Host Resistance Traits Research Articles

Chemotaxis and Motility of Spongospora subterranea Zoospores in Response to Potato Root Exudate Constituents and pH.

Spongospora subterranea f. sp. subterranea is an important pathogen of potato responsible for major losses in most potato growing regions of the world. Infection is initiated by biflagellated motile zoospores released from long-lived resting spores. Zoospore chemotaxis to the host plant root is widely believed to be stimulated by host root exudate compounds, although direct evidence is lacking. This study refined the traditional chemotaxis capillary assay, with which we provided the first empirical evidence of S. subterranea zoospore chemotaxis. Individual potato root exudate metabolites were either taxis neutral, inhibitory, or attractant to the zoospores. L-Glutamine was the strongest chemoattractant, while spermine was the most inhibitory. Zoospore motility and chemotaxis were constrained by strongly acidic or alkaline solutions of pH < 5.3 and >8.5, respectively. Beyond pH, ionic constituents of the test solution affected zoospore motility as Sorensen's phosphate buffer stalled zoospore motility, but HEPES buffer at the same concentration and pH had little or no negative motility effect. Zoospore motility, as characterized by several parameters, influenced chemotaxis. Among the parameters measured, total distance traveled was the best predictor of zoospore chemotaxis. The characterization of environmental and ecological effects on zoospore motility and chemotaxis highlights useful targets for S. subterranea disease control through manipulation of zoospore taxis or selection of host resistance traits.

Infectious disease ecology and evolution in a changing world.

Infectious disease ecology and evolution in a changing world.

Host-Parasite Co-Evolution in Real-Time: Changes in Honey Bee Resistance Mechanisms and Mite Reproductive Strategies.

Simple SummaryParasitic mites, Varroa destructor, are a major threat for Western honey bees, Apis mellifera, colonies globally. Nevertheless, some honey bee populations can survive infestations with this mite, probably due to behaviors that suppress parasite reproduction. However, possible changes in mites associated with these surviving bees and the potential variations of bee behavior over time are poorly understood. Here, we show that mites can change their reproduction when associated with surviving hosts and that the bee behaviors suppressing mite reproduction can vary over time. In a fully-crossed field experiment on Dutch surviving colonies (Amsterdam Water Dunes (AWD) selection), worker brood cell recapping and varroa sensitive hygiene (VSH) performed by bees and mite reproductive parameters were investigated. Neither recapping nor VSH were significantly expressed even though a previous study showed VSH in these AWD bees. A larger proportion of mites that co-evolved with AWD surviving bees reproduced compared to mites in routinely treated colonies, but had lower fecundity. Overall, our study suggests that honeybee colonies can survive infestations with these mites by not yet understood means and shows for the first time adaptive changes in the reproduction of their coevolved mites.Co-evolution is a major driving force shaping the outcome of host-parasite interactions over time. After host shifts, the lack of co-evolution can have a drastic impact on novel host populations. Nevertheless, it is known that Western honey bee (Apis mellifera) populations can cope with host-shifted ectoparasitic mites (Varroa destructor) by means of natural selection. However, adaptive phenotypic traits of the parasites and temporal variations in host resistance behavior are poorly understood. Here, we show that mites made adaptive shifts in reproductive strategy when associated with resistant hosts and that host resistance traits can change over time. In a fully-crossed field experiment, worker brood cells of local adapted and non-adapted (control) A. mellifera host colonies were infested with mites originating from both types of host colonies. Then, mite reproduction as well as recapping of cells and removal of infested brood (i.e., Varroa Sensitive Hygiene, VSH) by host workers were investigated and compared to data from the same groups of host colonies three years earlier. The data suggest adaptive shifts in mite reproductive strategies, because mites from adapted hosts have higher probabilities of reproduction, but lower fecundity, when infesting their associated hosts than mites in treated colonies. The results confirm that adapted hosts can reduce mite reproductive success. However, neither recapping of cells nor VSH were significantly expressed, even though the latter was significantly expressed in this adapted population three years earlier. This suggests temporal variation in the expression of adaptive host traits. It also appears as if mechanisms not investigated here were responsible for the reduced mite reproduction in the adapted hosts. In conclusion, a holistic view including mite adaptations and studies of the same parasite/host populations over time appears overdue to finally understand the mechanisms enabling survival of V. destructor-infested honey bee host colonies.

Selection for outbreeding in Varroa parasitising resistant honey bee (Apis mellifera) colonies

AbstractParasitism is expected to select for counter‐adaptations in the host: driving a coevolutionary arms race. However, human interference between honey bees (Apis mellifera) and Varroa mites removes the effect of natural selection and restricts the evolution of host counter‐adaptations. With full‐sibling mating common among Varroa, this can rapidly select for virulent, highly inbred, Varroa populations. We investigated how the evolution of host resistance could affect the infesting population of Varroa mites.We screened a Varroa‐resistant honey bee population near Toulouse, France, for a Varroa resistance trait: the inhibition of Varroa's reproduction in drone pupae. We then genotyped Varroa which had co‐infested a cell using microsatellites. Across all resistant honey bee colonies, Varroa's reproductive success was significantly higher in co‐infested cells but the distribution of Varroa between singly and multiply infested cells was not different from random. While there was a trend for increased reproductive success when Varroa of differing haplotypes co‐infested a cell, this was not significant. This suggests local mate competition, through the presence of another Varroa foundress in a pupal cell, may be enough to help Varroa overcome host resistance traits; with a critical mass of infesting Varroa overwhelming host resistance. However, the fitness trade‐offs associated with preferentially co‐infesting cells may be too high for Varroa to evolve a mechanism to identify already‐infested cells. The increased reproductive success of Varroa when co‐infesting resistant pupal cells may act as a release valve on the selective pressure for the evolution of counter resistance traits: helping to maintain a stable host–parasite relationship.

Prevention not cure: a review of methods to avoid sea lice infestations in salmon aquaculture

AbstractThe Atlantic salmon aquaculture industry still struggles with ectoparasitic sea lice despite decades of research and development invested into louse removal methods. In contrast, methods to prevent infestations before they occur have received relatively little research effort, yet may offer key benefits over treatment‐focused methods. Here, we summarise the range of potential and existing preventative methods, conduct a meta‐analysis of studies trialling the efficacy of existing preventative methods and discuss the rationale for a shift to the prevention‐focused louse management paradigm. Barrier technologies that minimise host–parasite encounter rates provide the greatest protection against lice, with a weighted median 76% reduction in infestation density in cages with plankton mesh ‘snorkels’ or ‘skirts’, and up to a 100% reduction for fully enclosed cages. Other methods such as geographic spatiotemporal management, manipulation of swimming depth, functional feeds, repellents and host cue masking can drive smaller reductions that may be additive when used in combination with barrier technologies. Finally, ongoing development of louse‐resistant salmon lineages may lead to long‐term improvements if genetic gain is maintained, while the development of an effective vaccine remains a key target. Preventative methods emphasise host resistance traits while simultaneously reducing host–parasite encounters. Effective implementation has the potential to dramatically reduce the need for delousing and thus improve fish welfare, productivity and sustainability in louse‐prone salmon farming regions.

Non-adaptive origins of evolutionary innovations increase network complexity in interacting digital organisms.

The origin of evolutionary innovations is a central problem in evolutionary biology. To what extent such innovations have adaptive or non-adaptive origins is hard to assess in real organisms. This limitation, however, can be overcome using digital organisms, i.e. self-replicating computer programs that mutate, evolve and coevolve within a user-defined computational environment. Here, we quantify the role of the non-adaptive origins of host resistance traits in determining the evolution of ecological interactions among host and parasite digital organisms. We find that host resistance traits arising spontaneously as exaptations increase the complexity of antagonistic host-parasite networks. Specifically, they lead to higher host phenotypic diversification, a larger number of ecological interactions and higher heterogeneity in interaction strengths. Given the potential of network architecture to affect network dynamics, such exaptations may increase the persistence of entire communities. Our in silico approach, therefore, may complement current theoretical advances aimed at disentangling the ecological and evolutionary mechanisms shaping species interaction networks.This article is part of the themed issue 'Process and pattern in innovations from cells to societies'.

Adaptive potential of maritime pine (Pinus pinaster) populations to the emerging pitch canker pathogen, Fusarium circinatum.

There is a concern on how emerging pests and diseases will affect the distribution range and adaptability of their host species, especially due to different conditions derived from climate change and growing globalization. Fusarium circinatum, which causes pitch canker disease in Pinus species, is an exotic pathogen of recent introduction in Spain that threatens its maritime pine (P. pinaster) stands. To predict the impact this disease will have on the species, we examine host resistance traits and their genetic architecture. Resistance phenotyping was done in a clonal provenance/progeny trial, using three-year-old cuttings artificially inoculated with the pathogen and maintained under controlled environmental conditions. A total number of 670 ramets were assessed, distributed in 10 populations, with a total of 47 families, 2 to 5 half-sibs per family, and 3–7 ramets per clone. High genetic variation was found at the three hierarchical levels studied: population, family and clone, being both additive and non-additive effects important. Narrow-sense and broad-sense heritability estimates were relatively high, with respective values of 0.43–0.58 and 0.51–0.8, depending on the resistance traits measured (lesion length, lesion length rate, time to wilting, and survival). These values suggest the species' high capacity of evolutionary response to the F. circinatum pathogen. A population originated in Northern Spain was the most resistant, while another from Morocco was the most susceptible. The total number of plants that did not show lesion development or presented a small lesion (length<30 mm) was 224 out of 670, indicating a high proportion of resistant trees in the offspring within the analyzed populations. We found large differences among populations and considerable genetic variation within populations, which should allow, through natural or artificial selection, the successful adaptation of maritime pine to pitch canker disease.

Assessment of genetic correlation between bacterial cold water disease resistance and spleen index in a domesticated population of rainbow trout: identification of QTL on chromosome Omy19.

Selective breeding of animals for increased disease resistance is an effective strategy to reduce mortality in aquaculture. However, implementation of selective breeding programs is limited by an incomplete understanding of host resistance traits. We previously reported results of a rainbow trout selection program that demonstrated increased survival following challenge with Flavobacterium psychrophilum, the causative agent of bacterial cold water disease (BCWD). Mechanistic study of disease resistance identified a positive phenotypic correlation between post-challenge survival and spleen somatic-index (SI). Herein, we investigated the hypothesis of a genetic correlation between the two traits influenced by colocalizing QTL. We evaluated the inheritance and calculated the genetic correlation in five year-classes of odd- and even-year breeding lines. A total of 322 pedigreed families (n = 25,369 fish) were measured for disease resistance, and 251 families (n = 5,645 fish) were evaluated for SI. Spleen index was moderately heritable in both even-year (h2 = 0.56±0.18) and odd-year (h2 = 0.60±0.15) lines. A significant genetic correlation between SI and BCWD resistance was observed in the even-year line (rg = 0.45±0.20, P = 0.03) but not in the odd-year line (rg = 0.16±0.12, P = 0.19). Complex segregation analyses of the even-year line provided evidence of genes with major effect on SI, and a genome scan of a single family, 2008132, detected three significant QTL on chromosomes Omy19, 16 and 5, in addition to ten suggestive QTL. A separate chromosome scan for disease resistance in family 2008132 identified a significant BCWD QTL on Omy19 that was associated with time to death and percent survival. In family 2008132, Omy19 microsatellite alleles that associated with higher disease resistance also associated with increased spleen size raising the hypothesis that closely linked QTL contribute to the correlation between these traits. To our knowledge, this is the first estimation of spleen size heritability and evidence for genetic linkage with specific disease resistance in a teleost fish.

Effects of genotypic variation in stem solidity on parasitism of a grass-mining insect

Host plant traits can play a significant role in influencing the importance, direction and intensity of tri-trophic interactions by both direct and indirect pathways. A major goal in applied tri-trophic research has been to determine whether breeding for host plant resistance traits can be combined with biological control to develop a more comprehensive control strategy. An important component of developing such a strategy is understanding how host resistance traits affect natural enemy–prey interactions for important pest insects. Here we examine the influence of genotypic variation in stem solidity, the primary trait conferring resistance against the wheat stem sawfly, Cephus cinctus, on parasitism of this major pest of wheat by its native braconid parasitoids. To do so, we conducted a field experiment in which we established replicate plots of 23 wheat genotypes that varied in levels of stem solidity, and quantified herbivore abundance and levels of parasitism across three sites in two years. Increasing stem solidity was associated with an approximately four-fold reduction in average parasitism rates, both across experimental plots and across wheat genotypes. Our analyses suggest that these effects were primarily direct, rather than indirectly mediated via effects of stem solidity on herbivore infestation levels or density. Interestingly, wheat genotype also had a significant influence on levels of parasitism, independent of its effects on stem solidity. Overall, our results suggest that although increasing stem solidity generally reduces parasitism, significant genotypic variability in average parasitism levels exist within solidity categories. Thus it may be possible to select resistant solid stemmed genotypes that also maintain relatively high parasitism levels. To our knowledge, our study is among the first to demonstrate a strong direct effect of genotypic variation in stem solidity on parasitism of grass mining insects, with important applied implications.

NONADDITIVE GENETIC COMPONENTS IN RESISTANCE OF THE RED FLOUR BEETLETRIBOLIUM CASTANAEUMAGAINST PARASITE INFECTION

Genetically coupled antagonistic coevolution between host and parasites can select for the maintenance of recombination in the host. Mechanistically, maintenance of recombination relies on epistatic interactions between resistance genes creating linkage disequilibria (LD). The role of epistasis in host resistance traits is however only partly understood. Therefore, we applied the joint scaling principle to assess epistasis and other nonadditive genetic components of two resistance traits, survival, and parasite spore load, in population crosses of the red flour beetle Tribolium castanaeum under infections with the microsporidian Nosema whitei. We found nonadditive components only in infected populations but not in control populations. The genetic architecture underlying survival under parasite infection was more complex than that of spore load. Accordingly, the observed negative correlation between survival and spore load was mainly based on a correlation between shared additive components. Breakdown of resistance was especially strong in F2 crosses between resistant lines indicating that multiple epistatic routes can lead to the same adaptation. In general, the wide range of nonoverlapping genetic components between crosses indicated that parasite resistance in T. castanaeum can be understood as a multi peaked fitness landscape with epistasis contributing substantially to phenotypic differentiation in resistance.

Mice Naturally Resistant to Yersinia pestis Δ pgm Strains Commonly Used in Pathogenicity Studies

We report that females of some substrains of inbred mouse strain 129 are resistant to systemic plague due to conditionally virulent Deltapgm strains of Yersinia pestis; however, fully virulent Y. pestis is not attenuated in these mice. Therefore, these mice offer a powerful system in which to map in parallel host resistance traits and opposing bacterial virulence properties for plague.

Genetic architecture of resistance to aphids and mites in a willow hybrid system.

Hybrid plants often differ in resistance to arthropods compared to the parental species from which they are derived. To better understand the relative contribution of genetic effects in influencing plant resistance to arthropods, we examined the genetic architecture of resistance in a willow hybrid system, Salix eriocephala, S. sericea, and their interspecific hybrids. Resistance to two arthropods, a willow leaf aphid (Chaitophorus sp.: Aphididae) and an eriophyoid mite (Aculops tetanothrix: Eriophyidae), were compared because resistance to different herbivores may be controlled by different traits and influenced by different genetic effects. We found additive and nonadditive genetic effects to be important in explaining the difference between willow species in resistance to aphids and mites. F2 hybrids exhibited low resistance to aphids, suggesting breakdown of favourable epistatic interactions that confer resistance. F2 hybrids, however, exhibited high resistance to mites, suggesting either the breakdown of interactions that affect traits used by mites in host location or the creation of favourable epistatic interactions. This study demonstrates the potential role of herbivores in affecting plant genetic structure, such that selection by herbivores can potentially lead to the creation of gene interactions that influence host resistance traits or host recognition traits used by the herbivore.

EFFECTS OF VECTOR BEHAVIOR AND HOST RESISTANCE ON MISTLETOE AGGREGATION

Understanding the factors affecting parasite aggregation in natural host populations is one of the central questions in parasite ecology. While different biological mechanisms giving rise to aggregation have been documented in the literature, the role of established parasites in vector attraction, and its importance in determining clumped parasite distributions has received less attention. In a two-year field study, we evaluated the importance of a bird vector, Mimus thenca (Mimidae), on the aggregation dynamics of the holoparasitic mistletoe, Tristerix aphyllus, on its cactus host, Echinopsis chilensis. Removal of T. aphyllus from cacti decreased the number of visits and the time spent by the bird vector, which resulted in a 3.5-fold lower seed deposition of the mistletoe on experimental hosts than on control hosts. Vector preference, however, was not the only factor affecting aggregation in this system. Spine length of the cactus acted as a first line of defense against parasitism, by discouraging bird perching on top of host columns. While heavily parasitized hosts received more seeds than unparasitized hosts, spines counteracted this effect. These results provide field evidence that parasite aggregation results from the balance between vector behavior and host resistance traits.

Genetic architecture of susceptibility to herbivores in hybrid willows.

We performed a common garden experiment using parental, F1, F2, and backcross willow hybrids to test the hypothesis that hybrid willows experience breakdown of resistance to herbivores. After exposing plants to herbivores in the field, we measured the densities/damage caused by 13 insect herbivores and one herbivorous mite. Using joint-scaling tests, we determined the contribution of additive, dominance, and epistasis to variation in susceptibility to herbivores (measured either as density or damage level) among the six genetic classes. We found the genetic architecture of susceptibility/resistance in the parental species to be complex, involving additive, dominance, and epistasis for each herbivore species. Although genic interactions altered plant susceptibility for each of the 14 herbivores, three distinct patterns of response of herbivores to hybrids were expressed. One pattern, observed in four herbivore species, supported the hypothesis of breakdown of resistance genes in recombinant hybrids. A second pattern, shown by six other herbivore species, supported the hypothesis of hybrid breakdown of host recognition genes. In other words, epistatic interactions for host recognition traits (probably oviposition/feeding stimulants or attractants) appeared to be important in determining herbivore abundance for those six species. The final patterns supported a structure of dominance, either for host recognition traits (in the case of three herbivore species) or for host resistance traits (for one herbivore species). The combination of differing responses of herbivore species, including members of the same genus and tribe, and the ubiquitous importance of epistasis suggests that many genes affect herbivore resistance in this hybrid willow system.