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Prey evolution on the time scale of predator-prey dynamics revealed by allele-specific quantitative PCR.

ABSTRACT: Using rotifer-algal microcosms, we tracked rapid evolution resulting from temporally changing natural selection in ecological predator-prey dynamics. We previously demonstrated that predator-prey oscillations in rotifer-algal laboratory microcosms are qualitatively altered by the presence of genetic variation within the prey. In that study, changes in algal gene frequencies were inferred from their effects on population dynamics but not observed directly. Here, we document rapid prey evolution in this system by directly observing changes in Chlorella vulgaris genotype frequencies as the abundances of these algae and their consumer, Brachionus calyciflorus, change through time. We isolated a group of algal clones that we could distinguish by using microsatellite-DNA markers, and developed an allele-specific quantitative PCR technique (AsQ-PCR) to quantify the frequencies of pairs of clones in mixed culture. We showed that two of these genotypes exhibited a fitness tradeoff in which one was more resistant to predation (more digestion-resistant), and the other had faster population growth under limiting nitrogen concentrations. A fully specified mathematical model for the rotifer-algal population and evolutionary dynamics predicted that these two clones would undergo a single oscillation in clonal frequencies followed by asymptotic fixation of the more resistant clone, rather than the recurrent oscillations previously observed with other algal clones. We used AsQ-PCR to confirm this prediction: the superior competitor dominated initially, but as rotifer densities increased, the more predator-resistant clone predominated.

SUBMITTER: Meyer JR

PROVIDER: S-EPMC1502293 | biostudies-literature | 2006 Jul

REPOSITORIES: biostudies-literature

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Prey evolution on the time scale of predator-prey dynamics revealed by allele-specific quantitative PCR.

Meyer Justin R JR Ellner Stephen P SP Hairston Nelson G NG Jones Laura E LE Yoshida Takehito T

Proceedings of the National Academy of Sciences of the United States of America 20060628 28

Using rotifer-algal microcosms, we tracked rapid evolution resulting from temporally changing natural selection in ecological predator-prey dynamics. We previously demonstrated that predator-prey oscillations in rotifer-algal laboratory microcosms are qualitatively altered by the presence of genetic variation within the prey. In that study, changes in algal gene frequencies were inferred from their effects on population dynamics but not observed directly. Here, we document rapid prey evolution i ...[more]

PMID: 16807296

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Project description:The dynamic nature of the SIV population during disease progression in the SIV/macaque model of AIDS and the factors responsible for its behavior have not been documented, largely owing to the lack of sufficient spatial and temporal sampling of both viral and host data from SIV-infected animals. In this study, we detail Bayesian coalescent inference of the changing collective intra-host viral effective population size (Ne ) from various tissues over the course of infection and its relationship with what we demonstrate is a continuously changing immune cell repertoire within the blood. Although the relative contribution of these factors varied among hosts and time points, the adaptive immune response best explained the overall periodic dynamic behavior of the effective virus population. Data exposing the nature of the relationship between the virus and immune cell populations revealed the plausibility of an eco-evolutionary mathematical model, which was able to mimic the large-scale oscillations in Ne through virus escape from relatively few, early immunodominant responses, followed by slower escape from several subdominant and weakened immune populations. The results of this study suggest that SIV diversity within the untreated host is governed by a predator-prey relationship, wherein differing phases of infection are the result of adaptation in response to varying immune responses. Previous investigations into viral population dynamics using sequence data have focused on single estimates of the effective viral population size (Ne ) or point estimates over sparse sampling data to provide insight into the precise impact of immune selection on virus adaptive behavior. Herein, we describe the use of the coalescent phylogenetic frame- work to estimate the relative changes in Ne over time in order to quantify the relationship with empirical data on the dynamic immune composition of the host. This relationship has allowed us to expand on earlier simulations to build a predator-prey model that explains the deterministic behavior of the virus over the course of disease progression. We show that sequential viral adaptation can occur in response to phases of varying immune pressure, providing a broader picture of the viral response throughout the entire course of progression to AIDS.

Project description:Heterogeneity among prey in their susceptibility to predation is a potentially important stabilizer of predator-prey interactions, reducing the magnitude of population oscillations and enhancing total prey population abundance. When microevolutionary responses of prey populations occur at time scales comparable to population dynamics, adaptive responses in prey defense can, in theory, stabilize predator-prey dynamics and reduce top-down effects on prey abundance. While experiments have tested these predictions, less explored are the consequences of the evolution of prey phenotypes that can persist in both vulnerable and invulnerable classes. We tested this experimentally using a laboratory aquatic system composed of the rotifer Brachionus calyciflorus as a predator and the prey Synura petersenii, a colony-forming alga that exhibits genetic variation in its propensity to form colonies and colony size (larger colonies are a defense against predators). Prey populations of either low initial genetic diversity and low adaptive capacity or high initial genetic diversity and high adaptive capacity were crossed with predator presence and absence. Dynamics measured over the last 127 days of the 167-day experiment revealed no effects of initial prey genetic diversity on the average abundance or temporal variability of predator populations. However, genetic diversity and predator presence/absence interactively affected prey population abundance and stability; diversity of prey had no effects in the absence of predators but stabilized dynamics and increased total prey abundance in the presence of predators. The size structure of the genetically diverse prey populations diverged from single strain populations in the presence of predators, showing increases in colony size and in the relative abundance of cells found in colonies. Our work sheds light on the adaptive value of colony formation and supports the general view that genetic diversity and intraspecific trait variation of prey can play a vital role in the short-term dynamics and stability of planktonic predator-prey systems.

Dataset Information

Prey evolution on the time scale of predator-prey dynamics revealed by allele-specific quantitative PCR.

Publications

Prey evolution on the time scale of predator-prey dynamics revealed by allele-specific quantitative PCR.

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