The probability of evolutionary rescue: towards a quantitative comparison between theory and evolution experiments

Evolutionary rescue occurs when a population genetically adapts to a new stressful environment that would otherwise cause its extinction. Forecasting the probability of persistence under stress, including emergence of drug resistance as a special case of interest, requires experimentally validated quantitative predictions. Here, we propose general analytical predictions, based on diffusion approximations, for the probability of evolutionary rescue. We assume a narrow genetic basis for adaptation to stress, as is often the case for drug resistance. First, we extend the rescue model of Orr & Unckless (Am. Nat. 2008 172, 160–169) to a broader demographic and genetic context, allowing the model to apply to empirical systems with variation among mutation effects on demography, overlapping generations and bottlenecks, all common features of microbial populations. Second, we confront our predictions of rescue probability with two datasets from experiments with Saccharomyces cerevisiae (yeast) and Pseudomonas fluorescens (bacterium). The tests show the qualitative agreement between the model and observed patterns, and illustrate how biologically relevant quantities, such as the per capita rate of rescue, can be estimated from fits of empirical data. Finally, we use the results of the model to suggest further, more quantitative, tests of evolutionary rescue theory.     

Tracking costs of virulence in natural populations of the wheat pathogen, Puccinia striiformis f.sp. tritici

Background  

Costs of adaptation play an important role in host-parasite coevolution. For parasites, evolving the ability to circumvent host resistance may trade off with subsequent growth or transmission. Such costs of virulence (sensu plant pathology) limit the spread of all-infectious genotypes and thus facilitate the maintenance of genetic polymorphism in both host and parasite. We investigated costs of three virulence factors in Puccinia striiformis f.sp. tritici, a fungal pathogen of wheat (Triticum aestivum).     

HOST GROWTH CONDITIONS INFLUENCE EXPERIMENTAL EVOLUTION OF LIFE HISTORY AND VIRULENCE OF A PARASITE WITH VERTICAL AND HORIZONTAL TRANSMISSION

In parasites with mixed modes of transmission, ecological conditions may determine the relative importance of vertical and horizontal transmission for parasite fitness. This may lead to differential selection pressure on the efficiency of the two modes of transmission and on parasite virulence. In populations with high birth rates, increased opportunities for vertical transmission may select for higher vertical transmissibility and possibly lower virulence. We tested this idea in experimental populations of the protozoan Paramecium caudatum and its bacterial parasite Holospora undulata. Serial dilution produced constant host population growth and frequent vertical transmission. Consistent with predictions, evolved parasites from this “high‐growth” treatment had higher fidelity of vertical transmission and lower virulence than parasites from host populations constantly kept near their carrying capacity (“low‐growth treatment”). High‐growth parasites also produced fewer, but more infectious horizontal transmission stages, suggesting the compensation of trade‐offs between vertical and horizontal transmission components in this treatment. These results illustrate how environmentally driven changes in host demography can promote evolutionary divergence of parasite life history and transmission strategies.     

Modelling the Dynamics of an Experimental Host-Pathogen Microcosm within a Hierarchical Bayesian Framework

The advantages of Bayesian statistical approaches, such as flexibility and the ability to acknowledge uncertainty in all parameters, have made them the prevailing method for analysing the spread of infectious diseases in human or animal populations. We introduce a Bayesian approach to experimental host-pathogen systems that shares these attractive features. Since uncertainty in all parameters is acknowledged, existing information can be accounted for through prior distributions, rather than through fixing some parameter values. The non-linear dynamics, multi-factorial design, multiple measurements of responses over time and sampling error that are typical features of experimental host-pathogen systems can also be naturally incorporated. We analyse the dynamics of the free-living protozoan Paramecium caudatum and its specialist bacterial parasite Holospora undulata. Our analysis provides strong evidence for a saturable infection function, and we were able to reproduce the two waves of infection apparent in the data by separating the initial inoculum from the parasites released after the first cycle of infection. In addition, the parameter estimates from the hierarchical model can be combined to infer variations in the parasite''s basic reproductive ratio across experimental groups, enabling us to make predictions about the effect of resources and host genotype on the ability of the parasite to spread. Even though the high level of variability between replicates limited the resolution of the results, this Bayesian framework has strong potential to be used more widely in experimental ecology.     

Ecological and genetic determinants of multiple infection and aggregation in a microbial host-parasite system

The number of parasites colonizing a host (termed 'multiple infection') is an important determinant of host-parasite interactions. In theory, multiple infection is determined by random mass action in genetically and spatially homogeneous populations of host and parasite. In real populations, deviations from these assumptions may strongly influence levels of multiple infection. We carried out inoculation experiments in microcosms of the freshwater protozoan Paramecium caudatum and its bacterial parasite Holospora undulata. Increasing parasite dose produced higher levels of (multiple) infection; more susceptible host genotypes also were more multiply infected. An overall pattern of parasite aggregation (excess of uninfected individuals and of individuals carrying larger numbers of parasites) indicated deviations from random mass-action transmission. Homogenizing spatial distributions of parasite and host in our microcosms did not affect aggregation, whereas aggregation was more pronounced in old than in new host clones. Thus, variation in susceptibility may arise over time within clonal populations. When sequentially inoculated, already established infections increased the probability of additional infection in generally resistant host clones, but decreased it in more susceptible clones. Hence, the role of multiple infection as a driver of epidemiological or evolutionary processes may vary among populations, depending on their precise genetic composition or infection history.     

Mixed inoculation alters infection success of strains of the endophyte Epichloë bromicola on its grass host Bromus erectus

Within-host competition in multiply infected hosts is considered an important component of host-parasite interactions, but experimental studies on the dynamics of multiple infections are still rare. We measured the infection frequencies of four strains of the fungal endophyte Epichloë bromicola on two genotypes of its host plant Bromus erectus after single- and double-strain inoculation. Double-strain inoculations resulted in fewer double, but more single, infections than expected on the basis of infection frequencies in single-strain inoculations. In most cases, only one of the two strains established an infection, and strains differed in their overall competitive ability. This pattern resembles the mutual exclusion scenarios in some theoretical models of parasite evolution. In addition, competitive ability varied with host genotype, which may represent a mechanism for the coexistence of strains in a population. Hence, considering the genetic variation in both host and parasite may be important for a better understanding of within-host dynamics and their role in epidemiology or (co)evolution.     

Is the Prunella (Lamiaceae) hybrid zone structured by an environmental gradient? Evidence from a reciprocaltransplant experiment

Hybrid zones may be structured by environmentally independent selection against intrinsically unfit hybrids (tension zone models), or by environmentally dependent fitness differences among parental species and hybrids (ecological selection-gradient models). A 30-m slope in a mountain grassland harbors a hybrid zone of the clonal perennials, Prunella grandiflora and P. vulgaris (Lamiaceae), with P. grandiflora in the upper, P. vulgaris in the lower, and both parental species and P. grandiflora × P. vulgaris Hybrids in a narrow middle part. We found gradients for soil depth and water content, and vegetation height and biomass along the slope. A reciprocal transplant experiment yielded crossing reaction norms for vegetative reproduction. Parental species were locally adapted to their home sites, while the three taxa did not differ in vegetative reproduction in the Hybrid transplant site. Local adaptation for vegetative reproduction of P. grandiflora was mediated through higher survival and that of P. vulgaris through higher ramet number, indicating adaptation of their clonal growth strategies (phalanx vs. guerrilla) to the different habitats. Hybrid performance was intermediate between that of the parental species in all three sites, although Hybrids flowered more often than the parental species in the Hybrid site. Our results support ecological selection-gradient rather than tension zone models.     

Quorum Sensing and Density-Dependent Dispersal in an Aquatic Model System

Many organisms use cues to decide whether to disperse or not, especially those related to the composition of their environment. Dispersal hence sometimes depends on population density, which can be important for the dynamics and evolution of sub-divided populations. But very little is known about the factors that organisms use to inform their dispersal decision. We investigated the cues underlying density-dependent dispersal in inter-connected microcosms of the freshwater protozoan Paramecium caudatum. In two experiments, we manipulated (i) the number of cells per microcosm and (ii) the origin of their culture medium (supernatant from high- or low-density populations). We found a negative relationship between population density and rates of dispersal, suggesting the use of physical cues. There was no significant effect of culture medium origin on dispersal and thus no support for chemical cues usage. These results suggest that the perception of density – and as a result, the decision to disperse – in this organism can be based on physical factors. This type of quorum sensing may be an adaptation optimizing small scale monitoring of the environment and swarm formation in open water.     

Cryopreservation of Holospora undulata, a bacterial parasite of the ciliate Paramecium caudatum

We investigated cryopreservation of horizontal transmission stages of Holospora undulata, a micronucleus-specific bacterial parasite of Paramecium caudatum. Unlike in previous studies on related Holospora species, protocols using glycerol as cryoprotectant failed entirely. In contrast, freezing with dimethyl sulfoxide (Me2SO) conserved infectiousness of nearly all replicate inocula, although infection success was considerably lower than that of fresh inocula. Infection probability was enhanced by increasing the Me2SO concentration from 5 to 10%, and by freezing at -196 degrees C rather than -80 degrees C. Prolonged storage of up to 3 months had no significant effect on the viability of the inocula.     

Stochastic environmental fluctuations drive epidemiology in experimental host–parasite metapopulations

Environmental fluctuations are important for parasite spread and persistence. However, the effects of the spatial and temporal structure of environmental fluctuations on host–parasite dynamics are not well understood. Temporal fluctuations can be random but positively autocorrelated, such that the environment is similar to the recent past (red noise), or random and uncorrelated with the past (white noise). We imposed red or white temporal temperature fluctuations on experimental metapopulations of Paramecium caudatum, experiencing an epidemic of the bacterial parasite Holospora undulata. Metapopulations (two subpopulations linked by migration) experienced fluctuations between stressful (5°C) and permissive (23°C) conditions following red or white temporal sequences. Spatial variation in temperature fluctuations was implemented by exposing subpopulations to the same (synchronous temperatures) or different (asynchronous temperatures) temporal sequences. Red noise, compared with white noise, enhanced parasite persistence. Despite this, red noise coupled with asynchronous temperatures allowed infected host populations to maintain sizes equivalent to uninfected populations. It is likely that this occurs because subpopulations in permissive conditions rescue declining subpopulations in stressful conditions. We show how patterns of temporal and spatial environmental fluctuations can impact parasite spread and host population abundance. We conclude that accurate prediction of parasite epidemics may require realistic models of environmental noise.