate features of disturbances, species traits, rapid evolution and dispersal. Multispecies microbial communities that experience antibiotic perturbation represent a key system with important medical dimensions. However, previous microbiome studies on this theme have relied on high-throughput sequencing data from uncultured species without the ability to explicitly account for the role of species traits and immigration. Here, we serially passage a 34-species defined bacterial community through different levels of pulse antibiotic disturbance, manipulating the presence or absence of species immigration. To understand the ecological community response measured using amplicon sequencing, we combine initial trait data measured for each species separately and metagenome sequencing data revealing adaptive mutations during the experiment. We found that the ecological community response was highly repeatable within the experimental treatments, which could be attributed in part to key species traits (antibiotic susceptibility and growth rate). Increasing antibiotic levels were also coupled with an increasing probability of species extinction, making species immigration critical for community resilience. Moreover, we detected signals of antibiotic-resistance evolution occurring within species at the same time scale, leaving evolutionary changes in communities despite recovery at the species compositional level. Together, these observations reveal a disturbance response that presents as classic species sorting, but is nevertheless accompanied by rapid within-species evolution.Peer reviewe

Strong selection and high mutation supply characterize experimental Chlorovirus evolution

Characterizing how viruses evolve expands our understanding of the underlying fundamental processes, such as mutation, selection and drift. One group of viruses whose evolution has not yet been extensively studied is the Phycodnaviridae, a globally abundant family of aquatic large double-stranded (ds)DNA (dsDNA) viruses. Here we studied the evolutionary change of Paramecium bursaria chlorella virus 1 during experimental coevolution with its algal host. We used pooled genome sequencing of six independently evolved populations to characterize genomic change over five time points. Across six experimental replicates involving either strong or weak demographic fluctuations, we found single nucleotide polymorphisms (SNPs) at sixty-seven sites. The occurrence of genetic variants was highly repeatable, with just two of the SNPs found in only a single experimental replicate. Three genes A122/123R, A140/145R and A540L showed an excess of variable sites, providing new information about potential targets of selection during Chlorella–Chlorovirus coevolution. Our data indicated that the studied populations were not mutation-limited and experienced strong positive selection. Our investigation highlighted relevant processes governing the evolution of aquatic large dsDNA viruses, which ultimately contributes to a better understanding of the functioning of natural aquatic ecosystems

Predator coevolution and prey trait variability determine species coexistence

Predation is one of the key ecological mechanisms allowing species coexisence and influencing biological diversity. However, ecological processes are subject to contemporary evolutionary change, and the degree to which predation affects diversity ultimately depends on the interplay between evolution and ecology. Furthermore, ecological interactions that influence species coexistence can be altered by reciprocal coevolution especially in the case of antagonistic interactions such as predation or parasitism. Here we used an experimental evolution approach to test for the role of initial trait variation in the prey population and coevolutionary hisory of the predator in the ecological dynamics of a two-species bacterial community predated by a ciliate. We found that initial trait variation both at the bacterial and ciliate level enhanced species coexistence, and that subsequent trait evolutionary trajectories depended on the initial genetic diversity present in the population. Our findings provide further support to the notion that the ecology-centric view of diversity maintenance must be reinvestigated in light of recent findings in the field of eco-evolutionary dynamics.Peer reviewe

Rapid contemporary evolution and clonal food web dynamics

Character evolution that affects ecological community interactions often occurs contemporaneously with temporal changes in population size, potentially altering the very nature of those dynamics. Such eco-evolutionary processes may be most readily explored in systems with short generations and simple genetics. Asexual and cyclically parthenogenetic organisms such as microalgae, cladocerans, and rotifers, which frequently dominate freshwater plankton communities, meet these requirements. Multiple clonal lines can coexist within each species over extended periods, until either fixation occurs or a sexual phase reshuffles the genetic material. When clones differ in traits affecting interspecific interactions, within-species clonal dynamics can have major effects on the population dynamics. We first consider a simple predator-prey system with two prey genotypes, parameterized with data on a well-studied experimental system, and explore how the extent of differences in defense against predation within the prey population determine dynamic stability versus instability of the system. We then explore how increased potential for evolution affects the community dynamics in a more general community model with multiple predator and multiple prey genotypes. These examples illustrate how microevolutionary "details" that enhance or limit the potential for heritable phenotypic change can have significant effects on contemporaneous community-level dynamics and the persistence and coexistence of species.Comment: 30 pages, 6 Figure

New insights and trends in undergraduate research: evidence from Jordan

Quality-filtered VCF file for treatment-replicate 2BV-II

Dual-stressor selection alters eco-evolutionary dynamics in experimental communities

Recognizing when and how rapid evolution drives ecological change is fundamental for our understanding of almost all ecological and evolutionary processes such as community assembly, genetic diversification and the stability of communities and ecosystems. Generally, rapid evolutionary change is driven through selection on genetic variation and is affected by evolutionary constraints, such as tradeoffs and pleiotropic effects, all contributing to the overall rate of evolutionary change. Each of these processes can be influenced by the presence of multiple environmental stressors reducing a population's reproductive output. Potential consequences of multistressor selection for the occurrence and strength of the link from rapid evolution to ecological change are unclear. However, understanding these is necessary for predicting when rapid evolution might drive ecological change. Here we investigate how the presence of two stressors affects this link using experimental evolution with the bacterium Pseudomonas fluorescens and its predator Tetrahymena thermophila. We show that the combination of predation and sublethal antibiotic concentrations delays the evolution of anti-predator defence and antibiotic resistance compared with the presence of only one of the two stressors. Rapid defence evolution drives stabilization of the predator-prey dynamics but this link between evolution and ecology is weaker in the two-stressor environment, where defence evolution is slower, leading to less stable population dynamics. Tracking the molecular evolution of whole populations over time shows further that mutations in different genes are favoured under multistressor selection. Overall, we show that selection by multiple stressors can significantly alter eco-evolutionary dynamics and their predictability.Peer reviewe