Sylvain Gandon

Local Adaptation and Gene-For-Gene Coevolution in a Metapopulation Model

In several reciprocal cross-infection experiments parasites were found to be significantly more adapted to their local host populations than to hosts from distant populations. We developed a metapopulation model, taking explicit account of both population densities and gene frequencies, to determine the influence of ecological and genetical parameters on the local adaptation of the parasites and on the spatial distribution of resistance and virulence genes. Our results point to the predominant effect of ecological parameters such as parasite growth rate and host and parasite migration rates on coevolutionary outcomes. In particular, the parasites are more likely to be adapted to their local host population than to allopatric hosts when the parasite migration rate is larger than the host migration rate. The opposite should be observed whenever hosts migrate more than parasites.

Imperfect vaccines and the evolution of pathogen virulence

Vaccines rarely provide full protection from disease. Nevertheless, partially effective (imperfect) vaccines may be used to protect both individuals and whole populations. We studied the potential impact of different types of imperfect vaccines on the evolution of pathogen virulence (induced host mortality) and the consequences for public health. Here we show that vaccines designed to reduce pathogen growth rate and/or toxicity diminish selection against virulent pathogens. The subsequent evolution leads to higher levels of intrinsic virulence and hence to more severe disease in unvaccinated individuals. This evolution can erode any population-wide benefits such that overall mortality rates are unaffected, or even increase, with the level of vaccination coverage. In contrast, infection-blocking vaccines induce no such effects, and can even select for lower virulence. These findings have policy implications for the development and use of vaccines that are not expected to provide full immunity, such as candidate vaccines for malaria.

Local adaptation, evolutionary potential and host-parasite coevolution: interactions between migration, mutation, population size and generation time

Local adaptation of parasites to their sympatric hosts has been investigated on different biological systems through reciprocal transplant experiments. Most of these studies revealed a local adaptation of the parasite. In several cases, however, parasites were found to be locally maladapted or neither adapted nor maladapted. In the present paper, we try to determine the causes of such variability in these results. We analyse a host–parasite metapopulation model and study the effect of several factors on the emergence of local adaptation: population sizes, mutation rates and migration rates for both the host and the parasite, and parasite generation time. We show that all these factors may act on local adaptation through their effects on the evolutionary potential of each species. In particular, we find that higher numbers of mutants or migrants do, in general, promote local adaptation. Interestingly, shorter parasite generation time does not always favour parasite local adaptation. When genetic variability is limiting, shorter generation time, via an increase of the strength of selection, decreases the capacity of the parasite to adapt to an evolving host.

The effect of migration on local adaptation in a coevolving host¿parasite system

Antagonistic coevolution between hosts and parasites in spatially structured populations can result in local adaptation of parasites; that is, the greater infectivity of local parasites than foreign parasites on local hosts. Such parasite specialization on local hosts has implications for human health and agriculture. By contrast with classic single-species population-genetic models, theory indicates that parasite migration between subpopulations might increase parasite local adaptation, as long as migration does not completely homogenize populations. To test this hypothesis we developed a system-specific mathematical model and then coevolved replicate populations of the bacterium Pseudomonas fluorescens and a parasitic bacteriophage with parasite only, with host only or with no migration. Here we show that patterns of local adaptation have considerable temporal and spatial variation and that, in the absence of migration, parasites tend to be locally maladapted. However, in accord with our model, parasite migration results in parasite local adaptation, but host migration alone has no significant effect.

LOCAL MALADAPTATION IN THE ANTHER-SMUT FUNGUS MICROBOTRYUM VIOLACEUM TO ITS HOST PLANT SILENE LATIFOLIA: EVIDENCE FROM A CROSS-INOCULATION EXPERIMENT

Conventional wisdom holds that parasites evolve more rapidly than their hosts and are therefore locally adapted, that is, better at exploiting sympatric than allopatric hosts. We studied local adaptation in the insect‐transmitted fungal pathogen Microbotryum violaceum and its host plant Silene latifolia. Infection success was tested in sympatric (local) and allopatric (foreign) combinations of pathogen and host from 14 natural populations from a metapopulation. Seedlings from up to 10 seed families from each population were exposed to sporidial suspensions from each of four fungal strains derived from the same population, from a near‐by population (< 10 km distance), and from two populations at an intermediate (< 30 km) and remote (< 170 km) distance, respectively. We obtained significant pathogen X plant interactions in infection success (proportion of diseased plants) at both fungal population and strain level. There was an overall pattern of local maladaptation of this pathogen: average fungal infection success was significantly lower on sympatric hosts (mean proportion of diseased plants = 0.32 ± 0.03 SE) than on allopatric hosts (0.40 ± 0.02). Five of the 14 fungal populations showed no strong reduction in infection success on sympatric hosts, and three even tended to perform better on sympatric hosts. This pattern is consistent with models of time‐lagged cycles predicting patterns of local adaptation in host‐parasite systems to emerge only on average. Several factors may restrict the evolutionary potential of this pathogen relative to that of its host. First, a predominantly selfing breeding system may limit its ability to generate new virulence types by sexual recombination, whereas the obligately outcrossing host 5. latifolia may profit from rearrangement of resistance alleles by random mating. Second, populations often harbor only a few infected individuals, so virulence variation may be further reduced by drift. Third, migration rates among host plant populations are much higher than among pathogen populations, possibly because pollinators prefer healthy over diseased plants. Migration among partly isolated populations may therefore introduce novel host plant resistance variants more often than novel parasite virulence variants. That migration contributes to the coevolutionary dynamics in this system is supported by the geographic pattern of infectivity. Infection success increased over the first 10–km range of host‐pathogen population distances, which is likely the natural range of gene exchange.

Insecticide Control of Vector-Borne Diseases: When Is Insecticide Resistance a Problem?

Many of the most dangerous human diseases are transmitted by insect vectors. After decades of repeated insecticide use, all of these vector species have demonstrated the capacity to evolve resistance to insecticides. Insecticide resistance is generally considered to undermine control of vector-transmitted diseases because it increases the number of vectors that survive the insecticide treatment. Disease control failure, however, need not follow from vector control failure. Here, we review evidence that insecticide resistance may have an impact on the quality of vectors and, specifically, on three key determinants of parasite transmission: vector longevity, competence, and behaviour. We argue that, in some instances, insecticide resistance is likely to result in a decrease in vector longevity, a decrease in infectiousness, or in a change in behaviour, all of which will reduce the vectorial capacity of the insect. If this effect is sufficiently large, the impact of insecticide resistance on disease management may not be as detrimental as previously thought. In other instances, however, insecticide resistance may have the opposite effect, increasing the insects vectorial capacity, which may lead to a dramatic increase in the transmission of the disease and even to a higher prevalence than in the absence of insecticides. Either way—and there may be no simple generality—the consequence of the evolution of insecticide resistance for disease ecology deserves additional attention.

Evolution of multihost parasites

Abstract Multihost parasites can infect different types of hosts or even different host species. Epidemiological models have shown the importance of the diversity of potential hosts for understanding the dynamics of infectious disease (e.g., the importance of reservoirs), but the consequences of this diversity for virulence and transmission evolution remain largely overlooked. Here, I present a general theoretical framework for the study of life-history evolution of multihost parasites. This analysis highlights the importance of epidemiology (the relative quality and quantity of different types of infected hosts) and between-trait constraints (both within and between different hosts) to parasite evolution. I illustrate these effects in different transmission scenarios under the simplifying assumption that parasites can infect only two types of hosts. These simple but contrasted evolutionary scenarios yield new insights into virulence evolution and the evolution of transmission routes among different hosts. Because many of the pathogens that have large public-health and agricultural impacts have complex life cycles, an understanding of their evolutionary dynamics could hold substantial benefits for management.

A practical guide to measuring local adaptation

Patterns of local adaptation are expected to emerge when selection is spatially heterogeneous and sufficiently strong relative to the action of other evolutionary forces. The observation of local adaptation thus provides important insight into evolutionary processes and the adaptive divergence of populations. The detection of local adaptation, however, suffers from several conceptual, statistical and methodological issues. Here, we provide practical recommendations regarding (1) the definition of local adaptation, (2) the analysis of transplant experiments and (3) the optimisation of the experimental design of local adaptation studies. Together, these recommendations provide a unified approach for measuring local adaptation and understanding the adaptive divergence of populations in a wide range of biological systems.

THE EVOLUTION OF SPECIFICITY IN EVOLVING AND COEVOLVING ANTAGONISTIC INTERACTIONS BETWEEN A BACTERIA AND ITS PHAGE

Abstract The evolution of exploitative specificity can be influenced by environmental variability in space and time and the intensity of trade-offs. Coevolution, the process of reciprocal adaptation in two or more species, can produce variability in host exploitation and as such potentially drive patterns in host and parasite specificity. We employed the bacterium Pseudomonas fluorescens SBW25 and its DNA phage Φ2 to investigate the role of coevolution in the evolution of phage infectivity range and its relation with phage growth rate. At the phage population level, coevolution led to the evolution of broader infectivity range, but without an associated decrease in phage growth rate relative to the ancestor, whereas phage evolution in the absence of bacterial evolution led to an increased growth rate but no increase in infectivity range. In contrast, both selection regimes led to phage adaptation (in terms of growth rates) to their respective bacterial hosts. At the level of individual phage genotypes, coevolution resulted in within-population diversification in generalist and specialist infectivity range types. This pattern was consistent with a multilocus gene-for-gene interaction, further confirmed by an observed cost of broad infectivity range for individual phage. Moreover, coevolution led to the emergence of bacterial genotype by phage genotype interactions in the reduction of bacterial growth rate by phage. Our study demonstrates that the strong reciprocal selective pressures underlying the process of coevolution lead to the emergence and coexistence of different strategies within populations and to specialization between selective environments.

Evolution of the distribution of dispersal distance under distance‐dependent cost of dispersal

Abstract We analyse the evolution of the distribution of dispersal distances in a stable and homogeneous environment in one‐ and two‐dimensional habitats. In this model, dispersal evolves to avoid the competition between relatives although some cost might be associated with this behaviour. The evolutionarily stable dispersal distribution is characterized by an equilibration of the fitness gains among all the different dispersal distances. This cost‐benefit argument has heuristic value and facilitates the comprehension of results obtained numerically. In particular, it explains why some minimal or maximal probability of dispersal may evolve at intermediate distances when the cost of dispersal function is an increasing function of distance. We also show that kin selection may favour long range dispersal even if the survival cost of dispersal is very high, provided the survival probability does not vanish at long distances.