Yannis Michalakis

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.

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.

Metapopulation Genetics and the Evolution of Dispersal

A Markovian extinction model that takes into account age structure of local populations allows consideration of the effects of demography and successional dynamics on the evolution of migration. Analytical expressions for the evolutionarily stable (ES) rates of dispersal are given for cases in which newly recolonized sites attain carrying capacity within a single season. Using a low-fecundity numerical model, we find that an increase of the level of site saturation increases the dispersal rate. Ecological successions and unequal local extinction rates between newly colonized sites and established populations strongly affect the ES dispersal rate. The frequency of genetic modifiers that enhance the rate of dispersal evolves negative correlations with deme age, with high-migration genotypes predominant among colonizers while progressively declining in frequency as a deme ages. This suggests that between-deme selection (colonization) favors migrants while within-deme selection favors low dispersers, which allows the coexistence of types with different dispersal rates. Because of the interaction between the two levels of selection, the relation between the ES dispersal rate and the deme maximal lifetime is nonmonotone. We suggest that life-history traits other than dispersal might also experience antagonistic selective forces at the between- and within-deme levels.

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.

HOST-DEPENDENT GENETIC STRUCTURE OF PARASITE POPULATIONS: DIFFERENTIAL DISPERSAL OF SEABIRD TICK HOST RACES

Abstract Despite the fact that parasite dispersal is likely to be one of the most important processes influencing the dynamics and coevolution of host‐parasite interactions, little information is available on the factors that affect it. In most cases, opportunities for parasite dispersal should be closely linked to host biology. Here we use microsatellite genetic markers to compare the population structure and dispersal of two host races of the seabird tick Ixodes uriae at the scale of the North Atlantic. Interestingly, tick populations showed high within‐population genetic variation and relatively low population differentiation. However, gene flow at different spatial scales seemed to depend on the host species exploited. The black‐legged kittiwake (Rissa tridactyla) had structured tick populations showing patterns of isolation by distance, whereas tick populations of the Atlantic puffin (Fratercula arctica) were only weakly structured at the largest scale considered. Host‐dependent rates of tick dispersal between colonies will alter infestation probabilities and local dynamics and may thus modify the adaptation potential of ticks to local hosts. Moreover, as I. uriae is a vector of the Lyme disease agent Borrelia burgdorferi sensu lato in both hemispheres, the large‐scale movements of birds and the subsequent dispersal of ticks will have important consequences for the dynamics and coevolutionary interactions of this microparasite with its different vertebrate and invertebrate hosts.

Host life history responses to parasitism

Parasites and their infections can adversely effect a hosts growth, reproduction and survival. These effects are often not immediate, but increase with time since infection. A general prediction from evolutionary biology is that hosts suffering from this type of infection should preferentially allocate resources towards reproduction, even if this is at the expense of their growth and survival. This review illustrates this argument with several empirical studies showing hosts behaving in this manner. These studies indicate that one way for hosts to reduce the costs of parasitism is by altering their life history traits to bring forward their schedule of reproduction.

Host specificity of a generalist parasite: genetic evidence of sympatric host races in the seabird tick Ixodes uriae

Due to the close association between parasites and their hosts, many ‘generalist’ parasites have a high potential to become specialized on different host species. We investigated this hypothesis for a common ectoparasite of seabirds, the tick Ixodes uriae that is often found in mixed host sites. We examined patterns of neutral genetic variation between ticks collected from Black‐legged kittiwakes (Rissa tridactyla) and Atlantic puffins (Fratercula arctica) in sympatry. To control for a potential distance effect, values were compared to differences among ticks from the same host in nearby monospecific sites. As predicted, there was higher genetic differentiation between ticks from different sympatric host species than between ticks from nearby allopatric populations of the same host species. Patterns suggesting isolation by distance were found among tick populations of each host group, but no such patterns existed between tick populations of different hosts. Overall, results suggest that host‐related selection pressures have led to the specialization of I. uriae and that host race formation may be an important diversifying mechanism in parasites.

The evolution of recombination in changing environments

Recombination generates under-represented genotypes by breaking down linkage disequilibrium between genes. Recent analyses have specified the conditions under which recombination is favored. These conditions are surprisingly sensitive to the form of selection and environmental change. This quantification makes it possible to use empirical measurements of critical parameters such as the form of epistasis, the rate of mutation, and the frequency of beneficial sweeps to assess different hypotheses for the evolution of recombination.

Evolution of parasite virulence against qualitative or quantitative host resistance.

We analysed the effects of two different modes of host resistance on the evolution of parasite virulence. Hosts can either adopt an all–or–nothing qualitative response (i.e. resistant hosts cannot be infected) or a quantitative form of resistance (i.e. which reduces the within–host growth rate of the parasite). We show that the mode of host resistance greatly affects the evolutionary outcome. Specifically, a qualitative form of resistance reduces parasite virulence, while a quantitative form of resistance generally selects for higher virulence.

Do outbreaks affect genetic population structure? A worldwide survey in Locusta migratoria, a pest plagued by microsatellite null alleles

An understanding of the role of factors intrinsic to a species’ life history in structuring contemporary genetic variation is a fundamental, but understudied, aspect of evolutionary biology. Here, we assessed the influence of the propensity to outbreak in shaping worldwide genetic variation in Locusta migratoria, a cosmopolitan pest well known for its expression of density‐dependent phase polyphenism. We scored 14 microsatellites in nine subspecies from 25 populations distributed over most of the species’ range in regions that vary in the historical frequency and extent of their outbreaks. We rejected the hypothesis that L. migratoria consists of two genetically distinct clusters adapted to habitats either rarely (nonoutbreaking) or cyclically (outbreaking) favourable to increases in population density. We also invalidated the current subspecific taxonomic classification based on morphometrics. Bayesian inferences indicated evidence of a homogenizing effect of outbreaks on L. migratoria population structure. Geographical and ecological barriers to gene flow in conjunction with historical events can also explain the observed patterns. By systematically assessing the effects of null alleles using computer simulations, we also provide a template for the analysis of microsatellite data sets characterized by a high prevalence of null alleles.