Detecting local adaptation in a natural plant-pathogen metapopulation: a laboratory vs. field transplant approach

Antagonistic coevolution between hosts and parasites in spatially structured populations can result in local adaptation of parasites. Traditionally parasite local adaptation has been investigated in field transplant experiments or in the laboratory under a constant environment. Despite the conceptual importance of local adaptation in studies of (co)evolution, to date no study has provided a comparative analysis of these two methods. Here, using information on pathogen population dynamics, I tested local adaptation of the specialist phytopathogen, Podosphaera plantaginis, to its host, Plantago lanceolata at three different spatial scales: sympatric host population, sympatric host metapopulation and allopatric host metapopulations. The experiment was carried out as a field transplant experiment with greenhouse-reared host plants from these three different origins introduced into four pathogen populations. In contrast to results of an earlier study performed with these same host and parasite populations under laboratory conditions, I did not find any evidence for parasite local adaptation. For interactions governed by strain-specific resistance, field studies may not be sensitive enough to detect mean parasite population virulence. Given that parasite transmission potential may be mediated by the abiotic environment and genotype-by-environment interactions, I suggest that relevant environmental variation should be incorporated into laboratory studies of parasite local adaptation.     

Spatial scale of local adaptation in a plant-pathogen metapopulation

The rate and scale of gene flow can strongly affect patterns of local adaptation in host-parasite interactions. I used data on regional pathogen occurrence to infer the scale of pathogen dispersal and to identify pathogen metapopulations in the interaction between Plantago lanceolata and its specialist phytopathogen, Podosphaera plantaginis. Frequent extinctions and colonizations were recorded in the metapopulations, suggesting substantial gene flow at this spatial scale. The level of pathogen local adaptation was assessed in a laboratory inoculation experiment at three different scales: in sympatric host populations, in sympatric host metapopulations and in allopatric host metapopulations. I found evidence for adaptation to sympatric host populations, as well as evidence indicating that local adaptation may extend to the scale of the sympatric host metapopulation. There was also variation among the metapopulations in the degree of pathogen local adaptation. This may be explained by regional differences in the rate of migration.     

Robustness of the outcome of adult bumblebee infection with a trypanosome parasite after varied parasite exposures during larval development

The outcome of defence by the invertebrate immunity has recently been shown to be more complex than previously thought. In particular, the outcome is affected by biotic and abiotic environmental variation, host genotype, parasite genotype and their interaction. Knowledge of conditions under which environmental variation affects the outcome of an infection is one important question that relates to this complexity. We here use the model system of the bumblebee, Bombus terrestris, infected by the trypanosome, Crithidia bombi, combined with a split-colony design to test the influence of the parasite environment during larval rearing on adult resistance. We find that genotype-specific interactions are maintained and adult resistance is not influenced. This demonstrates that environmental dependence of bumblebee-trypanosome interactions is not ubiquitous, and yet unknown constraints will maintain standard coevolutionary dynamics under such environmental deviations.     

Temperature-dependent costs of parasitism and maintenance of polymorphism under genotype-by-environment interactions

The maintenance of genetic variation for infection-related traits is often attributed to coevolution between hosts and parasites, but it can also be maintained by environmental variation if the relative fitness of different genotypes changes with environmental variation. To gain insight into how infection-related traits are sensitive to environmental variation, we exposed a single host genotype of the freshwater crustacean Daphnia magna to four parasite isolates (which we assume to represent different genotypes) of its naturally co-occurring parasite Pasteuria ramosa at 15, 20 and 25 degrees C. We found that the cost to the host of becoming infected varied with temperature, but the magnitude of this cost did not depend on the parasite isolate. Temperature influenced parasite fitness traits; we found parasite genotype-by-environment (G x E) interactions for parasite transmission stage production, suggesting the potential for temperature variation to maintain genetic variation in this trait. Finally, we tested for temperature-dependent relationships between host and parasite fitness traits that form a key component of models of virulence evolution, and we found them to be stable across temperatures.     

Surface carbohydrate composition of a tapeworm in its consecutive intermediate hosts: individual variation and fitness consequences

Carbohydrates on parasite surfaces have been shown to play an important role in host–parasite coevolution, mediating host non-self recognition and parasite camouflage. Parasites that switch hosts can change their surface molecules to remain undetected by the diverse immune systems of their different hosts. However, the question of individual variation in surface sugar composition and its relation to infectivity, virulence, immune evasion and growth of a parasite in its different hosts is as yet largely unexplored. We studied such fitness consequences of variation in surface sugars in a sympatric host–parasite system consisting of the cestode Schistocephalus solidus and its intermediate hosts, a copepod and the three-spined stickleback. Using lectins to analyse the sugar composition, we show that the tapeworm changes its surface according to the invertebrate or vertebrate host. Importantly, sugar composition seems to be genetically variable, as shown by differences among tapeworm sibships. These differences are related to variation in parasite fitness in its second intermediate host, i.e. infectivity and growth. Surface sugar composition may thus be a proximate correlate of the evolutionarily relevant variability in infectivity and virulence of parasites in different hosts.     

Host–parasite coevolution: genetic variation in a virus population and the interaction with a host gene

Host–parasite coevolution is considered to be an important factor in maintaining genetic variation in resistance to pathogens. Drosophila melanogaster is naturally infected by the sigma virus, a vertically transmitted and host‐specific pathogen. In fly populations, there is a large amount of genetic variation in the transmission rate from parent to offspring, much of which is caused by major‐effect resistance polymorphisms. We have found that there are similarly high levels of genetic variation in the rate of paternal transmission among 95 different isolates of the virus as in the host. However, when we examined a transmission‐blocking gene in the host, we found that it was effective across virus isolates. Therefore, the high levels of genetic variation observed in this system do not appear to be maintained because of coevolution resulting from interactions between this host gene and parasite genes.     

Aphid genotypes vary in their response to the presence of fungal endosymbionts in host plants

Genetic variation for fitness‐relevant traits may be maintained in natural populations by fitness differences that depend on environmental conditions. For herbivores, plant quality and variation in chemical plant defences can maintain genetic variation in performance. Apart from plant secondary compounds, symbiosis between plants and endosymbiotic fungi (endophytes) can produce herbivore‐toxic compounds. We show that there is significant variation among aphid genotypes in response to endophytes by comparing life‐history traits of 37 clones of the bird cherry‐oat aphid Rhopalosiphum padi feeding on endophyte‐free and endophyte‐infected tall fescue Lolium arundinaceum. Clonal variation for life‐history traits was large, and most clones performed better on endophyte‐free plants. However, the clones differed in the relative performance across the two environments, resulting in significant genotype × environment interactions for all reproductive traits. These findings suggest that natural variation in prevalence of endophyte infection can contribute to the maintenance of genetic diversity in aphid populations.     

Within‐ and among‐population variation in infectivity,latency and spore production in a host–pathogen system

In spatially structured populations, host–parasite coevolutionary potential depends on the distribution of genetic variation within and among populations. Inoculation experiments using the plant, Silene latifolia, and its fungal pathogen, Microbotryum violaceum, revealed little overall differentiation in infectivity/resistance, latency or spore production among host or pathogen populations. Within populations, fungal strains had similar means, but varied in performance across plant populations. Variation in resistance among seed families indicates the potential for parasite‐mediated selection, whereas there was little evidence for local pathogen genotype × plant genotype interactions assumed by most theoretical coevolution models. Lower spore production on sympatric than allopatric hosts confirmed local fungal maladaptation already observed for infectivity. Correlations between infectivity and latency or spore production suggest a common mechanism for variation in these traits. Our results suggest low variation available to this pathogen for tracking its coevolving host. This may be caused by random drift, breeding system or migration characteristic of metapopulation dynamics.     

Genetic and environmental components of phenotypic variation in body shape among populations of Atlantic cod (Gadus morhua L.)

A common-garden experiment was conducted on larvae to test for genetic differences in body shape among populations of Atlantic cod ( Gadus morhua ). Offspring from four north-west Atlantic regions were reared from hatching to postmetamorphosis at two temperatures (7 ± 1 °C and 11 ± 1 °C) and two food levels (1500 and 4500 prey L⁻¹). Body shape differed between populations and treatments. Population differences were greatest between south-west Scotian Shelf cod and those further north; the former were characterized by a deeper body, larger head, and longer caudal peduncle than cod from the other populations. Significant differences were also observed between two putative populations on the south-west Scotian Shelf, suggesting genetic divergence between spawning aggregations at small spatial scales (< 100 km). Temperature and food supply also influenced body shape, with the effect of the former being more pronounced. Individuals reared at the higher temperature or food level had a deeper body and a larger head than those reared at the lower temperature or food supply. Phenotypic responses to changes in the rearing environment also differed among populations, indicating genetic differences in phenotypic plasticity. Differences between populations in morphology and in phenotypic plasticity suggest genetic divergence at both large (> 1000 km) and small (< 100 km) spatial scales. The genetic differences at large spatial scales counteracted the expected effects of temperature differences in the wild, suggesting countergradient variation in morphology among these populations.  © 2006 Her Majesty the Queen in Right of Canada. Journal compilation © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 351–365.     

Association between DRD4 gene polymorphism and personality variation in great tits: a test across four wild populations

Polymorphisms in the dopamine receptor D4 gene (DRD4) have been related to individual variation in novelty‐seeking or exploratory behaviour in a variety of animals, including humans. Recently, the human DRD4 orthologue was sequenced in a wild bird, the great tit (Parus major) and a single nucleotide polymorphism in exon 3 of this gene (SNP830) was shown to be associated with variation in exploratory behaviour of lab‐raised individuals originating from a single wild population. Here we test the generality of this finding in a large sample of free‐living individuals from four European great tit populations, including the originally sampled population. We demonstrate that the association between SNP830 genotype and exploratory behaviour also exists in free‐living birds from the original population. However, in the other three populations we found only limited evidence for an association: in two populations the association appeared absent; while in one there was a nonsignificant tendency. We could not confirm a previously demonstrated interaction with another DRD4 polymorphism, a 15 bp indel in the promoter region (ID15). As yet unknown differences in genetic or environmental background could explain why the same genetic polymorphism (SNP830) has a substantial effect on exploratory behaviour in one population, explaining 4.5–5.8% of the total variance—a large effect for a single gene influencing a complex behavioural trait—but not in three others. The confirmation of an association between SNP830 genotype and personality‐related behaviour in a wild bird population warrants further research into potential fitness effects of the polymorphism, while also the population differences in the strength of the association deserve further investigation. Another important future challenge is the identification of additional loci influencing avian personality traits in the wild.     

Selection in a fluctuating environment leads to decreased genetic variation and facilitates the evolution of phenotypic plasticity

Changes in the environment are expected to induce changes in the quantitative genetic variation, which influences the ability of a population to adapt to environmental change. Furthermore, environmental changes are not constant in time, but fluctuate. Here, we investigate the effect of rapid, continuous and/or fluctuating temperature changes in the seed beetle Callosobruchus maculatus, using an evolution experiment followed by a split-brood experiment. In line with expectations, individuals responded in a plastic way and had an overall higher potential to respond to selection after a rapid change in the environment. After selection in an environment with increasing temperature, plasticity remained unchanged (or decreased) and environmental variation decreased, especially when fluctuations were added; these results were unexpected. As expected, the genetic variation decreased after fluctuating selection. Our results suggest that fluctuations in the environment have major impact on the response of a population to environmental change; in a highly variable environment with low predictability, a plastic response might not be beneficial and the response is genetically and environmentally canalized resulting in a low potential to respond to selection and low environmental sensitivity. Interestingly, we found greater variation for phenotypic plasticity after selection, suggesting that the potential for plasticity to evolve is facilitated after exposure to environmental fluctuations. Our study highlights that environmental fluctuations should be considered when investigating the response of a population to environmental change.