Red Queen Dynamics Research Articles

The Red Queen theory of recombination hotspots

Recombination hotspots are small chromosomal regions, where meiotic crossover events happen with high frequency. Recombination is initiated by a double-strand break (DSB) that requires the intervention of the molecular repair mechanism. The DSB repair mechanism may result in the exchange of homologous chromosomes (crossover) and the conversion of the allelic sequence that breaks into the one that does not break (biased gene conversion). Biased gene conversion results in a transmission advantage for the allele that does not break, thus preventing recombination and rendering recombination hotspots transient. How is it possible that recombination hotspots persist over evolutionary time (maintaining the average chromosomal crossover rate) when they are self-destructive? This fundamental question is known as the recombination hotspot paradox and has attracted much attention in recent years. Yet, that attention has not translated into a fully satisfactory answer. No existing model adequately explains all aspects of the recombination hotspot paradox. Here, we formulate an intragenomic conflict model resulting in Red Queen dynamics that fully accounts for all empirical observations regarding the molecular mechanisms of recombination hotspots, the nonrandom targeting of the recombination machinery to hotspots and the evolutionary dynamics of hotspot turnover.

IMPACT OF BACTERIAL MUTATION RATE ON COEVOLUTIONARY DYNAMICS BETWEEN BACTERIA AND PHAGES

Mutator bacteria are frequently found in natural populations of bacteria and although coevolution with parasitic viruses (phages) is thought to be one reason for their persistence, it remains unclear how the presence of mutators affects coevolutionary dynamics. We hypothesized that phages must themselves adapt more rapidly or go extinct, in the face of rapidly evolving mutator bacteria. We compared the coevolutionary dynamics of wild-type Pseudomonas fluorescens SBW25 with a lytic phage to the dynamics of an isogenic mutator of P. fluorescens SBW25 together with the same phage. At the beginning of the experiment both wild-type bacteria and mutator bacteria coevolved with phages. However, mutators rapidly evolved higher levels of sympatric resistance to phages. The phages were unable to "keep-up" with the mutator bacteria, and these rates of coevolution declined to less than the rates of coevolution between the phages and wild-type bacteria. By the end of the experiment, the sympatric resistance of the mutator bacteria was not significantly different to the sympatric resistance of the wild-type bacteria. This suggests that the importance of mutators in the coevolutionary interactions with a particular phage population is likely to be short-lived. More generally, the results demonstrate that coevolving enemies may escape from Red-Queen dynamics.

Chaotic Red Queen coevolution in three-species food chains

Coevolution between two antagonistic species follows the so-called 'Red Queen dynamics' when reciprocal selection results in an endless series of adaptation by one species and counteradaptation by the other. Red Queen dynamics are 'genetically driven' when selective sweeps involving new beneficial mutations result in perpetual oscillations of the coevolving traits on the slow evolutionary time scale. Mathematical models have shown that a prey and a predator can coevolve along a genetically driven Red Queen cycle. We found that embedding the prey-predator interaction into a three-species food chain that includes a coevolving superpredator often turns the genetically driven Red Queen cycle into chaos. A key condition is that the prey evolves fast enough. Red Queen chaos implies that the direction and strength of selection are intrinsically unpredictable beyond a short evolutionary time, with greatest evolutionary unpredictability in the superpredator. We hypothesize that genetically driven Red Queen chaos could explain why many natural populations are poised at the edge of ecological chaos. Over space, genetically driven chaos is expected to cause the evolutionary divergence of local populations, even under homogenizing environmental fluctuations, and thus to promote genetic diversity among ecological communities over long evolutionary time.

Fine-Tuning Translation Kinetics Selection as the Driving Force of Codon Usage Bias in the Hepatitis A Virus Capsid

Hepatitis A virus (HAV), the prototype of genus Hepatovirus, has several unique biological characteristics that distinguish it from other members of the Picornaviridae family. Among these, the need for an intact eIF4G factor for the initiation of translation results in an inability to shut down host protein synthesis by a mechanism similar to that of other picornaviruses. Consequently, HAV must inefficiently compete for the cellular translational machinery and this may explain its poor growth in cell culture. In this context of virus/cell competition, HAV has strategically adopted a naturally highly deoptimized codon usage with respect to that of its cellular host. With the aim to optimize its codon usage the virus was adapted to propagate in cells with impaired protein synthesis, in order to make tRNA pools more available for the virus. A significant loss of fitness was the immediate response to the adaptation process that was, however, later on recovered and more associated to a re-deoptimization rather than to an optimization of the codon usage specifically in the capsid coding region. These results exclude translation selection and instead suggest fine-tuning translation kinetics selection as the underlying mechanism of the codon usage bias in this specific genome region. Additionally, the results provide clear evidence of the Red Queen dynamics of evolution since the virus has very much evolved to re-adapt its codon usage to the environmental cellular changing conditions in order to recover the original fitness.

Red Queen Dynamics with Non-Standard Fitness Interactions

Antagonistic coevolution between hosts and parasites can involve rapid fluctuations of genotype frequencies that are known as Red Queen dynamics. Under such dynamics, recombination in the hosts may be advantageous because genetic shuffling can quickly produce disproportionately fit offspring (the Red Queen hypothesis). Previous models investigating these dynamics have assumed rather simple models of genetic interactions between hosts and parasites. Here, we assess the robustness of earlier theoretical predictions about the Red Queen with respect to the underlying host-parasite interactions. To this end, we created large numbers of random interaction matrices, analysed the resulting dynamics through simulation, and ascertained whether recombination was favoured or disfavoured. We observed Red Queen dynamics in many of our simulations provided the interaction matrices exhibited sufficient ‘antagonicity’. In agreement with previous studies, strong selection on either hosts or parasites favours selection for increased recombination. However, fast changes in the sign of linkage disequilibrium or epistasis were only infrequently observed and do not appear to be a necessary condition for the Red Queen hypothesis to work. Indeed, recombination was often favoured even though the linkage disequilibrium remained of constant sign throughout the simulations. We conclude that Red Queen-type dynamics involving persistent fluctuations in host and parasite genotype frequencies appear to not be an artefact of specific assumptions about host-parasite fitness interactions, but emerge readily with the general interactions studied here. Our results also indicate that although recombination is often favoured, some of the factors previously thought to be important in this process such as linkage disequilibrium fluctuations need to be reassessed when fitness interactions between hosts and parasites are complex.

The 30th anniversary of quasispecies

The meeting on ‘Quasispecies: past, present and future’ took place between 17 and 18 November 2008, in Barcelona, Spain, and was organized by J. Gomez, C. Lopez‐Galindez, M.A. Martinez & A. Mas. ![][1] A meeting was held in Barcelona, Spain, in November 2008 to celebrate the 30th anniversary of the publication of the article that described the extensive genetic heterogeneity of bacteriophage Qβ (Domingo et al , 1978), which is considered to mark the beginning of experimental studies on viral quasispecies. This meeting was held at the impressive fifteenth century building of the ancient Hospital de la Santa Creu in the old town of Barcelona, which is now the headquarters of the Institut d'Estudis Catalans, and was attended by C. Weissmann (Jupiter, FL, USA), M. Billeter (Zurich, Switzerland) and E. Domingo (Madrid, Spain), who were three early protagonists of the phage Qβ work at the University of Zurich in the 1970s. Several speakers presented their results on the theoretical aspects of the population dynamics of cells and viruses, the clinical implications of quasispecies, and extensions of the quasispecies concept to cellular genes and prions. The meeting was introduced by A. Mas (Albacete, Spain), who reflected on the increasing impact that quasispecies have had in the scientific literature over the past three decades, and quoted some of the key references on viral quasispecies (Martell et al , 1992; Meyerhans et al , 1989; Najera et al , 1995; Vignuzzi et al , 2006; for a historical review of the impact of quasispecies in virology, see Holland, 2006). The scientific presentations were opened by Weissmann and Domingo, who were the last and first authors of the 1978 paper, respectively. Their talks conveyed the scientific atmosphere of the 1970s—when molecular biology was carried out with few recombinant‐DNA techniques—to a young audience. Nucleic‐acid sequencing was in … [1]: /embed/graphic-1.gif

Small worlds and Red Queens in the Global Workspace: An information-theoretic approach

Networks of small worlds and Red Queen dynamic structures as analytic-descriptive methods are ubiquitous in expanding areas of research in the cognitive neurosciences, sociopsychological systems and parallel machine cognition. In the setting of the Baars Global Workspace theory, we apply a semantically oriented information-theoretic mechanism, making use of the Onsager relations of statistical physics and the geometry of associated networks. For such networks attention is paid to the concept of dynamic groupoids, their symmetries and other properties. In the case of structural networks influenced by the orbit equivalence relations of a groupoid action, we describe how crosstalk, the emergence of subnetwork giant components and noise induced opportunities contribute to the structure of small world networks and Red Queen dynamics. We create some dynamic models and show how these systems can be formally encapsulated within the idea of a groupoid atlas. Further, we utilize specific geometrical methods to describe the formation of geodesics in the corresponding networks, and include the holonomy concept as providing a geometric representation associated with a phase transition.

THE COST OF BEING COMMON: EVIDENCE FROM NATURALDAPHNIAPOPULATIONS

The Red Queen coevolutionary hypothesis predicts that parasites drive oscillations in host genotype frequencies due to frequency-dependent selection where common hosts are at disadvantage. However, examples of this phenomenon in natural populations are scarce. To examine if the Red Queen theory operates in the wild, we studied the genetic structure of populations of the crustacean waterflea (Daphnia), in relation to their infection levels, for which we collected multiple samples from a variety of lakes. The most common clone in a given population was often underinfected. This advantage, however, did not remain stable over time. Instead, the most common clone decreased in frequency over subsequent generations, indicating that parasites can track common clones. Such decreases were not observed in uninfected populations. Moreover, host clonal evenness was higher across the set of infected lakes compared to uninfected lakes; suggesting that any common clone is selected against when parasites are present. These results strongly suggest that Red Queen dynamics do operate in the wild.

The Red Queen revisited: reevaluating the age selectivity of Phanerozoic marine genus extinctions

Extinction risk is inversely related to genus age (time since first appearance) in most intervals of the Phanerozoic marine fossil record, in apparent contradiction to the macroevolutionary Red Queen's Hypothesis, which posits that extinction risk is independent of taxon age. Age-dependent increases in the mean species richness and geographic range of genera have been invoked to reconcile this genus-level observation with the presumed prevalence of Red Queen dynamics at the species level. Here we test these explanations with data from the Paleobiology Database. Multiple logistic regression demonstrates that the association of extinction risk with genus age is not adequately explained by species richness or geographic range: there is a residual association between age and extinction risk even when range and richness effects are accounted for. Throughout most of the Phanerozoic the age selectivity gradient is highest among the youngest age cohorts, whereas there is no association between age and extinction risk among older age cohorts. Some of the apparent age selectivity of extinction in the global fauna is attributable to differences in extinction rate among taxonomic groups, but extinction risk declines with genus age even within most taxonomic orders. Notable exceptions to this pattern include the Cambrian-Ordovician, latest Permian, Triassic, and Paleocene intervals. The association of age with extinction risk could reflect sampling heterogeneity or taxonomic practice more than biological reality, but at present it is difficult to evaluate or correct for such biases. Alternatively, the pattern may reflect consistent extinction selectivity on some as-yet unidentified covariate of genus age. Although this latter explanation is not compatible with a Red Queen model if most genus extinctions have resulted from biological interactions, it may be applicable if most genus extinctions have instead been caused by recurrent physical disturbances that repeatedly impose similar selective pressures.

Matching allele dynamics and coevolution in a minimal predator–prey replicator model

Abstract A minimal Lotka–Volterra type predator–prey model describing coevolutionary traits among entities with a strength of interaction influenced by a pair of haploid diallelic loci is studied with a deterministic time continuous model. We show a Hopf bifurcation governing the transition from evolutionary stasis to periodic Red Queen dynamics. If predator genotypes differ in their predation efficiency the more efficient genotype asymptotically achieves lower stationary concentrations.

CHAOTIC STABILITY IN SPATIALLY-RESOLVED HOST-PARASITE REPLICATORS: THE RED QUEEN ON A LATTICE

Evolutionary patterns of change are often linked to complex coupled responses associated to predator-prey, immune system-viruses or host–parasite interactions. Under some conditions, it has been postulated that the final outcome of such interactions are oscillatory patterns of genotypic and phenotypic change, generically labeled as Red Queen dynamics (RQD). In RQD, changes occur in a changing pattern ensuring the persistence of both partners at the cost of constant changing. In this paper, we analyze the dynamics of two populations of host-parasite replicators extended on a surface considering three scenarios associated to neutral landscapes on binary hypercubes. Stochastic simulations show three asymptotic dynamic states: (i) host survival and parasite extinction, (ii) host-parasite extinction, and (iii) a stable RQD scenario able to maintain chaotic oscillations. The RQD scenario is shown to be facilitated with the increase of the genotypic diversity associated to the increase of the length of the replicators. Such diversity, jointly with the inclusion of spatial degrees of freedom and mutation, can act as a stabilizing factor.

The Red Queen and the persistence of linkage-disequilibrium oscillations in finite and infinite populations

BackgroundThe Red Queen Hypothesis (RQH) suggests that the coevolutionary dynamics of host-parasite systems can generate selection for increased host recombination. Since host-parasite interactions often have a strong genetic basis, recombination between different hosts can increase the fraction of novel and potentially resistant offspring genotypes. A prerequisite for this mechanism is that host-parasite interactions generate persistent oscillations of linkage disequilibria (LD).ResultsWe use deterministic and stochastic models to investigate the persistence of LD oscillations and its impact on the RQH. The standard models of the Red Queen dynamics exhibit persistent LD oscillations under most circumstances. Here, we show that altering the standard model from discrete to continuous time or from simultaneous to sequential updating results in damped LD oscillations. This suggests that LD oscillations are structurally not robust. We then show that in a stochastic regime, drift can counteract this dampening and maintain the oscillations. In addition, we show that the amplitude of the oscillations and therefore the strength of the resulting selection for or against recombination are inversely proportional to the size of the (host) population.ConclusionWe find that host parasite-interactions cannot generally maintain oscillations in the absence of drift. As a consequence, the RQH can strongly depend on population size and should therefore not be interpreted as a purely deterministic hypothesis.

Methodologies for testing a pluralist idea for the maintenance of sex

The paradox of sex, despite decades of attention, remains unresolved. Recent efforts to gain insight into the nature of the mechanisms underlying the maintenance of sex have led to an emphasis on a pluralist approach, with a particular focus on interaction between multiple mechanisms. However, few empirical tests of pluralist models exist, perhaps due to the widely held assumption that major complications inevitably accompany such tests. Here, we address this issue by providing an overview of how testing of a pluralist idea for the maintenance of sex could be achieved. We also suggest a more specific methodology designed to test for interactive effects between Muller’s ratchet and Red Queen dynamics, two models that are widely seen as providing potentially general explanations for the maintenance of sex. © 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 89, 605–613.

On the track of the Red Queen: bark beetles, their nematodes, local climate and geographic parthenogenesis

Geographic parthenogenesis has been explained as resulting from parasite pressure (Red Queen hypothesis): several studies have found high degrees of sexuals where the prevalence of parasites is high. However, it is important to address whether prevalence of parasites mirrors risk of infection. We explored geographic parthenogenesis of Ips acuminatus bark beetles and their nematodes. Local climate is crucial for nematode stages outside the host, in spring and summer, and prevalence should thus be associated with those temperatures if prevalence reliably reflects exposure risk across populations. This was the case; however, high prevalence of a virulent nematode species was not associated with many sexuals, whereas highly sexual populations were characterized by high infection risk of benign nematodes. Low virulence of the latter makes Red Queen dynamics unlikely. Geographical patterns of parthenogenesis were instead associated with winter temperature and variance in temperature.

Coevolution of slow–fast populations: evolutionary sliding, evolutionary pseudo-equilibria and complex Red Queen dynamics

We study the interplay of ecological and evolutionary dynamics in communities composed of populations with contrasting time-scales. In such communities, genetic variation of individual traits can cause population transitions between stationary and cyclic ecological regimes, hence abrupt variations in fitness. Such abrupt variations raise ridges in the adaptive landscape, where the populations are poised between equilibrium and cyclic coexistence and along which evolutionary trajectories can remain sliding for long times or halt at special points called evolutionary pseudo-equilibria. These novel phenomena should be generic to all systems in which ecological interactions cause fitness to vary discontinuously. They are demonstrated by the analysis of a predator-prey community, with one adaptive trait for each population. The eco-evolutionary dynamics of the system show a number of other distinctive features, including evolutionary extinction and two forms of Red Queen dynamics. One of them is characterized by intermittent bouts of cyclic oscillations of the two populations.

MODE OF TRANSMISSION, HOST SWITCHING, AND ESCAPE FROM THE RED QUEEN BY VIVIPAROUS GYRODACTYLIDS (MONOGENOIDEA)

Compared to other monogenoidean groups, viviparous gyrodactylids exhibit extraordinary species diversity and broad host range. It has been suggested that this evolutionary success is associated with a suite of morphological and life-history traits that include, in part, continuous transmission (i.e., ability to infect new hosts throughout the gyrodactylid life cycle). Experiments were conducted to explore the putative adaptive advantage of continuous transmission within viviparous gyrodactylids during colonization of new host resources. Differences in infrapopulation growth, such as abundance, prevalence, and duration of the infection, of Gyrodactylus anisopharynx on 3 species of fish--Corydoras paleatus and Corydoras ehrhardti (both natural hosts) as well as Corydoras schwartzi (a host not known to harbor G. anisopharynx)--held under isolated and grouped conditions were determined. Results showed that infrapopulations of G. anisopharynx on C. paleatus and C. schwartzi had higher growth when the parasite had the opportunity for host transfer (grouped hosts). Infrapopulations of G. anisopharynx on isolated and grouped C. ehrhardti showed an opposite trend, although differences in mean duration and maximum abundance were not statistically different. Results obtained from experiments with C. paleatus and C. schwartzi support the hypothesis that continuous transmission in viviparous gyrodactylids enhances colonization success, probably by allowing initial avoidance of Red Queen dynamics. The absence of statistical differences between infrapopulations on isolated and grouped C. ehrhardti suggests that parasite dynamics may be influenced by factors other than continuous transmission in this host.

Temperature checks the Red Queen? Resistance and virulence in a fluctuating environment

AbstractNumerous studies have revealed genetic variation in resistance and susceptibility in host–parasite interactions and therefore the potential for frequency‐dependent selection (Red Queen dynamics). Few studies, if any, have considered the abiotic environment as a mediating factor in these interactions. Using the pea aphid, Acyrthosiphon pisum, and its fungal pathogen, Erynia neoaphidis, as a model host–parasite system, we demonstrate how temperature can mediate the expression of genotypic variation for susceptibility and virulence. Whilst previous studies have revealed among‐clone variation in aphid resistance to this pathogen, we show that resistance rankings derived from assessments at one temperature, are not conserved across differing temperature regimes. We suggest that variation in environmental temperature, through its nonlinear impact on parasite virulence and host defence, may contribute to the general lack of evidence for frequency‐dependent selection in field systems.

Correlational selection and the evolution of genomic architecture

We review and discuss the importance of correlational selection (selection for optimal character combinations) in natural populations. If two or more traits subject to multivariate selection are heritable, correlational selection builds favourable genetic correlations through the formation of linkage disequilibrium at underlying loci governing the traits. However, linkage disequilibria built up by correlational selection are expected to decay rapidly (ie, within a few generations), unless correlational selection is strong and chronic. We argue that frequency-dependent biotic interactions that have 'Red Queen dynamics' (eg, host-parasite interactions, predator-prey relationships or intraspecific arms races) often fuel chronic correlational selection, which is strong enough to maintain adaptive genetic correlations of the kind we describe. We illustrate these processes and phenomena using empirical examples from various plant and animal systems, including our own recent work on the evolutionary dynamics of a heritable throat colour polymorphism in the side-blotched lizard Uta stansburiana. In particular, male and female colour morphs of side-blotched lizards cycle on five- and two-generation (year) timescales under the force of strong frequency-dependent selection. Each morph refines the other morph in a Red Queen dynamic. Strong correlational selection gradients among life history, immunological and morphological traits shape the genetic correlations of the side-blotched lizard polymorphism. We discuss the broader evolutionary consequences of the buildup of co-adapted trait complexes within species, such as the implications for speciation processes.

Red Queen Dynamics, Competition and Critical Points in a Model of RNA Virus Quasispecies

RNA viruses offer a unique opportunity for the study of evolution at the molecular level. Recent experiments involving clonal populations of RNA viruses have shown that competition among virus strains of approximately equal relative fitness can result in the eventual competitive exclusion of one of the species. As competition proceeds in time, both the winners and the losers exhibited absolute gains in fitness, consistent with the “Red Queen” hypothesis of evolution. Further experiments involving closely related evolving quasispecies revealed a highly predictable nonlinear behavior suggesting a deterministic component in the underlying quasispecies dynamics. This is apparently in contradiction with the standard view of RNA virus evolution as a highly unpredictable process. In this paper we present a simple model which allows previous hypothesis to be tested and provides an interpretation for the observed experimental results.

Three mechanisms of Red Queen dynamics

Models describing systems of coevolving populations often have asymptotically non–equilibrium dynamics (Red Queen dynamics (RQD)). We claim that if evolution is much slower than ecological changes, RQD arises due to either fast ecological processes, slow genetical processes, or to their interaction. The three corresponding generic types of RQD can be studied using singular perturbation theory and have very different properties and biological implications. We present simple examples of ecological, genetical, and ecogenetical RQD and describe how they may be recognized in natural populations. In particular, ecogenetical RQD often involve alternations of long epochs with radically different dynamics.