Adaptation to the most abundant host genotype in an agricultural plant-pathogen system--potato late blight

This study investigated local adaptation of Phytophthora infestans populations, the causal agent of potato late blight, to two susceptible potato cultivars, each grown for a number of years and over large areas in separate French regions. We measured aggressiveness (quantitative pathogenicity) of each pathogen population to sympatric and allopatric hosts in a reciprocal cross-inoculation experiment. There was no evidence for specific host adaptation in this pathosystem. At both local and regional scales, the distribution of aggressiveness fits a pattern of adaptation to the most common host genotype. Our observations support the theoretical predictions that large pathogen dispersal rates and genetic drift, revealed by the comparisons of the genotypic structures of the populations tested, can lead to a local adaptation pattern detectable only at a large spatial scale. The unravelling of adaptive patterns at different spatial scales can be used for a more efficient management of the disease.     

GENETIC DIFFERENTIATION OF FITNESS-ASSOCIATED TRAITS AMONG RAPIDLY EVOLVING POPULATIONS OF THE SOAPBERRY BUG

In this study we used reciprocal rearing experiments to test the hypothesis that there is a genetic basis for the adaptive differences in host-use traits among host-associated soapberry bug populations (described in Carroll and Boyd 1992). These experiments were conducted on two host races from Florida, in which differences in beak length and development were found between natural populations on a native host plant species and those on a recently introduced plant species (colonized mainly post-1950). Performance was generally superior on the host species from which each lab population originated (i.e., on the “Home” host species): in analysis of variance, there was significant population-by-host interaction for size, development time, and growth rate. These results indicate that the population differences in nature are evolved rather than host induced. Increased performance on the introduced host was accompanied by reduced performance on the native host, a pattern that could theoretically promote further differentiation between the host races.     

Accumulation and exchange of parasites during adaptive radiation in an ancient lake

In the ancient Lake Baikal, Russia, amphipod crustaceans have undergone a spectacular adaptive radiation, resulting in a diverse community of species. A survey of microsporidian parasites inhabiting endemic and non-endemic amphipod host species at the margins of Lake Baikal indicates that the endemic amphipods harbour many microsporidian parasite groups associated with amphipods elsewhere in Eurasia. While these parasites may have undergone a degree of adaptive radiation within the lake, there is little evidence of host specificity. Furthermore, a lack of reciprocal monophyly indicates that exchanges of microsporidia between Baikalian and non-Baikalian hosts have occurred frequently in the past and may be ongoing. Conversely, limitations to parasite exchange between Baikalian and non-Baikalian host populations at the margins of the lake are implied by differences in parasite prevalence and lack of shared microsporidian haplotypes between the two host communities. While amphipod hosts have speciated sympatrically within Lake Baikal, the parasites appear instead to have accumulated, moving into the lake from external amphipod populations on multiple occasions to exploit the large and diverse community of endemic amphipods in Lake Baikal.     

Eco‐evolutionary dynamics in a coevolving host–virus system

Eco‐evolutionary dynamics have been shown to be important for understanding population and community stability and their adaptive potential. However, coevolution in the framework of eco‐evolutionary theory has not been addressed directly. Combining experiments with an algal host and its viral parasite, and mathematical model analyses we show eco‐evolutionary dynamics in antagonistic coevolving populations. The interaction between antagonists initially resulted in arms race dynamics (ARD) with selective sweeps, causing oscillating host–virus population dynamics. However, ARD ended and populations stabilised after the evolution of a general resistant host, whereas a trade‐off between host resistance and growth then maintained host diversity over time (trade‐off driven dynamics). Most importantly, our study shows that the interaction between ecology and evolution had important consequences for the predictability of the mode and tempo of adaptive change and for the stability and adaptive potential of populations.     

Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation

Antagonistic coevolution is a critical force driving the evolution of diversity, yet the selective processes underpinning reciprocal adaptive changes in nature are not well understood. Local adaptation studies demonstrate partner impacts on fitness and adaptive change, but do not directly expose genetic processes predicted by theory. Specifically, we have little knowledge of the relative importance of fluctuating selection vs. arms-race dynamics in maintaining polymorphism in natural systems where metapopulation processes predominate. We conducted cross-year epidemiological, infection and genetic studies of multiple wild host and pathogen populations in the Linum-Melampsora association. We observed asynchronous phenotypic fluctuations in resistance and infectivity among demes. Importantly, changes in allelic frequencies at pathogen infectivity loci, and in host recognition of these genetic variants, correlated with disease prevalence during natural epidemics. These data strongly support reciprocal coevolution maintaining balanced resistance and infectivity polymorphisms, and highlight the importance of characterising spatial and temporal dynamics in antagonistic interactions.     

Rapidly evolving adaptations to host ecology and nutrition in the soapberry bug

With reciprocal rearing experiments, we tested the hypothesis that adaptive differences in host-use traits among soapberry bug populations have a genetic basis. These experiments were conducted with two host races from Florida, an ancestral-type one on a native host plant species and a derived one on a recently introduced plant species (colonized mainly post-1950), on whose seed crops this insect depends for growth and reproduction. Compared to the native host species, the introduced host produces larger seed crops over a much briefer annual period. Its seeds are also significantly higher in lipids and lower in nitrogen. The bug populations exhibit greater juvenile survivorship on their home hosts; that is, the derived population survives better on seeds of the introduced host than does its ancestral-type counterpart, and vice versa. Regardless of the rearing host, populations from the introduced host lay much smaller eggs, and fecundity measures show a more complex pattern than does survivorship: the ancestral-type population produces eggs at the same rate on each host, while the derived population is less fecund on the native host and exhibits enhanced fecundity on the introduced host. These results indicate that the population differences are evolved rather than host-induced. They appear to be adaptive responses to host differences in the spatial and temporal distribution of seed availability and nutritional quality, and show that increased performance on the alien host has evolved with surprising speed and magnitude, with concomitant reductions in performance on the original host.     

HOST SPECIALIZATION DIFFERENTIATES CRYPTIC SPECIES OF FEATHER-FEEDING LICE

Parasite species with differentiated host-specific populations provide a natural opportunity to explore factors involved in parasite diversification. Columbicola macrourae is a species of ectoparasitic feather louse currently recognized from 15 species of New World pigeons and doves. Mitochondrial sequences reveal five divergent haplotype clusters within C. macrourae , suggesting cryptic species. Each cluster is relatively host specific, with only one or a few hosts. We conducted a reciprocal transfer experiment with two of these lineages to test whether host use has an adaptive component. Our results demonstrate that the fitness of each lineage is considerably higher on its native host than on the novel host suggesting that one or more selective agents favor host specialization by the different lineages. In addition, we were able to morphologically separate individual lice from the two experimental lineages using discriminant function analysis. Furthermore, differences in the size of these louse lineages match differences in the size of their respective hosts, paralleling the strong correlation between parasite and host body size across the genus Columbicola . Together, these results suggest that selection in this cryptic species complex reflects selection across the whole genus, and that this selection, in part, contributes to the maintenance of host specialization.     

Evolution of host resistance: looking for coevolutionary hotspots at small spatial scales

Natural plant populations are often found to be extremely diverse in their resistance to pathogens. While the potential of pathogens in driving the evolution of resistance in hosts has been widely recognized, empirical evidence linking disease dynamics to host population genetic structure has remained scarce. Here I show that current coevolutionary selection for resistance can be divergent even on a very fine spatial scale. In a natural plant-pathogen metapopulation, disease occurrence patterns were highly aggregated over space and time within host populations. A laboratory inoculation experiment showed higher resistance within areas of the host populations where encounter rates with the pathogen have been high. Higher resistance to sympatric than to allopatric strains of the pathogen suggests that this change has taken place as a response to local selection. These results constitute evidence of adaptive microevolution of resistance resulting from disease epidemics in natural plant-pathogen associations, and highlight the importance of finding the relevant scale at which to address questions of current coevolutionary selection.     

Changes in reciprocal herkogamy during the tristyly-distyly transition in Oxalis alpina increase efficiency in pollen transfer

Although the spatial separation of sexual organs within a flower (herkogamy) has been interpreted as a mechanism that promotes efficient pollen transfer, there have been few attempts to relate variation in herkogamy to probabilities of pollen flow. Here, we used a heterostylous species with variation in reciprocal herkogamy to test this hypothesis. We measured legitimate and illegitimate pollen flow with fluorescent dyes in four selected populations of Oxalis alpina corresponding to the extremes of a previously reported evolutionary gradient from tristyly to distyly. After the breakdown of tristyly, the observed increment in reciprocal herkogamy between the long and short morphs was associated with a 30% increase in the proportion of dye received from compatible illegitimate pollinations. In all populations, the most likely effective pollen vectors were two Heterosarus bee species. Our results support the adaptive value of reciprocal herkogamy in promoting efficient pollen transfer in heterostylous species.     

T-cell Subsets and Antifungal Host Defenses

It has been long appreciated that protective immunity against fungal pathogens is dependent on activation of cellular adaptive immune responses represented by T lymphocytes. The T-helper (Th)1/Th2 paradigm has proven to be essential for the understanding of protective adaptive host responses. Studies that have examined the significance of regulatory T cells in fungal infection, and the recent discovery of a new T-helper subset called Th17 have provided crucial information for understanding the complementary roles played by the various T-helper lymphocytes in systemic versus mucosal antifungal host defense. This review provides an overview of the role of the various T-cell subsets during fungal infections and the reciprocal regulation between the T-cell subsets contributing to the tailored host response against fungal pathogens.     

Sexual signalling in female crested macaques and the evolution of primate fertility signals

Background

Host-parasite coevolution can lead to local adaptation of either parasite or host if there is specificity (GxG interactions) and asymmetric evolutionary potential between host and parasite. This has been demonstrated both experimentally and in field studies, but a substantial proportion of studies fail to detect such clear-cut patterns. One explanation for this is that adaptation can be masked by counter-adaptation by the antagonist. Additionally, genetic architecture underlying the interaction is often highly complex thus preventing specific adaptive responses. Here, we have employed a reciprocal cross-infection experiment to unravel the adaptive responses of two components of fitness affecting both parties with different complexities of the underlying genetic architecture (i.e. mortality and spore load). Furthermore, our experimental coevolution of hosts (Tribolium castaneum) and parasites (Nosema whitei) included paired replicates of naive hosts from identical genetic backgrounds to allow separation between host- and parasite-specific responses.

Results

In hosts, coevolution led to higher resistance and altered resistance profiles compared to paired control lines. Host genotype × parasite genotype interactions (G_H × G_P) were observed for spore load (the trait of lower genetic complexity), but not for mortality. Overall parasite performance correlated with resistance of its matching host coevolution background reflecting a directional and unspecific response to strength of selection during coevolution. Despite high selective pressures exerted by the obligatory killing parasite, and host- and parasite-specific mortality profiles, no general pattern of local adaptation was observed, but one case of parasite maladaptation was consistently observed on both coevolved and control host populations. In addition, the use of replicate control host populations in the assay revealed one case of host maladaptation and one case of parasite adaptation that was masked by host counter-adaptation, suggesting the presence of complex and probably dynamically changing fitness landscapes.

Conclusions

Our results demonstrate that the use of replicate naive populations can be a useful tool to differentiate between host and parasite adaptation in complex and dynamic fitness landscapes. The absence of clear local adaptation patterns during coevolution with a sexual host showing a complex genetic architecture for resistance suggests that directional selection for generality may be more important attributes of host-parasite coevolution than commonly assumed.     

EVOLUTIONARY GENETICS OF OVIPOSITION PREFERENCE IN SWALLOWTAIL BUTTERFLIES

Models of the evolution of host shifts and speciation in phytophagous insects are often built upon the assumption that host selection is under simple genetic control, perhaps even a single locus. The genetic basis for differences in host-plant preference by ovipositing insects was investigated using two closely related species of swallowtail butterfly, Papilio oregonius and P. zelicaon, which differ in the plant families on which females oviposit. Both species had been shown previously to vary within populations in host selection. A combination of analyses using reciprocal interspecific crosses and isofemale strains within populations indicated that oviposition preference in these species is determined significantly by one or more loci on the X chromosome, which female Lepidoptera inherit only paternally. Hence, preferences in hybrid females tended toward the paternal species. This is the first insect group for which partial control of oviposition preference has been localized onto a particular chromosome. In addition, one or more loci on another chromosome(s) appear to contribute to preference, as indicated by the partially intermediate preferences of some hybrid crosses. The overall differences in preference in the reciprocal interspecific hybrids were restricted to differences in the distribution of eggs laid among the local host plants of these two Papilio species; the reciprocal crosses did not differ in the small percentage of eggs laid on a novel potential host species. The variation in host selection found among the isofemale strains reinforces earlier results for these strains, indicating that there is genetic variation in host selection within these populations. Overall, the results indicate that the evolution of oviposition preference in these species involves genetic changes at two or more chromosomes with the X chromosome playing an important role in determining preference.     

Antagonistic coevolution with parasites increases the cost of host deleterious mutations

The fitness consequences of deleterious mutations are sometimes greater when individuals are parasitized, hence parasites may result in the more rapid purging of deleterious mutations from host populations. The significance of host deleterious mutations when hosts and parasites antagonistically coevolve (reciprocal evolution of host resistance and parasite infectivity) has not previously been experimentally investigated. We addressed this by coevolving the bacterium Pseudomonas fluorescens and a parasitic bacteriophage in laboratory microcosms, using bacteria with high and low mutation loads. Directional coevolution between bacterial resistance and phage infectivity occurred in all populations. Bacterial population fitness, as measured by competition experiments with ancestral genotypes in the absence of phage, declined with time spent coevolving. However, this decline was significantly more rapid in bacteria with high mutation loads, suggesting the cost of bacterial resistance to phage was greater in the presence of deleterious mutations (synergistic epistasis). As such, resistance to phage was more costly to evolve in the presence of a high mutation load. Consistent with these data, bacteria with high mutation loads underwent less rapid directional coevolution with their phage populations, and showed lower levels of resistance to their coevolving phage populations. These data suggest that coevolution with parasites increases the rate at which deleterious mutations are purged from host populations.     

Recursive adaptation in action: allochronic isolation and divergence of host-associated populations of the apple maggot fly,Rhagoletis pomonella,following its recent introduction to the western USA

An outstanding issue in the study of insect host races concerns the idea of ‘recursive adaptive divergence’, whereby adaptation can occur repeatedly across space and/or time, and the most recent adaptive episode is defined by one or more previously similar cases. The host plant shift of the apple maggot fly, Rhagoletis pomonella (Walsh) (Diptera: Tephritidae, Carpomyini), from ancestral downy hawthorn [Crataegus mollis (Torr. & A. Gray) Scheele] to introduced, domesticated apple (Malus domestica Borkh.) in the eastern USA has long served as a model system for investigating ecologically driven host race formation in phytophagous insect specialists. Here, we report results from an annual geography survey of eclosion time demonstrating a similar ecological pattern among nascent host-associated populations of the fly recently introduced ca. 40 years ago from its native range in the east into the Pacific Northwest (PNW) region of the USA. Specifically, using data collected from 25 locations across 5 years, we show that apple-infesting fly populations in the PNW have rapidly and repeatedly shifted (and maintained differences in) their adult eclosion life-history timing to infest two novel hawthorn hosts with different fruiting phenologies – a native species (Crataegus douglasii Lindl.) and an introduced species (Crataegus monogyna Jacq.) – generating partial allochronic reproductive isolation in the process. The shifts in the PNW parallel the classic case of host race formation in the eastern USA, but have occurred bi-directionally to two hawthorn species with phenologies slightly earlier (black hawthorn) and significantly later (ornamental hawthorn) than apple. Our results imply that R. pomonella can both possess and retain extensive-standing variation (i.e., ‘adaptive memory’) in diapause traits, even following introductions, to rapidly and temporally track novel phenological host opportunities when they arise. Thus, ‘specialized’ host races may not constitute evolutionary dead ends. Rather, adaptive phenotypic and genetic memory may carry over from one host shift to the next, recursively facilitating host race formation in phytophagous insects.     

Divergence in host use ability of a marine herbivore from two habitat types

We studied ecological divergence of host use ability in a generalist marine herbivore living in two distinct host plant assemblages. We collected Idotea balthica isopods from three populations dominated by the brown alga Fucus vesiculosus and three dominated by the seagrass Zostera marina. In two reciprocal common garden feeding experiments for adult and laboratory‐born juvenile isopods, we found that isopods from both assemblages performed better with their sympatric dominant host species than did isopods allopatric to this host. This indicates parallel divergence of populations according to the sympatric host plant assemblage. Furthermore, initial body size and body size‐dependent mortality differed between populations from the two assemblages. In nature, this may result in lower fitness of immigrants compared with that of residents and consequently reinforce divergence of the populations. Finally, we discuss how phenotypic plasticity and maternal and random effects may associate with the results.     

Symbiont-induced speciation

Speciation induced by parasitic or mutualistic symbionts has been suggested for taxa ranging from plants to insects to monkeys. Previous models for symbiont-induced speciation have been based upon hybrid inferiority and selection for reinforcement genes. Taken on their own, however, such models have severe theoretical limitations and little empirical support. Two conditions that may favour symbiont-induced speciation are presented here: (1) interaction norms in which the outcomes of host/symbiont interactions differ between environments and (2) differential coadaptation of host and symbiont populations between environments or along an environmental gradient. Symbiont-induced speciation can be considered as one form of 'mixed-process coevolution': reciprocal evolution in which adaptation of a population of one species to a population of a second species (or coadaptation of the populations) causes the population of the second species to become reproductively isolated from other populations.     

Evolution of tolerance in an invasive weed after reassociation with its specialist herbivore

The interaction between the European wild parsnip Pastinaca sativa and its coevolved florivore the parsnip webworm Depressaria pastinacella, established in North America for over 150 years, has resulted in evolution of local chemical phenotype matching. The recent invasion of New Zealand by webworms, exposing parsnips there to florivore selection for the first time, provided an opportunity to assess rates of adaptive response in a real‐time experiment. We planted reciprocal common gardens in the USA and NZ with seeds from (1) US populations with a long history of webworm association; (2) NZ populations that had never been infested and (3) NZ populations infested for 3 years (since 2007) or 6 years (since 2004). We measured impacts of florivory on realized fitness, reproductive effort and pollination success and measured phenotypic changes in infested NZ populations relative to uninfested NZ populations to determine whether rapid adaptive evolution in response to florivory occurred. Irrespective of country of origin or location, webworms significantly reduced plant fitness. Webworms reduced pollination success in small plants but not in larger plants. Although defence chemistry remained unchanged, plants in infested populations were larger after 3–6 years of webworm florivory. As plant size is a strong predictor of realized fitness, evolution of large size as a component of florivore tolerance may occur more rapidly than evolution of enhanced chemical defence.     

Geographical divergence in host use ability of a marine herbivore in alga–grazer interaction

When the selective environment differs geographically, local herbivore populations may diverge in their host use ability and adapt locally to exploit the sympatric host population. We tested whether populations of the marine generalist herbivore Idotea baltica have diverged in host us ability and whether they locally adapted to exploit the sympatric population of their main host species, the bladderwrack Fucus vesiculosus. We fed isopods from three local populations reciprocally with the sympatric and two allopatric populations of the host. The bladderwrack populations varied in their quality as food for isopods suggesting variation in the selective environment. The ability to exploit the main host showed considerable divergence among the isopod populations. There was no significant interaction between host and isopod origin, indicating that the patterns observed in the reciprocal feeding experiment could be explained by differences in overall suitability of the hosts and differences in overall performance of the isopod populations. Isopod population that was sympatric to a bladderwrack population with low phlorotannin content showed high performance on the algae from the sympatric but low performance on the algae from the two allopatric populations. Performance of isopods, especially in this population, decreased quickly with the increasing phlorotannin content of food algae. We therefore hypothesize that the isopods adapted to a low phlorotannin content were unable to utilize high-phlorotannin algae efficiently. Isopod populations sympatric to the high-phlorotannin bladderwrack populations may be generally better adapted to deal with phlorotannins, being thereby able to utilize a range of bladderwrack populations.     

Phenotypic plasticity and local adaptation favor range expansion of a Neotropical palm

One of the most intriguing questions in plant ecology is which evolutionary strategy allows widely distributed species to increase their ecological range and grow in changing environmental conditions. Phenotypic plasticity and local adaptations are major processes governing species range margins, but little is known about their relative contribution for tree species distribution in tropical forest regions. We investigated the relative role of phenotypic plasticity and local adaptation in the ecological distribution of the widespread palm Euterpe edulis in the Brazilian Atlantic Forest. Genetic sampling and experiments were performed in old‐growth remnants of two forest types with higher (Seasonal Semideciduous Forests vs. Submontane Rainforest) and lower biogeographic association and environmental similarities (Submontane Rainforest vs. Restinga Forest). We first assessed the molecular genetic differentiation among populations, focusing on the group of loci potentially under selection in each forest, using single‐nucleotide polymorphism (SNPs) outliers. Further, we looked for potential adaptive divergence among populations in a common garden experiment and in reciprocal transplants for two plant development phases: seedling establishment and sapling growth. Analysis with outlier loci indicated that all individuals from the Semideciduous Forest formed a single group, while another group was formed by overlapping individuals from Submontane Rainforest and Restinga Forest. Molecular differentiation was corroborated by reciprocal transplants, which yielded strong evidence of local adaptations for seedling establishment in the biogeographically divergent Rainforest and Semideciduous Forest, but not for Restinga Forest and Submontane Rainforest. Phenotypic plasticity for palm seedling establishment favors range expansion to biogeographically related or recently colonized forest types, while persistence in the newly colonized ecosystem may be favored by local adaptations if climatic conditions diverge over time, reducing gene flow between populations. SNPs obtained by next‐generation sequencing can help exploring adaptive genetic variation in tropical trees, which impose several challenges to the use of reciprocal transplants.     

Long-run bacteria-phage coexistence dynamics under natural habitat conditions in an environmental biotechnology system

Bacterial viruses are widespread and abundant across natural and engineered habitats. They influence ecosystem functioning through interactions with their hosts. Laboratory studies of phage–host pairs have advanced our understanding of phenotypic and genetic diversification in bacteria and phages. However, the dynamics of phage–host interactions have been seldom recorded in complex natural environments. We conducted an observational metagenomic study of the dynamics of interaction between Gordonia and their phages using a three-year data series of samples collected from a full-scale wastewater treatment plant. The aim was to obtain a comprehensive picture of the coevolution dynamics in naturally evolving populations at relatively high time resolution. Coevolution was followed by monitoring changes over time in the CRISPR loci of Gordonia metagenome-assembled genome, and reciprocal changes in the viral genome. Genome-wide analysis indicated low strain variability of Gordonia, and almost clonal conservation of the trailer end of the CRISPR loci. Incorporation of newer spacers gave rise to multiple coexisting bacterial populations. The host population carrying a shorter CRISPR locus that contain only ancestral spacers, which has not acquired newer spacers against the coexisting phages, accounted for more than half of the total host abundance in the majority of samples. Phages genome co-evolved by introducing directional changes, with no preference for mutations within the protospacer and PAM regions. Metagenomic reconstruction of time-resolved variants of host and viral genomes revealed how the complexity at the population level has important consequences for bacteria-phage coexistence.Subject terms: Microbial ecology, Metagenomics, Bacteriophages